Frequency response of vestibular reflexes in neck, back, and lower limb muscles

Vestibular pathways form short-latency disynaptic connections with neck motoneurons, whereas they form longer-latency disynaptic and polysynaptic connections with lower limb motoneurons. We quantified frequency responses of vestibular reflexes in neck, back, and lower limb muscles to explain between-muscle differences. Two hypotheses were evaluated: 1) that muscle-specific motor-unit properties influence the bandwidth of vestibular reflexes; and 2) that frequency responses of vestibular reflexes differ between neck, back, and lower limb muscles because of neural filtering. Subjects were exposed to electrical vestibular stimuli over bandwidths of 0–25 and 0–75 Hz while recording activity in sternocleidomastoid, splenius capitis, erector spinae, soleus, and medial gastrocnemius muscles. Coherence between stimulus and muscle activity revealed markedly larger vestibular reflex bandwidths in neck muscles (0–70 Hz) than back (0–15 Hz) or lower limb muscles (0–20 Hz). In addition, vestibular reflexes in back and lower limb muscles undergo low-pass filtering compared with neck-muscle responses, which span a broader dynamic range. These results suggest that the wider bandwidth of head-neck biomechanics requires a vestibular influence on neck-muscle activation across a larger dynamic range than lower limb muscles. A computational model of vestibular afferents and a motoneuron pool indicates that motor-unit properties are not primary contributors to the bandwidth filtering of vestibular reflexes in different muscles. Instead, our experimental findings suggest that pathway-dependent neural filtering, not captured in our model, contributes to these muscle-specific responses. Furthermore, gain-phase discontinuities in the neck-muscle vestibular reflexes provide evidence of destructive interaction between different reflex components, likely via indirect vestibular-motor pathways.

Extracting phase-dependent human vestibular reflexes during locomotion using both time and frequency correlation approaches

Daily activities, such as walking, may require dynamic modulation of vestibular input onto motoneurons. This dynamic modulation is difficult to identify in humans due to limitations in the delivery and analysis of current vestibular probes, such as galvanic vestibular stimulation. Stochastic vestibular stimulation, however, provides an alternative method to extract human vestibular reflexes. Here, we used time-dependent coherence and time-dependent cross-correlation, coupled with stochastic vestibular stimulation, to investigate the phase dependency of human vestibular reflexes during locomotion. We found that phase-dependent activity from the medial gastrocnemius muscles is correlated with the vestibular signals over the 2- to 20-Hz bandwidth during the stance phase of locomotion. Vestibular-gastrocnemius coherence and time-dependent cross-correlations reached maximums at 21 ± 4 and 23 ± 8% of the step cycle following heel contact and before the period of maximal electromyographic activity (38 ± 5%). These results demonstrate 1) the effectiveness of these techniques in extracting the phase-dependent modulation of vestibulomuscular coupling during a cyclic task; 2) that vestibulomuscular coupling is phasically modulated during locomotion; and 3) that the period of strongest vestibulomuscular coupling does not correspond to the period of maximal electromyographic activity in the gastrocnemius. Therefore, we have shown that stochastic vestibular stimulation, coupled with time-frequency decomposition, provides an effective tool to assess the contribution of vestibular ex-afference to the muscular control during locomotion.

Ataxia telangiectasia: a “disease model” to understand the cerebellar control of vestibular reflexes

Experimental animal models have suggested that the modulation of the amplitude and direction of vestibular reflexes are important functions of the vestibulocerebellum and contribute to the control of gaze and balance. These critical vestibular functions have been infrequently quantified in human cerebellar disease. In 13 subjects with ataxia telangiectasia (A-T), a disease associated with profound cerebellar cortical degeneration, we found abnormalities of several key vestibular reflexes. The vestibuloocular reflex (VOR) was measured by eye movement responses to changes in head rotation. The vestibulocollic reflex (VCR) was assessed with cervical vestibular-evoked myogenic potentials (cVEMPs), in which auditory clicks led to electromyographic activity of the sternocleidomastoid muscle. The VOR gain (eye velocity/head velocity) was increased in all subjects with A-T. An increase of the VCR, paralleling that of the VOR, was indirectly suggested by an increase in cVEMP amplitude. In A-T subjects, alignment of the axis of eye rotation was not with that of head rotation. Subjects with A-T thus manifested VOR cross-coupling, abnormal eye movements directed along axes orthogonal to that of head rotation. Degeneration of the Purkinje neurons in the vestibulocerebellum probably underlie these deficits. This study offers insights into how the vestibulocerebellum functions in healthy humans. It may also be of value to the design of treatment trials as a surrogate biomarker of cerebellar function that does not require controlling for motivation or occult changes in motor strategy on the part of experimental subjects.