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

Task-level goals such as maintaining standing balance are achieved through coordinated muscle activity. Consistent and individualized groupings of synchronously activated muscles can be estimated from muscle recordings in terms of motor modules or muscle synergies, independent of their temporal activation. The structure of motor modules can change with motor training, neurological disorders, and rehabilitation, but the central and peripheral mechanisms underlying motor module structure remain unclear. To assess the role of peripheral somatosensory input on motor module structure, we evaluated changes in the structure of motor modules for reactive balance recovery following pyridoxine-induced large-fiber peripheral somatosensory neuropathy in previously collected data in four adult cats. Somatosensory fiber loss, quantified by postmortem histology, varied from mild to severe across cats. Reactive balance recovery was assessed using multidirectional translational support-surface perturbations over days to weeks throughout initial impairment and subsequent recovery of balance ability. Motor modules within each cat were quantified by non-negative matrix factorization and compared in structure over time. All cats exhibited changes in the structure of motor modules for reactive balance recovery after somatosensory loss, providing evidence that somatosensory inputs influence motor module structure. The impact of the somatosensory disturbance on the structure of motor modules in well-trained adult cats indicates that somatosensory mechanisms contribute to motor module structure, and therefore may contribute to some of the pathological changes in motor module structure in neurological disorders. These results further suggest that somatosensory nerves could be targeted during rehabilitation to influence pathological motor modules for rehabilitation.NEW & NOTEWORTHY Stable motor modules for reactive balance recovery in well-trained adult cats were disrupted following pyridoxine-induced peripheral somatosensory neuropathy, suggesting somatosensory inputs contribute to motor module structure. Furthermore, the motor module structure continued to change as the animals regained the ability to maintain standing balance, but the modules generally did not recover pre-pyridoxine patterns. These results suggest changes in somatosensory input and subsequent learning may contribute to changes in motor module structure in pathological conditions.

Absence of postural muscle synergies for balance after spinal cord transection.

Although cats that have been spinalized can also be trained to stand and step with full weight support, directionally appropriate long-latency responses to perturbations are impaired, suggesting that these behaviors are mediated by distinct neural mechanisms. However, it remains unclear whether these responses reflect an attenuated postural response using the appropriate muscular coordination patterns for balance or are due to fundamentally different neural mechanisms such as increased muscular cocontraction or short-latency stretch responses. Here we used muscle synergy analysis on previously collected data to identify whether there are changes in the spatial organization of muscle activity for balance within an animal after spinalization. We hypothesized that the modular organization of muscle activity for balance control is disrupted by spinal cord transection. In each of four animals, muscle synergies were extracted from postural muscle activity both before and after spinalization with nonnegative matrix factorization. Muscle synergy number was reduced after spinalization in three animals and increased in one animal. However, muscle synergy structure was greatly altered after spinalization with reduced direction tuning, suggesting little consistent organization of muscle activity. Furthermore, muscle synergy recruitment was correlated to subsequent force production in the intact but not spinalized condition. Our results demonstrate that the modular structure of sensorimotor feedback responses for balance control is severely disrupted after spinalization, suggesting that the muscle synergies for balance control are not accessible by spinal circuits alone. Moreover, we demonstrate that spinal mechanisms underlying weight support are distinct from brain stem mechanisms underlying directional balance control.

Stabilization and mobility of the head, neck and trunk in horses during overground locomotion: comparisons with humans and other primates.

Segmental kinematics were investigated in horses during overground locomotion and compared with published reports on humans and other primates to determine the impact of a large neck on rotational mobility (> 20 deg.) and stability (< or = 20 deg.) of the head and trunk. Three adult horses (Equus caballus) performing walks, trots and canters were videotaped in lateral view. Data analysis included locomotor velocity, segmental positions, pitch and linear displacements and velocities, and head displacement frequencies. Equine, human and monkey skulls and cervical spines were measured to estimate eye and vestibular arc length during head pitch displacements. Horses stabilized all three segments in all planes during all three gaits, unlike monkeys and humans who make large head pitch and yaw rotations during walks, and monkeys that make large trunk pitch rotations during gallops. Equine head angular displacements and velocities, with some exceptions during walks, were smaller than in humans and other primates. Nevertheless, owing to greater off-axis distances, orbital and vestibular arc lengths remained larger in horses, with the exception of head-neck axial pitch during trots, in which equine arc lengths were smaller than in running humans. Unlike monkeys and humans, equine head peak-frequency ranges fell within the estimated range in which inertia has a compensatory stabilizing effect. This inertial effect was typically over-ridden, however, by muscular or ligamentous intervention. Thus, equine head pitch was not consistently compensatory, as reported in humans. The equine neck isolated the head from the trunk enabling both segments to provide a spatial reference frame.

Bilateral vestibular loss in cats leads to active destabilization of balance during pitch and roll rotations of the support surface.

Although the balance difficulties accompanying vestibular loss are well known, the underlying cause remains unclear. We examined the role of vestibular inputs in the automatic postural response (APR) to pitch and roll rotations of the support surface in freely standing cats before and in the first week after bilateral labyrinthectomy. Support surface rotations accelerate the body center of mass toward the downhill side. The normal APR consists of inhibition in the extensors of the uphill limbs and excitation in the downhill limbs to decelerate the body and maintain the alignment of the limbs with respect to earth-vertical. After vestibular lesion, cats were unstable during rotation perturbations and actively pushed themselves downhill rather than uphill, using a postural response that was opposite to that seen in the control trials. The extensors of the uphill rather than downhill limbs were activated, whereas those of the downhill limbs were inhibited rather than being excited. We propose that vestibular inputs provide an important reference to earth-vertical, which is critical to computing the appropriate postural response during active orientation to the vertical. In the absence of this vestibular information, subjects orient to the support surface using proprioceptive inputs, which drives the body downhill resulting in instability and falling. This is consistent with current models of sensory integration for computation of body posture and orientation.

Muscle synergy organization is robust across a variety of postural perturbations.

We recently showed that four muscle synergies can reproduce multiple muscle activation patterns in cats during postural responses to support surface translations. We now test the robustness of functional muscle synergies, which specify muscle groupings and the active force vectors produced during postural responses under several biomechanically distinct conditions. We aimed to determine whether such synergies represent a generalized control strategy for postural control or if they are merely specific to each postural task. Postural responses to multidirectional translations at different fore-hind paw distances and to multidirectional rotations at the preferred stance distance were analyzed. Five synergies were required to adequately reconstruct responses to translation at the preferred stance distance-four were similar to our previous analysis of translation, whereas the fifth accounted for the newly added background activity during quiet stance. These five control synergies could account for > 80% total variability or r2 > 0.6 of the electromyographic and force tuning curves for all other experimental conditions. Forces were successfully reconstructed but only when they were referenced to a coordinate system that rotated with the limb axis as stance distance changed. Finally, most of the functional muscle synergies were similar across all of the six cats in terms of muscle synergy number, synergy activation patterns, and synergy force vectors. The robustness of synergy organization across perturbation types, postures, and animals suggests that muscle synergies controlling task-variables are a general construct used by the CNS for balance control.

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.

A limited set of muscle synergies for force control during a postural task.

Recently developed computational techniques have been used to reduce muscle activation patterns of high complexity to a simple synergy organization and to bring new insights to the long-standing degrees of freedom problem in motor control. We used a nonnegative factorization approach to identify muscle synergies during postural responses in the cat and to examine the functional significance of such synergies for natural behaviors. We hypothesized that the simplification of neural control afforded by muscle synergies must be matched by a similar reduction in degrees of freedom at the biomechanical level. Electromyographic data were recorded from 8-15 hindlimb muscles of cats exposed to 16 directions of support surface translation. Results showed that as few as four synergies could account for >95% of the automatic postural response across all muscles and all directions. Each synergy was activated for a specific set of perturbation directions, and moreover, each was correlated with a unique vector of endpoint force under the limb. We suggest that, within the context of active balance control, postural synergies reflect a neural command signal that specifies endpoint force of a limb.

Ratio of shear to load ground-reaction force may underlie the directional tuning of the automatic postural response to rotation and translation.

This study sought to identify the sensory signals that encode perturbation direction rapidly enough to shape the directional tuning of the automatic postural response. We compared reactions to 16 directions of pitch and roll rotation and 16 directions of linear translation in the horizontal plane in freely standing cats. Rotations and translations that displaced the center of mass in the same direction relative to the feet evoked similar patterns of muscle activity and active ground-reaction force, suggesting the presence of a single, robust postural strategy for stabilizing the center of mass in both rotation and translation. Therefore we postulated there should be a common sensory input that encodes the direction of the perturbation and leads to the directional tuning of the early electromyographic burst in the postural response. We compared the mechanical changes induced by rotations and translations prior to the active, postural response. The only consistent feature common to the full range of rotation and translation directions was the initial change in ground-reaction force angle. Other variables including joint angles, ground-reaction force magnitudes, center of pressure, and center of mass in space showed opposite or nonsignificant changes for rotation and translation. Change in force angle at the paw reflects the ratio of loading force to slip force, analogous to slips during finger grip tasks. We propose that cutaneous sensors in the foot soles detect change in ground-reaction force angle and provide the critical input underlying the directional tuning of the automatic postural response for balance.

Automatic postural responses are delayed by pyridoxine-induced somatosensory loss.

Pyridoxine given in large doses is thought to destroy selectively the large-diameter peripheral sensory nerve fibers, leaving motor fibers intact. This study examined the effects of pyridoxine-induced somatosensory loss on automatic postural responses to sudden displacements of the support surface in the standing cat. Two cats were trained to stand on four force plates mounted on a movable platform. They were given pyridoxine (350 mg/kg, i.p.) on 2 successive days (0 and 1). Electromyographic (EMG) activity was recorded from selected hindlimb muscles during linear ramp-and-hold platform displacements in each of 12 directions at 15 cm/sec. In control trials onset latencies of evoked activity in hindlimb flexor and extensor muscles ranged from 40 to 65 msec after the onset of platform acceleration. After injection the EMG latencies increased over days, becoming two to three times longer than controls by day 7. Excursions of the body center of mass (CoM) in the direction opposite to that of platform translation were significantly greater at day 7 compared with controls, and the time at which the CoM subsequently reversed direction was delayed. Both animals were ataxic from day 2 onward. Histological analysis of cutaneous and muscle nerves in the hindlimb revealed a significant loss of fibers in the group I range. Our results suggest that large afferent fibers are critical for the timing of automatic postural responses to ensure coordinated control of the body CoM and balance after unexpected disturbances of the support surface.