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Muscle spindles relay vital mechanosensory information for movement and posture, but muscle spindle feedback is coupled to skeletal motion by a compliant tendon. Little is known about the effects of tendon compliance on muscle spindle feedback during movement, and the complex firing of muscle spindles make these effects difficult to predict. Our goal was to investigate changes in muscle spindle firing using added series elastic elements (SEEs) to mimic a more compliant tendon, and to characterize the accompanying changes in firing with respect to muscle-tendon unit (MTU) and muscle fascicle displacements (recorded via sonomicrometry). Sinusoidal, ramp-hold-release, and triangular stretches were analyzed to examine potential changes in muscle spindle instantaneous firing rates (IFRs) in locomotor-and perturbation-like stretches as well as history dependence. Added SEEs effectively reduced overall MTU stiffness and generally reduced muscle spindle firing rates, but the effect differed across stretch types. During sinusoidal stretches, peak firing rates were reduced and IFR was strongly correlated with fascicle velocity. During ramp stretches, SEEs reduced the dynamic and static responses of the spindle during lengthening but had no effect on initial bursts at the onset of stretch. Notably, IFR was negatively related to fascicle displacement during the hold phase. During triangular stretches, SEEs reduced the mean IFR during the first and second stretches, affecting the history dependence of mean IFR. Overall, these results demonstrate that tendon compliance may attenuate muscle spindle feedback during movement, but these changes cannot be fully explained by reduced muscle fascicle length and velocity.New FindingsWhat is the central question of the study?Little is known about the effects of tendon compliance on muscle spindle function. We asked whether increasing the series compliance the muscle-tendon unit muscle spindle Ia responses to stretch. We also test the relationship between muscle spindle firing rates and muscle fascicle biomechanics.What is the main finding and its importance?Muscle spindle firing was generally attenuated with added series compliance, with the exception of the initial burst at the onset of stretch. Overall, the changes depended upon stretch profiles, and could not be fully explained by muscle fascicle length and velocity.

Balance impairments are common in cerebral palsy (CP). When balance is perturbed by backward support surface translations, children with CP have increased co-activation of the plantar flexors and tibialis anterior muscle as compared to typically developing (TD) children. However, it is unclear whether increased muscle co-activation is used as a compensation strategy to improve balance control or is a consequence of impaired reciprocal inhibition. During translational perturbations, increased joint stiffness due to co-activation might aid standing balance control by resisting movement of the body with respect to the feet. However, during rotational perturbations, increased joint stiffness will hinder balance control as it couples body to platform rotation. Hence, we expect increased muscle co-activation in response to rotational perturbations if co-activation is caused by reduced reciprocal inhibition but not if it is merely a compensation strategy.We perturbed standing balance by combined backward translational and toe-up rotational perturbations in 20 children with CP and 20 TD children. Our perturbation protocol induced a backward movement of the center of mass requiring balance correcting activity in the plantar flexors followed by a forward movement of the center of mass requiring balance correcting activity in the tibialis anterior.We found that the switch from plantar flexor to tibialis anterior activity upon reversal of the center of mass movement was less pronounced in children with CP than in TD children leading to increased co-activation of the plantar flexors and tibialis anterior throughout the response. Therefore, our results suggest that a reduction in reciprocal inhibition causes muscle co-activation in reactive standing balance in CP.

Locomotion results from the interactions of highly nonlinear neural and biomechanical dynamics. Accordingly, understanding gait dynamics across behavioral conditions and individuals based on detailed modeling of the underlying neuromechanical system has proven difficult. Here, we develop a data-driven and generative modeling approach that recapitulates the dynamical features of gait behaviors to enable more holistic and interpretable characterizations and comparisons of gait dynamics. Specifically, gait dynamics of multiple individuals are predicted by a dynamical model that defines a common, low-dimensional, latent space to compare group and individual differences. We find that highly individualized dynamics – i.e., gait signatures – for healthy older adults and stroke survivors during treadmill walking are conserved across gait speed. Gait signatures further reveal individual differences in gait dynamics, even in individuals with similar functional deficits. Moreover, components of gait signatures can be biomechanically interpreted and manipulated to reveal their relationships to observed spatiotemporal joint coordination patterns. Lastly, the gait dynamics model can predict the time evolution of joint coordination based on an initial static posture. Our gait signatures framework thus provides a generalizable, holistic method for characterizing and predicting cyclic, dynamical motor behavior that may generalize across species, pathologies, and gait perturbations.

BackgroundA common perspective in post-stroke gait training is that walking at the fastest safe speed maximizes the quality of gait biomechanics, with limited detrimental effects on compensatory biomechanics and inter-limb asymmetry. Thisfastest is bestperspective is highly relevant to treadmill training paradigms, as mass high-intensity stepping practice with high-quality biomechanics can improve walking function and reinforce desirable gait patterns. However, it is unclear if walking at the fastest safe speed maximizes the quality of (i.e., optimizes) post-stroke gait biomechanics across variables, individuals, and walking function levels, or if there exists a significant cost (i.e., benefit lost) of walking at the fastest speed when fastest is not optimal.MethodsHere, we determined if walking at the fastest speed optimized 16 biomechanical magnitude and inter-limb asymmetry variables, in 14 low- (n=7) and high-functioning (n=7) stroke survivors. Participants walked at six speeds ranging from their self-selected to fastest safe speed. To characterize the relative benefit of optimizing, rather than maximizing, gait speed for each variable, we compared the biomechanical cost (i.e., immediate speed-induced change versus the self-selected speed) of walking at the fastest versus the optimal speed. Finally, we used linear regression to characterize how each variable’s quality changed with absolute speed.ResultsAcross speeds, 50% of magnitude and 17% of asymmetry variables were optimized at the fastest speed, but which variables were optimized differed between participants. Compared to walking at the optimal speed for each variable, the fastest speed elicited large biomechanical costs for some inter-limb asymmetry variables (difference in Cohen’sd=0.1-0.9). Both low- and high-function subgroups exhibited significant positive correlations between walking speed and paretic-leg trailing limb angle, peak ankle moment, and peak hip and ankle power magnitudes (all pConclusionsThese results refine the perspective thatfastest is best, showing that the training speeds that maximize gait quality may not be the fastest for all individuals and biomechanical variables. Individual-specific stroke gait quality metrics encompassing multiple biomechanical variables are needed to guide gait speed optimization for precision rehabilitation.

System identification of a dynamic environment using a robotic device utilizes physical perturbations in the form of displacement or force. To obtain an accurate system model, physical perturbations must be informative, which can be characterized by their spectral properties. The process of generating physical perturbations by using a robotic device often leads to spectral property degradation in the high-frequency region due to the dynamics of robot motion control and discrete-time signal processing. Spectral flatness is a metric applicable to quantifying the fidelity of the robotic system and quality of physical perturbations on an external object. This letter introduces a new metric named Band-limited Spectral Flatness Gain (BLSFG) to evaluate the physical perturbation quality relative to the input reference over a frequency band of interest. Motion control of a manipulandum that generates pseudorandom position perturbations for human sensorimotor system identification is considered as a representative example. The closed-loop system dynamics of the position control is characterized and optimized based on the BLSFG. Results suggest that a certain underdamped closed-loop property is advantageous to improve the spectral flatness of a degraded continuous-time pseudorandom reference. A high BLSFG is achieved when the resonance frequency of the closed-loop system is close to the update frequency of the pseudorandom sequence.

Postural responses to similar perturbations of standing balance vary widely within and across subjects. Here, we identified two sources of variability and their interactions by combining experimental observations with computational modeling: differences in posture at perturbation onset across trials and differences in task-level goals across subjects. We first collected postural responses to unpredictable backward support-surface translations during standing in 10 young adults. We found that maximal trunk lean in postural responses to backward translations were highly variable both within subjects (mean of ranges = 28.3°) and across subjects (range of means = 39.9°). Initial center of mass (COM) position was correlated with maximal trunk lean during the response, but this relation was subject specific (R(2) = 0.29–0.82). We then used predictive simulations to assess causal relations and interactions with task-level goal. Our simulations showed that initial posture explains the experimentally observed intrasubject variability with a more anterior initial COM position increasing the use of the hip strategy. Differences in task-level goal explain observed intersubject variability with prioritizing effort minimization leading to ankle strategies and prioritizing stability leading to hip strategies. Interactions between initial posture and task-level goal explain observed differences in intrasubject variability across subjects. Our findings suggest that variability in initial posture due to increased sway as observed in older adults might increase the occurrence of less stable postural responses to perturbations. Insight in factors causing movement variability will advance our ability to study the origin of differences between groups and conditions. NEW & NOTEWORTHY Responses to perturbations of standing balance vary both within and between individuals. By combining experimental observations with computational modeling, we identified causes of observed kinematic variability in healthy young adults. First, we found that trial-by-trial differences in posture at perturbation onset explain most of the kinematic variability observed within subjects. Second, we found that differences in prioritizing effort versus stability explained differences in the postural response as well as differences in trial-by-trial variability across subjects.

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.

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.

Postural muscle activity precedes voluntary movements of the upper limbs. The traditional view of this activity is that it anticipates perturbations to balance caused by the movement of a limb. However, findings from reach-based paradigms have shown that postural adjustments can initiate center of mass displacement for mobility rather than minimize its displacement for stability. Within this context, altering reaching distance beyond the base of support would place increasing constraints on equilibrium during stance. If the underlying composition of anticipatory postural activity is linked to stability, coordination between muscles (i.e., motor modules) may evolve differently as equilibrium constraints increase. We analyzed the composition of motor modules in functional trunk muscles as participants performed multidirectional reaching movements to targets within and beyond the arm’s length. Bilateral trunk and reaching arm muscle activity were recorded. Despite different trunk requirements necessary for successful movement, and the changing biomechanical (i.e., postural) constraints that accompany alterations in reach distance, nonnegative matrix factorization identified functional motor modules derived from preparatory trunk muscle activity that shared common features. Relative similarity in modular weightings (i.e., composition) and spatial activation profiles that reflect movement goals across tasks necessitating differing levels of trunk involvement provides evidence that preparatory postural adjustments are linked to the same task priorities (i.e., movement generation rather than stability). NEW & NOTEWORTHY Reaching within and beyond arm’s length places different task constraints upon the required trunk motion necessary for successful movement execution. The identification of constant modular features, including functional muscle weightings and spatial tuning, lend support to the notion that preparatory postural adjustments of the trunk are tied to the same task priorities driving mobility, regardless of the future postural constraints.

Although Parkinson disease (PD) causes profound balance impairments, we know very little about how PD impacts the sensorimotor networks we rely on for automatically maintaining balance control. In young healthy people and animals, muscles are activated in a precise temporal and spatial organization when the center of body mass (CoM) is unexpectedly moved that is largely automatic and determined by feedback of CoM motion. Here, we show that PD alters the sensitivity of the sensorimotor feedback transformation. Importantly, sensorimotor feedback transformations for balance in PD remain temporally precise, but become spatially diffuse by recruiting additional muscle activity in antagonist muscles during balance responses. The abnormal antagonist muscle activity remains precisely time-locked to sensorimotor feedback signals encoding undesirable motion of the body in space. Further, among people with PD, the sensitivity of abnormal antagonist muscle activity to CoM motion varies directly with the number of recent falls. Our work shows that in people with PD, sensorimotor feedback transformations for balance are intact but disinhibited in antagonist muscles, likely contributing to balance deficits and falls.

Despite decades of research, we lack a mechanistic framework capable of predicting how movement-related signals are transformed into the diversity of muscle spindle afferent firing patterns observed experimentally, particularly in naturalistic behaviors. Here, a biophysical model demonstrates that well-known firing characteristics of muscle spindle Ia afferents – including dependence on movement history, and nonlinear scaling with muscle stretch velocity – emerge from first principles of muscle contractile mechanics. Further, mechanical interactions of the muscle spindle with muscle-tendon dynamics reveal how motor commands to the muscle (alpha drive) versus muscle spindle (gamma drive) can cause highly variable and complex activity during active muscle contraction and muscle stretch that defy simple explanation. Depending on the neuromechanical conditions, the muscle spindle model output appears to “encode” aspects of muscle force, yank, length, stiffness, velocity, and/or acceleration, providing an extendable, multiscale, biophysical framework for understanding and predicting proprioceptive sensory signals in health and disease.

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.

Leg rigidity is associated with frequent falls in people with Parkinson’s disease (PD), suggesting a potential role in functional balance and gait impairments. Changes in neural state due to secondary tasks, e.g. activation maneuvers, can exacerbate (or “activate”) rigidity, possibly increasing the risk of falls. However, the subjective interpretation and coarse classification of the standard clinical rigidity scale has prohibited the systematic, objective assessment of resting and activated leg rigidity. The pendulum test is an objective diagnostic method that we hypothesized would be sensitive enough to characterize resting and activated leg rigidity.We recorded kinematic data during the pendulum test in 15 individuals with PD, spanning a range of leg rigidity severity (slight to severe). From the recorded data of leg swing kinematics we measured biomechanical outcomes including first swing excursion, first extension peak, number and duration of the oscillations, resting angle, relaxation index, maximum and minimum angular velocity. We examined associations between biomechanical outcomes and clinical leg rigidity score. We evaluated the effect of increasing rigidity through activation maneuvers on biomechanical outcomes. Finally, we assessed whether either biomechanical outcomes or changes in outcomes with activation were associated with fall history.Our results suggest that the biomechanical assessment of the pendulum test can objectively quantify leg rigidity among people with PD. We found that the presence of marked rigidity during clinical exam significantly impacted biomechanical outcomes, i.e. first extension peak, number of oscillations, relaxation index and maximum angular velocity. No differences in the effect of activation maneuvers between groups with clinically assessed moderate and marked rigidity were observed, suggesting that activated rigidity may be independent of resting rigidity and should be scored as independent variables. Moreover, we found that fall history was more common among people whose rigidity was increased with a secondary task, as measured by biomechanical outcomes.We conclude that different mechanisms contributing to resting and activated rigidity may play an important yet unexplored functional role in balance impairments. The pendulum test may contribute to a better understanding of fundamental mechanisms underlying motor symptoms in PD, evaluating the efficacy of treatments, and predicting the risk of falls.

A software tool for synchronization of video with signals would be of broad general use to behavioral neuroscientists. A new program, calledneurotic(NEUROscience Tool for Interactive Characterization), allows users to review and annotate signal data synchronized with video, performs simple initial analyses including signal filtering and spike detection, is easy to use, and supports a variety of file formats. The program also facilitates collaborations by using a portable specification for loading and processing data and retrieving data files from online sources. Two examples are shown in which the software is used to explore experimental datasets with extracellular nerve or muscle recordings and simultaneous video of behavior. The configuration specification for controlling how data are located, loaded, processed, and plotted is also summarized. Algorithms for spike detection and burst detection are demonstrated. This new program could be used in many applications in which behavior and signals need to be analyzed together.

Although Parkinson disease (PD) causes profound balance impairments, we know very little about how PD impacts the sensorimotor networks we rely on for automatically maintaining balance control. In young healthy people and animals, muscles are activated in a precise temporal and spatial organization when the center of body mass (CoM) is unexpectedly moved that is largely automatic and determined by feedback of CoM motion. Here, we show that PD alters the sensitivity of the sensorimotor feedback transformation. Importantly, sensorimotor feedback transformations for balance in PD remain temporally precise, but become spatially diffuse by recruiting additional muscle activity in antagonist muscles during balance responses. The abnormal antagonist muscle activity remains precisely time-locked to sensorimotor feedback signals encoding undesirable motion of the body in space. Further, among people with PD, the sensitivity of abnormal antagonist muscle activity to CoM motion varies directly with the number of recent falls. Our work shows that in people with PD, sensorimotor feedback transformations for balance are intact but disinhibited in antagonist muscles, likely contributing to balance deficits and falls.