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.@en

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.@en

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.@en

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.@en

During standing balance, vestibular signals encode head movement and are transformed into coordinates that are relevant to maintaining upright posture of the whole body. This transformation must account for head-on-body orientation as well as the muscle actions generating the postural response. Here, we investigate whether this transformation is dependent upon a muscle’s ability to stabilize the body along the direction of a vestibular disturbance. Subjects were braced on top of a robotic balance system that simulated the mechanics of standing while being exposed to an electrical vestibular stimulus that evoked a craniocentric vestibular error of head roll. The balance system was limited to move in a single plane while the vestibular error direction was manipulated by having subjects rotate their head in yaw. Vestibular-evoked muscle responses were greatest when the vestibular error was aligned with the balance direction and decreased to zero as the two directions became orthogonal. This demonstrates that muscles respond only to the component of the error that is aligned with the balance direction and thus relevant to the balance task, not to the cumulative afferent activity, as expected for vestibulospinal reflex loops. When we reversed the relationship between balancing motor commands and associated vestibular sensory feedback, the direction of vestibular-evoked ankle compensatory responses was also reversed. This implies that the nervous system quickly reassociates new relationships between vestibular sensory signals and motor commands related to maintaining balance. These results indicate that vestibular-evoked muscle activity is a highly flexible balance response organized to compensate for vestibular disturbances.@en

During standing balance, vestibular signals encode head movement and are transformed into coordinates that are relevant to maintaining upright posture of the whole body. This transformation must account for head-on-body orientation as well as the muscle actions generating the postural response. Here, we investigate whether this transformation is dependent upon a muscle’s ability to stabilize the body along the direction of a vestibular disturbance. Subjects were braced on top of a robotic balance system that simulated the mechanics of standing while being exposed to an electrical vestibular stimulus that evoked a craniocentric vestibular error of head roll. The balance system was limited to move in a single plane while the vestibular error direction was manipulated by having subjects rotate their head in yaw. Vestibular-evoked muscle responses were greatest when the vestibular error was aligned with the balance direction and decreased to zero as the two directions became orthogonal. This demonstrates that muscles respond only to the component of the error that is aligned with the balance direction and thus relevant to the balance task, not to the cumulative afferent activity, as expected for vestibulospinal reflex loops. When we reversed the relationship between balancing motor commands and associated vestibular sensory feedback, the direction of vestibular-evoked ankle compensatory responses was also reversed. This implies that the nervous system quickly reassociates new relationships between vestibular sensory signals and motor commands related to maintaining balance. These results indicate that vestibular-evoked muscle activity is a highly flexible balance response organized to compensate for vestibular disturbances.@en

Human upright posture of both the head and body is facilitated by the CNS’s ability to integrate multiple sensory feedback signals, as well as its discernibility of the motor commands that maintain this stabilization. The vestibular organ in particular detects motion of the head-in-space, which is transformed according to on-going head and body orientation into appropriate motor responses. However, when motor commands do not contribute to the control of standing posture, and are incongruent with their expected sensory consequences, vestibulomuscular responses in the lower limb undergo unconscious suppression. In this study, we investigated whether vestibular response suppression occurs in neck muscles under conditions where the muscles are active but not engaged in a task to balance the head. In addition, we examined the effects of head orientation to identify spatial transformation of vestibular reflex responses. Eight subje cts were exposed to stochastic vestibular stimulation (0-75 Hz) in a seated condition while their head was either free or fixed, and rotated at either 0 or 60°. In head-free conditions, subjects were asked to rotate their head 60° to the left in order to activate agonist neck muscle pairs (sternocleidomastoid - SCM and splenius capitis - SPL). In headfixed conditions, subjects performed isometric neck muscle contractions in yaw at orientations of 0° and 60°, as well as flexion, extension and co-contraction at an orientation of 0°. Intramuscular EMG was collected bilaterally in SCM and SPL muscles. Muscle responses correlated to the in put stimuli were significant (P < 0.05) for all conditions provided the muscle was used in contraction. Neither muscle underwent the expected vestibulomuscular suppression when not engaged in the balance task (i.e. head-fixed). Nevertheless, the magnitude of the SPL responses decreased by 22% when the head was fixed whereas SCM responses were unaffected. The effect of head fixation only in SPL suggests differences in neural pathways across muscles, possibly via alternative pathways known to exist in the SPL from the well-established monosynaptic vestibulospinal inputs in SCM and SPL. For both muscles, the effect of orientation and force direction had no effect on muscles responses. Since the stimulation is fixed relative to the head, the same muscles are activated to respond to the input stimulus at both orientations and all force directions. These results indicate that the vestibular pathways connecting neck muscles are less susceptible to suppression than lower limb muscles, most likely because the monosynaptic inputs innervating them are subject to less central control.@en

Human upright posture of both the head and body is facilitated by the CNS’s ability to integrate multiple sensory feedback signals, as well as its discernibility of the motor commands that maintain this stabilization. The vestibular organ in particular detects motion of the head-in-space, which is transformed according to on-going head and body orientation into appropriate motor responses. However, when motor commands do not contribute to the control of standing posture, and are incongruent with their expected sensory consequences, vestibulomuscular responses in the lower limb undergo unconscious suppression. In this study, we investigated whether vestibular response suppression occurs in neck muscles under conditions where the muscles are active but not engaged in a task to balance the head. In addition, we examined the effects of head orientation to identify spatial transformation of vestibular reflex responses. Eight subje cts were exposed to stochastic vestibular stimulation (0-75 Hz) in a seated condition while their head was either free or fixed, and rotated at either 0 or 60°. In head-free conditions, subjects were asked to rotate their head 60° to the left in order to activate agonist neck muscle pairs (sternocleidomastoid - SCM and splenius capitis - SPL). In headfixed conditions, subjects performed isometric neck muscle contractions in yaw at orientations of 0° and 60°, as well as flexion, extension and co-contraction at an orientation of 0°. Intramuscular EMG was collected bilaterally in SCM and SPL muscles. Muscle responses correlated to the in put stimuli were significant (P < 0.05) for all conditions provided the muscle was used in contraction. Neither muscle underwent the expected vestibulomuscular suppression when not engaged in the balance task (i.e. head-fixed). Nevertheless, the magnitude of the SPL responses decreased by 22% when the head was fixed whereas SCM responses were unaffected. The effect of head fixation only in SPL suggests differences in neural pathways across muscles, possibly via alternative pathways known to exist in the SPL from the well-established monosynaptic vestibulospinal inputs in SCM and SPL. For both muscles, the effect of orientation and force direction had no effect on muscles responses. Since the stimulation is fixed relative to the head, the same muscles are activated to respond to the input stimulus at both orientations and all force directions. These results indicate that the vestibular pathways connecting neck muscles are less susceptible to suppression than lower limb muscles, most likely because the monosynaptic inputs innervating them are subject to less central control.@en

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.@en