Bilateral vestibular loss leads to active destabilization of balance during voluntary head turns in the standing cat

The purpose of this study was to determine the source of postural instability in labyrinthectomized cats during lateral head turns. Cats were trained to maintain the head in a forward orientation and then perform a rapid, large-amplitude head turn to left or right in yaw, while standing freely on a force platform. Head turns were biomechanically complex with the primary movement in the yaw plane accompanied by an ipsilateral ear-down roll and nose-down pitch. Cats used a strategy of pushing off by activating extensors of the contralateral forelimb while using all four limbs to produce a rotational moment of force about the vertical axis. After bilateral labyrinthectomy, the initial components of the head turn and accompanying postural responses were hypermetric, but otherwise similar to those produced before the lesion. However, near the time of peak yaw velocity, the lesioned cats produced an unexpected burst in extensors of the contralateral limbs that thrust the body to the ipsilateral side, leading to falls. This postural error was in the frontal (roll) plane, even though the primary movement was a rotation in the horizontal (yaw) plane. The response error decreased in amplitude with compensation but did not disappear. We conclude that lack of vestibular input results in active destabilization of balance during voluntary head movement. We postulate that the postural imbalance arises from the misperception that the trunk was rolling contralaterally, based on signals from neck proprioceptors in the absence of vestibular inputs.     

Spatial alignment of rotational and static tilt responses of vestibulospinal neurons in the cat.

The responses of vestibulospinal neurons to 0.5-Hz, whole-body rotations in three-dimensional space and static tilts of whole-body position were studied in decerebrate and alert cats. The neurons' spatial properties for earth-vertical rotations were characterized by maximum and minimum sensitivity vectors (R(max) and R(min)) in the cat's horizontal plane. The orientation of a neuron's R(max) was not consistently related to the orientation of its maximum sensitivity vector for static tilts (T(max)). The angular difference between R(max) and T(max) was widely distributed between 0 degrees and 150 degrees, and R(max) and T(max) were aligned (i.e., within 45 degrees of each other) for only 44% (14/32) of the neurons. The alignment of R(max) and T(max) was not correlated with the neuron's sensitivity to earth-horizontal rotations, or to the orientation of R(max) in the horizontal plane. In addition, the extent to which a neuron exhibited spatiotemporal convergent (STC) behavior in response to vertical rotations was independent of the angular difference between R(max) and T(max). This suggests that the high incidence of STC responses in our sample (56%) reflects not only canal-otolith convergence, but also the presence of static and dynamic otolith inputs with misaligned directionality. The responses of vestibulospinal neurons reflect a complex combination of static and dynamic vestibular inputs that may be required by postural reflexes that vary depending on head, trunk, and limb orientation, or on the frequency of stimulation.     

Neck,trunk and limb muscle responses during postural perturbations in humans

Summary This study examined the EMG onsets of leg, trunk, and neck muscles in 10 standing human subjects in response to support surface anterior and posterior translations, and to plantar and dorsiflexion rotations. The objective of the study was to test the hypothesis that the responses radiating upward from distal leg muscles represent part of a large ascending synergy encompassing axial muscles along the entire length of the body. If these responses are not ascending, then the muscles of the neck, and possibly the trunk, can be independently activated by vestibular, proprioceptive or visual inputs. We analysed the timing of postural muscle responses within and between body segments in order to determine whether they maintained a consistent temporal relationship under translational and rotational platform movement paradigms. Our results did not strongly support an ascending pattern of activation in all directions of platform perturbation. Temporal differences between activation patterns to platform perturbations in the forward or backward directions were revealed. In response to posterior platform translations we observed an ascending pattern of muscle responses along the extensor surface of the body. In addition, responses elicited in the neck flexor and abdominal muscles occurred as early as those of the stretched ankle muscles. This pattern of upward radiation from stretched ankle muscles was not as clear for anterior platform displacements, where early neck flexor muscle responses were observed during the ascending sequence on the flexor surface of the body. Platform rotations caused fewer responses in the neck and upper trunk muscles than translations, and all muscle responses occurred simultaneously rather than sequentially. Probable differences in the stimulation of vestibular and neck proprioceptive inputs and the mechanical demands of the rotation and translation paradigms are discussed.     

Somatosensory loss increases vestibulospinal sensitivity

To determine whether subjects with somatosensory loss show a compensatory increase in sensitivity to vestibular stimulation, we compared the amplitude of postural lean in response to four different intensities of bipolar galvanic stimulation in subjects with diabetic peripheral neuropathy (PNP) and age-matched control subjects. To determine whether healthy and neuropathic subjects show similar increases in sensitivity to galvanic vestibular stimulation when standing on unstable surfaces, both groups were exposed to galvanic stimulation while standing on a compliant foam surface. In these experiments, a 3-s pulse of galvanic current was administered to subjects standing with eyes closed and their heads turned toward one shoulder (anodal current on the forward mastoid). Anterior body tilt, as measured by center of foot pressure (CoP), increased proportionately with increasing galvanic vestibular stimulation intensity for all subjects. Subjects with peripheral neuropathy showed larger forward CoP displacement in response to galvanic stimulation than control subjects. The largest differences between neuropathy and control subjects were at the highest galvanic intensities, indicating an increased sensitivity to vestibular stimulation. Neuropathy subjects showed a larger increase in sensitivity to vestibular stimulation when standing on compliant foam than control subjects. The effect of galvanic stimulation was larger on the movement of the trunk segment in space than on the body's center of mass (CoM) angle, suggesting that the vestibular system acts to control trunk orientation rather than to control whole body posture. This study provides evidence for an increase in the sensitivity of the postural control system to vestibular stimulation when somatosensory information from the surface is disrupted either by peripheral neuropathy or by standing on an unstable surface. Simulations from a simple model of postural orientation incorporating feedback from the vestibular and somatosensory systems suggest that the increase in body lean in response to galvanic current in subjects with neuropathy could be reproduced only if central vestibular gain was increased when peripheral somatosensory gain was decreased. The larger effects of galvanic vestibular stimulation on the trunk than on the body's CoM suggest that the vestibular system may act to control postural orientation via control of the trunk in space.     

Incorporating voluntary unilateral knee flexion into balance corrections elicited by multi-directional perturbations to stance

Positive effects on lateral center of mass (CoM) shifts during balance recovery have been seen with voluntarily unilateral arm raising but not with voluntarily bilateral knee flexion. To determine whether unilateral voluntary knee movements can be effectively incorporated into balance corrections we perturbed the balance of 30 young healthy subjects using multi-directional rotations of the support surface while they simultaneously executed unilateral knee flexion. Combined pitch and roll rotations (7.5° and 60°/s) were presented randomly in six different directions. Subjects were tested in four stance conditions: balance perturbation only (PO); cued flexion of one knee only (KO); combined support surface rotation and cued (at rotation onset) flexion of the uphill knee, contralateral to tilt (CONT), or of the downhill knee, ipsilateral to tilt (IPS). Outcome measures were CoM motion and biomechanical and electromyography (EMG) responses of the legs, arms and trunk. Predicted measures (PO+KO) were compared with combined measures (CONT or IPS). Unilateral knee flexion of the uphill knee (CONT) provided considerable benefit in balance recovery. Subjects rotated their pelvis more to the uphill side than predicted. Downhill knee bending (IPS) also had a positive effect on CoM motion because of a greater than predicted simultaneous lateral shift of the pelvis uphill. KO leg muscle activity showed anticipatory postural activity (APA) with similar profiles to early balance correcting responses. Onsets of muscle responses and knee velocities were earlier for PO, CONT, and IPS compared to KO conditions. EMG response amplitudes for CONT and IPS conditions were generally not different from the PO condition and therefore smaller than predicted. Later stabilizing responses at 400 ms had activation amplitudes generally equal to those predicted from the PO+KO conditions. Our results suggest that because EMG patterns of anticipatory postural activity of voluntary unilateral knee flexion and early balance corrections have similar profiles, the CNS is easily able to incorporate voluntary activation associated with unilateral knee flexion into automatic postural responses. Furthermore, the effect on movement strategies appears to be non-linear. These findings may have important implications for the rehabilitation of balance deficits.     

Differences in coding provided by proprioceptive and vestibular sensory signals may contribute to lateral instability in vestibular loss subjects

One of the signatures of balance deficits observed in vestibular loss subjects is the greater instability in the roll compared to pitch planes. Directional differences in the timing and strengths of vestibular and proprioceptive sensory signals between roll and pitch may lead to a greater miscalculation of roll than pitch motion of the body in space when vestibular input is absent. For this reason, we compared the timing and amplitude of vestibular information, (observable in stimulus-induced head accelerations when subjects are tilted in different directions), with that of proprioceptive information caused by stimulus induced rotations of ankle and hip joints [observable as short latency (SL) stretch responses in leg and trunk muscle EMG activity]. We attempted to link the possible mode of sensory interaction with the deficits in balance control. Six subjects with bilaterally absent vestibular function and 12 age-matched controls were perturbed, while standing, in 8 directions of pitch and roll support surface rotation in random order. Body segment movements were recorded with a motion analysis system, head accelerations with accelerometers, and muscle activity with surface EMG. Information on stimulus pitch motion was available sequentially. Pitch movements of the support surface were best coded in amplitude by ankle rotation velocity, and by head vertical linear acceleration, which started at 13 ms after the onset of ankle rotation. EMG SL reflex responses in soleus with onsets at 46 ms provided a distal proprioceptive correlate to the pitch motion. Roll information on the stimulus was available simultaneously. Hip adduction and lumbo-sacral angular velocity were represented neurally as directionally specific short latency stretch and unloading reflexes in the bilateral gluteus medius muscles and paraspinal muscles with onsets at 28 ms. Roll angular accelerations of the head coded roll amplitude and direction at the same time (31 ms). Significant differences in amplitude coding between vestibular loss subjects and controls were only observed as a weaker coding between stimulus motion and head roll and head lateral linear accelerations. The absence of vestibular inputs in vestibular loss subjects led to characteristic larger trunk in motion in roll in the direction of tilt compared to pitch with respect to controls. This was preceded by less uphill flexion and no downhill extension of the legs in vestibular loss subjects. Downhill arm abduction responses were also greater. These results suggest that in man vestibular inputs provide critical information necessary for the appropriate modulation of roll balance-correcting responses in the form of stabilising knee and arm movements. The simultaneous arrival of roll sensory information in controls may indicate that proprioceptive and vestibular signals can only be interpreted correctly when both are present. Thus, roll proprioceptive information may be interpreted inaccurately in vestibular loss subjects, leading to an incorrect perception of body tilt and insufficient uphill knee flexion, especially as cervico-collic signals appear less reliable in these subjects as an alternative sensory input.     

Noncommutative updating of perceived self-orientation in three dimensions

After whole body rotations around an earth-vertical axis in darkness, subjects can indicate their orientation in space with respect to their initial orientation reasonably well. This is possible because the brain is able to mathematically integrate self-velocity information provided by the vestibular system to obtain self-orientation, a process called path integration. For rotations around multiple axes, however, computations are more demanding to accurately update self-orientation with respect to space. In such a case, simple integration is no longer sufficient because of the noncommutativity of rotations. We investigated whether such updating is possible after three-dimensional whole body rotations and whether the noncommutativity of three-dimensional rotations is taken into account. The ability of ten subjects to indicate their spatial orientation in the earth-horizontal plane was tested after different rotational paths from upright to supine positions. Initial and final orientations of the subjects were the same in all cases, but the paths taken were different, and so were the angular velocities sensed by the vestibular system. The results show that seven of the ten subjects could consistently indicate their final orientation within the earth-horizontal plane. Thus perceived final orientation was independent of the path taken, i.e., the noncommutativity of rotations was taken into account.     

Processing of vestibular inputs by the medullary lateral tegmental field of conscious cats: implications for generation of motion sickness

The dorsolateral reticular formation of the caudal medulla, the lateral tegmental field (LTF), participates in generating vomiting. LTF neurons exhibited complex responses to vestibular stimulation in decerebrate cats, indicating that they received converging inputs from a variety of labyrinthine receptors. Such a convergence pattern of vestibular inputs is appropriate for a brain region that participates in generating motion sickness. Since responses of brainstem neurons to vestibular stimulation can differ between decerebrate and conscious animals, the current study examined the effects of whole-body rotations in vertical planes on the activity of LTF neurons in conscious felines. Wobble stimuli, fixed-amplitude tilts, the direction of which moves around the animal at a constant speed, were used to determine the response vector orientation, and also to ascertain whether neurons had spatial–temporal convergence (STC) behavior (which is due to the convergence of vestibular inputs with different spatial and temporal properties). The proportion of LTF neurons with STC behavior in conscious animals (25 %) was similar to that in decerebrate cats. Far fewer neurons in other regions of the feline brainstem had STC behavior, confirming findings that many LTF neurons receive converging inputs from a variety of labyrinthine receptors. However, responses to vertical plane vestibular stimulation were considerably different in decerebrate and conscious felines for LTF neurons lacking STC behavior. In decerebrate cats, most LTF neurons had graviceptive responses to rotations, similar to those of otolith organ afferents. However, in conscious animals, the response properties were similar to those of semicircular canal afferents. These differences show that higher centers of the brain that are removed during decerebration regulate the labyrinthine inputs relayed to the LTF, either by gating connections in the brainstem or by conveying vestibular inputs directly to the region.     

Vestibular and somatosensory contributions to responses to head and body displacements in stance

The relative contribution of vestibular and somatosensory information to triggering postural responses to external body displacements may depend on the task and on the availability of sensory information in each system. To separate the contribution of vestibular and neck mechanisms to the stabilization of upright stance from that of lower body somatosensory mechanisms, responses to displacements of the head alone were compared with responses to displacements of the head and body, in both healthy subjects and in patients with profound bilateral vestibular loss. Head displacements were induced by translating two 1-kg weights suspended on either side of the head at the level of the mastoid bone, and body displacements were induced translating the support surface. Head displacements resulted in maximum forward and backward head accelerations similar to those resulting from body displacements, but were not accompanied by significant center of body mass, ankle, knee, or hip motions. We tested the effect of disrupting somatosensory information from the legs on postural responses to head or body displacements by sway-referencing the support surface. The subjects' eyes were closed during all testing to eliminate the effects of vision. Results showed that head displacements alone can trigger medium latency (48–84 ms) responses in the same leg and trunk muscles as body displacements. Nevertheless, it is unlikely that vestibular signals alone normally trigger directionally specific postural responses to support surface translations in standing humans because: (1) initial head accelerations resulting from body and head displacements were in opposite directions, but were associated with activation of the same leg and trunk postural muscles; (2) muscle responses to displacements of the head alone were only one third of the amplitude of responses to body displacements with equivalent maximum head accelerations; and (3) patients with profound bilateral vestibular loss showed patterns and latencies of leg and trunk muscle responses to body displacements similar to those of healthy subjects. Altering somatosensory information, by sway-referencing the support surface, increased the amplitude of ankle muscle activation to head displacements and reduced the amplitude of ankle muscle activation to body displacements, suggesting context-specific reweighting of vestibular and somatosensory inputs for posture. In contrast to responses to body displacements, responses to direct head displacements appear to depend upon a vestibulospinal trigger, since trunk and leg muscle responses to head displacements were absent in patients who had lost vestibular function as adults. Patients who lost vestibular function as infants, however, had near normal trunk and leg response to head displacements, suggesting a substitution of upper trunk and neck somatosensory inputs for missing vestibular inputs during development.     

Response of vestibular neurons to head rotations in vertical planes. II. Response to neck stimulation and vestibular-neck interaction

1. We have studied the responses of neurons in the lateral and descending vestibular nuclei of decerebrate cats to stimulation of neck receptors, produced by rotating the body in vertical planes with the head stationary. The responses to such neck stimulation were compared with the responses to vestibular stimulation produced by whole-body tilt, described in the preceding paper. 2. After determining the optimal vertical plane of neck rotation (response vector orientation), the dynamics of the neck response were studied over a frequency range of 0.02-1 Hz. The majority of the neurons were excited by neck rotations that brought the chin toward the ipsilateral side; most neurons responded better to roll than to pitch rotations. The typical neck response showed a low-frequency phase lead of 30 degrees, increasing to 60 degrees at higher frequencies, and a gain that increased about threefold per decade. 3. Neck input was found in about one-half of the vestibular-responsive neurons tested with vertical rotations. The presence of a neck response was correlated with the predominant vestibular input to these neurons; neck input was most prevalent on neurons with vestibular vector orientations near roll and receiving convergent vestibular input, either input from both ipsilateral vertical semicircular canals, or from canals plus the otolith organs. 4. Neurons with both vestibular and neck responses tend to have the respective orientation vectors pointing in opposite directions, i.e., a head tilt that produces an excitatory vestibular response would produce an inhibitory neck response. In addition, the gain components of these responses were similar. These results suggest that during head movements on a stationary body, these opposing neck and vestibular inputs will cancel each other. 5. Cancellation was observed in 12 out of 27 neurons tested with head rotation in the mid-frequency range. For most of the remaining neurons, the response to such a combined stimulus was greatly attenuated: the vestibular and neck interaction was largely antagonistic. 6. Neck response dynamics were similar to those of the vestibular input in many neurons, permitting cancellation to take place over a wide range of stimulus frequencies. Another pattern of interaction, observed in some neurons with canal input, produced responses to head rotation that had a relatively constant gain and remained in phase with position over the entire frequency range; such neurons possibly code head position in space.     

Effects of lesion of the interstitial nucleus of Cajal on vestibular nuclear neurons activated by vertical vestibular stimulation

Summary 1. Experiments were performed in cats anesthetized with nitrous oxide to study the effects of INC lesions on responses of vestibular nuclear neurons during sinusoidal rotations of the head in the vertical (pitch) plane. Responses of neurons in the INC region were recorded during pitch rotations at 0.15 Hz. A great majority of these neurons did not respond to static pitch tilts, and they seemed to respond either to anterior or to posterior semicircular canal inputs with a peak phase lag of 140 deg (re head acceleration). 2. Responses of vestibular nuclei neurons in intact cats were recorded during pitch rotations at the same frequency (0.15 Hz). Neurons that seemed to respond to vertical semicircular canal inputs showed peak phase lags of 90 deg relative to head acceleration, whereas neurons that responded to static pitch tilts showed peak phase shifts near 0 deg. These results indicate that responses of neurons in the INC region lag those of vestibular neurons by about 50 deg, suggesting that the former neurons possess a phase-lagging (i.e. integrated) vestibular signal. 3. Responses of vestibular neurons in cats that had received electrolytic lesions of bilateral INCs 1–2 weeks previously were recorded during pitch rotations at the same frequency (0.15 Hz). Neurons that presumably responded to vertical semicircular canal inputs showed a peak phase lag of 60 deg relative to head acceleration, a significant decrease of the phase lag compared to normal, whereas responses near 0 deg were unchanged. Gain values of individual cells also significantly dropped from 2.07 ± 0.67 spikes · s⁻¹/deg · s⁻²2 (mean ± SD; normal cats) to 1.27 ± 0.68 spikes · s⁻²/deg · s⁻² (INC lesioned cats) at 0.15 Hz. When responses of vestibular neurons were studied during pitch rotations in the range of 0.044–0.49 Hz in these cats, a large decrease of the phase lag was observed at lower frequencies, whereas the slopes of phase lag curves of vestibular neurons in intact cats were rather flat. 4. Procaine infusion into the bilateral INCs not only resulted in a decrease of 20–50 deg in the phase lag in responses of vestibular neurons that had lagged head acceleration by 90–140 deg before procaine infusion, but also dropped the gain of the response to rotation by an average of 31%, whereas responses of neurons that had showed phase shifts near 0 deg were not influenced consistently. Simultaneous recording of the vestibular neurons and the vertical vestibuloocular reflex (VOR) indicated that the phase advance and gain drop of vestibular neurons occurred earlier than those of the VOR. These results exclude the possibility that the change in dynamic response of vestibular neurons after procaine infusion is due to depression of general brain stem activity that may lead to the phase advance of the VOR, and suggest that the decrease of the phase lag and gain drop in responses of the vestibular neurons was caused by removal of the phase-lagging, feedback signal coming from the INC to the vestibular nuclei.     

Responses of vestibular nucleus neurons to tilt following chronic bilateral removal of vestibular inputs

Recordings were made from the vestibular nuclei of decerebrate cats that had undergone a combined bilateral labyrinthectomy and vestibular neurectomy 49-103 days previously and allowed to recover. Responses of neurons were recorded to tilts in multiple vertical planes at frequencies ranging from 0.05 to 1 Hz and amplitudes up to 15 degrees. Many spontaneously active neurons were present in the vestibular nuclei; the mean firing rate of these cells was 43 +/- 5 (SEM) spikes/s. The spontaneous firing of the neurons was irregular: the coefficient of variation was 0.86 +/- 0.14. The firing of 27% of the neurons was modulated by tilt. The plane of tilt that elicited the maximal response was typically within 25 degrees of pitch. The response gain was approximately 1 spikes/s/degree across stimulus frequencies. The response phase was near stimulus position at low frequencies, and lagged position slightly at higher frequencies (average of 35 +/- 9 degrees at 0.5 Hz). The source of the inputs eliciting modulation of vestibular nucleus activity during tilt in animals lacking vestibular inputs is unknown, but could include receptors in the trunk or limbs. These findings show that activation of vestibular nucleus neurons during vertical rotations is not exclusively the result of labyrinthine inputs, and suggest that limb and trunk inputs may play an important role in graviception and modulating vestibular-elicited reflexes.     

Spatial and temporal response properties of the vestibulocollic reflex in decerebrate cats

Vestibulocollic reflex responses of several neck muscles in decerebrate cats were studied during angular rotations of the whole body in a large number of vertical and horizontal rotation planes, at frequencies from 0.07 to 1.6 Hz. Vestibulocollic responses were compared to eye muscle and forelimb muscle vestibular responses. Electromyographic activity was recorded by fine wires inserted in biventer cervicis, complexus, longus capitis, obliquus capitis inferior, occipitoscapularis, rectus capitis major, splenius, lateral rectus, and triceps brachii. At frequencies of approximately 0.5 Hz and above, neck muscle electromyographic response gains were sinusoidal functions of stimulus orientation within a set of vertical or horizontal planes, and a muscle's response phase remained constant across rotation planes, or reversed by 180 degrees. Response patterns at high frequencies were consistent with vestibulocollic reflex activation by semicircular canals through brain circuitry that modifies canal dynamics. At frequencies of approximately 0.5 Hz and above, the stimulus orientation in which a given neck muscle's response was maximal remained nearly constant across frequencies. Thus, we used responses to rotations at high frequencies to calculate axes of maximal response of each muscle in three-dimensional space. Lateral rectus, obliquus, and to a lesser extent, splenius and longus capitus were activated predominantly by horizontal rotations. Biventer was activated predominantly by pitch, triceps predominantly by roll, and complexus, occipitoscapularis, and rectus major significantly excited by rotations in all three coordinate planes. In some cases, at frequencies less than 0.5 Hz, neck muscle response phase varied depending on the vertical plane in which the cat was rotated, and the optimal response plane was poorly defined and varied with frequency. These responses indicated that, at some frequencies, neck muscle activity can result from summation of inputs with differing spatial orientation and dynamics (spatial-temporal convergence). Differences between responses to vertical and horizontal rotations suggested that low-frequency spatial-temporal convergence behavior of the vestibulocollic reflex during vertical rotations was due to convergent semicircular canal and otolith receptor inputs.(ABSTRACT TRUNCATED AT 400 WORDS)     

Responses of caudal vestibular nucleus neurons of conscious cats to rotations in vertical planes, before and after a bilateral vestibular neurectomy

Although many previous experiments have considered the responses of vestibular nucleus neurons to rotations and translations of the head, little data are available regarding cells in the caudalmost portions of the vestibular nuclei (CVN), which mediate vestibulo-autonomic responses among other functions. This study examined the responses of CVN neurons of conscious cats to rotations in vertical planes, both before and after a bilateral vestibular neurectomy. None of the units included in the data sample had eye movement-related activity. In labyrinth-intact animals, some CVN neurons (22%) exhibited graviceptive responses consistent with inputs from otolith organs, but most (55%) had dynamic responses with phases synchronized with stimulus velocity. Furthermore, the large majority of CVN neurons had response vector orientations that were aligned either near the roll or vertical canal planes, and only 18% of cells were preferentially activated by pitch rotations. Sustained head-up rotations of the body provide challenges to the cardiovascular system and breathing, and thus the response dynamics of the large majority of CVN neurons were dissimilar to those of posturally-related autonomic reflexes. These data suggest that vestibular influences on autonomic control mediated by the CVN are more complex than previously envisioned, and likely involve considerable processing and integration of signals by brainstem regions involved in cardiovascular and respiratory regulation. Following a bilateral vestibular neurectomy, CVN neurons regained spontaneous activity within 24 h, and a very few neurons (<10%) responded to vertical tilts <15° in amplitude. These findings indicate that nonlabyrinthine inputs are likely important in sustaining the activity of CVN neurons; thus, these inputs may play a role in functional recovery following peripheral vestibular lesions.     

Vestibular influences on human postural control in combinations of pitch and roll planes reveal differences in spatiotemporal processing

The present study examined the influence of bilateral peripheral vestibular loss (BVL) in humans on postural responses to multidirectional surface rotations in the pitch and roll planes. Specifically, we examined the effects of vestibular loss on the directional sensitivity, timing, and amplitude of early stretch, balance correcting, and stabilizing reactions in postural leg and trunk muscles as well as changes in ankle torque and trunk angular velocity following multidirectional rotational perturbations of the support surface. Fourteen normal healthy adults and five BVL patients stood on a dual axis rotating platform which rotated 7.5° at 50°/s through eight different directions of pitch and roll combinations separated by 45°. Directions were randomized within a series of 44 perturbation trials which were presented first with eyes open, followed by a second series of trials with eyes closed. Vestibular loss did not influence the range of activation or direction of maximum sensitivity for balance correcting responses (120–220 ms). Response onsets at approximately 120 ms were normal in tibialis anterior (TA), soleus (SOL), paraspinals (PARAS), or quadriceps muscles. Only SOL muscle activity demonstrated a 38- to 45-ms delay for combinations of forward (toe-down) and roll perturbations in BVL patients. The amplitude of balance correcting responses in leg muscles between 120 and 220 ms was, with one exception, severely reduced in BVL patients for eyes open and eyes closed conditions. SOL responses were decreased bilaterally for toe-up and toe-down perturbations, but more significantly reduced in the downhill (load-bearing) leg for combined roll and pitch perturbations. TA was significantly reduced bilaterally for toe-up perturbations, and in the downhill leg for backward roll perturbations. Forward perturbations, however, elicited significantly larger TA activity in BVL between 120 and 220 ms compared to normals, which would act to further destabilize the body. As a result of these changes in response amplitudes, BVL patients had reduced balance correcting ankle torque between 160 and 260 ms and increased torque between 280 and 380 ms compared to normals. There were no differences in the orientation of the resultant ankle torque vectors between BVL and normals, both of which were oriented primarily along the pitch plane. For combinations of backward (toe-up) and roll perturbations BVL patients had larger balance correcting and stabilizing reactions (between 350 and 700 ms) in PARAS than normals and these corresponded to excessive trunk pitch and roll velocities. During roll perturbations, trunk velocities in BVL subjects after 200 ms were directed along directions different from those of normals. Furthermore, roll instabilities appeared later than those of pitch particularly for backward roll perturbations. The results of the study show that combinations of roll and pitch surface rotations yield important spatiotemporal information, especially with respect to trunk response strategies changed by BVL which are not revealed by pitch plane perturbations alone. Our results indicate that vestibular influences are earlier for the pitch plane and are directed to leg muscles, whereas roll control is later and focused on trunk muscles. Electronic Publication     

Weight support and balance during perturbed stance in the chronic spinal cat

The intact cat maintains balance during unexpected disturbances of stance through automatic postural responses that are stereotyped and rapid. The extent to which the chronic spinal cat can maintain balance during stance is unclear, and there have been no quantitative studies that examined this question directly. This study examined whether the isolated lumbosacral cord of the chronic spinal cat can generate automatic postural responses in the hindlimbs during translation of the support surface. Responses to 16 directions of linear translation in the horizontal plane were quantified before and after spinalization at the T(6) level in terms of forces exerted by each paw against the support, motion of the body segments (kinematics), and electromyographic (EMG) activity. After spinalization, the cats were trained on a daily basis to stand on the force platform, and all four cats were able to support their full body weight. The cats usually required assistance for balance or stability in the horizontal plane, which was provided by an experimenter exerting gentle lateral force at the level of the hips. Three of the four animals could maintain independent stance for a brief period (10 s) after the experimenter stabilized them. The fourth cat maintained weight support but always required assistance with balance. Perturbations were delivered during the periods of independent stance in three cats and during assisted stance in the fourth. A response to translation in the spinal cats was observed only in those muscles that were tonically active to maintain stance and never in the flexors. Moreover, latencies were increased and amplitudes of activation were diminished compared with control. Nevertheless, flexors and extensors were recruited easily during behaviors such as paw shake and stepping. It is concluded that centers above the lumbosacral cord are required for the full elaboration of automatic postural responses. Although the spinal cat can achieve good weight support, it cannot maintain balance during stance except for brief periods and within narrow limits. This limited stability is probably achieved through spinal reflex mechanisms and the stiffness characteristics of the tonically active extensors.     

Parallel processing of multisensory information concerning self-motion

Summary Cats trained to stand on a platform exhibit postural responses to dynamic tilting that appear to be based on an internal reference model of body geometry and the environment rather than directly on sensory inputs, as in a classical reflex chain. The data presented show an independent control of global variables of limb geometry, the length and the orientation, resulting from a parallel processing of multisensory inputs into separate central representations of body tilt. Limb length and orientation changes have completely different response dynamics and can be decoupled by appropriate manipulation of sensory information about self-motion.     

Postural coactivation and adaptation in the sway stabilizing responses of normals and patients with bilateral vestibular deficit

Summary The experiments were designed to test two hypotheses and their corollaries: 1. That adaptation of EMG responses to support surface rotations is due to a decrease in the gain of proprioceptively triggered long-loop stretch reflexes (Nashner 1976), and that the adaptation is dependent on a normally functioning vestibular system (Nashner et al. 1982); 2. That EMG responses to rotations are generated primarily by vestibulo-spinal reflexes triggered by head accelerations (Allum and Pfaltz 1985) and comprise a coactivation of opposing leg muscles (Allum and Büdingen 1979). Adaptation with successive dorsi-flexive rotations of the support surface was investigated in the EMG responses of the ankle muscles, soleus (SOL) and tibialis anterior (TA), as well as the neck muscles, trapezius (TRAP) and splenius capitis (SPLEN CAP), both for normal subjects and for patients with bilateral peripheral vestibular deficit. Both normals and patients who first received the stimulus with their eyes open demonstrated decreasing activation at medium latency (ML), that is, with an onset at about 125 ms, and long latency (LL) responses with an onset ca 200 ms. This was the case for both ankle and neck muscles when the EMG response areas for the first 3 and second 7 of 10 trials were compared. Ankle muscle responses in the patients were diminished in area with respect to normals both with the eyes open and with the eyes closed. Ankle torque recordings from the patients were also smaller in amplitude, and these attenuated differently from normal torque responses. Functional coupling of the opposing ML and LL SOL and TA muscle responses was confirmed by the nearly coincident onset times and significantly correlated EMG response areas. At ML, ankle torque was highly correlated with TA activity when the influence of SOL was controlled. At LL, SOL activity was highly correlated with torque when the influence of TA was controlled. The delay of torque adaptation beyond the period of ML activity in normals, but not in the patients was attributed to the proportionally balanced coactivated muscle patterns producing a consistent force output and level of stability in normals. The results indicate that the adaptation in EMG response amplitudes during a sway stabilisation task is not dependent on a normally functioning vestibular system nor on visual inputs but rather appears to be due to a generalized habituation in the postural control system. Evidence against a change in the gain of proprioceptively triggered long loop reflexes being responsible for adaptation is based on the fact that the adaptation is not restricted to the stretched SOL muscle but includes its agonist, TA, and that the adaptation is not local but also occurs in neck muscles. The results supported the hypothesis that postural reflexes to support surface rotations may well be triggered by stretch reflexes in the lower leg or neck muscles, however, their amplitude modulation is overwhelmingly under the control of vestibulo-spinal signals.     

Neuronal response sensitivity to bidirectional off-vertical axis rotations: a dimension of imbalance in the bilateral vestibular nuclei of cats after unilateral labyrinthectomy

In decerebrate cats after acute hemilabyrinthectomy, the response sensitivity of extracellularly recorded vestibular nuclear neurons on the lesioned and labyrinth-intact sides were examined quantitatively during constant velocity off-vertical axis rotations with an aim to elucidate the functional contribution of otolithic inputs to the ipsilateral and contralateral vestibular nuclei. The bidirectional response sensitivity, delta, was determined as the ratio of the gain during clockwise to that during counterclockwise rotations. A continuum of response sensitivity was identified: one-dimensional neurons showed symmetrically bidirectional response patterns, while two-dimensional neurons showed asymmetrically bidirectional patterns that in some cases approached unidirectional patterns with change in velocity. The proportion of two-dimensional neurons was significantly increased after acute hemilabyrinthectomy. Two-dimensional neurons that responded only to one direction of rotation in at least one of the velocities tested were described as unidirectional neurons. This unidirectional response pattern was observed in one-third of the entire neuronal population studied, but not in cats with both labyrinths intact, thus suggesting that such prominent broadly tuned responses are normally masked by converging otolithic inputs from the contralateral side. These neurons were found in higher proportion on the lesioned side than on the labyrinth-intact side. Among the 70% of unidirectional neurons that exhibited bidirectional response at some velocities and unidirectional response at others, prominent shifts in delta values (i.e. between 0/infinity and finite values) with velocity can be computed for each neuron. The shifts in delta values correlated with large shifts in the response dynamics and spatial orientation as the response pattern changed with velocity. The response orientations of the unidirectional neurons pointed in all directions on the horizontal plane. When all the two-dimensional neurons (i.e. both the unidirectionally and bidirectionally responsive ones) were pooled, imbalances in the distribution of the response orientations and in response gain were found between the ipsilateral-side-down/head-down half-circle and the contralateral-side-down/head-up half-circle on the labyrinth-intact side, but not on the lesioned side. These results, derived from spatiotemporal processing of gravitational signals, reveal a novel dimension of imbalance between neuronal populations in the two vestibular nuclear complexes after acute lesion of one labyrinth. This feature would provide, on the one hand, deranged cues of spatial orientation and direction during slow head excursions and, on the other, a framework for the dynamic behavioral deficits associated with hemilabyrinthectomy.     

Properties of cerebellar fastigial neurons during translation, rotation, and eye movements

The most medial of the deep cerebellar nuclei, the fastigial nucleus (FN), receives sensory vestibular information and direct inhibition from the cerebellar vermis. We investigated the signal processing in the primate FN by recording single-unit activities during translational motion, rotational motion, and eye movements. Firing rate modulation during horizontal plane translation in the absence of eye movements was observed in all non-eye-movement-sensitive cells and 26% of the pursuit eye-movement-sensitive neurons in the caudal FN. Many non-eye-movement-sensitive cells recorded in the rostral FN of three fascicularis monkeys exhibited convergence of signals from both the otolith organs and the semicircular canals. At low frequencies of translation, the majority of these rostral FN cells changed their firing rates in phase with head velocity rather than linear acceleration. As frequency increased, FN vestibular neurons exhibited a wide range of response dynamics with most cells being characterized by increasing phase leads as a function of frequency. Unlike cells in the vestibular nuclei, none of the rostral FN cells responded to rotational motion alone, without simultaneously exhibiting sensitivity to translational motion. Modulation during earth-horizontal axis rotation was observed in more than half (77%) of the neurons, although with smaller gains than during translation. In contrast, only 47% of the cells changed their firing rates during earth-vertical axis rotations in the absence of a dynamic linear acceleration stimulus. These response properties suggest that the rostral FN represents a main processing center of otolith-driven information for inertial motion detection and spatial orientation.