Convergence of Vestibular and Neck Proprioceptive Sensory Signals in the Cerebellar Interpositus

Abstract

The cerebellar interpositus nucleus (IN) contributes to controlling voluntary limb movements. We hypothesized that the vestibular signals within the IN might be transformed into coordinates describing the body’s movement, appropriate for controlling limb movement. We tested this hypothesis by recording from IN neurons in alert squirrel monkeys during vestibular and proprioceptive stimulation produced during (1) yaw head-on-trunk rotation about the C1–C2 axis while in an orthograde posture and (2) lateral side-to-side flexion about the C6 –T3 axis while in a pronograde posture. Neurons (44/67) were sensitive to vestibular stimulation (23/44 to rotation and translation, 14/44 to rotation only, 7/44 to translation only). Most neurons responded during contralateral movement. Neurons (29/44) had proprioceptive responses; the majority (21/29) were activated during neck rotation and lateral flexion. In all 29 neurons with convergent vestibular and neck proprioceptive input those inputs functionally canceled each other during all combined sensory stimulation, whether in the orthograde or pronograde posture. These results suggest that two distinct populations of IN neurons exist, each of which has vestibular sensitivity. One population carries vestibular signals that describe the head’s movement in space as is traditional for vestibular signals without proprioceptive signals. A second population of neurons demonstrated precise matching of vestibular and proprioceptive signals, even for complicated stimuli, which activated the semicircular canals and otolith organs and involved both rotation and flexion in the spine. Such neurons code body (not head) motion in space, which may be the appropriate platform for controlling limb movements.

Sensory convergence in the parieto-insular vestibular cortex

“…Vestibular signals in the vestibular nuclei combine with oculomotor signals rather than visual signals (Baker and Berthoz 1974;King et al 1976). Many vestibular responses in the vestibular nuclei, cerebellum, and ventro-posterior thalamus combined with neck proprioceptive signals in precise ways to code either head velocity in space or body velocity in space (Gdowski and McCrea 2000;McCrea 2008b, 2009;Brooks and Cullen 2009;Luan et al 2013). Although some of the neurons reported here have signals consistent with coding body velocity in space, they are a small portion of the responses we found.…”

Development of an optogenetic toolkit for neural circuit dissection in squirrel monkeys

“…Their relatively large brains (Fig. 1a) display similar functional organization to rhesus monkeys and humans [112][113][114] , and researchers have leveraged this homology to study the neurophysiology of the vestibular system [115][116][117] , sleep 118 , audition 119,120 , vocalization [121][122][123] , motor control 124 , and many other neuroscientific questions.…”

Vestibular nucleus neurons respond to hindlimb movement in the decerebrate cat

“…A number of studies have focused on the integration of labyrinthine and neck proprioceptive signals in the vestibular nuclei and the deep cerebellar nuclei (Anastasopoulos and Mergner 1982;Boyle and Pompeiano 1981;Brooks and Cullen 2009;Kasper et al 1988;Luan et al 2013;Roy and Cullen 2004;Wilson et al 1990). The modulation of vestibular signals (carrying information about head-in-space movement) by neck proprioceptive signals (carrying information about head relative to body movement) provides body-inspace information to the central nervous system, which has been hypothesized to serve as an important reference frame for generating motor commands that produce postural adjustments (Brooks and Cullen 2009;Cullen et al 2011;Goldberg et al 2012).…”