Search

BackgroundAerobic exercise elicits striking effects on neuroplasticity and cognitive executive function but is poorly understood after stroke.ObjectiveWe tested the effect of 4 weeks of aerobic exercise training on inhibitory and facilitatory elements of cognitive executive function and electroencephalography (EEG) markers of cortical inhibition and facilitation. We investigated relationships between stimulus-evoked cortical responses, blood lactate levels during training, and aerobic fitness post-intervention.MethodsTwelve individuals with chronic (>6mo) stroke completed an intensive aerobic exercise intervention (40-mins, 3x/week). Electroencephalography and motor response times were assessed during congruent (response facilitation) and incongruent (response inhibition) stimuli of a Flanker task. Aerobic fitness capacity was assessed as VO2-peak during a treadmill test pre- and post-intervention. Blood lactate was assessed acutely (ResultsFollowing exercise training, the response inhibition speed increased while response facilitation remained unchanged. A relationship between earlier cortical N2 response and faster response inhibition emerged post-intervention. Individuals who produced higher lactate during exercise training achieved faster response inhibition and tended to show earlier cortical N2 responses post-intervention. There were no associations between VO2-peak and metrics of behavioral or neurophysiologic function.ConclusionsThese findings provide novel evidence for selective benefits of aerobic exercise on inhibitory control during the initial 4-week period after initiation of exercise training, and implicate a potential therapeutic effect of lactate on post-stroke cortical inhibitory function.Trial RegistrationClinicalTrials.govIdentifier:NCT03760016. First posted: November 30, 2018.https://clinicaltrials.gov/ct2/show/NCT03760016

Task-level goals such as maintaining standing balance are achieved through coordinated muscle activity. Consistent and individualized groupings of synchronously activated muscles can be estimated from muscle recordings in terms of motor modules or muscle synergies, independent of their temporal activation. The structure of motor modules can change with motor training, neurological disorders, and rehabilitation, but the central and peripheral mechanisms underlying motor module structure remain unclear. To assess the role of peripheral somatosensory input on motor module structure, we evaluated changes in the structure of motor modules for reactive balance recovery following pyridoxine-induced large-fiber peripheral somatosensory neuropathy in previously collected data in four adult cats. Somatosensory fiber loss, quantified by postmortem histology, varied from mild to severe across cats. Reactive balance recovery was assessed using multidirectional translational support-surface perturbations over days to weeks throughout initial impairment and subsequent recovery of balance ability. Motor modules within each cat were quantified by non-negative matrix factorization and compared in structure over time. All cats exhibited changes in the structure of motor modules for reactive balance recovery after somatosensory loss, providing evidence that somatosensory inputs influence motor module structure. The impact of the somatosensory disturbance on the structure of motor modules in well-trained adult cats indicates that somatosensory mechanisms contribute to motor module structure, and therefore may contribute to some of the pathological changes in motor module structure in neurological disorders. These results further suggest that somatosensory nerves could be targeted during rehabilitation to influence pathological motor modules for rehabilitation. NEW & NOTEWORTHY Stable motor modules for reactive balance recovery in well-trained adult cats were disrupted following pyridoxine-induced peripheral somatosensory neuropathy, suggesting somatosensory inputs contribute to motor module structure. Furthermore, the motor module structure continued to change as the animals regained the ability to maintain standing balance, but the modules generally did not recover pre-pyridoxine patterns. These results suggest changes in somatosensory input and subsequent learning may contribute to changes in motor module structure in pathological conditions.

Background Reactive balance recovery evokes a negative peak of cortical electroencephalography (EEG) activity (N1) that is simultaneous to brainstem-mediated automatic balance-correcting muscle activity. This study follows up on an observation from a previous study, in which N1 responses were larger in individuals who seemed to have greater difficulty responding to support-surface perturbations. Research Question We hypothesized that people engage more cortical activity when balance recovery is more challenging. We predicted that people with lower balance ability would exhibit larger cortical N1 responses during balance perturbations. Methods In 20 healthy young adults (11 female, ages 19–38) we measured the amplitude of the cortical N1 response evoked by 48 backward translational support-surface perturbations of unpredictable timing and amplitude. Perturbations included a Small (8 cm) perturbation that was identical across participants, as well as Medium (13−15 cm) and Large (18−22 cm) perturbations scaled to participant height to control for height-related differences in perturbation difficulty. To assess individual differences in balance ability, we measured the distance traversed on a narrow (0.5-inch wide) 12-foot beam across 6 trials. We tested whether the cortical N1 response amplitude was correlated to balance ability across participants. Results Cortical N1 amplitudes in response to standing balance perturbations (54 ± 18 μV) were inversely correlated to the distance traveled in the difficult beam-walking task (R2 = 0.20, p = 0.029). Further, there was a significant interaction between performance on the beam-walking task and the effect of perturbation magnitude on the cortical N1 response amplitude, whereby individuals who performed worse on the beam-walking task had greater increases in N1 amplitudes with increases in perturbation magnitude. Significance Cortical N1 response amplitudes may reflect greater cortical involvement in balance recovery when challenged. This increased cortical involvement may reflect cognitive processes such as greater perceived threat or attention to balance, which have the potential to influence subsequent motor control.

Mechanisms underlying associations between balance and cognitive impairments in older adults with and without Parkinson’s disease are poorly understood. Balance disturbances evoke a cortical N1 response that is associated with both balance and cognitive abilities in unimpaired populations. We hypothesized that the N1 response reflects neural mechanisms that are shared between balance and cognitive function, and would therefore be associated with both balance and cognitive impairments in Parkinson’s disease. Although N1 responses did not differ at the group level, they showed different associations with balance and cognitive function in the Parkinson’s disease vs. control groups. In the control group, higher N1 amplitudes were correlated with lower cognitive set shifting ability and lower balance confidence. However, in Parkinson’s disease, narrower N1 widths (i.e., shorter durations) were associated with greater parkinsonian motor symptom severity, lower balance ability and confidence, lower mobility, and lower overall cognitive function. Despite different relationships across populations, the present results suggest the N1 response reflects neural processes related to both balance and cognitive function. A better understanding of neural mechanisms linking balance and cognitive function could provide insight into associations between balance and cognitive decline in aging populations.

1.AbstractThe mechanisms underlying associations between cognitive set shifting impairments and balance dysfunction are unclear. Cognitive set shifting refers to the ability to flexibly adjust behavior to changes in task rules or contexts, which could be involved in flexibly adjusting balance recovery behavior to different contexts, such as the direction the body is falling. Prior studies found associations between cognitive set shifting impairments and severe balance dysfunction in populations experiencing frequent falls. The objective of this study was to test whether cognitive set shifting ability is expressed in successful balance recovery behavior in older adults with high clinical balance ability (N=19, 71 ± 7 years, 6 female). We measured cognitive set shifting ability using the Trail Making Test and clinical balance ability using the miniBESTest. For most participants, cognitive set shifting performance (Trail Making Test B-A = 37 ± 20s) was faster than normative averages (46s for comparable age and education levels), and balance ability scores (miniBESTest = 25 ± 2 / 28) were above the threshold for fall risk (23 for people between 70-80 years). Reactive balance recovery in response to support-surface translations in anterior and posterior directions was assessed in terms of body motion, muscle activity, and brain activity. Across participants, lower cognitive set shifting ability was associated with smaller peak center of mass displacement during balance recovery, lower directional specificity of late phase balance-correcting muscle activity (i.e., greater antagonist muscle activity 200-300ms after perturbation onset), and larger cortical N1 responses (100-200ms). None of these measures were associated with clinical balance ability. Our results suggest that cognitive set shifting ability is expressed in balance recovery behavior even in the absence of profound clinical balance disability. Specifically, our results suggest that lower flexibility in cognitive task performance is associated with lower ability to incorporate the directional context into the cortically-mediated later phase of the motor response. The resulting antagonist activity and stiffer balance behavior may help explain associations between cognitive set shifting impairments and frequent falls.

Cortical beta oscillations (13&ndash, 30 Hz) reflect sensorimotor processing, but are not well understood in balance recovery. We hypothesized that sensorimotor cortical activity would increase under challenging balance conditions. We predicted greater beta power when balance was challenged, either by more difficult perturbations or by lower balance ability. In 19 young adults, we measured beta power over motor cortical areas (electroencephalography, Cz electrode) during three magnitudes of backward support -surface translations. Peak beta power was measured during early (50&ndash, 150 ms), late (150&ndash, 250 ms), and overall (0&ndash, 400 ms) time bins, and wavelet-based analyses quantified the time course of evoked beta power. An ANOVA was used to compare peak beta power across perturbation magnitudes in each time bin. We further tested the association between perturbation-evoked beta power and individual balance ability measured in a challenging beam walking task. Beta power increased ~50 ms after perturbation, and to a greater extent in larger perturbations. Lower individual balance ability was associated with greater beta power in only the late (150&ndash, 250 ms) time bin. These findings demonstrate greater sensorimotor cortical engagement under more challenging balance conditions, which may provide a biomarker for reduced automaticity in balance control that could be used in populations with neurological impairments.

The cortical N1 response to balance perturbation is observed in electroencephalography recordings simultaneous to automatic balance-correcting muscle activity. We recently observed larger cortical N1s in individuals who had greater difficulty resisting compensatory steps, suggesting the N1 may be influenced by stepping or changes in response strategy. Here, we test whether the cortical N1 response is influenced by stepping (planned steps versus feet-in-place) or prior planning (planned vs. unplanned steps). We hypothesized that prior planning of a step would reduce the amplitude of the cortical N1 response to balance perturbations. In 19 healthy young adults (ages 19–38; 8 men and 11 women), we measured the cortical N1 amplitude evoked by 48 backward translational support-surface perturbations of unpredictable timing and amplitude in a single experimental session. Participants were asked to plan a stepping reaction on half of perturbations, but to resist stepping otherwise. Perturbations included an easy (8 cm, 16 cm/s) perturbation that was identical across participants and did not naturally elicit compensatory steps, and a height-adjusted difficult (18–22 cm, 38–42 cm/s) perturbation that frequently elicited compensatory steps despite instructions to resist stepping. In contrast to our hypothesis, cortical N1 response amplitudes did not differ between planned and unplanned stepping reactions, but cortical responses were 11% larger with the execution of planned compensatory steps compared with nonstepping responses to difficult perturbations. These results suggest a possible role for the cortical N1 in the execution of compensatory steps for balance recovery, and this role is not influenced by whether the compensatory step was planned before the perturbation. NEW & NOTEWORTHY The cortical N1 response to balance perturbation is larger when executing compensatory steps, suggesting a relationship between the cortical N1 and subsequent motor behavior. Additionally, the cortical N1 response is not impacted by prior planning of the stepping reaction, suggesting that predictability of the motor outcome does not impact the N1 in the same way as predictability of the perturbation stimulus.

The role of cortical activity in standing balance is unclear. Here we tested whether perturbation-evoked cortical responses share sensory input with simultaneous balance-correcting muscle responses. We hypothesized that the acceleration-dependent somatosensory signals that drive the initial burst of the muscle automatic postural response also drive the simultaneous perturbation-evoked cortical N1 response. We measured in healthy young adults ( n = 16) the initial burst of the muscle automatic postural response (100–200 ms), startle-related muscle responses (100–200 ms), and the perturbation-evoked cortical N1 potential, i.e., a negative peak in cortical EEG activity (100–200 ms) over the supplementary motor area. Forward and backward translational support-surface balance perturbations were applied at four levels of acceleration and were unpredictable in timing, direction, and acceleration. Our results from averaged and single-trial analyses suggest that although cortical and muscle responses are evoked by the same perturbation stimulus, their amplitudes are independently modulated. Although both muscle and cortical responses increase with acceleration, correlations between single-trial muscle and cortical responses were very weak. Furthermore, across subjects, the scaling of muscle responses to acceleration did not correspond to scaling of cortical responses to acceleration. Moreover, we observed a reduction in cortical response amplitude across trials that was related to a reduction in startle-related—but not balance-correcting—muscle activity. Therefore, cortical response attenuation may be related to a reduction in perceived threat rather than motor adaptation or changes in sensory inflow. We conclude that the cortical N1 reflects integrated sensory inputs simultaneously related to brain stem-mediated balance-correcting muscle responses and startle reflexes. NEW & NOTEWORTHY Reactive balance recovery requires sensory inputs to be transformed into appropriate balance-correcting motor responses via brain stem circuits; these are accompanied by simultaneous and poorly understood cortical responses. We used single-trial analyses to dissociate muscle and cortical response modulation with perturbation acceleration. Although muscle and cortical responses share sensory inputs, they have independent scaling mechanisms. Attenuation of cortical responses with experience reflected attenuation of brain stem-mediated startle responses rather than the amplitude of balance-correcting motor responses.

Detecting and correcting errors is essential to successful action. Studies on response monitoring have examined scalp event-related potentials (ERPs) following the commission of motor slips in speeded-response tasks, focusing on a frontocentral negativity (i.e., error-related negativity or ERN). Sensorimotor neurophysiologists investigating cortical monitoring of reactive balance recovery behavior observe a strikingly similar pattern of scalp ERPs following externally imposed postural errors, including a brief frontocentral negativity that has been referred to as the balance N1. We integrate and review relevant literature from these discrepant fields to suggest shared underlying mechanisms and potential benefits of collaboration across fields. Unlike the cognitive tasks leveraged to study the ERN, balance perturbations afford precise experimental control of postural errors to elicit balance N1s that are an order of magnitude larger than the ERN and drive robust and well-characterized adaptation of behavior within an experimental session. Many factors that modulate the ERN, including motivation, perceived consequences, perceptual salience, expectation, development, and aging are likewise known to modulate the balance N1. We propose that the ERN and balance N1 reflect common neural activity for detecting errors. Collaboration across fields could help clarify the functional significance of the ERN, and poorly understood interactions between motor and cognitive impairments.