52 results on '"Lindberg PG"'
Search Results
2. Contribution of a Tablet-Based Tests to the Diagnosis of Neurocognitive Disorders in Older Adults: A Feasibility Study.
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Um Din N, Maronnat F, Le Boterff Q, Otmane S, Badra F, Lindberg PG, and Belmin J
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- Humans, Aged, Male, Female, Aged, 80 and over, Neuropsychological Tests, Neurocognitive Disorders diagnosis, Geriatric Assessment methods, Feasibility Studies, Computers, Handheld
- Abstract
Neurocognitive diseases are diagnosed in specialized centers such as memory clinics, where the waiting time can be long. The reference assessment involves a battery of tests carried out by a specialized team. Facilitating screening in primary care using new technologies could make it possible to appropriately direct care pathways towards specialist care. This work aimed to set up a battery of questionnaires, cognitive and manual dexterity tests on a digital tablet to screen people with cognitive impairment. Three groups of people are recruited from a memory consultation: people with major neurocognitive disorders, people with mild neurocognitive disorders and people with no cognitive impairment. Initial results in geriatric settings show that the digital tablet assessment test is feasible and well accepted, but that manual dexterity assessment needs to be adapted to the bodily particularities of the very old.
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- 2024
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3. Alterations of tactile and anatomical spatial representations of the hand after stroke.
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Dupin L, Gerardin E, Térémetz M, Hamdoun S, Turc G, Maier MA, Baron JC, and Lindberg PG
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- Humans, Male, Female, Middle Aged, Aged, Adult, Space Perception physiology, Touch physiology, Paresis physiopathology, Stroke physiopathology, Stroke complications, Hand physiopathology, Touch Perception physiology
- Abstract
Stroke often causes long-term motor and somatosensory impairments. Motor planning and tactile perception rely on spatial body representations. However, the link between altered spatial body representations, motor deficit and tactile spatial coding remains unclear. This study investigates the relationship between motor deficits and alterations of anatomical (body) and tactile spatial representations of the hand in 20 post-stroke patients with upper limb hemiparesis. Anatomical and tactile spatial representations were assessed from 10 targets (nails and knuckles) respectively cued verbally by their anatomical name or using tactile stimulations. Two distance metrics (hand width and finger length) and two structural measures (relative organization of targets positions and angular deviation of fingers from their physical posture) were computed and compared to clinical assessments, normative data and lesions sites. Over half of the patients had altered anatomical and/or tactile spatial representations. Metrics of tactile and anatomical representations showed common variations, where a wider hand representation was linked to more severe motor deficits. In contrast, alterations in structural measures were not concomitantly observed in tactile and anatomical representations and did not correlate with clinical assessments. Finally, a preliminary analysis showed that specific alterations in tactile structural measures were associated with dorsolateral prefrontal stroke lesions. This study reveals shared and distinct characteristics of anatomical and tactile hand spatial representations, reflecting different mechanisms that can be affected differently after stroke: metrics and location of tactile and anatomical representations were partially shared while the structural measures of tactile and anatomical representations had distinct characteristics., Competing Interests: Declaration of competing interest None., (Copyright © 2024 The Author(s). Published by Elsevier Ltd.. All rights reserved.)
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- 2024
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4. Increased dual-task interference during upper limb movements in stroke exceeding that found in aging - a systematic review and meta-analysis.
- Author
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Lindberg PG, AmirShemiraniha N, Krewer C, Maier MA, and Hermsdörfer J
- Abstract
Objective: To determine whether dual-task interference during upper limb tasks is increased in patients after stroke compared to healthy older subjects and to compare magnitude of stroke-induced change in interference to that explained by aging., Methods: We conducted a systematic literature search in MEDLINE, CINAHL, Google Scholar and PEDro databases up to October 2023 for studies on upper limb dual-tasks in stroke and elderly healthy subjects. Eleven upper limb dual-task studies in stroke patients and 11 studies in healthy older subjects were identified and systematically reviewed. A meta-analysis was performed on seven stroke studies and on five studies in healthy older subjects that included control groups., Results: Most stroke studies investigated proximal arm movements with kinematic measures, but few studies evaluated manual dexterity. In contrast, studies in healthy older subjects used more distal (finger tapping) tasks. The meta-analysis showed that stroke patients had on average a 19% (CI 95% = 1.0-37.3) increase in dual-task interference compared to age-matched healthy controls ( Z = 2.06, p = 0.04). Older healthy subjects showed greater dual-task interference compared to younger subjects (19% greater, CI 95% = 6.5-31.2, Z = 2.98, p = 0.003)., Conclusion: Meta-analysis revealed an increase in dual-task interference during upper limb movements in stroke patients, exceeding age-related changes, supporting the presence of subclinical impairments in divided attention post-stroke that may impede motor recovery., Competing Interests: MAM and PGL have patented the method for multidimensional measurement of manual dexterity (WO2016184935A3). PL is a founding member of Dextrain company commercializing innovation. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision., (Copyright © 2024 Lindberg, AmirShemiraniha, Krewer, Maier and Hermsdörfer.)
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- 2024
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5. Post-Stroke Impairments of Manual Dexterity and Finger Proprioception: Their Contribution to Upper Limb Activity Capacity.
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van Ravestyn C, Gerardin E, Térémetz M, Hamdoun S, Baron JC, Calvet D, Vandermeeren Y, Turc G, Maier MA, Rosso C, Mas JL, Dupin L, and Lindberg PG
- Subjects
- Adult, Aged, Female, Humans, Male, Middle Aged, Motor Activity physiology, Motor Skills physiology, Paresis physiopathology, Paresis etiology, Fingers physiopathology, Fingers physiology, Proprioception physiology, Stroke physiopathology, Stroke complications, Upper Extremity physiopathology
- Abstract
Background: Knowing how impaired manual dexterity and finger proprioception affect upper limb activity capacity is important for delineating targeted post-stroke interventions for upper limb recovery., Objectives: To investigate whether impaired manual dexterity and finger proprioception explain variance in post-stroke activity capacity, and whether they explain more variance than conventional clinical assessments of upper limb sensorimotor impairments., Methods: Activity capacity and hand sensorimotor impairments were assessed using clinical measures in N = 42 late subacute/chronic hemiparetic stroke patients. Dexterity was evaluated using the Dextrain Manipulandum to quantify accuracy of visuomotor finger force-tracking (N = 36), timing of rhythmic tapping (N = 36), and finger individuation (N = 24), as well as proprioception (N = 27). Stepwise multivariate and hierarchical linear regression models were used to identify impairments best explaining activity capacity., Results: Dexterity and proprioceptive components significantly increased the variance explained in activity capacity: (i) Box and Block Test was best explained by baseline tonic force during force-tracking and tapping frequency (adjusted R
2 = .51); (ii) Motor Activity Log was best explained by success rate in finger individuation (adjusted R2 = .46); (iii) Action Research Arm Test was best explained by release of finger force and proprioceptive measures (improved reaction time related to use of proprioception; adjusted R2 = .52); and (iv) Moberg Pick-Up test was best explained by proprioceptive function (adjusted R2 = .18). Models excluding dexterity and proprioception variables explained up to 19% less variance., Conclusions: Manual dexterity and finger proprioception explain unique variance in activity capacity not captured by conventional impairment measures and should be assessed when considering the underlying causes of post-stroke activity capacity limitations.URL: https://www.clinicaltrials.gov. Unique identifier: NCT03934073., Competing Interests: Declaration of Conflicting InterestsThe author(s) declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: MT, MAM, and PGL have patented the method for multidimensional measurement of manual dexterity (WO2016184935A3). MT and PGL are founding members of start-up company Dextrain (started in 2021) who owns the commercial rights. MT now works for the start-up full-time. PGL, head of the scientific board, reports no financial gain in advising the company. CR is a member of the scientific board of the company but receives no financial benefits. The other authors report no financial interests or potential conflicts of interest.- Published
- 2024
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6. Cortical activations associated with spatial remapping of finger touch using EEG.
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Alouit A, Gavaret M, Ramdani C, Lindberg PG, and Dupin L
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- Humans, Fingers physiology, Hand physiology, Electroencephalography, Somatosensory Cortex, Touch physiology, Touch Perception physiology
- Abstract
The spatial coding of tactile information is functionally essential for touch-based shape perception and motor control. However, the spatiotemporal dynamics of how tactile information is remapped from the somatotopic reference frame in the primary somatosensory cortex to the spatiotopic reference frame remains unclear. This study investigated how hand position in space or posture influences cortical somatosensory processing. Twenty-two healthy subjects received electrical stimulation to the right thumb (D1) or little finger (D5) in three position conditions: palm down on right side of the body (baseline), hand crossing the body midline (effect of position), and palm up (effect of posture). Somatosensory-evoked potentials (SEPs) were recorded using electroencephalography. One early-, two mid-, and two late-latency neurophysiological components were identified for both fingers: P50, P1, N125, P200, and N250. D1 and D5 showed different cortical activation patterns: compared with baseline, the crossing condition showed significant clustering at P1 for D1, and at P50 and N125 for D5; the change in posture showed a significant cluster at N125 for D5. Clusters predominated at centro-parietal electrodes. These results suggest that tactile remapping of fingers after electrical stimulation occurs around 100-125 ms in the parietal cortex., (© The Author(s) 2024. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)
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- 2024
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7. Neurophysiological explorations across the spectrum of psychosis, autism, and depression, during wakefulness and sleep: protocol of a prospective case-control transdiagnostic multimodal study (DEMETER).
- Author
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Lucarini V, Alouit A, Yeh D, Le Coq J, Savatte R, Charre M, Louveau C, Houamri MB, Penaud S, Gaston-Bellegarde A, Rio S, Drouet L, Elbaz M, Becchio J, Pourchet S, Pruvost-Robieux E, Marchi A, Moyal M, Lefebvre A, Chaumette B, Grice M, Lindberg PG, Dupin L, Piolino P, Lemogne C, Léger D, Gavaret M, Krebs MO, and Iftimovici A
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- Young Adult, Adolescent, Humans, Adult, Wakefulness, Case-Control Studies, Depression, Brain, Sleep, Electroencephalography methods, Autistic Disorder diagnosis, Autism Spectrum Disorder diagnosis, Depressive Disorder, Major, Psychotic Disorders
- Abstract
Background: Quantitative electroencephalography (EEG) analysis offers the opportunity to study high-level cognitive processes across psychiatric disorders. In particular, EEG microstates translate the temporal dynamics of neuronal networks throughout the brain. Their alteration may reflect transdiagnostic anomalies in neurophysiological functions that are impaired in mood, psychosis, and autism spectrum disorders, such as sensorimotor integration, speech, sleep, and sense of self. The main questions this study aims to answer are as follows: 1) Are EEG microstate anomalies associated with clinical and functional prognosis, both in resting conditions and during sleep, across psychiatric disorders? 2) Are EEG microstate anomalies associated with differences in sensorimotor integration, speech, sense of self, and sleep? 3) Can the dynamic of EEG microstates be modulated by a non-drug intervention such as light hypnosis?, Methods: This prospective cohort will include a population of adolescents and young adults, aged 15 to 30 years old, with ultra-high-risk of psychosis (UHR), first-episode psychosis (FEP), schizophrenia (SCZ), autism spectrum disorder (ASD), and major depressive disorder (MDD), as well as healthy controls (CTRL) (N = 21 × 6), who will be assessed at baseline and after one year of follow-up. Participants will undergo deep phenotyping based on psychopathology, neuropsychological assessments, 64-channel EEG recordings, and biological sampling at the two timepoints. At baseline, the EEG recording will also be coupled to a sensorimotor task and a recording of the characteristics of their speech (prosody and turn-taking), a one-night polysomnography, a self-reference effect task in virtual reality (only in UHR, FEP, and CTRL). An interventional ancillary study will involve only healthy controls, in order to assess whether light hypnosis can modify the EEG microstate architecture in a direction opposite to what is seen in disease., Discussion: This transdiagnostic longitudinal case-control study will provide a multimodal neurophysiological assessment of clinical dimensions (sensorimotor integration, speech, sleep, and sense of self) that are disrupted across mood, psychosis, and autism spectrum disorders. It will further test the relevance of EEG microstates as dimensional functional biomarkers., Trial Registration: ClinicalTrials.gov Identifier NCT06045897., (© 2023. The Author(s).)
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- 2023
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8. Efficacy of interactive manual dexterity training after stroke: a pilot single-blinded randomized controlled trial.
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Térémetz M, Hamdoun S, Colle F, Gerardin E, Desvilles C, Carment L, Charron S, Cuenca M, Calvet D, Baron JC, Turc G, Maier MA, Rosso C, Mas JL, and Lindberg PG
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- Humans, Single-Blind Method, Prospective Studies, Recovery of Function, Treatment Outcome, Upper Extremity, Stroke complications, Stroke Rehabilitation
- Abstract
Objective: To compare the efficacy of Dextrain Manipulandum™ training of dexterity components such as force control and independent finger movements, to dose-matched conventional therapy (CT) post-stroke., Methods: A prospective, single-blind, pilot randomized clinical trial was conducted. Chronic-phase post-stroke patients with mild-to-moderate dexterity impairment (Box and Block Test (BBT) > 1) received 12 sessions of Dextrain or CT. Blinded measures were obtained before and after training and at 3-months follow-up. Primary outcome was BBT-change (after-before training). Secondary outcomes included changes in motor impairments, activity limitations and dexterity components. Corticospinal excitability and short intracortical inhibition (SICI) were measured using transcranial magnetic stimulation., Results: BBT-change after training did not differ between the Dextrain (N = 21) vs CT group (N = 21) (median [IQR] = 5[2-7] vs 4[2-7], respectively; P = 0.36). Gains in BBT were maintained at the 3-month post-training follow-up, with a non-significant trend for enhanced BBT-change in the Dextrain group (median [IQR] = 3[- 1-7.0], P = 0.06). Several secondary outcomes showed significantly larger changes in the Dextrain group: finger tracking precision (mean ± SD = 0.3 ± 0.3N vs - 0.1 ± 0.33N; P < 0.0018), independent finger movements (34.7 ± 25.1 ms vs 7.7 ± 18.5 ms, P = 0.02) and maximal finger tapping speed (8.4 ± 7.1 vs 4.5 ± 4.9, P = 0.045). At follow-up, Dextrain group showed significantly greater improvement in Motor Activity Log (median/IQR = 0.7/0.2-0.8 vs 0.2/0.1-0.6, P = 0.05). Across both groups SICI increased in patients with greater BBT-change (Rho = 0.80, P = 0.006). Comparing Dextrain subgroups with maximal grip force higher/lower than median (61.2%), BBT-change was significantly larger in patients with low vs high grip force (7.5 ± 5.6 vs 2.9 ± 2.8; respectively, P = 0.015)., Conclusions: Although immediate improvements in gross dexterity post-stroke did not significantly differ between Dextrain training and CT, our findings suggest that Dextrain enhances recovery of several dexterity components and reported hand-use, particularly when motor impairment is moderate (low initial grip force). Findings need to be confirmed in a larger trial. Trial registration ClinicalTrials.gov NCT03934073 (retrospectively registered)., (© 2023. The Author(s).)
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- 2023
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9. A tablet-based quantitative assessment of manual dexterity for detection of early psychosis.
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Le Boterff Q, Rabah A, Carment L, Bendjemaa N, Térémetz M, Alouit A, Levy A, Tanguy G, Morin V, Amado I, Cuenca M, Turc G, Maier MA, Krebs MO, and Lindberg PG
- Abstract
Background: We performed a pilot study on whether tablet-based measures of manual dexterity can provide behavioral markers for detection of first-episode psychosis (FEP), and whether cortical excitability/inhibition was altered in FEP., Methods: Behavioral and neurophysiological testing was undertaken in persons diagnosed with FEP ( N = 20), schizophrenia (SCZ, N = 20), autism spectrum disorder (ASD, N = 20), and in healthy control subjects ( N = 20). Five tablet tasks assessed different motor and cognitive functions: Finger Recognition for effector (finger) selection and mental rotation, Rhythm Tapping for temporal control, Sequence Tapping for control/memorization of motor sequences, Multi Finger Tapping for finger individuation, and Line Tracking for visuomotor control. Discrimination of FEP (from other groups) based on tablet-based measures was compared to discrimination through clinical neurological soft signs (NSS). Cortical excitability/inhibition, and cerebellar brain inhibition were assessed with transcranial magnetic stimulation., Results: Compared to controls, FEP patients showed slower reaction times and higher errors in Finger Recognition, and more variability in Rhythm Tapping. Variability in Rhythm Tapping showed highest specificity for the identification of FEP patients compared to all other groups (FEP vs. ASD/SCZ/Controls; 75% sensitivity, 90% specificity, AUC = 0.83) compared to clinical NSS (95% sensitivity, 22% specificity, AUC = 0.49). Random Forest analysis confirmed FEP discrimination vs. other groups based on dexterity variables (100% sensitivity, 85% specificity, balanced accuracy = 92%). The FEP group had reduced short-latency intra-cortical inhibition (but similar excitability) compared to controls, SCZ, and ASD. Cerebellar inhibition showed a non-significant tendency to be weaker in FEP., Conclusion: FEP patients show a distinctive pattern of dexterity impairments and weaker cortical inhibition. Easy-to-use tablet-based measures of manual dexterity capture neurological deficits in FEP and are promising markers for detection of FEP in clinical practice., Competing Interests: MT and PL own shares in Dextrain company (www.dextrain.com) which develops and commercializes solutions for measurement and rehabilitation of manual dexterity. MT, MM, and PL have a patent on the DexTrain manipulandum (WO2020070305A1) and method for evaluating manual dexterity (WO2016184935A2). The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest., (Copyright © 2023 Le Boterff, Rabah, Carment, Bendjemaa, Térémetz, Alouit, Levy, Tanguy, Morin, Amado, Cuenca, Turc, Maier, Krebs and Lindberg.)
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- 2023
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10. Validity, Intra-Rater Reliability and Normative Data of the Neuroflexor™ Device to Measure Spasticity of the Ankle Plantar Flexors after Stroke.
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Pennati GV, Carment L, Godbolt AK, Plantin J, Borg J, and Lindberg PG
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- Humans, Reproducibility of Results, Ankle Joint, Lower Extremity, Muscle Spasticity, Ankle, Stroke
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Objective: Quantification of lower limb spasticity after stroke and the differentiation of neural from passive muscle resistance remain key clinical challenges. The aim of this study was to validate the novel NeuroFlexor foot module, to assess the intrarater reliability of measurements and to identify normative cut-off values., Methods: Fifteen patients with chronic stroke with clinical history of spasticity and 18 healthy subjects were examined with the NeuroFlexor foot module at controlled velocities. Elastic, viscous and neural components of passive dorsiflexion resistance were quantified (in Newton, N). The neural component, reflecting stretch reflex mediated resistance, was validated against electromyography activity. A test-retest design with a 2-way random effects model permitted study of intra-rater reliability. Finally, data from 73 healthy subjects were used to establish cutoff values according to mean + 3 standard deviations and receiver operating characteristic curve analysis., Results: The neural component was higher in stroke patients, increased with stretch velocity and correlated with electromyography amplitude. Reliability was high for the neural component (intraclass correlation coefficient model 2.1 (ICC2,1) ≥ 0.903) and good for the elastic component (ICC2,1 ≥ 0.898). Cutoff values were identified, and all patients with neural component above the limit presented pathological electromyography amplitude (area under the curve (AUC) = 1.00, sensitivity = 100%, specificity = 100%)., Conclusion: The NeuroFlexor may offer a clinically feasible and non-invasive way to objectively quantify lower limb spasticity.
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- 2023
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11. Longitudinal changes in functional connectivity in speech motor networks in apraxia of speech after stroke.
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Hybbinette H, Östberg P, Schalling E, Deboussard C, Plantin J, Borg J, and Lindberg PG
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Objective: The cerebral substrates of apraxia of speech (AOS) recovery remain unclear. Resting state fMRI post stroke can inform on altered functional connectivity (FC) within cortical language networks. Some initial studies report reduced FC between bilateral premotor cortices in patients with AOS, with lowest FC in patients with the most severe AOS. However, longitudinal FC studies in stroke are lacking. The aims of the present longitudinal study in early post stroke patients with AOS were (i) to compare connectivity strength in AOS patients to that in left hemisphere (LH) lesioned stroke patients without a speech-language impairment, (ii) to investigate the relation between FC and severity of AOS, aphasia and non-verbal oral apraxia (NVOA) and (iii) to investigate longitudinal changes in FC, from the subacute phase to the chronic phase to identify predictors of AOS recovery., Methods: Functional connectivity measures and comprehensive speech-language assessments were obtained at 4 weeks and 6 months after stroke in nine patients with AOS after a LH stroke and in six LH lesioned stroke patients without speech-language impairment. Functional connectivity was investigated in a network for speech production: inferior frontal gyrus (IFG), anterior insula (aINS), and ventral premotor cortex (vPMC), all bilaterally to investigate signs of adaptive or maladaptive changes in both hemispheres., Results: Interhemispheric vPMC connectivity was significantly reduced in patients with AOS compared to LH lesioned patients without speech-language impairment. At 6 months, the AOS severity was associated with interhemispheric aINS and vPMC connectivity. Longitudinal changes in FC were found in individuals, whereas no significant longitudinal change in FC was found at the group level. Degree of longitudinal AOS recovery was strongly associated with interhemispheric IFG connectivity strength at 4 weeks., Conclusion: Early interhemispheric IFG connectivity may be a strong predictor of AOS recovery. The results support the importance of interhemispheric vPMC connection in speech motor planning and severity of AOS and suggest that also bilateral aINS connectivity may have an impact on AOS severity. These findings need to be validated in larger cohorts., Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest., (Copyright © 2022 Hybbinette, Östberg, Schalling, Deboussard, Plantin, Borg and Lindberg.)
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- 2022
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12. Age- and task-dependent effects of cerebellar tDCS on manual dexterity and motor learning-A preliminary study.
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Lindberg PG, Verneau M, Boterff QL, Cuenca-Maia M, Baron JC, and Maier MA
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- Humans, Aged, Cerebellum physiology, Learning physiology, Fingers, Movement, Transcranial Direct Current Stimulation methods
- Abstract
Objectives: The role of the cerebellum in motor learning of dexterous control and interaction with aging remains incompletely understood. We compared the effect of age and cerebellar transcranial direct current stimulation (CRB-tDCS) on motor learning in two different manual dexterity tasks, visuomotor force control vs. effector selection (independent finger movements)., Methods: Twenty younger and 20 older adults were randomized (double-blinded) to anodal or sham CRB-tDCS during dexterity training over three consecutive days, and followed-up at day 10. Motor learning was measured as (i) overall learning (across 10 days), (ii) within-day (short-term) learning, (iii) between-day learning (consolidation), and (iv) retention (long-term learning; day 3 to day 10)., Results: Younger and older subjects showed significant overall learning in both tasks. Subjects with poor initial performance showed stronger learning. No effects of CRB-tDCS were observed in younger adults. A significant Age*CRB-tDCS interaction showed that CRB-tDCS improved within-day learning in finger independence (improved reaction time in effector selection) in older adults. However, a significant Age*CRB-tDCS interaction showed that CRB-tDCS impacted consolidation negatively in older subjects. No stimulation effects were found on retention. Finally, we found that degree of within-day learning in finger independence (change in reaction times) correlated with baseline (pre-training) reaction times in both young and old subjects., Discussion: The results suggest that CRB-tDCS may improve short-term learning of manual dexterity in older adults in a task-dependent manner, specifically in difficult tasks requiring effector (action) selection. However, cerebellar tDCS stimulation may also interfere with consolidation in older subjects. These results need confirmation in a larger sample., Competing Interests: Declaration of Competing Interest MAM and PGL have patented a method for measurement of manual dexterity (EP2659835A1). MV, QLB, MC, and JCB declare no competing interests., (Copyright © 2022 Elsevier Masson SAS. All rights reserved.)
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- 2022
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13. Motor inhibition and its contribution to recovery of dexterous hand use after stroke.
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Plantin J, Godbolt AK, Pennati GV, Laurencikas E, Fransson P, Baron JC, Maier MA, Borg J, and Lindberg PG
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Recovery of dexterous hand use is critical for functional outcome after stroke. Grip force recordings can inform on maximal motor output and modulatory and inhibitory cerebral functions, but how these actually contribute to recovery of dexterous hand use is unclear. This cohort study used serially assessed measures of hand kinetics to test the hypothesis that behavioural measures of motor modulation and inhibition explain dexterity recovery beyond that explained by measures of motor output alone. We also investigated the structural and functional connectivity correlates of grip force control recovery. Eighty-nine adults (median age = 54 years, 26% females) with first-ever ischaemic or haemorrhagic stroke and persistent arm and hand paresis were assessed longitudinally, at 3 weeks, and at 3 and 6 months after stroke. Kinetic measures included: maximal grip force, accuracy of precision and power grip force control, and ability to release force abruptly. Dexterous hand use was assessed clinically with the Box and Block Test and motor impairment with the upper extremity Fugl-Meyer Assessment. Structural and functional MRI was used to assess weighted corticospinal tract lesion load, voxel-based lesion symptom mapping and interhemispheric resting-state functional connectivity. Fifty-three per cent of patients had severe initial motor impairment and a majority still had residual force control impairments at 6 months. Force release at 3 weeks explained 11% additional variance of Box and Block Test outcome at 6 months, above that explained by initial scores (67%). Other kinetic measures did not explain additional variance of recovery. The predictive value of force release remained significant when controlling for corticospinal tract lesion load and clinical measures. Corticospinal tract lesion load correlated with recovery in grip force control measures. Lesions involving the parietal operculum, insular cortex, putamen and fronto-striatal tracts were also related to poorer force modulation and release. Lesions to fronto-striatal tracts explained an additional 5% of variance in force release beyond the 43% explained by corticospinal injury alone. Interhemispheric functional connectivity did not relate to force control recovery. We conclude that not only voluntary force generation but also force release (reflecting motor inhibition) are important for recovery of dexterous hand use after stroke. Although corticospinal injury is a main determinant of recovery, lesions to integrative somatosensory areas and fronto-parietal white matter (involved in motor inhibition) explain additional variance in post-stroke force release recovery. Our findings indicate that post-stroke upper limb motor impairment profiling, which is essential for targeted treatment, should consider both voluntary grasp generation and inhibition., (© The Author(s) 2022. Published by Oxford University Press on behalf of the Guarantors of Brain.)
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- 2022
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14. A novel tablet-based application for assessment of manual dexterity and its components: a reliability and validity study in healthy subjects.
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Rabah A, Le Boterff Q, Carment L, Bendjemaa N, Térémetz M, Dupin L, Cuenca M, Mas JL, Krebs MO, Maier MA, and Lindberg PG
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- Adult, Hand, Healthy Volunteers, Humans, Middle Aged, Reproducibility of Results, Upper Extremity, Stroke
- Abstract
Background: We developed five tablet-based tasks (applications) to measure multiple components of manual dexterity., Aim: to test reliability and validity of tablet-based dexterity measures in healthy participants., Methods: Tasks included: (1) Finger recognition to assess mental rotation capacity. The subject taps with the finger indicated on a virtual hand in three orientations (reaction time, correct trials). (2) Rhythm tapping to evaluate timing of finger movements performed with, and subsequently without, an auditory cue (inter-stimulus interval). (3) Multi-finger tapping to assess independent finger movements (reaction time, correct trials, unwanted finger movements). (4) Sequence tapping to assess production and memorization of visually cued finger sequences (successful taps). (5) Line-tracking to assess movement speed and accuracy while tracking an unpredictably moving line on the screen with the fingertip (duration, error). To study inter-rater reliability, 34 healthy subjects (mean age 35 years) performed the tablet tasks twice with two raters. Relative reliability (Intra-class correlation, ICC) and absolute reliability (Standard error of measurement, SEM) were established. Task validity was evaluated in 54 healthy subjects (mean age 49 years, range: 20-78 years) by correlating tablet measures with age, clinical dexterity assessments (time taken to pick-up objects in Box and Block Test, BBT and Moberg Pick Up Test, MPUT) and with measures obtained using a finger force-sensor device., Results: Most timing measures showed excellent reliability. Poor to excellent reliability was found for correct trials across tasks, and reliability was poor for unwanted movements. Inter-session learning occurred in some measures. Age correlated with slower and more variable reaction times in finger recognition, less correct trials in multi-finger tapping, and slower line-tracking. Reaction times correlated with those obtained using a finger force-sensor device. No significant correlations between tablet measures and BBT or MPUT were found. Inter-task correlation among tablet-derived measures was weak., Conclusions: Most tablet-based dexterity measures showed good-to-excellent reliability (ICC ≥ 0.60) except for unwanted movements during multi-finger tapping. Age-related decline in performance and association with finger force-sensor measures support validity of tablet measures. Tablet-based components of dexterity complement conventional clinical dexterity assessments. Future work is required to establish measurement properties in patients with neurological and psychiatric disorders., (© 2022. The Author(s).)
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- 2022
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15. Shrinking of spatial hand representation but not of objects across the lifespan.
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Dupin L, Cuenca M, Baron JC, Maier MA, and Lindberg PG
- Subjects
- Adult, Aged, Body Image, Hand, Humans, Middle Aged, Space Perception, Touch, Young Adult, Longevity, Touch Perception
- Abstract
Perception and action are based on cerebral spatial representations of the body and the external world. However, spatial representations differ from the physical characteristics of body and external space (e.g., objects). It remains unclear whether these discrepancies are related to functional requirements of action and are shared between different spatial representations, indicating common brain processes. We hypothesized that distortions of spatial hand representation would be affected by age, sensorimotor practice and external space representation. We assessed hand representations using tactile and verbal localization tasks and quantified object representation in three age groups (20-79 yrs, total n = 60). Our results show significant shrinking of spatial hand representations (hand width) with age, unrelated to sensorimotor functions. No such shrinking occurred in spatial object representations despite some common characteristics with hand representations. Therefore, spatial properties of body representation partially share characteristics of object representation but also evolve independently across the lifespan., Competing Interests: Declaration of competing interest The authors declare that they have no competing interests., (Copyright © 2021. Published by Elsevier Ltd.)
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- 2022
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16. Effects of 60 Min Electrostimulation With the EXOPULSE Mollii Suit on Objective Signs of Spasticity.
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Pennati GV, Bergling H, Carment L, Borg J, Lindberg PG, and Palmcrantz S
- Abstract
Background: The EXOPULSE Mollii method is an innovative full-body suit approach for non-invasive electrical stimulation, primarily designed to reduce disabling spasticity and improve motor function through the mechanism of reciprocal inhibition. This study aimed to evaluate the effectiveness of one session of stimulation with the EXOPULSE Mollii suit at different stimulation frequencies on objective signs of spasticity and clinical measures, and the subjective perceptions of the intervention. Methods: Twenty patients in the chronic phase after stroke were enrolled in a cross-over, double-blind controlled study. Electrical stimulation delivered through EXOPULSE Mollii was applied for 60 min at two active frequencies (20 and 30 Hz) and in OFF-settings (placebo) in a randomized order, every second day. Spasticity was assessed with controlled-velocity passive muscle stretches using the NeuroFlexor hand and foot modules. Surface electromyography (EMG) for characterizing flexor carpi radialis, medial gastrocnemius, and soleus muscles activation, Modified Ashworth Scale and range of motion were used as complementary tests. Finally, a questionnaire was used to assess the participants' perceptions of using the EXOPULSE Mollii suit. Results: At group level, analyses showed no significant effect of stimulation at any frequency on NeuroFlexor neural component (NC) and EMG amplitude in the upper or lower extremities ( p > 0.35). Nevertheless, the effect was highly variable at the individual level, with eight patients exhibiting reduced NC (>1 N) in the upper extremity after stimulation at 30 Hz, 5 at 20 Hz and 3 in OFF settings. All these patients presented severe spasticity at baseline, i.e., NC > 8 N. Modified Ashworth ratings of spasticity and range of motion did not change significantly after stimulation at any frequency. Finally, 75% of participants reported an overall feeling of well-being during stimulation, with 25% patients describing a muscle-relaxing effect on the affected hand and/or foot at both 20 and 30 Hz. Conclusions: The 60 min of electrical stimulation with EXOPULSE Mollii suit did not reduce spasticity consistently in the upper and lower extremities in the chronic phase after stroke. Findings suggest a need for further studies in patients with severe spasticity after stroke including repeated stimulation sessions. Clinical Trial Registration: https://clinicaltrials.gov/ct2/show/NCT04076878, identifier: NCT04076878., Competing Interests: The NeuroFlexor instrument has been patented (WO/2008/121067), and the PL is a shareholder in the manufacturing company Aggero MedTech AB. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest., (Copyright © 2021 Pennati, Bergling, Carment, Borg, Lindberg and Palmcrantz.)
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- 2021
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17. Spatial hand representation in anorexia nervosa: a controlled pilot study.
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Verbe J, Lindberg PG, Gorwood P, Dupin L, and Duriez P
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- Adult, Behavior, Body Dissatisfaction, Female, Humans, Male, Young Adult, Anorexia Nervosa diagnosis, Anorexia Nervosa psychology, Hand anatomy & histology, Hand physiology, Movement
- Abstract
Body representation distortion (BRD) is a core criterion of Anorexia Nervosa (AN), and is usually assessed subjectively, focusing on body shape. We aimed to develop a new assessment to evaluate body representation independently from socially-mediated body image, on a body part with low emotional salience (hands). In a monocentric open label pilot study, we measured hand representations based on explicit (verbal) and implicit (tactile) instructions. Participants, with eyes closed, had to point targeted locations (knuckles and nails of each finger) based on verbal instructions and tactile stimulations to evaluate body representations respectively. Ratios between hand width and finger length were compared between AN (n = 31) and controls (n = 31) and correlated with current body mass index, AN subtype and disease duration. To control that hand distortion was specific to body representation, we also assessed object representation. Hand representation's width/length ratio was significantly increased in patients with AN, whereas no difference was found in object representation. We found no correlation between hand wideness and clinical traits related to eating disorders. Our results propose that BRD is not limited to body parts with high emotional salience, strengthening the hypothesis that anorexia nervosa is associated with profound unspecific BRD., (© 2021. The Author(s).)
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- 2021
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18. Outcome measures used in trials on gait rehabilitation in multiple sclerosis: A systematic literature review.
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Santisteban L, Teremetz M, Irazusta J, Lindberg PG, and Rodriguez-Larrad A
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- Humans, Multiple Sclerosis physiopathology, Patient Reported Outcome Measures, Randomized Controlled Trials as Topic, Spatio-Temporal Analysis, Walk Test, Gait Analysis methods, Multiple Sclerosis rehabilitation
- Abstract
Background: Multiple Sclerosis (MS) is associated with impaired gait and a growing number of clinical trials have investigated efficacy of various interventions. Choice of outcome measures is crucial in determining efficiency of interventions. However, it remains unclear whether there is consensus on which outcome measures to use in gait intervention studies in MS., Objective: We aimed to identify the commonly selected outcome measures in randomized controlled trials (RCTs) on gait rehabilitation interventions in people with MS. Additional aims were to identify which of the domains of the International Classification of Functioning, Disability and Health (ICF) are the most studied and to characterize how outcome measures are combined and adapted to MS severity., Methods: Pubmed, Cochrane Central, Embase and Scopus databases were searched for RCT studies on gait interventions in people living with MS according to PRISMA guidelines., Results: In 46 RCTs, we identified 69 different outcome measures. The most used outcome measures were 6-minute walking test and the Timed Up and Go test, used in 37% of the analyzed studies. They were followed by gait spatiotemporal parameters (35%) most often used to inform on gait speed, cadence, and step length. Fatigue was measured in 39% of studies. Participation was assessed in 50% of studies, albeit with a wide variety of scales. Only 39% of studies included measures covering all ICF levels, and Participation measures were rarely combined with gait spatiotemporal parameters (only two studies)., Conclusions: Selection of outcome measures remains heterogenous in RCTs on gait rehabilitation interventions in MS. However, there is a growing consensus on the need for quantitative gait spatiotemporal parameter measures combined with clinical assessments of gait, balance, and mobility in RCTs on gait interventions in MS. Future RCTs should incorporate measures of fatigue and measures from Participation domain of ICF to provide comprehensive evaluation of trial efficacy across all levels of functioning., Competing Interests: The authors have declared that no competing interests exist.
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- 2021
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19. Recovery and Prediction of Bimanual Hand Use After Stroke.
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Plantin J, Verneau M, Godbolt AK, Pennati GV, Laurencikas E, Johansson B, Krumlinde-Sundholm L, Baron JC, Borg J, and Lindberg PG
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- Adult, Aged, Cognitive Dysfunction diagnosis, Cognitive Dysfunction etiology, Female, Humans, Longitudinal Studies, Magnetic Resonance Imaging, Male, Middle Aged, Paresis diagnosis, Paresis etiology, Prognosis, Severity of Illness Index, Stroke complications, Stroke diagnosis, Cognitive Dysfunction physiopathology, Connectome, Hand physiopathology, Outcome Assessment, Health Care, Paresis physiopathology, Psychomotor Performance physiology, Recovery of Function physiology, Stroke physiopathology
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Objective: To determine similarities and differences in key predictors of recovery of bimanual hand use and unimanual motor impairment after stroke., Method: In this prospective longitudinal study, 89 patients with first-ever stroke with arm paresis were assessed at 3 weeks and 3 and 6 months after stroke onset. Bimanual activity performance was assessed with the Adult Assisting Hand Assessment Stroke (Ad-AHA), and unimanual motor impairment was assessed with the Fugl-Meyer Assessment (FMA). Candidate predictors included shoulder abduction and finger extension measured by the corresponding FMA items (FMA-SAFE; range 0-4) and sensory and cognitive impairment. MRI was used to measure weighted corticospinal tract lesion load (wCST-LL) and resting-state interhemispheric functional connectivity (FC)., Results: Initial Ad-AHA performance was poor but improved over time in all (mild-severe) impairment subgroups. Ad-AHA correlated with FMA at each time point ( r > 0.88, p < 0.001), and recovery trajectories were similar. In patients with moderate to severe initial FMA, FMA-SAFE score was the strongest predictor of Ad-AHA outcome ( R
2 = 0.81) and degree of recovery ( R2 = 0.64). Two-point discrimination explained additional variance in Ad-AHA outcome ( R2 = 0.05). Repeated analyses without FMA-SAFE score identified wCST-LL and cognitive impairment as additional predictors. A wCST-LL >5.5 cm3 strongly predicted low to minimal FMA/Ad-AHA recovery (≤10 and 20 points respectively, specificity = 0.91). FC explained some additional variance to FMA-SAFE score only in unimanual recovery., Conclusion: Although recovery of bimanual activity depends on the extent of corticospinal tract injury and initial sensory and cognitive impairments, FMA-SAFE score captures most of the variance explained by these mechanisms. FMA-SAFE score, a straightforward clinical measure, strongly predicts bimanual recovery., Clinicaltrialsgov Identifier: NCT02878304., Classification of Evidence: This study provides Class I evidence that the FMA-SAFE score predicts bimanual recovery after stroke., (Copyright © 2021 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.)- Published
- 2021
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20. Recovery of Apraxia of Speech and Aphasia in Patients With Hand Motor Impairment After Stroke.
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Hybbinette H, Schalling E, Plantin J, Nygren-Deboussard C, Schütz M, Östberg P, and Lindberg PG
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Objective: Aphasia and apraxia of speech (AOS) after stroke frequently co-occur with a hand motor impairment but few studies have investigated stroke recovery across motor and speech-language domains. In this study, we set out to test the shared recovery hypothesis. We aimed to (1) describe the prevalence of AOS and aphasia in subacute stroke patients with a hand motor impairment and (2) to compare recovery across speech-language and hand motor domains. In addition, we also explored factors predicting recovery from AOS. Methods: Seventy participants with mild to severe paresis in the upper extremity were assessed; 50% of these ( n = 35) had left hemisphere (LH) lesions. Aphasia, AOS and hand motor assessments and magnetic resonance imaging were conducted at 4 weeks (A1) and at 6 months (A2) after stroke onset. Recovery was characterized in 15 participants showing initial aphasia that also had complete follow-up data at 6 months. Results: All participants with AOS and/or aphasia had LH lesions. In LH lesioned, the prevalence of aphasia was 71% and of AOS 57%. All participants with AOS had aphasia; 80% of the participants with aphasia also had AOS. Recovery in aphasia ( n = 15) and AOS ( n = 12) followed a parallel pattern to that observed in hand motor impairment and recovery correlated positively across speech-language and motor domains. The majority of participants with severe initial aphasia and AOS showed a limited but similar amount of recovery across domains. Lesion volume did not correlate with results from behavioral assessments, nor with recovery. The initial aphasia score was the strongest predictor of AOS recovery. Conclusion: Our findings confirm the common occurrence of AOS and aphasia in left hemisphere stroke patients with a hand motor impairment. Recovery was similar across speech-language and motor domains, even in patients with severe impairment, supporting the shared recovery hypothesis and that similar brain recovery mechanisms are involved in speech-language and motor recovery post stroke. These observations contribute to the knowledge of AOS and its relation to motor and language functions and add information that may serve as a basis for future studies of post stroke recovery. Studies including neuroimaging and/or biological assays are required to gain further knowledge on shared brain recovery mechanisms., Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest., (Copyright © 2021 Hybbinette, Schalling, Plantin, Nygren-Deboussard, Schütz, Östberg and Lindberg.)
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- 2021
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21. Neural noise and cortical inhibition in schizophrenia.
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Carment L, Dupin L, Guedj L, Térémetz M, Cuenca M, Krebs MO, Amado I, Maier MA, and Lindberg PG
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- Adult, Evoked Potentials, Motor physiology, Female, Humans, Male, Middle Aged, Motor Cortex physiology, Photic Stimulation methods, Transcranial Magnetic Stimulation methods, Young Adult, Electromyography methods, Hand Strength physiology, Neural Inhibition physiology, Psychomotor Performance physiology, Schizophrenia physiopathology, Schizophrenic Psychology
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Background: Neural information processing is subject to noise and this leads to variability in neural firing and behavior. Schizophrenia has been associated with both more variable motor control and impaired cortical inhibition, which is crucial for excitatory/inhibitory balance in neural commands., Hypothesis: In this study, we hypothesized that impaired intracortical inhibition in motor cortex would contribute to task-related motor noise in schizophrenia., Methods: We measured variability of force and of electromyographic (EMG) activity in upper limb and hand muscles during a visuomotor grip force-tracking paradigm in patients with schizophrenia (N = 25), in unaffected siblings (N = 17) and in healthy control participants (N = 25). Task-dependent primary motor cortex (M1) excitability and inhibition were assessed using transcranial magnetic stimulation (TMS)., Results: During force maintenance patients with schizophrenia showed increased variability in force and EMG, despite similar mean force and EMG magnitudes. Compared to healthy controls, patients with schizophrenia also showed increased M1 excitability and reduced cortical inhibition during grip-force tracking. EMG variability and force variability correlated negatively to cortical inhibition in patients with schizophrenia. EMG variability also correlated positively to negative symptoms. Siblings had similar variability and cortical inhibition compared to controls. Increased EMG and force variability indicate enhanced motor noise in schizophrenia, which relates to reduced motor cortex inhibition., Conclusion: The findings suggest that excessive motor noise in schizophrenia may arise from an imbalance of M1 excitation/inhibition of GABAergic origin. Thus, higher motor noise may provide a useful marker of impaired cortical inhibition in schizophrenia., Competing Interests: Declaration of competing interest The authors declare that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome., (Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.)
- Published
- 2020
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22. Common vs. Distinct Visuomotor Control Deficits in Autism Spectrum Disorder and Schizophrenia.
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Carment L, Khoury E, Dupin L, Guedj L, Bendjemaa N, Cuenca M, Maier MA, Krebs MO, Lindberg PG, and Amado I
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- Adult, Female, Humans, Male, Phenotype, Autism Spectrum Disorder complications, Autism Spectrum Disorder physiopathology, Psychomotor Disorders complications, Psychomotor Disorders physiopathology, Schizophrenia complications, Schizophrenia physiopathology
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Autism spectrum disorder (ASD) and schizophrenia (SCZ) are neurodevelopmental disorders with partly overlapping clinical phenotypes including sensorimotor impairments. However, direct comparative studies on sensorimotor control across these two disorders are lacking. We set out to compare visuomotor upper limb impairment, quantitatively, in ASD and SCZ. Patients with ASD (N = 24) were compared to previously published data from healthy control participants (N = 24) and patients with SCZ (N = 24). All participants performed a visuomotor grip force-tracking task in single and dual-task conditions. The dual-task (high cognitive load) presented either visual distractors or required mental addition during grip force-tracking. Motor inhibition was measured by duration of force release and from principal component analysis (PCA) of the participant's force-trajectory. Common impairments in patients with ASD and SCZ included increased force-tracking error in single-task condition compared to controls, a further increase in error in dual-task conditions, and prolonged duration of force release. These three sensorimotor impairments were found in both patient groups. In contrast, distinct impairments in patients with ASD included greater error under high cognitive load and delayed onset of force release compared to SCZ. The PCA inhibition component was higher in ASD than SCZ and controls, correlated to duration of force release, and explained group differences in tracking error. In conclusion, sensorimotor impairments related to motor inhibition are common to ASD and SCZ, but more severe in ASD, consistent with enhanced neurodevelopmental load in ASD. Furthermore, impaired motor anticipation may represent a further specific impairment in ASD. Autism Res 2020, 13: 885-896. © 2020 International Society for Autism Research, Wiley Periodicals, Inc. LAY SUMMARY: Autism spectrum disorder (ASD) and schizophrenia (SCZ) are neurodevelopmental disorders with partly overlapping and partly distinct clinical symptoms. Sensorimotor impairments rank among these symptoms, but it is less clear whether they are shared or distinct. In this study, we showed using a grip force task that sensorimotor impairments related to motor inhibition are common to ASD and SCZ, but more severe in ASD. Impaired motor anticipation may represent a further specific impairment in ASD., (© 2020 International Society for Autism Research, Wiley Periodicals, Inc.)
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- 2020
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23. Recovery and Prediction of Dynamic Precision Grip Force Control After Stroke.
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Pennati GV, Plantin J, Carment L, Roca P, Baron JC, Pavlova E, Borg J, and Lindberg PG
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- Adult, Female, Humans, Male, Middle Aged, Thumb physiopathology, Time Factors, Hand Strength, Stroke physiopathology
- Abstract
Background and Purpose- Dexterous object manipulation, requiring generation and control of finger forces, is often impaired after stroke. This study aimed to describe recovery of precision grip force control after stroke and to determine clinical and imaging predictors of 6-month performance. Methods- Eighty first-ever stroke patients with varying degrees of upper limb weakness were evaluated at 3 weeks, 3 months, and 6 months after stroke. Twenty-three healthy individuals of comparable age were also studied. The Strength-Dexterity test was used to quantify index finger and thumb forces during compression of springs of varying length in a precision grip. The coordination between finger forces (CorrForce), along with Dexterity-score and Repeatability-score, was calculated. Anatomical magnetic resonance imaging was used to calculate weighted corticospinal tract lesion load (wCST-LL). Results- CorrForce, Dexterity-score, and Repeatability-score in the affected hand were dramatically lower at each time point compared with the less-affected hand and the control group, even in patients with mild motor impairment according to Fugl-Meyer assessment. Improved performance over time occurred in CorrForce and Dexterity-score but not in Repeatability-score. The Fugl-Meyer assessment hand subscale, sensory function, and wCST-LL best predicted CorrForce and Dexterity-score status at 6 months (R
2 =0.56 and 0.87, respectively). wCST-LL explained substantial variance in CorrForce (R2 =0.34) and Dexterity-score (R2 =0.50) at 6 months; two-point discrimination and Fugl-Meyer score accounted for considerable additional variance. Absence of recovery in CorrForce was predicted by wCST-LL >4 cc and in Dexterity-score by wCST-LL >6 cc. Conclusions- Findings highlight persisting deficits in the ability to grasp and control finger forces after stroke. wCST-LL was the strongest predictor of performance at 6 months, but early two-point discrimination and Fugl-Meyer score had substantial additional predictive value. Registration- URL: https://www.clinicaltrials.gov. Unique identifier: NCT02878304.- Published
- 2020
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24. Predictive Modulation of Corticospinal Excitability and Implicit Encoding of Movement Probability in Schizophrenia.
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Dupin L, Carment L, Guedj L, Cuenca M, Krebs MO, Maier MA, Amado I, and Lindberg PG
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- Adult, Case-Control Studies, Electromyography, Electrophysiological Phenomena, Female, Humans, Male, Middle Aged, Probability, Reaction Time, Young Adult, Cortical Excitability, Motor Cortex physiopathology, Movement, Psychomotor Performance, Pyramidal Tracts physiopathology, Schizophrenia physiopathology, Siblings, Transcranial Magnetic Stimulation
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The ability to infer from uncertain information is impaired in schizophrenia and is associated with hallucinations and false beliefs. The accumulation of information is a key process for generating a predictive internal model, which statistically estimates an outcome from a specific situation. This study examines if updating the predictive model by the accumulation of information in absence of feedback is impaired in schizophrenia. We explored the implicit adaptation to the probability of being instructed to perform a movement (33%-Go, 50%-Go, or 66%-Go) in a Go/NoGo task in terms of reaction times (RTs), electromyographic activity, and corticospinal excitability (CSE) of primary motor cortex (M1). CSE was assessed at two time points to evaluate prediction of the upcoming instruction based on previously accumulated information: at rest (preceding the warning signal) and at the Go/NoGo signal onset. Three groups were compared: patients with schizophrenia (n = 20), unaffected siblings (n = 16), and healthy controls (n = 20). Controls and siblings showed earlier movement onset and increased CSE with higher Go probability. CSE adaptation seemed long-lasting, because the two CSE measures, at least 1500 ms apart, strongly correlated. Patients with schizophrenia failed to show movement onset (RT) adaptation and modulation of CSE. In contrast, all groups decreased movement duration with increasing Go probability. Modulation of CSE in the anticipatory phase of the potential movement reflected the estimation of upcoming response probability in unaffected controls and siblings. Impaired modulation of CSE supports the hypothesis that implicit adaptation to probabilistic context is altered in schizophrenia., (© The Author(s) 2018. Published by Oxford University Press on behalf of the Maryland Psychiatric Research Center. All rights reserved. For permissions, please email: journals.permissions@oup.com.)
- Published
- 2019
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25. Quantitative Assessment of Hand Spasticity After Stroke: Imaging Correlates and Impact on Motor Recovery.
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Plantin J, Pennati GV, Roca P, Baron JC, Laurencikas E, Weber K, Godbolt AK, Borg J, and Lindberg PG
- Abstract
Objective: This longitudinal observational study investigated how neural stretch-resistance in wrist and finger flexors develops after stroke and relates to motor recovery, secondary complications, and lesion location. Methods: Sixty-one patients were assessed at 3 weeks (T1), three (T2), and 6 months (T3) after stroke using the NeuroFlexor method and clinical tests. Magnetic Resonance Imaging was used to calculate weighted corticospinal tract lesion load (wCST-LL) and to perform voxel-based lesion symptom mapping. Results: NeuroFlexor assessment demonstrated spasticity (neural component [NC] >3.4N normative cut-off) in 33% of patients at T1 and in 51% at T3. Four subgroups were identified: early Severe spasticity ( n = 10), early Moderate spasticity ( n = 10), Late developing spasticity ( n = 17) and No spasticity ( n = 24). All except the Severe spasticity group improved significantly in Fugl-Meyer Assessment (FMA-HAND) to T3. The Severe and Late spasticity groups did not improve in Box and Blocks Test. The Severe spasticity group showed a 25° reduction in passive range of movement and more frequent arm pain at T3. wCST-LL correlated positively with NC at T1 and T3, even after controlling for FMA-HAND and lesion volume. Voxel-based lesion symptom mapping showed that lesioned white matter below cortical hand knob correlated positively with NC. Conclusion: Severe hand spasticity early after stroke is negatively associated with hand motor recovery and positively associated with the development of secondary complications. Corticospinal tract damage predicts development of spasticity. Early quantitative hand spasticity measurement may have potential to predict motor recovery and could guide targeted rehabilitation interventions after stroke.
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- 2019
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26. Editorial: Promoting Manual Dexterity Recovery After Stroke.
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Lotze M and Lindberg PG
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- 2019
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27. Impaired attentional modulation of sensorimotor control and cortical excitability in schizophrenia.
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Carment L, Dupin L, Guedj L, Térémetz M, Krebs MO, Cuenca M, Maier MA, Amado I, and Lindberg PG
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- Adult, Case-Control Studies, Female, Humans, Male, Saccades physiology, Transcranial Magnetic Stimulation, Young Adult, Attention physiology, Cortical Excitability physiology, Neural Inhibition physiology, Psychomotor Performance physiology, Schizophrenia physiopathology
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Impairments in attentional, working memory and sensorimotor processing have been consistently reported in schizophrenia. However, the interaction between cognitive and sensorimotor impairments and the underlying neural mechanisms remains largely uncharted. We hypothesized that altered attentional processing in patients with schizophrenia, probed through saccadic inhibition, would partly explain impaired sensorimotor control and would be reflected as altered task-dependent modulation of cortical excitability and inhibition. Twenty-five stabilized patients with schizophrenia, 17 unaffected siblings and 25 healthy control subjects were recruited. Subjects performed visuomotor grip force-tracking alone (single-task condition) and with increased cognitive load (dual-task condition). In the dual-task condition, two types of trials were randomly presented: trials with visual distractors (requiring inhibition of saccades) or trials with addition of numbers (requiring saccades and addition). Both dual-task trial types required divided visual attention to the force-tracking target and to the distractor or number. Gaze was measured during force-tracking tasks, and task-dependent modulation of cortical excitability and inhibition were assessed using transcranial magnetic stimulation. In the single-task, patients with schizophrenia showed increased force-tracking error. In dual-task distraction trials, force-tracking error increased further in patients, but not in the other two groups. Patients inhibited fewer saccades to distractors, and the capacity to inhibit saccades explained group differences in force-tracking performance. Cortical excitability at rest was not different between groups and increased for all groups during single-task force-tracking, although, to a greater extent in patients (80%) compared to controls (40%). Compared to single-task force-tracking, the dual-task increased cortical excitability in control subjects, whereas patients showed decreased excitability. Again, the group differences in cortical excitability were no longer significant when failure to inhibit saccades was included as a covariate. Cortical inhibition was reduced in patients in all conditions, and only healthy controls increased inhibition in the dual-task. Siblings had similar force-tracking and gaze performance as controls but showed altered task-related modulation of cortical excitability and inhibition in dual-task conditions. In patients, neuropsychological scores of attention correlated with visuomotor performance and with task-dependant modulation of cortical excitability. Disorganization symptoms were greatest in patients with weakest task-dependent modulation of cortical excitability. This study provides insights into neurobiological mechanisms of impaired sensorimotor control in schizophrenia showing that deficient divided visual attention contributes to impaired visuomotor performance and is reflected in impaired modulation of cortical excitability and inhibition. In siblings, altered modulation of cortical excitability and inhibition is consistent with a genetic risk for cortical abnormality., (© The Author(s) (2019). Published by Oxford University Press on behalf of the Guarantors of Brain.)
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- 2019
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28. Individual recovery profiles of manual dexterity, and relation to corticospinal lesion load and excitability after stroke -a longitudinal pilot study.
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Birchenall J, Térémetz M, Roca P, Lamy JC, Oppenheim C, Maier MA, Mas JL, Lamy C, Baron JC, and Lindberg PG
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- Aged, Evoked Potentials, Motor, Female, Fingers, Humans, Longitudinal Studies, Male, Middle Aged, Pilot Projects, Prospective Studies, Pyramidal Tracts injuries, Transcranial Magnetic Stimulation, Treatment Outcome, Motor Skills, Pyramidal Tracts pathology, Pyramidal Tracts physiopathology, Recovery of Function, Stroke pathology, Stroke physiopathology, Stroke Rehabilitation
- Abstract
Objectives: In this longitudinal pilot study, we investigated how manual dexterity recovery was related to corticospinal tract (CST) injury and excitability, in six patients undergoing conventional rehabilitation., Methods: Key components of manual dexterity, namely finger force control, finger tapping rate and independence of finger movements, were quantified. Structural MRI was obtained to calculate CST lesion load. CST excitability was assessed by measuring rest motor threshold (RMT) and the amplitude of motor evoked potentials (MEPs) using transcranial magnetic stimulation (TMS). Measurements were obtained at two weeks, three and six months post-stroke., Results: At six months post-stroke, complete recovery of hand gross motor impairment (i.e., maximal Fugl-Meyer score for hand) had occurred in three patients and four patients had recovered ability to accurately control finger force. However, tapping rate and independence of finger movements remained impaired in all six patients at six months. Recovery in hand gross motor impairment and finger force control occurred in patients with smaller CST lesion load and almost complete recovery of CST excitability, although RMT or MEP size remained slightly altered in the stroke-affected hemisphere compared to the unaffected hemisphere. The two patients with poorest recovery showed persistent absence of MEPs and greatest structural injury to CST., Discussion: The findings support good motor recovery being overall correlated with smaller CST lesion, and with almost complete recovery of CST excitability. However, impairment of manual dexterity persisted despite recovery in gross hand movements and grasping abilities, suggesting involvement of additional brain structures for fine manual tasks., (Copyright © 2018 Elsevier Masson SAS. All rights reserved.)
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- 2019
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29. Manual Dexterity and Aging: A Pilot Study Disentangling Sensorimotor From Cognitive Decline.
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Carment L, Abdellatif A, Lafuente-Lafuente C, Pariel S, Maier MA, Belmin J, and Lindberg PG
- Abstract
Manual dexterity measures can be useful for early detection of age-related functional decline and for prediction of cognitive decline. However, what aspects of sensorimotor function to assess remains unclear. Manual dexterity markers should be able to separate impairments related to cognitive decline from those related to healthy aging. In this pilot study, we aimed to compare manual dexterity components in patients diagnosed with cognitive decline (mean age: 84 years, N = 11) and in age comparable cognitively intact elderly subjects (mean age: 78 years, N = 11). In order to separate impairments due to healthy aging from deficits due to cognitive decline we also included two groups of healthy young adults (mean age: 26 years, N = 10) and middle-aged adults (mean age: 41 years, N = 8). A comprehensive quantitative evaluation of manual dexterity was performed using three tasks: (i) visuomotor force tracking, (ii) isochronous single finger tapping with auditory cues, and (iii) visuomotor multi-finger tapping. Results showed a highly significant increase in force tracking error with increasing age. Subjects with cognitive decline had increased finger tapping variability and reduced ability to select the correct tapping fingers in the multi-finger tapping task compared to cognitively intact elderly subjects. Cognitively intact elderly subjects and those with cognitive decline had prolonged force release and reduced independence of finger movements compared to young adults and middle-aged adults. The findings suggest two different patterns of impaired manual dexterity: one related to cognitive decline and another related to healthy aging. Manual dexterity tasks requiring updating of performance, in accordance with (temporal or spatial) task rules maintained in short-term memory, are particularly affected in cognitive decline. Conversely, tasks requiring online matching of motor output to sensory cues were affected by age, not by cognitive status. Remarkably, no motor impairments were detected in patients with cognitive decline using clinical scales of hand function. The findings may have consequences for the development of manual dexterity markers of cognitive decline.
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- 2018
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30. Manual Dexterity in Schizophrenia-A Neglected Clinical Marker?
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Térémetz M, Carment L, Brénugat-Herne L, Croca M, Bleton JP, Krebs MO, Maier MA, Amado I, and Lindberg PG
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Impaired manual dexterity is commonly observed in schizophrenia. However, a quantitative description of key sensorimotor components contributing to impaired dexterity is lacking. Whether the key components of dexterity are differentially affected and how they relate to clinical characteristics also remains unclear. We quantified the degree of dexterity in 35 stabilized patients with schizophrenia and in 20 age-matched control subjects using four visuomotor tasks: (i) force tracking to quantify visuomotor precision, (ii) sequential finger tapping to measure motor sequence recall, (iii) single-finger tapping to assess temporal regularity, and (iv) multi-finger tapping to measure independence of finger movements. Diverse clinical and neuropsychological tests were also applied. A patient subgroup ( N = 15) participated in a 14-week cognitive remediation protocol and was assessed before and after remediation. Compared to control subjects, patients with schizophrenia showed greater error in force tracking, poorer recall of tapping sequences, decreased tapping regularity, and reduced degree of finger individuation. A composite performance measure discriminated patients from controls with sensitivity = 0.79 and specificity = 0.9. Aside from force-tracking error, no other dexterity components correlated with antipsychotic medication. In patients, some dexterity components correlated with neurological soft signs, Positive and Negative Syndrome Scale (PANSS), or neuropsychological scores. This suggests differential cognitive contributions to these components. Cognitive remediation lead to significant improvement in PANSS, tracking error, and sequence recall (without change in medication). These findings show that multiple aspects of sensorimotor control contribute to impaired manual dexterity in schizophrenia. Only visuomotor precision was related to antipsychotic medication. Good diagnostic accuracy and responsiveness to treatment suggest that manual dexterity may represent a useful clinical marker in schizophrenia.
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- 2017
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31. Does dystonic muscle activity affect sense of effort in cervical dystonia?
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Carment L, Maier MA, Sangla S, Guiraud V, Mesure S, Vidailhet M, Lindberg PG, and Bleton JP
- Subjects
- Adult, Aged, Analysis of Variance, Electromyography methods, Feedback, Sensory physiology, Female, Humans, Male, Middle Aged, Muscle, Skeletal physiopathology, Vibration, Dystonia physiopathology, Muscle Contraction, Neck Muscles physiopathology, Torticollis physiopathology
- Abstract
Background: Focal dystonia has been associated with deficient processing of sense of effort cues. However, corresponding studies are lacking in cervical dystonia (CD). We hypothesized that dystonic muscle activity would perturb neck force control based on sense of effort cues., Methods: Neck extension force control was investigated in 18 CD patients with different clinical features (7 with and 11 without retrocollis) and in 19 control subjects. Subjects performed force-matching and force-maintaining tasks at 5% and 20% of maximum voluntary contraction (MVC). Three task conditions were tested: i) with visual force feedback, ii) without visual feedback (requiring use of sense of effort), iii) without visual feedback, but with neck extensor muscle vibration (modifying muscle afferent cues). Trapezius muscle activity was recorded using electromyography (EMG)., Results: CD patients did not differ in task performance from healthy subjects when using visual feedback (ANOVA, p>0.7). In contrast, when relying on sense of effort cues (without visual feedback, 5% MVC), force control was impaired in patients without retrocollis (p = 0.006), but not in patients with retrocollis (p>0.2). Compared to controls, muscle vibration without visual feedback significantly affected performance in patients with retrocollis (p<0.001), but not in patients without retrocollis. Extensor EMG during rest, included as covariate in ANOVA, explained these group differences., Conclusion: This study shows that muscle afferent feedback biases sense of effort cues when controlling neck forces in patients with CD. The bias acts on peripheral or central sense of effort cues depending on whether the task involves dystonic muscles. This may explain why patients with retrocollis more accurately matched isometric neck extension forces. This highlights the need to consider clinical features (pattern of dystonic muscles) when evaluating sensorimotor integration in CD., Competing Interests: LC reports grants from Université Pierre et Marie Curie, Paris VI, outside the submitted work. SS reports personal fees from Allergan, personal fees from Ipsen, personal fees from Merz-Pharma, outside the submitted work. VG has nothing to disclose. SM reports grants from Fondation Paul Bennetot, outside the submitted work. MV reports grants from INSERM, grants from APHP, grants from APTES, grants from France Parkinson, grants from AMADYS, personal fees from Movement Disorders Society, outside the submitted work; and Member of the advisory board for Merz and Medtronic. PGL reports grants from Gloria and Jacques Gosweiler Foundation, outside the submitted work and owns shares in Aggero MedTech AB, a company commercializing a measurement instrument for spasticity. In addition, PGL and MAM have patented a method for measurement of manual dexterity (EP2659835A1). JPB reports personal fees from MERZ-PHARMA, personal fees from IPSEN, grants from AMADYS, grants from AFREK, outside the submitted work. This does not alter the authors’ adherence to PLOS ONE policies on sharing data and materials.
- Published
- 2017
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32. Altered cortical processing of motor inhibition in schizophrenia.
- Author
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Lindberg PG, Térémetz M, Charron S, Kebir O, Saby A, Bendjemaa N, Lion S, Crépon B, Gaillard R, Oppenheim C, Krebs MO, and Amado I
- Subjects
- Adult, Antipsychotic Agents therapeutic use, Brain Mapping, Electromyography methods, Evoked Potentials, Motor drug effects, Evoked Potentials, Motor physiology, Female, Humans, Male, Motor Cortex drug effects, Neural Inhibition drug effects, Neural Inhibition physiology, Schizophrenia drug therapy, Transcranial Magnetic Stimulation methods, gamma-Aminobutyric Acid therapeutic use, Motor Cortex physiopathology, Schizophrenia physiopathology
- Abstract
Inhibition is considered a key mechanism in schizophrenia. Short-latency intracortical inhibition (SICI) in the motor cortex is reduced in schizophrenia and is considered to reflect locally deficient γ-aminobutyric acid (GABA)-ergic modulation. However, it remains unclear how SICI is modulated during motor inhibition and how it relates to neural processing in other cortical areas. Here we studied motor inhibition Stop signal task (SST) in stabilized patients with schizophrenia (N = 28), healthy siblings (N = 21) and healthy controls (n = 31) matched in general cognitive status and educational level. Transcranial magnetic stimulation (TMS) and functional magnetic resonance imaging (fMRI) were used to investigate neural correlates of motor inhibition. SST performance was similar in patients and controls. SICI was modulated by the task as expected in healthy controls and siblings but was reduced in patients with schizophrenia during inhibition despite equivalent motor inhibition performance. fMRI showed greater prefrontal and premotor activation during motor inhibition in schizophrenia. Task-related modulation of SICI was higher in subjects who showed less inhibition-related activity in pre-supplementary motor area (SMA) and cingulate motor area. An exploratory genetic analysis of selected markers of inhibition (GABRB2, GAD1, GRM1, and GRM3) did not explain task-related differences in SICI or cortical activation. In conclusion, this multimodal study provides direct evidence of a task-related deficiency in SICI modulation in schizophrenia likely reflecting deficient GABA-A related processing in motor cortex. Compensatory activation of premotor areas may explain similar motor inhibition in patients despite local deficits in intracortical processing. Task-related modulation of SICI may serve as a useful non-invasive GABAergic marker in development of therapeutic strategies in schizophrenia., (Copyright © 2016 Elsevier Ltd. All rights reserved.)
- Published
- 2016
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33. Upper Limb Outcome Measures Used in Stroke Rehabilitation Studies: A Systematic Literature Review.
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Santisteban L, Térémetz M, Bleton JP, Baron JC, Maier MA, and Lindberg PG
- Subjects
- Humans, Arm physiopathology, Stroke Rehabilitation
- Abstract
Background: Establishing which upper limb outcome measures are most commonly used in stroke studies may help in improving consensus among scientists and clinicians., Objective: In this study we aimed to identify the most commonly used upper limb outcome measures in intervention studies after stroke and to describe domains covered according to ICF, how measures are combined, and how their use varies geographically and over time., Methods: Pubmed, CinHAL, and PeDRO databases were searched for upper limb intervention studies in stroke according to PRISMA guidelines and477 studies were included., Results: In studies 48different outcome measures were found. Only 15 of these outcome measures were used in more than 5% of the studies. The Fugl-Meyer Test (FMT)was the most commonly used measure (in 36% of studies). Commonly used measures covered ICF domains of body function and activity to varying extents. Most studies (72%) combined multiple outcome measures: the FMT was often combined with the Motor Activity Log (MAL), the Wolf Motor Function Test and the Action Research Arm Test, but infrequently combined with the Motor Assessment Scale or the Nine Hole Peg Test. Key components of manual dexterity such as selective finger movements were rarely measured. Frequency of use increased over a twelve-year period for the FMT and for assessments of kinematics, whereas other measures, such as the MAL and the Jebsen Taylor Hand Test showed decreased use over time. Use varied largely between countries showing low international consensus., Conclusions: The results showed a large diversity of outcome measures used across studies. However, a growing number of studies used the FMT, a neurological test with good psychometric properties. For thorough assessment the FMT needs to be combined with functional measures. These findings illustrate the need for strategies to build international consensus on appropriate outcome measures for upper limb function after stroke.
- Published
- 2016
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34. Normative NeuroFlexor data for detection of spasticity after stroke: a cross-sectional study.
- Author
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Pennati GV, Plantin J, Borg J, and Lindberg PG
- Subjects
- Adult, Aged, Cross-Sectional Studies, Female, Humans, Male, Middle Aged, Movement physiology, Muscle Spasticity etiology, Accelerometry instrumentation, Muscle Spasticity diagnosis, Stroke complications
- Abstract
Background and Objective: The NeuroFlexor is a novel instrument for quantification of neural, viscous and elastic components of passive movement resistance. The aim of this study was to provide normative data and cut-off values from healthy subjects and to use these to explore signs of spasticity at the wrist and fingers in patients recovering from stroke., Methods: 107 healthy subjects (age range 28-68 years; 51 % females) and 39 stroke patients (age range 33-69 years; 33 % females), 2-4 weeks after stroke, were assessed with the NeuroFlexor. Cut-off values based on mean + 3SD of the reference data were calculated. In patients, the modified Ashworth scale (MAS) was also applied., Results: In healthy subjects, neural component was 0.8 ± 0.9 N (mean ± SD), elastic component was 2.7 ± 1.1 N, viscous component was 0.3 ± 0.3 N and resting tension was 5.9 ± 1 N. Age only correlated with elastic component (r = -0.3, p = 0.01). Elasticity and resting tension were higher in males compared to females (p = 0.001) and both correlated positively with height (p = 0.01). Values above healthy population cut-off were observed in 16 patients (41 %) for neural component, in 2 (5 %) for elastic component and in 23 (59 %) for viscous component. Neural component above cut-off did not correspond well to MAS ratings. Ten patients with MAS = 0 had neural component values above cut-off and five patients with MAS ≥ 1 had neural component within normal range., Conclusion: This study provides NeuroFlexor cut-off values that are useful for detection of spasticity in the early phase after stroke.
- Published
- 2016
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35. Correlation of force control with regional spinal DTI in patients with cervical spondylosis without signs of spinal cord injury on conventional MRI.
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Lindberg PG, Sanchez K, Ozcan F, Rannou F, Poiraudeau S, Feydy A, and Maier MA
- Subjects
- Cross-Sectional Studies, Female, Humans, Male, Middle Aged, Diffusion Tensor Imaging methods, Magnetic Resonance Imaging methods, Spinal Cord pathology, Spondylosis pathology
- Abstract
Objectives: The aim of this study was to investigate spinal cord structure in patients with cervical spondylosis where conventional MRI fails to reveal spinal cord damage., Methods: We performed a cross-sectional study of patients with cervical spondylosis without conventional MRI findings of spinal cord damage and healthy controls. Subjects were studied using spinal diffusion tensor imaging (DTI), precision grip and foot force-tracking tasks, and a clinical examination including assessment of neurological signs. A regional analysis of lateral and medial spinal white matter across multiple cervical levels (C1-C5) was performed., Results: DTI revealed reduced fractional anisotropy (FA) and increased radial diffusivity (RD) in the lateral spinal cord at the level of greatest compression (lowest Pavlov ratio) in patients (p < 0.05). Patients with spondylosis had greater error and longer release duration in both grip and foot force-tracking. Similar spinal cord deficits were present in patients without neurological signs. Increased error in grip and foot tracking (low accuracy) correlated with increased RD in the lateral spinal cord at the level of greatest compression (p ≤ 0.01)., Conclusions: Spinal DTI can detect subtle spinal cord damage of functional relevance in cervical spondylosis, even in patients without signs on conventional T2-imaging and without neurological signs., Key Points: DTI reveals spinal cord changes in cervical spondylosis with few symptoms. DTI changes were present despite normal spinal cord on conventional MRI. DTI parameters correlated with force control accuracy in hand and foot. Spinal DTI is a promising technique for patients with cervical spondylosis.
- Published
- 2016
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36. A novel method for the quantification of key components of manual dexterity after stroke.
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Térémetz M, Colle F, Hamdoun S, Maier MA, and Lindberg PG
- Subjects
- Adult, Aged, Arm physiopathology, Female, Fingers physiopathology, Hand physiopathology, Hand Strength, Humans, Male, Middle Aged, Paresis physiopathology, Paresis rehabilitation, Psychomotor Performance, Motor Skills, Stroke physiopathology
- Abstract
Background: A high degree of manual dexterity is a central feature of the human upper limb. A rich interplay of sensory and motor components in the hand and fingers allows for independent control of fingers in terms of timing, kinematics and force. Stroke often leads to impaired hand function and decreased manual dexterity, limiting activities of daily living and impacting quality of life. Clinically, there is a lack of quantitative multi-dimensional measures of manual dexterity. We therefore developed the Finger Force Manipulandum (FFM), which allows quantification of key components of manual dexterity. The purpose of this study was (i) to test the feasibility of using the FFM to measure key components of manual dexterity in hemiparetic stroke patients, (ii) to compare differences in dexterity components between stroke patients and controls, and (iii) to describe individual profiles of dexterity components in stroke patients., Methods: 10 stroke patients with mild-to-moderate hemiparesis and 10 healthy subjects were recruited. Clinical measures of hand function included the Action Research Arm Test and the Moberg Pick-Up Test. Four FFM tasks were used: (1) Finger Force Tracking to measure force control, (2) Sequential Finger Tapping to measure the ability to perform motor sequences, (3) Single Finger Tapping to measure timing effects, and (4) Multi-Finger Tapping to measure the ability to selectively move fingers in specified combinations (independence of finger movements)., Results: Most stroke patients could perform the tracking task, as well as the single and multi-finger tapping tasks. However, only four patients performed the sequence task. Patients showed less accurate force control, reduced tapping rate, and reduced independence of finger movements compared to controls. Unwanted (erroneous) finger taps and overflow to non-tapping fingers were increased in patients. Dexterity components were not systematically related among each other, resulting in individually different profiles of deficient dexterity. Some of the FFM measures correlated with clinical scores., Conclusions: Quantifying some of the key components of manual dexterity with the FFM is feasible in moderately affected hemiparetic patients. The FFM can detect group differences and individual profiles of deficient dexterity. The FFM is a promising tool for the measurement of key components of manual dexterity after stroke and could allow improved targeting of motor rehabilitation.
- Published
- 2015
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37. Neural and nonneural contributions to wrist rigidity in Parkinson's disease: an explorative study using the NeuroFlexor.
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Zetterberg H, Frykberg GE, Gäverth J, and Lindberg PG
- Subjects
- Aged, Cross-Sectional Studies, Female, Humans, Male, Middle Aged, Muscle Rigidity pathology, Parkinson Disease pathology, Wrist pathology, Muscle Rigidity physiopathology, Parkinson Disease physiopathology, Wrist physiopathology
- Abstract
Objective: The NeuroFlexor is a novel method incorporating a biomechanical model for the measurement of neural and nonneural contributions to resistance induced by passive stretch. In this study, we used the NeuroFlexor method to explore components of passive movement resistance in the wrist and finger muscles in subjects with Parkinson's disease (PD)., Methods: A cross-sectional comparison was performed in twenty-five subjects with PD with clinically identified rigidity and 14 controls. Neural (NC), elastic (EC), and viscous (VC) components of the resistance to passive extension of the wrist were calculated using the NeuroFlexor. Measurements were repeated during a contralateral activation maneuver., Results: PD subjects showed greater total resistance (P < 0.001) and NC (P = 0.002) compared to controls. EC and VC did not differ significantly between groups. Contralateral activation maneuver resulted in increased NC in the PD group but this increase was due to increased resting tension. Total resistance and NC correlated with clinical ratings of rigidity and with bradykinesia., Conclusions: The findings suggest that stretch induced reflex activity, but not nonneural resistance, is the major contributor to rigidity in wrist muscles in PD. The NeuroFlexor is a potentially valuable clinical and research tool for quantification of rigidity.
- Published
- 2015
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38. Deficient grip force control in schizophrenia: behavioral and modeling evidence for altered motor inhibition and motor noise.
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Teremetz M, Amado I, Bendjemaa N, Krebs MO, Lindberg PG, and Maier MA
- Subjects
- Adult, Feedback, Sensory, Humans, Male, Middle Aged, Psychomotor Performance, Schizophrenic Psychology, Young Adult, Hand Strength, Schizophrenia physiopathology
- Abstract
Whether upper limb sensorimotor control is affected in schizophrenia and how underlying pathological mechanisms may potentially intervene in these deficits is still being debated. We tested voluntary force control in schizophrenia patients and used a computational model in order to elucidate potential cerebral mechanisms underlying sensorimotor deficits in schizophrenia. A visuomotor grip force-tracking task was performed by 17 medicated and 6 non-medicated patients with schizophrenia (DSM-IV) and by 15 healthy controls. Target forces in the ramp-hold-and-release paradigm were set to 5 N and to 10% maximal voluntary grip force. Force trajectory was analyzed by performance measures and Principal Component Analysis (PCA). A computational model incorporating neural control signals was used to replicate the empirically observed motor behavior and to explore underlying neural mechanisms. Grip task performance was significantly lower in medicated and non-medicated schizophrenia patients compared to controls. Three behavioral variables were significantly higher in both patient groups: tracking error (by 50%), coefficient of variation of force (by 57%) and duration of force release (up by 37%). Behavioral performance did not differ between patient groups. Computational simulation successfully replicated these findings and predicted that decreased motor inhibition, together with an increased signal-dependent motor noise, are sufficient to explain the observed motor deficits in patients. PCA also suggested altered motor inhibition as a key factor differentiating patients from control subjects: the principal component representing inhibition correlated with clinical severity. These findings show that schizophrenia affects voluntary sensorimotor control of the hand independent of medication, and suggest that reduced motor inhibition and increased signal-dependent motor noise likely reflect key pathological mechanisms of the sensorimotor deficit.
- Published
- 2014
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39. Sensitivity of the NeuroFlexor method to measure change in spasticity after treatment with botulinum toxin A in wrist and finger muscles.
- Author
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Gäverth J, Eliasson AC, Kullander K, Borg J, Lindberg PG, and Forssberg H
- Subjects
- Adult, Aged, Botulinum Toxins, Type A administration & dosage, Female, Fingers, Humans, Male, Middle Aged, Muscle Spasticity rehabilitation, Neuromuscular Agents administration & dosage, Prospective Studies, Stroke drug therapy, Stroke Rehabilitation, Treatment Outcome, Wrist Joint, Young Adult, Botulinum Toxins, Type A therapeutic use, Muscle Spasticity drug therapy, Neuromuscular Agents therapeutic use, Range of Motion, Articular
- Abstract
Objective: The NeuroFlexor objectively quantifies the neural, elastic and viscous components of passive movement resistance in wrist and finger flexor muscles. In this study we investigated the sensitivity of the NeuroFlexor to changes in spasticity induced by treatment with botulinum toxin type A (BoNT-A)., Design: Prospective observational design., Subjects: A convenience sample of 22 adults with post-stroke upper limb spasticity scheduled for botulinum toxin treatment., Methods: BoNT-A was given according to individual treatment plans. NeuroFlexor assessments were made before treatment and 4 and 12 weeks after., Results: At group level, spasticity decreased significantly at 4 weeks (expected time of maximum effect) (p = 0.04). At 12 weeks, spasticity had rebounded and no longer differed significantly from baseline (p = 0.64), i.e. in line with the pharmacodynamics of BoNT-A. At the individual level, 7 participants showed a reduction in spasticity greater than the measurement error. The reduction was dose-dependent (r(20) = 0.66, p < 0.001), and largest in participants with the highest dose., Conclusion: At the group level, the sensitivity of NeuroFlexor is good enough to detect reduction in spasticity after treatment with BoNT-A. Further work is needed to establish the sensitivity of NeuroFlexor on an individual level.
- Published
- 2014
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40. Impaired force control in writer's cramp showing a bilateral deficit in sensorimotor integration.
- Author
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Bleton JP, Teremetz M, Vidailhet M, Mesure S, Maier MA, and Lindberg PG
- Subjects
- Adult, Aged, Aged, 80 and over, Female, Humans, Male, Middle Aged, Young Adult, Dystonic Disorders physiopathology, Hand Strength physiology, Psychomotor Performance physiology
- Abstract
Background: Abnormal cortical processing of sensory inputs has been found bilaterally in writer's cramp (WC). This study tested the hypothesis that patients with WC have an impaired ability to adjust grip forces according to visual and somatosensory cues in both hands., Methods: A unimanual visuomotor force-tracking task and a bimanual sense of effort force-matching task were performed by WC patients and healthy controls., Results: In visuomotor tracking, WC patients showed increased error, greater variability, and longer release duration than controls. In the force-matching task, patients underestimated, whereas controls overestimated, the force applied in the other hand. Visuomotor tracking and force matching were equally impaired in both the symptomatic and nonsymptomatic hand in WC patients., Conclusions: This study provides evidence of bilaterally impaired grip-force control in WC, when using visual or sense of effort cues. This suggests a generalized subclinical deficit in sensorimotor integration in WC., (Copyright © 2013 Movement Disorder Society.)
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- 2014
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41. Diffusion tensor imaging of the median nerve in recurrent carpal tunnel syndrome - initial experience.
- Author
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Lindberg PG, Feydy A, Le Viet D, Maier MA, and Drapé JL
- Subjects
- Adult, Aged, Aged, 80 and over, Female, Follow-Up Studies, Humans, Male, Middle Aged, Recurrence, Reproducibility of Results, Carpal Tunnel Syndrome diagnosis, Diffusion Tensor Imaging methods, Median Nerve pathology
- Abstract
Objectives: To investigate median nerve structure in patients with recurrent carpal tunnel syndrome (CTS) using diffusion tensor imaging (DTI) and to relate DTI changes to anatomical MRI and to measures of median nerve function., Methods: Median nerve structure was quantified according to DTI in patients with recurrent CTS and in healthy controls of similar age. Anatomical MRI was used to identify the presence of nerve compression and fibrosis. Median nerve function was measured using electromyography, a force-tracking task (accuracy of precision grip control) and clinical measures., Results: Patients showed reduced apparent diffusion coefficient (ADC), reduced axial diffusivity (AD) and radial diffusivity (RD) along the median nerve compared with controls (P < 0.001). Patients with endoneural fibrosis had the greatest reductions in ADC and in RD. ADC and AD correlated positively with nerve conduction velocity (R = 0.54 and R = 0.68, respectively) and fractional anisotropy correlated negatively with error during force-tracking (R = -0.58)., Conclusions: A specific pattern of DTI changes in the median nerve was identified in patients with recurrent CTS. Fibrosis may be underlying these structural changes. The correlations with nerve conduction velocity and accuracy of force control suggest that DTI is a promising technique in the study of median nerve structure in recurrent CTS., Key Points: • Diffusion tensor imaging (DTI) offers further possibilities in musculoskeletal magnetic resonance imaging. • DTI reveals median nerve changes in recurrent carpal tunnel syndrome. • DTI changes were greater with signs of median nerve fibrosis. • DTI parameters correlated with nerve conduction and force control measures. • DTI is a promising technique in recurrent carpal tunnel syndrome.
- Published
- 2013
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42. Test-retest and inter-rater reliability of a method to measure wrist and finger spasticity.
- Author
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Gäverth J, Sandgren M, Lindberg PG, Forssberg H, and Eliasson AC
- Subjects
- Adult, Aged, Aged, 80 and over, Chronic Disease, Elasticity, Female, Hand Joints, Humans, Male, Middle Aged, Observer Variation, Range of Motion, Articular physiology, Reproducibility of Results, Young Adult, Fingers physiopathology, Muscle Spasticity rehabilitation, Stroke Rehabilitation, Wrist physiopathology
- Abstract
Objective: To describe the reliability of an instrument (Neuro- Flexor) designed to be used in the clinic for quantification of the relative contribution of spasticity, elasticity and viscosity to resistance during passive wrist movements., Design: A test-retest and inter-rater reliability study., Subjects: A convenience sample of 34 adults with chronic stroke with spasticity in the hand, and a reference group of 10 healthy persons., Methods: Two raters assessed the participants with the NeuroFlexor. Elastic, viscous and neural components of passive movement resistance were quantified at the wrist. Test-retest and inter-rater intraclass correlation coefficient (ICC2.1) were calculated for each component for both raters and two sessions. Degree of measurement error was evaluated using the coefficient of variation and the repeatability coefficient., Results: Reliability was high for the neural component (test-retest: 0.90-0.96; inter-rater: 0.90-0.94), fair to good for the elastic component (test-retest: 0.79-0.88; inter-rater: 0.76-0.76), and fair to high for the viscous component (test-retest: 0.88-0.90; inter-rater: 0.75-0.80). Based on test-retest data, the coefficients of variation for the neural, elastic and viscous components were 25%, 26% and 16%, respectively, and the repeatability coefficients were 1.798, 1.897 and 1.404, respectively., Conclusion: The NeuroFlexor instrument is a reliable measure of spasticity and of muscle elasticity and viscosity in individuals with wrist and finger muscle resistance to passive stretch after stroke.
- Published
- 2013
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43. Measures of spinal canal stenosis and relationship to spinal cord structure in patients with cervical spondylosis.
- Author
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Lindberg PG, Feydy A, Sanchez K, Rannou F, and Maier MA
- Subjects
- Aged, Case-Control Studies, Diffusion Tensor Imaging, Female, Humans, Image Interpretation, Computer-Assisted, Male, Middle Aged, Predictive Value of Tests, Severity of Illness Index, Magnetic Resonance Imaging methods, Spinal Stenosis pathology, Spondylosis pathology
- Abstract
Objectives: Spinal canal stenosis is often measured on anatomical magnetic resonance imaging (MRI) to estimate the degree of spinal cord compression. This study examined whether two quantitative measures of spinal canal stenosis taken from anatomical MRI are related to spinal cord white-matter integrity in patients with cervical spondylosis measured by diffusion tensor imaging (DTI)., Patients and Methods: DTI and T2-weighted MRI of the cervical spinal cord were performed in 15 patients with cervical spondylosis and ten healthy control subjects of similar age. Severity of stenosis was calculated using Pavlov's ratio and the space-available-for-cord (SAC) technique., Results: Patients had significantly lower Pavlov's ratios and SAC (C2-C3, C4-C5 and C6-C7), lower fractional anisotropy (FA; C2-C3 and C4-C5) and higher radial diffusivity (C2-C3, C4-C5 and C6-C7) than the controls. In patients, only Pavlov's ratio correlated with mean FA (R=0.66, P=0.008). Variations in Pavlov's ratio and FA also showed a similar pattern across cervical levels., Conclusion: Pavlov's ratio is a better predictor of spinal cord integrity than the SAC and, therefore, may be more relevant clinically for the evaluation of stenosis in patients with cervical spondylosis., (Copyright © 2011 Elsevier Masson SAS. All rights reserved.)
- Published
- 2012
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44. Affected and unaffected quantitative aspects of grip force control in hemiparetic patients after stroke.
- Author
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Lindberg PG, Roche N, Robertson J, Roby-Brami A, Bussel B, and Maier MA
- Subjects
- Adult, Aged, Arm physiopathology, Female, Hand physiopathology, Humans, Male, Middle Aged, Paresis etiology, Stroke complications, Hand Strength physiology, Paresis physiopathology, Stroke physiopathology
- Abstract
Adequate grip force modulation is critical to manual dexterity and often impaired in hemiparetic stroke patients. Previous studies in hemiparetic patients suggest that aspects of grip force control may be differently affected by the lesion. We developed a visuomotor power grip force-tracking task allowing quantification of tracking error, force variability and release duration. We investigated force control in 24 chronic stroke patients with varying severity of hemiparesis and in healthy control subjects. Force tracking was performed at 10, 20, and 30% maximal voluntary contraction (MVC). Control subjects were also tested at absolute force levels similar to those of the patients. Patients tracking with their paretic hand at similar relative (%MVC) grip force levels showed increased error, force variability and release duration, but surprisingly, there was no difference in tracking error or variability between patients and control subjects performing at similar absolute force levels. Furthermore, patients improved their tracking performance across repeated blocks similar to control subjects. Release duration, however, was increased (also in the non-paretic hand), was force-independent and did not correlate with MVC strength. Of the three performance measures, only release duration explained some of the variance in arm and hand function (Frenchay Arm Test score), independent of MVC strength. The findings show (i) that hemiparetic stroke patients preserve the ability to modulate (generate and maintain) power grip force within their limited force range and (ii) that MVC grip strength and duration of grip release are differently affected and are two complementary predictors of arm function after stroke., (Copyright © 2012 Elsevier B.V. All rights reserved.)
- Published
- 2012
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45. Validation of a new biomechanical model to measure muscle tone in spastic muscles.
- Author
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Lindberg PG, Gäverth J, Islam M, Fagergren A, Borg J, and Forssberg H
- Subjects
- Adult, Aged, Algorithms, Chronic Disease, Elasticity, Electromyography, Female, Humans, Male, Middle Aged, Muscle Contraction physiology, Muscle, Skeletal physiology, Nerve Block, Paresis etiology, Paresis physiopathology, Reflex, Stretch physiology, Reproducibility of Results, Stroke complications, Stroke physiopathology, Upper Extremity physiology, Viscosity, Biomechanical Phenomena, Models, Neurological, Muscle Spasticity physiopathology, Muscle Tonus physiology, Muscle, Skeletal physiopathology
- Abstract
Background: There is no easy and reliable method to measure spasticity, although it is a common and important symptom after a brain injury., Objective: The aim of this study was to develop and validate a new method to measure spasticity that can be easily used in clinical practice., Methods: A biomechanical model was created to estimate the components of the force resisting passive hand extension, namely (a) inertia (IC), (b) elasticity (EC), (c) viscosity (VC), and (d) neural components (NC). The model was validated in chronic stroke patients with varying degree of hand spasticity. Electromyography (EMG) was recorded to measure the muscle activity induced by the passive stretch., Results: The model was validated in 3 ways: (a) NC was reduced after an ischemic nerve block, (b) NC correlated with the integrated EMG across subjects and in the same subject during the ischemic nerve block, and (c) NC was velocity dependent. In addition, the total resisting force and NC correlated with the modified Ashworth score. According to the model, the neural and nonneural components varied between patients. In most of the patients, but not in all, the NC dominated., Conclusions: The results suggest that the model allows valid measurement of spasticity in the upper extremity of chronic stroke patients and that it can be used to separate the neural component induced by the stretch reflex from resistance caused by altered muscle properties.
- Published
- 2011
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46. Commentary on "spasticity or reversible muscle hypertonia?".
- Author
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Lindberg PG, Maier MA, and Borg J
- Subjects
- Humans, Motor Neuron Disease classification, Muscle Hypertonia classification, Muscle Spasticity classification
- Published
- 2011
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47. Wallerian degeneration in lateral cervical spinal cord detected with diffusion tensor imaging in four chronic stroke patients.
- Author
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Lindberg PG, Bensmail D, Bussel B, Maier MA, and Feydy A
- Subjects
- Aged, Anisotropy, Cervical Vertebrae, Diffusion Tensor Imaging, Female, Humans, Male, Middle Aged, Stroke complications, Wallerian Degeneration etiology, Pyramidal Tracts pathology, Spinal Cord pathology, Stroke pathology, Wallerian Degeneration pathology
- Abstract
Background and Purpose: wallerian degeneration (WD) in descending motor tracts after stroke is described at the level of the internal capsule and the brainstem. We investigated whether diffusion tensor imaging (DTI) can detect degeneration in the lateral cervical spinal cord after stroke., Methods: DTI at 1.5 T of the cervical spinal cord was performed in 4 chronic hemiparetic patients after ischemic stroke. Stroke lesions included the corticospinal tract. DTI was also performed in 12 healthy controls. Diffusion parameters were obtained for left and right (i) half and (ii) lateral spinal cord extending from C2 to C7., Results: relative fractional anisotropy (FA) in the lateral tracts on the affected side compared with the unaffected side (left/right) was reduced in stroke patients as compared with controls (P= .007). FA was lowest in patients with severe upper limb hemiparesis. Relative apparent diffusion coefficient in the lateral tracts was increased in the patients (P= .03)., Conclusions: this study provides preliminary evidence that DTI at 1.5 T can be used for identification and quantification of WD in the lateral cervical spinal cord in stroke patients. This may prove useful for prognosis of motor outcome after stroke.
- Published
- 2011
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48. White matter organization in cervical spinal cord relates differently to age and control of grip force in healthy subjects.
- Author
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Lindberg PG, Feydy A, and Maier MA
- Subjects
- Adolescent, Adult, Aged, Female, Humans, Magnetic Resonance Imaging methods, Male, Middle Aged, Young Adult, Aging physiology, Cervical Vertebrae physiology, Hand Strength physiology, Nerve Fibers, Myelinated physiology, Spinal Cord physiology
- Abstract
Diffusion tensor imaging (DTI) can be used to elucidate relations between CNS structure and function. We hypothesized that the degree of spinal white matter organization relates to the accuracy of control of grip force. Healthy subjects of different age were studied using DTI and visuomotor tracking of precision grip force. The latter is a prime component of manual dexterity. A regional analysis of spinal white matter [fractional anisotropy (FA)] across multiple cervical levels (C2-C3, C4-C5, and C6-C7) and in different regions of interest (left and right lateral or medial spinal cord) was performed. FA was highest at the C2-C3 level, higher on the right than the left side, and higher in the lateral than in the medial spinal cord (p < 0.001). FA of whole cervical spinal cord (C2-C7) was lower in subjects with high tracking error (r = -0.56, p = 0.004) and decreased with age (r = -0.63, p = 0.001). A multiple regression analysis revealed an independent contribution of each predictor (semipartial correlations: age, r = -0.55, p < 0.001; tracking error, r = -0.49, p = 0.003). The closest relation between FA and tracking error was found at the C6-C7 level in the lateral spinal cord, in which the corticospinal tract innervates spinal circuitry controlling hand and digit muscles. FA of the medial spinal cord correlated consistently with age across all cervical levels, whereas FA of the lateral spinal cord did not. The results suggest (1) a functionally relevant specialization of lateral spinal cord white matter and (2) an increased sensitivity to age-related decline in medial spinal cord white matter in healthy subjects.
- Published
- 2010
- Full Text
- View/download PDF
49. Cortical activity in relation to velocity dependent movement resistance in the flexor muscles of the hand after stroke.
- Author
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Lindberg PG, Gäverth J, Fagergren A, Fransson P, Forssberg H, and Borg J
- Subjects
- Adult, Aged, Female, Hand innervation, Humans, Male, Middle Aged, Motor Neurons physiology, Muscle, Skeletal innervation, Muscle, Skeletal physiology, Range of Motion, Articular, Reflex, Stretch physiology, Sensory Receptor Cells physiology, Cerebral Cortex physiology, Hand physiology, Magnetic Resonance Imaging, Movement physiology, Muscle Spasticity physiopathology, Stroke physiopathology
- Abstract
Background: The role of spinal networks in spasticity is well investigated, but little is known about possible cortical contributions to hypertonicity across a joint., Objective: The authors hypothesized that there are cortical activation correlates to spasticity in stroke patients with increased muscle tone of the wrist flexors., Methods: Stroke patients and controls were scanned using event-related functional magnetic resonance imaging (fMRI) during slow and fast passive movements of the hand with simultaneous recording of passive movement resistance (PMR)., Results: Control participants had velocity-dependent activity (greater for slow than fast movements) of 2 types, in areas that were also more active in passive movement than rest (eg, relative increase in activation in contralateral S1 and M1 was greater for slow than fast) and in areas that were also more active in rest than passive movement (eg, relative decrease in activation in occipital areas and ipsilateral precentral gyrus was greater for fast than slow). In the patient group, with large interindividual variation of spasticity, we found an association between PMR and the velocity-dependent activity in ipsilateral S1 (area 3b) extending into M1 (area 4a), contralateral cingulate cortex, supplementary motor area (SMA), Brodmann Area 45 (BA 45), and cerebellum. Post hoc testing also revealed a similar correlation in S1 and M1 bilaterally in controls and showed that patients activated ipsilateral S1 and M1 more than controls in the velocity-dependent condition., Conclusions: The findings suggest the possibility of ipsilateral sensory and motor cortical involvement in spasticity after stroke, which warrant further investigation.
- Published
- 2009
- Full Text
- View/download PDF
50. Wallerian degeneration of the corticofugal tracts in chronic stroke: a pilot study relating diffusion tensor imaging, transcranial magnetic stimulation, and hand function.
- Author
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Lindberg PG, Skejø PH, Rounis E, Nagy Z, Schmitz C, Wernegren H, Bring A, Engardt M, Forssberg H, and Borg J
- Subjects
- Adult, Aged, Chronic Disease, Female, Hand innervation, Hand physiology, Humans, Male, Middle Aged, Pilot Projects, Predictive Value of Tests, Pyramidal Tracts physiopathology, Recovery of Function, Stroke physiopathology, Wallerian Degeneration physiopathology, Diffusion Magnetic Resonance Imaging, Pyramidal Tracts pathology, Stroke pathology, Transcranial Magnetic Stimulation, Wallerian Degeneration pathology
- Abstract
Objective: This study tested the hypothesis that degeneration of the corticofugal tracts (CFTs) is related to poor functional outcome in the upper limb after stroke., Methods: . The authors used diffusion tensor imaging to determine the degree of white matter integrity of the CFT (FA(AH/UH)) in chronic stroke patients and controls. The functional integrity of the corticospinal pathway was examined using transcranial magnetic stimulation. Recruitment curves and silent period duration were measured. The relationship between FA(AH/UH) and functional outcome of the upper limb was also assessed using a battery of upper limb function tests., Results: In patients, FA( AH/UH) correlated positively with the slope of recruitment curves (RC(AH/UH)) and grip strength. FA(AH/UH) also correlated negatively with the silent period duration (SP(AH/UH)). According to the FA(AH/UH), patients were also classified into groups with minimal or extensive Wallerian degeneration (WD). Patients with more extensive WD had poorer grip strength, dexterity, and range of movement., Conclusions: The authors' results suggest that structural and functional integrity of the CFT is essential to maintain function of the upper limb after stroke.
- Published
- 2007
- Full Text
- View/download PDF
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