Firing Behavior of Vestibular Neurons During Active and Passive Head Movements: Vestibulo-Spinal and Other Non-Eye-Movement Related Neurons

Abstract

The firing behavior of 51 non-eye movement related central vestibular neurons that were sensitive to passive head rotation in the plane of the horizontal semicircular canal was studied in three squirrel monkeys whose heads were free to move in the horizontal plane. Unit sensitivity to active head movements during spontaneous gaze saccades was compared with sensitivity to passive head rotation. Most units (29/35 tested) were activated at monosynaptic latencies following electrical stimulation of the ipsilateral vestibular nerve. Nine were vestibulo-spinal units that were antidromically activated following electrical stimulation of the ventromedial funiculi of the spinal cord at C1. All of the units were less sensitive to active head movements than to passive whole body rotation. In the majority of cells (37/51, 73%), including all nine identified vestibulo-spinal units, the vestibular signals related to active head movements were canceled. The remaining units (n = 14, 27%) were sensitive to active head movements, but their responses were attenuated by 20-75%. Most units were nearly as sensitive to passive head-on-trunk rotation as they were to whole body rotation; this suggests that vestibular signals related to active head movements were cancelled primarily by subtraction of a head movement efference copy signal. The sensitivity of most units to passive whole body rotation was unchanged during gaze saccades. A fundamental feature of sensory processing is the ability to distinguish between self-generated and externally induced sensory events. Our observations suggest that the distinction is made at an early stage of processing in the vestibular system.

Brain Stem Pursuit Pathways: Dissociating Visual, Vestibular, and Proprioceptive Inputs During Combined Eye-Head Gaze Tracking

“…In addition, EH neurons are not the only neurons within the vestibular nucleus that show differences regarding their sensitivity to passive activation of neck proprioceptors for these two species. Other second-order neurons, namely position-vestibular-pause neurons and vestibular-only neurons appear to be influenced by passive neck activation in squirrel monkey McCrea 1999, 2000;Gdowski et al 2001;McCrea et al 1999) but not in rhesus monkey Cullen 2001, 2002).…”

“…These results are consistent with previous studies (Chen-Huang and McCrea 1999;Cullen at al. 1993;Gdowski and McCrea 1999;McFarland and Fuchs 1992;Scudder and Fuchs 1992). For the neurons that burst, the bias discharge (bias sac ), eye-position sensitivity (k sac ), and eye-velocity sensitivity (r sac ) were estimated for each neuron using the model, FR(t) ϭ bias sac ϩ k sac * eye position(t-lat) ϩ r sac * eye velocity(t-lat) (saccade model).…”

Multiple Reference Frames for Motion in the Primate Cerebellum

“…sp/sec/g, Spikes/second/gravity. the head was fixed relative to the body versus rotations where the head was allowed to rotate freely McCrea et al, 1999;Roy and Cullen, 2001). Yet, the majority of VN neurons were closer to head than body coordinates.…”

“…Extensive convergence of vestibular and somatosensory signals has been reported in motion-sensitive areas of the brainstem vestibular nuclei (VN), cerebellar cortex (e.g., anterior and posterior cerebellar vermis), and deep cerebellar nuclei (Boyle and Pompeiano, 1981;Anastasopoulos and Mergner, 1982;Wilson et al, 1990;Manzoni et al, 1998Manzoni et al, , 1999McCrea, 1999, 2000;McCrea et al, 1999). At present, it is not known whether this convergence reflects an underlying reference frame transformation to compute body motion in space.…”

Immunoreactivity for calcium-binding proteins defines subregions of the vestibular nuclear complex of the cat

“…Second, no major output arises from cells confined to only one of the nuclei. For example, vestibulospinal fibers arise from cells in the inferior and medial vestibular nuclei as well as from the lateral nucleus (Peterson and Coulter 1977;Akaike 1983;Bankoul and Neuhuber 1992;Donevan et al 1992;Rose et al 1996;McCrea et al 1999;Wilson and Schor 1999). Third, within each nucleus, afferent fibers from different sensory structures are not uniformly distributed but found in restricted regions (Imagawa et al 1995;Naito et al 1995).…”