Distinct Cortical Correlates of Perception and Motor Function in Balance Control.

Fluctuations in brain activity alter how we perceive our body and generate movements but have not been investigated in functional whole-body behaviors. During reactive balance, we recently showed that evoked brain activity is associated with the balance ability in young individuals. Furthermore, in PD, impaired whole-body motion perception in reactive balance is associated with impaired balance. Here, we investigated the brain activity during the whole-body motion perception in reactive balance in young adults (9 female, 10 male). We hypothesized that both ongoing and evoked cortical activity influences the efficiency of information processing for successful perception and movement during whole-body behaviors. We characterized two cortical signals using electroencephalography localized to the SMA: (1) the "N1," a perturbation-evoked potential that decreases in amplitude with expectancy and is larger in individuals with lower balance function, and (2) preperturbation ß power, a transient rhythm that favors maintenance of the current sensorimotor state and is inversely associated with tactile perception. In a two-alternative forced choice task, participants judged whether pairs of backward support surface perturbations during standing were in the "same" or "different" direction. As expected, lower whole-body perception was associated with lower balance ability. Within a perturbation pair, N1 attenuation was larger on correctly perceived trials and associated with better balance, but not perception. In contrast, preperturbation ß power was higher on incorrectly perceived trials and associated with poorer perception, but not balance. Together, ongoing and evoked cortical activity have unique roles in information processing that give rise to distinct associations with perceptual and balance ability.

Combined translational and rotational perturbations of standing balance reveal contributions of reduced reciprocal inhibition to balance impairments in children with cerebral palsy.

Balance impairments are common in cerebral palsy. When balance is perturbed by backward support surface translations, children with cerebral palsy have increased co-activation of the plantar flexors and tibialis anterior muscle as compared to typically developing children. However, it is unclear whether increased muscle co-activation is a compensation strategy to improve balance control or is a consequence of reduced reciprocal inhibition. During translational perturbations, increased joint stiffness due to co-activation might aid balance control by resisting movement of the body with respect to the feet. In contrast, during rotational perturbations, increased joint stiffness will hinder balance control as it couples body to platform rotation. Therefore, 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 cerebral palsy and 20 typically developing children. Perturbations induced forward followed by backward movement of the center of mass. We evaluated reactive muscle activity and the relation between center of mass movement and reactive muscle activity using a linear feedback model based on center of mass kinematics. In typically developing children, perturbations induced plantar flexor balance correcting muscle activity followed by tibialis anterior balance correcting muscle activity, which was driven by center of mass movement. In children with cerebral palsy, the switch from plantar flexor to tibialis anterior activity was less pronounced than in typically developing children due to increased muscle co-activation of the plantar flexors and tibialis anterior throughout the response. Our results thus suggest that a reduction in reciprocal inhibition causes muscle co-activation in reactive standing balance in children with cerebral palsy.

Precise cortical contributions to sensorimotor feedback control during reactive balance.

The role of the cortex in shaping automatic whole-body motor behaviors such as walking and balance is poorly understood. Gait and balance are typically mediated through subcortical circuits, with the cortex becoming engaged as needed on an individual basis by task difficulty and complexity. However, we lack a mechanistic understanding of how increased cortical contribution to whole-body movements shapes motor output. Here we use reactive balance recovery as a paradigm to identify relationships between hierarchical control mechanisms and their engagement across balance tasks of increasing difficulty in young adults. We hypothesize that parallel sensorimotor feedback loops engaging subcortical and cortical circuits contribute to balance-correcting muscle activity, and that the involvement of cortical circuits increases with balance challenge. We decomposed balance-correcting muscle activity based on hypothesized subcortically- and cortically-mediated feedback components driven by similar sensory information, but with different loop delays. The initial balance-correcting muscle activity was engaged at all levels of balance difficulty. Its onset latency was consistent with subcortical sensorimotor loops observed in the lower limb. An even later, presumed, cortically-mediated burst of muscle activity became additionally engaged as balance task difficulty increased, at latencies consistent with longer transcortical sensorimotor loops. We further demonstrate that evoked cortical activity in central midline areas measured using electroencephalography (EEG) can be explained by a similar sensory transformation as muscle activity but at a delay consistent with its role in a transcortical loop driving later cortical contributions to balance-correcting muscle activity. These results demonstrate that a neuromechanical model of muscle activity can be used to infer cortical contributions to muscle activity without recording brain activity. Our model may provide a useful framework for evaluating changes in cortical contributions to balance that are associated with falls in older adults and in neurological disorders such as Parkinson's disease.

Intrafusal cross-bridge dynamics shape history-dependent muscle spindle responses to stretch.

Computational models can be critical to linking complex properties of muscle spindle organs to the sensory information that they encode during behaviours such as postural sway and locomotion where few muscle spindle recordings exist. Here, we augment a biophysical muscle spindle model to predict the muscle spindle sensory signal. Muscle spindles comprise several intrafusal muscle fibres with varied myosin expression and are innervated by sensory neurons that fire during muscle stretch. We demonstrate how cross-bridge dynamics from thick and thin filament interactions affect the sensory receptor potential at the spike initiating region. Equivalent to the Ia afferent's instantaneous firing rate, the receptor potential is modelled as a linear sum of the force and rate change of force (yank) of a dynamic bag1 fibre and the force of a static bag2/chain fibre. We show the importance of inter-filament interactions in (i) generating large changes in force at stretch onset that drive initial bursts and (ii) faster recovery of bag fibre force and receptor potential following a shortening. We show how myosin attachment and detachment rates qualitatively alter the receptor potential. Finally, we show the effect of faster recovery of receptor potential on cyclic stretch-shorten cycles. Specifically, the model predicts history-dependence in muscle spindle receptor potentials as a function of inter-stretch interval (ISI), pre-stretch amplitude and the amplitude of sinusoidal stretches. This model provides a computational platform for predicting muscle spindle response in behaviourally relevant stretches and can link myosin expression seen in healthy and diseased intrafusal muscle fibres to muscle spindle function.

Attenuation of muscle spindle firing with artificially increased series compliance during stretch of relaxed muscle.

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 makes 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-and-hold and triangular stretches were analysed to examine potential changes in muscle spindle instantaneous firing rates (IFRs) in locomotor- and perturbation-like stretches as well as serial 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 and mean firing rates were not reduced and IFR was best-correlated with fascicle velocity. During ramp stretches, SEEs reduced the initial burst, dynamic and static responses of the spindle. 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 serial 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 or velocity, or MTU force.

Discovering individual-specific gait signatures from data-driven models of neuromechanical dynamics.

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.

Voluntary muscle coactivation in quiet standing elicits reciprocal rather than coactive agonist-antagonist control of reactive balance.

Muscle coactivation increases in challenging balance conditions as well as with advanced age and mobility impairments. Increased muscle coactivation can occur both in anticipation of (feedforward) and in reaction to (feedback) perturbations, however, the causal relationship between feedforward and feedback muscle coactivation remains elusive. Here, we hypothesized that feedforward muscle coactivation would increase both the body's initial mechanical resistance due to muscle intrinsic properties and the later feedback-mediated muscle coactivation in response to postural perturbations. Young adults voluntarily increased leg muscle coactivation using visual biofeedback before support-surface perturbations. In contrast to our hypothesis, feedforward muscle coactivation did not increase the body's initial intrinsic resistance to perturbations, nor did it increase feedback muscle coactivation. Rather, perturbations with feedforward muscle coactivation elicited a medium- to long-latency increase of feedback-mediated agonist activity but a decrease of feedback-mediated antagonist activity. This reciprocal rather than coactivation effect on ankle agonist and antagonist muscles enabled faster reactive ankle torque generation, reduced ankle dorsiflexion, and reduced center of mass (CoM) motion. We conclude that in young adults, voluntary feedforward muscle coactivation can be independently modulated with respect to feedback-mediated muscle coactivation. Furthermore, our findings suggest feedforward muscle coactivation may be useful for enabling quicker joint torque generation through reciprocal, rather than coactivated, agonist-antagonist feedback muscle activity. As such our results suggest that behavioral context is critical to whether muscle coactivation functions to increase agility versus stability.NEW & NOTEWORTHY Feedforward and feedback muscle coactivation are commonly observed in older and mobility impaired adults and are considered strategies to improve stability by increasing body stiffness prior to and in response to perturbations. In young adults, voluntary feedforward coactivation does not necessarily increase feedback coactivation in response to perturbations. Instead, feedforward coactivation enabled faster ankle torques through reciprocal agonist-antagonist muscle activity. As such, coactivation may promote either agility or stability depending on the behavioral context.

History-dependent muscle resistance to stretch remains high after small, posturally relevant pre-movements.

The contributions of intrinsic muscle fiber resistance during mechanical perturbations to standing and other postural behaviors are unclear. Muscle short-range stiffness is known to vary depending on the current level and history of the muscle's activation, as well as the muscle's recent movement history; this property has been referred to as history dependence or muscle thixotropy. However, we currently lack sufficient data about the degree to which muscle stiffness is modulated across posturally relevant characteristics of muscle stretch and activation. We characterized the history dependence of muscle's resistance to stretch in single, permeabilized, activated, muscle fibers in posturally relevant stretch conditions and activation levels. We used a classic paired muscle stretch paradigm, varying the amplitude of a 'conditioning' triangular stretch-shorten cycle followed by a 'test' ramp-and-hold imposed after a variable inter-stretch interval. We tested low (<15%), intermediate (15-50%) and high (>50%) muscle fiber activation levels, evaluating short-range stiffness and total impulse in the test stretch. Muscle fiber resistance to stretch remained high at conditioning amplitudes of <1% optimal fiber length, L0, and inter-stretch intervals of >1 s, characteristic of healthy standing postural sway. An ∼70% attenuation of muscle resistance to stretch was reached at conditioning amplitudes of >3% L0 and inter-stretch intervals of <0.1 s, characteristic of larger, faster postural sway in balance-impaired individuals. The thixotropic changes cannot be predicted solely on muscle force at the time of stretch. Consistent with the disruption of muscle cross-bridges, muscle resistance to stretch during behavior can be substantially attenuated if the prior motion is large enough and/or frequent enough.

An approximate stochastic optimal control framework to simulate nonlinear neuro-musculoskeletal models in the presence of noise.

Optimal control simulations have shown that both musculoskeletal dynamics and physiological noise are important determinants of movement. However, due to the limited efficiency of available computational tools, deterministic simulations of movement focus on accurately modelling the musculoskeletal system while neglecting physiological noise, and stochastic simulations account for noise while simplifying the dynamics. We took advantage of recent approaches where stochastic optimal control problems are approximated using deterministic optimal control problems, which can be solved efficiently using direct collocation. We were thus able to extend predictions of stochastic optimal control as a theory of motor coordination to include muscle coordination and movement patterns emerging from non-linear musculoskeletal dynamics. In stochastic optimal control simulations of human standing balance, we demonstrated that the inclusion of muscle dynamics can predict muscle co-contraction as minimal effort strategy that complements sensorimotor feedback control in the presence of sensory noise. In simulations of reaching, we demonstrated that nonlinear multi-segment musculoskeletal dynamics enables complex perturbed and unperturbed reach trajectories under a variety of task conditions to be predicted. In both behaviors, we demonstrated how interactions between task constraint, sensory noise, and the intrinsic properties of muscle influence optimal muscle coordination patterns, including muscle co-contraction, and the resulting movement trajectories. Our approach enables a true minimum effort solution to be identified as task constraints, such as movement accuracy, can be explicitly imposed, rather than being approximated using penalty terms in the cost function. Our approximate stochastic optimal control framework predicts complex features, not captured by previous simulation approaches, providing a generalizable and valuable tool to study how musculoskeletal dynamics and physiological noise may alter neural control of movement in both healthy and pathological movements.

The balance N1 and the ERN correlate in amplitude across individuals in small samples of younger and older adults.

The error-related negativity (ERN) is a neural correlate of error monitoring often used to investigate individual differences in developmental, mental health, and adaptive contexts. However, limited experimental control over errors presents several confounds to its measurement. An experimentally controlled disturbance to standing balance evokes the balance N1, which we previously suggested may share underlying mechanisms with the ERN based on a number of shared features and factors. We now measure whether the balance N1 and ERN are correlated across individuals within two small groups (N = 21 young adults and N = 20 older adults). ERNs were measured in arrow flanker tasks using hand and foot response modalities (ERN-hand and ERN-foot). The balance N1 was evoked by sudden slip-like movements of the floor while standing. The ERNs and the balance N1 showed good and excellent internal consistency, respectively, and were correlated in amplitude in both groups. One principal component strongly loaded on all three evoked potentials, suggesting that the majority of individual differences are shared across the three ERPs. However, there remains a significant component of variance shared between the ERN-hand and ERN-foot beyond what they share with the balance N1. It is unclear whether this component of variance is specific to the arrow flanker task, or something fundamentally related to error processing that is not evoked by a sudden balance disturbance. If the balance N1 were to reflect error processing mechanisms indexed by the ERN, balance paradigms offer several advantages in terms of experimental control over errors.

Evidence for constancy in the modularity of trunk muscle activity preceding reaching: implications for the role of preparatory postural activity.

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.

Interactions between initial posture and task-level goal explain experimental variability in postural responses to perturbations of standing balance.

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 (R2 = 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.

Balance perturbation-evoked cortical N1 responses are larger when stepping and not influenced by motor planning.

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.

Reorganization of motor modules for standing reactive balance recovery following pyridoxine-induced large-fiber peripheral sensory neuropathy in cats.

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.

Motor module generalization across balance and walking is impaired after stroke.

Muscle coordination is often impaired after stroke, leading to deficits in the control of walking and balance. In this study, we examined features of muscle coordination associated with reduced walking performance in chronic stroke survivors using motor module (a.k.a. muscle synergy) analysis. We identified differences between stroke survivors and age-similar neurotypical controls in the modular control of both overground walking and standing reactive balance. In contrast to previous studies that demonstrated reduced motor module number poststroke, our cohort of stroke survivors did not exhibit a reduction in motor module number compared with controls during either walking or reactive balance. Instead, the pool of motor modules common to walking and reactive balance was smaller, suggesting reduced generalizability of motor module function across behaviors. The motor modules common to walking and reactive balance tended to be less variable and more distinct, suggesting more reliable output compared with motor modules specific to either behavior. Greater motor module generalization in stroke survivors was associated with faster walking speed, more normal step length asymmetry, and narrower step widths. Our work is the first to show that motor module generalization across walking and balance may help to distinguish important and clinically relevant differences in walking performance across stroke survivors that would have been overlooked by examining only a single behavior. Finally, because similar relationships between motor module generalization and walking performance have been demonstrated in healthy young adults and individuals with Parkinson's disease, this suggests that motor module generalization across walking and balance may be important for well-coordinated walking. NEW & NOTEWORTHY This is the first work to simultaneously examine neuromuscular control of walking and standing reactive balance in stroke survivors. We show that motor module generalization across these behaviors (i.e., recruiting common motor modules) is reduced compared with controls and is associated with slower walking speeds, asymmetric step lengths, and larger step widths. This is true despite no between-group differences in module number, suggesting that motor module generalization across walking and balance is important for well-coordinated walking.

Dissociation of muscle and cortical response scaling to balance perturbation acceleration.

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.

Elastic tissue forces mask muscle fiber forces underlying muscle spindle Ia afferent firing rates in stretch of relaxed rat muscle.

Stretches of relaxed cat and rat muscle elicit similar history-dependent muscle spindle Ia firing rates that resemble history-dependent forces seen in single activated muscle fibers ( Nichols and Cope, 2004). Owing to thixotropy, whole musculotendon forces and muscle spindle firing rates are history dependent during stretch of relaxed cat muscle, where both muscle force and muscle spindle firing rates are elevated in the first stretch in a series of stretch-shorten cycles ( Blum et al., 2017). By contrast, rat musculotendon exhibits only mild thixotropy, such that the measured forces when stretched cannot explain history-dependent muscle spindle firing rates in the same way ( Haftel et al., 2004). We hypothesized that history-dependent muscle spindle firing rates elicited in stretch of relaxed rat muscle mirror history-dependent muscle fiber forces, which are masked at the level of whole musculotendon force by extracellular tissue force. We removed estimated extracellular tissue force contributions from recorded musculotendon force using an exponentially elastic tissue model. We then showed that the remaining estimated muscle fiber force resembles history-dependent muscle spindle firing rates recorded simultaneously. These forces also resemble history-dependent forces recorded in stretch of single activated fibers that are attributed to muscle cross-bridge mechanisms ( Campbell and Moss, 2000). Our results suggest that history-dependent muscle spindle firing in both rats and cats arise from history-dependent forces owing to thixotropy in muscle fibers.

Yank: the time derivative of force is an important biomechanical variable in sensorimotor systems.

The derivative of force with respect to time does not have a standard term in physics. As a consequence, the quantity has been given a variety of names, the most closely related being 'rate of force development'. The lack of a proper name has made it difficult to understand how different structures and processes within the sensorimotor system respond to and shape the dynamics of force generation, which is critical for survival in many species. We advocate that ∂[Formula: see text]/∂t be termed 'yank', a term that has previously been informally used and never formally defined. Our aim in this Commentary is to establish the significance of yank in how biological motor systems are organized, evolve and adapt. Further, by defining the quantity in mathematical terms, several measurement variables that are commonly reported can be clarified and unified. In this Commentary, we first detail the many types of motor function that are affected by the magnitude of yank generation, especially those related to time-constrained activities. These activities include escape, prey capture and postural responses to perturbations. Next, we describe the multi-scale structures and processes of the musculoskeletal system that influence yank and can be modified to increase yank generation. Lastly, we highlight recent studies showing that yank is represented in the sensory feedback system, and discuss how this information is used to enhance postural stability and facilitate recovery from postural perturbations. Overall, we promote an increased consideration of yank in studying biological motor and sensory systems.

Force encoding in muscle spindles during stretch of passive muscle.

Muscle spindle proprioceptive receptors play a primary role in encoding the effects of external mechanical perturbations to the body. During externally-imposed stretches of passive, i.e. electrically-quiescent, muscles, the instantaneous firing rates (IFRs) of muscle spindles are associated with characteristics of stretch such as length and velocity. However, even in passive muscle, there are history-dependent transients of muscle spindle firing that are not uniquely related to muscle length and velocity, nor reproduced by current muscle spindle models. These include acceleration-dependent initial bursts, increased dynamic response to stretch velocity if a muscle has been isometric, and rate relaxation, i.e., a decrease in tonic IFR when a muscle is held at a constant length after being stretched. We collected muscle spindle spike trains across a variety of muscle stretch kinematic conditions, including systematic changes in peak length, velocity, and acceleration. We demonstrate that muscle spindle primary afferents in passive muscle fire in direct relationship to muscle force-related variables, rather than length-related variables. Linear combinations of whole muscle-tendon force and the first time derivative of force (dF/dt) predict the entire time course of transient IFRs in muscle spindle Ia afferents during stretch (i.e., lengthening) of passive muscle, including the initial burst, the dynamic response to lengthening, and rate relaxation following lengthening. Similar to acceleration scaling found previously in postural responses to perturbations, initial burst amplitude scaled equally well to initial stretch acceleration or dF/dt, though later transients were only described by dF/dt. The transient increase in dF/dt at the onset of lengthening reflects muscle short-range stiffness due to cross-bridge dynamics. Our work demonstrates a critical role of muscle cross-bridge dynamics in history-dependent muscle spindle IFRs in passive muscle lengthening conditions relevant to the detection and sensorimotor response to mechanical perturbations to the body, and to previously-described history-dependence in perception of limb position.

Neuromuscular responses differ between slip-induced falls and recoveries in older adults.

How does the robust control of walking and balance break down during a fall? Here, as a first step in identifying the neuromuscular determinants of falls, we tested the hypothesis that falls and recoveries are characterized by differences in neuromuscular responses. Using muscle synergy analysis, conventional onset latencies, and peak activity, we identified differences in muscle coordination between older adults who fell and those who recovered from a laboratory-induced slip. We found that subjects who fell recruited fewer muscle synergies than those who recovered, suggesting a smaller motor repertoire. During slip trials, compared with subjects who recovered, subjects who fell had delayed knee flexor and extensor onset times in the leading/slip leg, as well as different muscle synergy structure involving those muscles. Therefore, the ability to coordinate muscle activity around the knee in a timely manner may be critical to avoiding falls from slips. Unique to subjects who fell during slip trials were greater bilateral (interlimb) muscle activation and the recruitment of a muscle synergy with excessive coactivation. These differences in muscle coordination between subjects who fell and those who recovered could not be explained by differences in gait-related variables at slip onset (i.e., initial motion state) or variations in slip difficulty, suggesting that differences in muscle coordination may reflect differences in neural control of movement rather than biomechanical constraints imposed by perturbation or initial walking mechanics. These results are the first step in determining the causation of falls from the perspective of muscle coordination. They suggest that there may be a neuromuscular basis for falls that could provide new insights into treatment and prevention. Further research comparing the muscle coordination and mechanics of falls and recoveries within subjects is necessary to establish the neuromuscular causation of falls. NEW & NOTEWORTHY: A central question relevant to the prevention of falls is: How does the robust control of walking and balance break down during a fall? Previous work has focused on muscle coordination during successful balance recoveries or the kinematics and kinetics of falls. Here, for the first time, we identified differences in the spatial and temporal coordination of muscles among older adults who fell and those who recovered from an unexpected slip.