Learning to stand with sensorimotor delays generalizes across directions and from hand to leg effectors.

Humans receive sensory information from the past, requiring the brain to overcome delays to perform daily motor skills such as standing upright. Because delays vary throughout the body and change over a lifetime, it would be advantageous to generalize learned control policies of balancing with delays across contexts. However, not all forms of learning generalize. Here, we use a robotic simulator to impose delays into human balance. When delays are imposed in one direction of standing, participants are initially unstable but relearn to balance by reducing the variability of their motor actions and transfer balance improvements to untrained directions. Upon returning to normal standing, aftereffects from learning are observed as small oscillations in control, yet they do not destabilize balance. Remarkably, when participants train to balance with delays using their hand, learning transfers to standing with the legs. Our findings establish that humans use experience to broadly update their neural control to balance with delays.

Using Galvanic Vestibular Stimulation to Induce Post-Roll Illusion in a Fixed-Base Flight Simulator.

INTRODUCTION: The illusions of head motion induced by galvanic vestibular stimulation (GVS) can be used to compromise flight performance of pilots in fixed-base simulators. However, the stimuli used in the majority of studies fail to mimic disorientation in realistic flight because they are independent from the simulated aircraft motion. This study investigated the potential of bilateral-bipolar GVS coupled to aircraft roll in a fixed-base simulator to mimic vestibular spatial disorientation illusions, specifically the "post-roll illusion" observed during flight.METHODS: There were 14 nonpilot subjects exposed to roll stimuli in a flight simulator operating in a fixed-base mode. GVS was delivered via carbon rubber electrodes on the mastoid processes. The electrical stimulus was driven by the high-pass filtered aircraft roll rate to mimic the semicircular canals' physiological response. The post-roll test scenarios excluded outside visual cues or instruments and required subjects to actively maintain a constant bank angle after an abrupt stop following a passive prolonged roll maneuver. The anticipated outcome was an overshot in roll elicited by the GVS signal.RESULTS: The responses across subjects showed large variability, with less than a third aligning with the post-roll illusion. Subjective ratings suggest that the high-pass filtered GVS stimuli were mild and did not induce a clear sense of roll direction. However, uncontrolled head movements during stimulation might have obscured the intended effects of GVS-evoked illusory head movements.CONCLUSION: The mild and transient GVS stimuli used in this study, together with the uncontrolled head movements, did not convincingly mimic the post-roll illusion.Houben MMJ, Stuldreher IV, Forbes PA, Groen EL. Using galvanic vestibular stimulation to induce post-roll illusion in a fixed-base flight simulator. Aerosp Med Hum Perform. 2024; 95(2):84-92.

The Neural Basis for Biased Behavioral Responses Evoked by Galvanic Vestibular Stimulation in Primates.

Noninvasive electrical stimulation of the vestibular system in humans has become an increasingly popular tool with a broad range of research and clinical applications. However, common assumptions regarding the neural mechanisms that underlie the activation of central vestibular pathways through such stimulation, known as galvanic vestibular stimulation (GVS), have not been directly tested. Here, we show that GVS is encoded by VIIIth nerve vestibular afferents with nonlinear dynamics that differ markedly from those predicted by current models. GVS produced asymmetric activation of both semicircular canal and otolith afferents to the onset versus offset and cathode versus anode of applied current, that in turn produced asymmetric eye movement responses in three awake-behaving male monkeys. Additionally, using computational methods, we demonstrate that the experimentally observed nonlinear neural response dynamics lead to an unexpected directional bias in the net population response when the information from both vestibular nerves is centrally integrated. Together our findings reveal the neural basis by which GVS activates the vestibular system, establish that neural response dynamics differ markedly from current predictions, and advance our mechanistic understanding of how asymmetric activation of the peripheral vestibular system alters vestibular function. We suggest that such nonlinear encoding is a general feature of neural processing that will be common across different noninvasive electrical stimulation approaches.SIGNIFICANCE STATEMENT Here, we show that the application of noninvasive electrical currents to the vestibular system (GVS) induces more complex responses than commonly assumed. We recorded vestibular afferent activity in macaque monkeys exposed to GVS using a setup analogous to human studies. GVS evoked notable asymmetries in irregular afferent responses to cathodal versus anodal currents. We developed a nonlinear model explaining these GVS-evoked afferent responses. Our model predicts that GVS induces directional biases in centrally integrated head motion signals and establishes electrical stimuli that recreate physiologically plausible sensations of motion. Altogether, our findings provide new insights into how GVS activates the vestibular system, which will be vital to advancing new clinical and biomedical applications.

Predicting occupant head displacements in evasive maneuvers; tuning and comparison of a rotational based and a translational based neck muscle controller.

Objective: Real-life car crashes are often preceded by an evasive maneuver, which can alter the occupant posture and muscle state. To simulate the occupant response in such maneuvers, human body models (HBMs) with active muscles have been developed. The aim of this study was to implement an omni-directional rotational head-neck muscle controller in the SAFER HBM and compare the bio-fidelity of the HBM with a rotational controller to the HBM with a translational controller, in simulations of evasive maneuvers. Methods: The rotational controller was developed using an axis-angle representation of head rotations, with x, y, and z components in the axis. Muscle load sharing was based on rotational direction in the simulation and muscle activity recorded in three volunteer experiments in these directions. The gains of the rotational and translational controller were tuned to minimize differences between translational and rotational head displacements of the HBM and volunteers in braking and lane change maneuvers using multi-objective optimizations. Bio-fidelity of the model with tuned controllers was evaluated objectively using CORrelation and Analysis (CORA). Results: The results indicated comparable performance for both controllers after tuning, with somewhat higher bio-fidelity for rotational kinematics with the translational controller. After tuning, good or excellent bio-fidelity was indicated for both controllers in the loading direction (forward in braking, and lateral in lane change), with CORA scores of 0.86-0.99 and 0.93-0.98 for the rotational and translational controllers, respectively. For rotational displacements, and translational displacements in the other directions, bio-fidelity ranged from poor to excellent, with slightly higher average CORA scores for the HBM with the translational controller in both braking and lane changing. Time-averaged muscle activity was within one standard deviation of time-averaged muscle activity from volunteers. Conclusion: Overall, the results show that when tuned, both the translational and rotational controllers can be used to predict the occupant response to an evasive maneuver, allowing for the inclusion of evasive maneuvers prior to a crash in evaluation of vehicle safety. The rotational controller shows potential in controlling omni-directional head displacements, but the translational controller outperformed the rotational controller. Thus, for now, the recommendation is to use the translational controller with tuned gains.

Age-related impairments and influence of visual feedback when learning to stand with unexpected sensorimotor delays.

Background: While standing upright, the brain must accurately accommodate for delays between sensory feedback and self-generated motor commands. Natural aging may limit adaptation to sensorimotor delays due to age-related decline in sensory acuity, neuromuscular capacity and cognitive function. This study examined balance learning in young and older adults as they stood with robot-induced sensorimotor delays. Methods: A cohort of community dwelling young (mean = 23.6 years, N = 20) and older adults (mean = 70.1 years, N = 20) participated in this balance learning study. Participants stood on a robotic balance simulator which was used to artificially impose a 250 ms delay into their control of standing. Young and older adults practiced to balance with the imposed delay either with or without visual feedback (i.e., eyes open or closed), resulting in four training groups. We assessed their balance behavior and performance (i.e., variability in postural sway and ability to maintain upright posture) before, during and after training. We further evaluated whether training benefits gained in one visual condition transferred to the untrained condition. Results: All participants, regardless of age or visual training condition, improved their balance performance through training to stand with the imposed delay. Compared to young adults, however, older adults had larger postural oscillations at all stages of the experiments, exhibited less relative learning to balance with the delay and had slower rates of balance improvement. Visual feedback was not required to learn to stand with the imposed delay, but it had a modest effect on the amount of time participants could remain upright. For all groups, balance improvements gained from training in one visual condition transferred to the untrained visual condition. Conclusion: Our study reveals that while advanced age partially impairs balance learning, the older nervous system maintains the ability to recalibrate motor control to stand with initially destabilizing sensorimotor delays under differing visual feedback conditions.

Unperceived motor actions of the balance system interfere with the causal attribution of self-motion.

The instability of human bipedalism demands that the brain accurately senses balancing self-motion and determines whether movements originate from self-generated actions or external disturbances. Here, we challenge the longstanding notion that this process relies on a single representation of the body and world to accurately perceive postural orientation and organize motor responses to control balance self-motion. Instead, we find that the conscious sense of balance can be distorted by the corrective control of upright standing. Using psychophysics, we quantified thresholds to imposed perturbations and balance responses evoking cues of self-motion that are (in)distinguishable from corrective balance actions. When standing immobile, participants clearly perceived imposed perturbations. Conversely, when freely balancing, participants often misattributed their own corrective responses as imposed motion because their balance system had detected, integrated, and responded to the perturbation in the absence of conscious perception. Importantly, this only occurred for perturbations encoded ambiguously with balance-correcting responses and that remained below the natural variability of ongoing balancing oscillations. These findings reveal that our balance system operates on its own sensorimotor principles that can interfere with causal attribution of our actions, and that our conscious sense of balance depends critically on the source and statistics of induced and self-generated motion cues.

Learning to stand with unexpected sensorimotor delays.

Human standing balance relies on self-motion estimates that are used by the nervous system to detect unexpected movements and enable corrective responses and adaptations in control. These estimates must accommodate for inherent delays in sensory and motor pathways. Here, we used a robotic system to simulate human standing about the ankles in the anteroposterior direction and impose sensorimotor delays into the control of balance. Imposed delays destabilized standing, but through training, participants adapted and re-learned to balance with the delays. Before training, imposed delays attenuated vestibular contributions to balance and triggered perceptions of unexpected standing motion, suggesting increased uncertainty in the internal self-motion estimates. After training, vestibular contributions partially returned to baseline levels and larger delays were needed to evoke perceptions of unexpected standing motion. Through learning, the nervous system accommodates balance sensorimotor delays by causally linking whole-body sensory feedback (initially interpreted as imposed motion) to self-generated balance motor commands.

When standing, neurons in the brain send signals to skeletal muscles so we can adjust our movements to stay upright based on the requirements from the surrounding environment. The long nerves needed to connect our brain, muscles and sensors lead to considerable time delays (up to 160 milliseconds) between sensing the environment and the generation of balance-correcting motor signals. Such delays must be accounted for by the brain so it can adjust how it regulates balance and compensates for unexpected movements. Aging and neurological disorders can lead to lengthened neural delays, which may result in poorer balance. Computer modeling suggests that we cannot maintain upright balance if delays are longer than 300-340 milliseconds. Directly assessing the destabilizing effects of increased delays in human volunteers can reveal how capable the brain is at adapting to this neurological change. Using a custom-designed robotic balance simulator, Rasman et al. tested whether healthy volunteers could learn to balance with delays longer than the predicted 300-340 millisecond limit. In a series of experiments, 46 healthy participants stood on the balance simulator which recreates the physical sensations and neural signals for balancing upright based on a computer-driven virtual reality. This unique device enabled Rasman et al. to artificially impose delays by increasing the time between the generation of motor signals and resulting whole-body motion. The experiments showed that lengthening the delay between motor signals and whole-body motion destabilized upright standing, decreased sensory contributions to balance and led to perceptions of unexpected movements. Over five days of training on the robotic balance simulator, participants regained their ability to balance, which was accompanied by recovered sensory contributions and perceptions of expected standing, despite the imposed delays. When a subset of participants was tested three months later, they were still able to compensate for the increased delay. The experiments show that the human brain can learn to overcome delays up to 560 milliseconds in the control of balance. This discovery may have important implications for people who develop balance problems because of older age or neurologic diseases like multiple sclerosis. It is possible that robot-assisted training therapies, like the one in this study, could help people overcome their balance impairments.

Stabilization demands of walking modulate the vestibular contributions to gait.

Stable walking relies critically on motor responses to signals of head motion provided by the vestibular system, which are phase-dependent and modulated differently within each muscle. It is unclear, however, whether these vestibular contributions also vary according to the stability of the walking task. Here we investigate how vestibular signals influence muscles relevant for gait stability (medial gastrocnemius, gluteus medius and erector spinae)-as well as their net effect on ground reaction forces-while humans walked normally, with mediolateral stabilization, wide and narrow steps. We estimated local dynamic stability of trunk kinematics together with coherence of electrical vestibular stimulation (EVS) with muscle activity and mediolateral ground reaction forces. Walking with external stabilization increased local dynamic stability and decreased coherence between EVS and all muscles/forces compared to normal walking. Wide-base walking also decreased vestibulomotor coherence, though local dynamic stability did not differ. Conversely, narrow-base walking increased local dynamic stability, but produced muscle-specific increases and decreases in coherence that resulted in a net increase in vestibulomotor coherence with ground reaction forces. Overall, our results show that while vestibular contributions may vary with gait stability, they more critically depend on the stabilization demands (i.e. control effort) needed to maintain a stable walking pattern.

Vestibular attenuation to random-waveform galvanic vestibular stimulation during standing and treadmill walking.

The ability to move and maintain posture is critically dependent on motion and orientation information provided by the vestibular system. When this system delivers noisy or erred information it can, in some cases, be attenuated through habituation. Here we investigate whether multiple mechanisms of attenuation act to decrease vestibular gain due to noise added using supra-threshold random-waveform galvanic vestibular stimulation (GVS). Forty-five participants completed one of three conditions. Each condition consisted of two 4-min standing periods with stimulation surrounding a 1-h period of either walking with stimulation, walking without stimulation, or sitting quietly. An instrumented treadmill recorded horizontal forces at the feet during standing and walking. We quantified response attenuation to GVS by comparing vestibular stimulus-horizontal force gain between conditions. First stimulus exposure caused an 18% decrease in gain during the first 40 s of standing. Attenuation recommenced only when subjects walked with stimulation, resulting in a 38% decrease in gain over 60 min that did not transfer to standing following walking. The disparity in attenuation dynamics and absent carry over between standing and walking suggests that two mechanisms of attenuation, one associated with first exposure to the stimulus and another that is task specific, may act to decrease vestibulomotor gain.

Absence of Nonlinear Coupling Between Electric Vestibular Stimulation and Evoked Forces During Standing Balance.

The vestibular system encodes motion and orientation of the head in space and is essential for negotiating in and interacting with the world. Recently, random waveform electric vestibular stimulation has become an increasingly common means of probing the vestibular system. However, many of the methods used to analyze the behavioral response to this type of stimulation assume a linear relationship between frequencies in the stimulus and its associated response. Here we examine this stimulus-response frequency linearity to determine the validity of this assumption. Forty-five university-aged subjects stood on a force-plate for 4 min while receiving vestibular stimulation. To determine the linearity of the stimulus-response relationship we calculated the cross-frequency power coupling between a 0 and 25 Hz bandwidth limited white noise stimulus and induced postural responses, as measured using the horizontal forces acting at the feet. Ultimately, we found that, on average, the postural response to a random stimulus is linear across stimulation frequencies. This result supports the use of analysis methods that depend on the assumption of stimulus-response frequency linearity, such as coherence and gain, which are commonly used to analyze the body's response to random waveform electric stimuli.

Variance based weighting of multisensory head rotation signals for verticality perception.

We tested the hypothesis that the brain uses a variance-based weighting of multisensory cues to estimate head rotation to perceive which way is up. The hypothesis predicts that the known bias in perceived vertical, which occurs when the visual environment is rotated in a vertical-plane, will be reduced by the addition of visual noise. Ten healthy participants sat head-fixed in front of a vertical screen presenting an annulus filled with coloured dots, which could rotate clockwise or counter-clockwise at six angular velocities (1, 2, 4, 6, 8, 16°/s) and with six levels of noise (0, 25, 50, 60, 75, 80%). Participants were required to keep a central bar vertical by rotating a hand-held dial. Continuous adjustments of the bar were required to counteract low-amplitude low-frequency noise that was added to the bar's angular position. During visual rotation, the bias in verticality perception increased over time to reach an asymptotic value. Increases in visual rotation velocity significantly increased this bias, while the addition of visual noise significantly reduced it, but did not affect perception of visual rotation velocity. The biasing phenomena were reproduced by a model that uses a multisensory variance-weighted estimate of head rotation velocity combined with a gravito-inertial acceleration signal (GIA) from the vestibular otoliths. The time-dependent asymptotic behaviour depends on internal feedback loops that act to pull the brain's estimate of gravity direction towards the GIA signal. The model's prediction of our experimental data furthers our understanding of the neural processes underlying human verticality perception.

Neural Mechanisms Underlying High-Frequency Vestibulocollic Reflexes In Humans And Monkeys.

The vestibulocollic reflex is a compensatory response that stabilizes the head in space. During everyday activities, this stabilizing response is evoked by head movements that typically span frequencies from 0 to 30 Hz. Transient head impacts, however, can elicit head movements with frequency content up to 300-400 Hz, raising the question whether vestibular pathways contribute to head stabilization at such high frequencies. Here, we first established that electrical vestibular stimulation modulates human neck motor unit (MU) activity at sinusoidal frequencies up to 300 Hz, but that sensitivity increases with frequency up to a low-pass cutoff of ∼70-80 Hz. To examine the neural substrates underlying the low-pass dynamics of vestibulocollic reflexes, we then recorded vestibular afferent responses to the same electrical stimuli in monkeys. Vestibular afferents also responded to electrical stimuli up to 300 Hz, but in contrast to MUs their sensitivity increased with frequency up to the afferent resting firing rate (∼100-150 Hz) and at higher frequencies afferents tended to phase-lock to the vestibular stimulus. This latter nonlinearity, however, was not transmitted to neck motoneurons, which instead showed minimal phase-locking that decreased at frequencies >75 Hz. Similar to human data, we validated that monkey muscle activity also exhibited low-pass filtered vestibulocollic reflex dynamics. Together, our results show that neck MUs are activated by high-frequency signals encoded by primary vestibular afferents, but undergo low-pass filtering at intermediate stages in the vestibulocollic reflex. These high-frequency contributions to vestibular-evoked neck muscle responses could stabilize the head during unexpected head transients.SIGNIFICANCE STATEMENT Vestibular-evoked neck muscle responses rely on accurate encoding and transmission of head movement information to stabilize the head in space. Unexpected transient events, such as head impacts, are likely to push the limits of these neural pathways since their high-frequency features (0-300 Hz) extend beyond the frequency bandwidth of head movements experienced during everyday activities (0-30 Hz). Here, we demonstrate that vestibular primary afferents encode high-frequency stimuli through frequency-dependent increases in sensitivity and phase-locking. When transmitted to neck motoneurons, these signals undergo low-pass filtering that limits neck motoneuron phase-locking in response to stimuli >75 Hz. This study provides insight into the neural dynamics producing vestibulocollic reflexes, which may respond to high-frequency transient events to stabilize the head.

Virtual signals of head rotation induce gravity-dependent inferences of linear acceleration.

KEY POINTS: Considerable debate exists regarding whether electrical vestibular stimuli encoded by vestibular afferents induce a net signal of linear acceleration, rotation or a combination of the two. This debate exists because an isolated signal of head rotation encoded by the vestibular afferents can cause perceptions of both linear and angular motion. We recorded participants' perceptions in different orientations relative to gravity and predicted their responses by modelling the effect of electrical vestibular stimuli on vestibular afferents and a current model of central vestibular processing. We show that, even if electrical vestibular stimuli are encoded as a net signal of head rotation, participants perceive both linear acceleration and rotation motions, provided the electrical stimulation-induced rotational vector has a component orthogonal to gravity. The emergence of a perception of linear acceleration from a single rotational input signal clarifies the origins of the neural mechanisms underlying electrical vestibular stimulation. ABSTRACT: Electrical vestibular stimulation (EVS) is an increasingly popular biomedical tool for generating sensations of virtual motion in humans, for which the mechanism of action is a topic of considerable debate. Contention surrounds whether the evoked vestibular afferent activity encodes a signal of net rotation and/or linear acceleration. Central processing of vestibular self-motion signals occurs through an internal representation of gravity that can lead to inferred linear accelerations in absence of a true inertial acceleration. Applying this model to virtual signals of rotation evoked by EVS, we predict that EVS will induce behaviours attributed to both angular and linear motion, depending on the head orientation relative to gravity. To demonstrate this, 18 subjects indicated their perceived motion during sinusoidal EVS when in one of four head/body positions orienting the gravitational vector parallel or orthogonal to the EVS rotation vector. During stimulation, participants selected one simulated movement from seven that corresponded best to what they perceived. Participants' responses in each orientation were predicted by a model combining the influence of EVS on vestibular afferents with known mechanisms of vestibular processing. When the EVS rotation vector had a component orthogonal to gravity, human perceptual responses were consistent with a non-zero central estimate of interaural or superior-inferior linear acceleration. The emergence of a perception of linear acceleration from a single rotational input signal clarifies the origins of the neural mechanisms underlying EVS, which has important implications for its use in human biomedical or sensory augmentation applications.

The Vestibular Drive for Balance Control Is Dependent on Multiple Sensory Cues of Gravity.

Vestibular signals, which encode head movement in space as well as orientation relative to gravity, contribute to the ongoing muscle activity required to stand. The strength of this vestibular contribution changes with the presence and quality of sensory cues of balance. Here we investigate whether the vestibular drive for standing balance also depends on different sensory cues of gravity by examining vestibular-evoked muscle responses when independently varying load and gravity conditions. Standing subjects were braced by a backboard structure that limited whole-body sway to the sagittal plane while load and vestibular cues of gravity were manipulated by: (a) loading the body downward at 1.5 and 2 times body weight (i.e., load cues), and/or (b) exposing subjects to brief periods (20 s) of micro- (<0.05 g) and hyper-gravity (∼1.8 g) during parabolic flights (i.e., vestibular cues). A stochastic electrical vestibular stimulus (0-25 Hz) delivered during these tasks evoked a vestibular-error signal and corrective muscles responses that were used to assess the vestibular drive to standing balance. With additional load, the magnitude of the vestibular-evoked muscle responses progressively increased, however, when these responses were normalized by the ongoing muscle activity, they decreased and plateaued at 1.5 times body weight. This demonstrates that the increased muscle activity necessary to stand with additional load is accompanied a proportionally smaller increase in vestibular input. This reduction in the relative vestibular contribution to balance was also observed when we varied the vestibular cues of gravity, but only during an absence (<0.05 g) and not an excess (∼1.8 g) of gravity when compared to conditions with normal 1 g gravity signals and equivalent load signals. Despite these changes, vestibular-evoked responses were observed in all conditions, indicating that vestibular cues of balance contribute to upright standing even in the near absence of a vestibular signal of gravity (i.e., micro-gravity). Overall, these experiments provide evidence that both load and vestibular cues of gravity influence the vestibular signal processing for the control of standing balance.

Neural substrates, dynamics and thresholds of galvanic vestibular stimulation in the behaving primate.

Galvanic vestibular stimulation (GVS) uses the external application of electrical current to selectively target the vestibular system in humans. Despite its recent popularity for the assessment/treatment of clinical conditions, exactly how this non-invasive tool activates the vestibular system remains an open question. Here we directly investigate single vestibular afferent responses to GVS applied to the mastoid processes of awake-behaving monkeys. Transmastoid GVS produces robust and parallel activation of both canal and otolith afferents. Notably, afferent activation increases with intrinsic neuronal variability resulting in constant GVS-evoked neuronal detection thresholds across all afferents. Additionally, afferent tuning differs for GVS versus natural self-motion stimulation. Using a stochastic model of repetitive activity in afferents, we largely explain the main features of GVS-evoked vestibular afferent dynamics. Taken together, our results reveal the neural substrate underlying transmastoid GVS-evoked perceptual, ocular and postural responses-information that is essential to advance GVS applicability for biomedical uses in humans.

Sensorimotor control of standing balance.

For most individuals, balancing upright is a simple task that requires little effort. The inherent difficulties associated with standing balance are not revealed until a pathology or injury impairs its control. Fundamentally, standing upright requires us to balance our unstable whole-body load within a small base of support. Small movements of the upright body are detected by various sensory receptors, all encoding these movements through their own coordinate system with specific dynamics. The balance controller filters, processes, and integrates sensory cues of body motion to produce an error signal between predicted and actual sensory consequences of balance-related movements. Compensatory motor commands are generated in response to this error to maintain upright standing. In the present review, we first briefly describe the biomechanics and sensor dynamics of standing balance. We further review sensorimotor and perceptual approaches revealing operational principles of the balance system, along with computational approaches that explore control processes underlying upright stance. Finally, we present robotic tools that virtualize the sensory consequences, biomechanics, and/or environmental factors inherent to the standing balance task. Throughout, we emphasize works that combine sensorimotor, computational, and/or robotics approaches to highlight the task dependency, multisensory cue combinations, cortical-subcortical contributions, and internal representations underpinning balance control.

Sensorimotor Manipulations of the Balance Control Loop-Beyond Imposed External Perturbations.

Standing balance relies on the integration of multiple sensory inputs to generate the motor commands required to stand. Mechanical and sensory perturbations elicit compensatory postural responses that are interpreted as a window into the sensorimotor processing involved in balance control. Popular methods involve imposed external perturbations that disrupt the control of quiet stance. Although these approaches provide critical information on how the balance system responds to external disturbances, the control mechanisms involved in correcting for these errors may differ from those responsible for the regulation of quiet standing. Alternative approaches use manipulations of the balance control loop to alter the relationship between sensory and motor cues. Coupled with imposed perturbations, these manipulations of the balance control loop provide unique opportunities to reveal how sensory and motor signals are integrated to control the upright body. In this review, we first explore imposed perturbation approaches that have been used to investigate the neural control of standing balance. We emphasize imposed perturbations that only elicit balance responses when the disturbing stimuli are relevant to the balance task. Next, we highlight manipulations of the balance control loop that, when carefully implemented, replicate and/or alter the sensorimotor dynamics of quiet standing. We further describe how manipulations of the balance control loop can be used in combination with imposed perturbations to characterize mechanistic principles underlying the control of standing balance. We propose that recent developments in the use of robotics and sensory manipulations will continue to enable new possibilities for simulating and/or altering the sensorimotor control of standing beyond compensatory responses to imposed external perturbations.

Electrical Vestibular Stimuli Evoke Robust Muscle Activity in Deep and Superficial Neck Muscles in Humans.

Neck muscle activity evoked by vestibular stimuli is a clinical measure for evaluating the function of the vestibular apparatus. Cervical vestibular-evoked myogenic potentials (cVEMP) are most commonly measured in the sternocleidomastoid muscle (and more recently the splenius capitis muscle) in response to air-conducted sound, bone-conducted vibration or electrical vestibular stimuli. It is currently unknown, however, whether and how other neck muscles respond to vestibular stimuli. Here we measured activity bilaterally in the sternocleidomastoid, splenius capitis, sternohyoid, semispinalis capitis, multifidus, rectus capitis posterior, and obliquus capitis inferior using indwelling electrodes in two subjects exposed to binaural bipolar electrical vestibular stimuli. All recorded neck muscles responded to the electrical vestibular stimuli (0-100 Hz) provided they were active. Furthermore, the evoked responses were inverted on either side of the neck, consistent with a coordinated contribution of all left-right muscle pairs acting as antagonists in response to the electrically-evoked vestibular error of head motion. Overall, our results suggest that, as previously observed in cat neck muscles, broad connections exist between the human vestibular system and neck motoneurons and highlight the need for future investigations to establish their neural connections.

Dynamic head-neck stabilization and modulation with perturbation bandwidth investigated using a multisegment neuromuscular model.

The human head-neck system requires continuous stabilization in the presence of gravity and trunk motion. We investigated contributions of the vestibulocollic reflex (VCR), the cervicocollic reflex (CCR), and neck muscle co-contraction to head-in-space and head-on-trunk stabilization, and investigated modulation of the stabilization strategy with the frequency content of trunk perturbations and the presence of visual feedback. We developed a multisegment cervical spine model where reflex gains (VCR and CCR) and neck muscle co-contraction were estimated by fitting the model to the response of young healthy subjects, seated and exposed to anterior-posterior trunk motion, with frequency content from 0.3 up to 1, 2, 4 and 8Hz, with and without visual feedback. The VCR contributed to head-in-space stabilization with a strong reduction of head rotation (<8Hz) and a moderate reduction of head translation (>1Hz). The CCR contributed to head-on-trunk stabilization with a reduction of head rotation and head translation relative to the trunk (<2Hz). The CCR also proved essential to stabilize the individual intervertebral joints and prevent neck buckling. Co-contraction was estimated to be of minor relevance. Control strategies employed during low bandwidth perturbations most effectively reduced head rotation and head relative displacement up to 3Hz while control strategies employed during high bandwidth perturbations reduced head global translation between 1 and 4Hz. This indicates a shift from minimizing head-on-trunk rotation and translation during low bandwidth perturbations to minimizing head-in-space translation during high bandwidth perturbations. Presence of visual feedback had limited effects suggesting increased usage of vestibular feedback.

Dynamic head-neck stabilization in cervical dystonia.

BACKGROUND: Effective sensorimotor integration is essential to modulate (adapt) neck stabilization strategies in response to varying tasks and disturbances. This study evaluates the hypothesis that relative to healthy controls cervical dystonia patients have an impaired ability to modulate afferent feedback for neck stabilization with changes in the frequency content of mechanical perturbations. METHODS: We applied anterior-posterior displacement perturbations (110s) on the torso of seated subjects, while recording head-neck kinematics and muscular activity. We compared low bandwidth (0.2-1.2Hz) and high bandwidth (0.2-8Hz) perturbations where our previous research showed a profound modulation of stabilization strategies in healthy subjects. Cervical dystonia patients and age matched controls performed two tasks: (1) maintain head forward posture and (2) allow dystonia to dictate head posture. FINDINGS: Patients and controls demonstrated similar kinematic and muscular responses. Patient modulation was similar to that of healthy controls (P>0.05); neck stiffness and afferent feedback decreased with high bandwidth perturbations. During the head forward task patients had an increased neck stiffness relative to controls (P<0.05), due to increased afferent feedback. INTERPRETATION: The unaffected modulation of head-neck stabilization (both kinematic and muscular) in patients with cervical dystonia does not support the hypothesis of impaired afferent feedback modulation for neck stabilization.