Multiple Reference Frames for Motion in the Primate Cerebellum

Abstract

Knowledge of body motion through space is necessary for spatial orientation, self-motion perception, and postural control. Yet, sensory afferent signals may not directly provide such information to the brain. Because motion detected by the vestibular end organs is encoded in a head-fixed frame of reference, a coordinate transformation is thus required to encode body motion. In this study, we investigated whether cerebellar motion-sensitive neurons encode the translation of the body through space. We systematically changed both the direction of motion relative to the body and the static orientation of the head relative to the trunk. The activities of motion-sensitive neurons in the most medial of the deep cerebellar nuclei, the rostral fastigial nucleus, were compared with those in the brainstem vestibular nuclei. We found a distributed representation of reference frames for motion in the rostral fastigial nucleus, in contrast to cells in the vestibular nuclei, which primarily encoded motion in a head-fixed reference frame. This differential representation of motionrelated information implies potential differences in the functional roles of these areas.

Vestibular Signals in Primate Thalamus: Properties and Origins

“…Cerebellothalamic pathways for vestibular signal transmission to the cortex have not been specifically described. Nevertheless, neurons in the fastigial and anterior interposed nuclei exhibit strong vestibular modulation (Gardner and Fuchs, 1975;Büttner et al, 1991;Siebold et al, 1997Siebold et al, , 1999Zhou et al, 2001;Angelaki et al, 2004;Shaikh et al, 2004Shaikh et al, , 2005a. Furthermore, thalamic projections from these nuclei primarily terminate in VL (Fig.…”

“…Neurons in the fastigial and anterior interposed nuclei also modulate their firing rates during vestibular stimulation (Gardner and Fuchs, 1975;Büttner et al, 1991;Siebold et al, 1997;Zhou et al, 2001;Shaikh et al, 2004Shaikh et al, , 2005a. Furthermore, neuroanatomical studies have clearly shown cerebellar nuclei (CN) projections to the thalamus, particularly to the VL (Stanton, 1980;Asanuma et al, 1983;Thach, 1987;Sakai et al, 1996;Middleton and Strick, 1997).…”

Visual and Nonvisual Contributions to Three-Dimensional Heading Selectivity in the Medial Superior Temporal Area

“…originate in different spatial reference frames. Specifically, visual motion signals originate in retinal coordinates Maioli, 1996, 1997;Bremmer et al, 1997), whereas vestibular signals are head/body centered (Shaikh et al, 2004). It is often assumed that optic flow signals must first be converted into a headcentered reference frame, before being useful for heading perception (Royden, 1994;Royden et al, 1994;Banks et al, 1996).…”

Evidence for a reference frame transformation of vestibular signal contributions to voluntary reaching

“…Recent studies suggest that Purkinje cells in the posterior cerebellar vermis (nodulus and ventral uvula) encode such spatially transformed canal signals (Angelaki et al 2010;Yakusheva et al 2007). Other studies have provided evidence that deep cerebellar neurons in the rostral fastigial nucleus and Purkinje cells in the anterior vermis carry vestibular signals that have been at least partially transformed into a body-centered reference frame (Kleine et al 2004;Manzoni et al 1999;Shaikh et al 2004). Furthermore, a recent study has explicitly shown that, for movements in the horizontal plane, many neurons in the rostral fastigial nuclei combine vestibular and neck proprioceptive signals precisely as required to compute body motion (Brooks and Cullen 2009).…”