Differential Sensorimotor Processing of Vestibulo-Ocular Signals during Rotation and Translation

Abstract

Rotational and translational vestibulo-ocular reflexes (RVOR and TrVOR) function to maintain stable binocular fixation during head movements. Despite similar functional roles, differences in behavioral, neuroanatomical, and sensory afferent properties suggest that the sensorimotor processing may be partially distinct for the RVOR and TrVOR. To investigate the currently poorly understood neural correlates for the TrVOR, the activities of eye movement-sensitive neurons in the rostral vestibular nuclei were examined during pure translation and rotation under both stable gaze and suppression conditions. Two main conclusions were made. First, the 0.5 Hz firing rates of cells that carry both sensory head movement and motor-like signals during rotation were more strongly related to the oculomotor output than to the vestibular sensory signal during translation. Second, neurons the firing rates of which increased for ipsilaterally versus contralaterally directed eye movements (eye-ipsi and eye-contra cells, respectively) exhibited distinct dynamic properties during TrVOR suppression. Eye-ipsi neurons demonstrated relatively flat dynamics that was similar to that of the majority of vestibular-only neurons. In contrast, eye-contra cells were characterized by low-pass filter dynamics relative to linear acceleration and lower sensitivities than eye-ipsi cells. In fact, the main secondary eye-contra neuron in the disynaptic RVOR pathways (position-vestibular-pause cell) that exhibits a robust modulation during RVOR suppression did not modulate during TrVOR suppression. To explain these results, a simple model is proposed that is consistent with the known neuroanatomy and postulates differential projections of sensory canal and otolith signals onto eye-contra and eye-ipsi cells, respectively, within a shared premotor circuitry that generates the VORs.

Multiple Reference Frames for Motion in the Primate Cerebellum

“…All neural responses were obtained from vestibular-only (VO) neurons. These neurons were recorded from rostral portions of the medial and lateral VN within 1 mm of areas where eye movement-sensitive cells were recorded (Angelaki et al, 2001;Dickman and Angelaki, 2002). In the FN, neurons were recorded in the rostral portions of the nucleus, anterior to all pursuit-related and saccaderelated cells that we consistently encountered in the caudal FN (Gardner and Fuchs, 1975;Buttner et al, 1991).…”

“…In the FN, neurons were recorded in the rostral portions of the nucleus, anterior to all pursuit-related and saccaderelated cells that we consistently encountered in the caudal FN (Gardner and Fuchs, 1975;Buttner et al, 1991). To characterize cells as VO or eye movement-sensitive, a standard protocol was used, including rotations, fixations, and smooth pursuit eye movements (Angelaki et al, 2001).…”

Vestibular Signals in Primate Thalamus: Properties and Origins

“…The recording platform allowed electrode penetrations to cover areas of the thalamus bilaterally. Search coils were also chronically implanted for measuring eye movements (for details, see Angelaki et al, , 2001Meng et al, 2005). The surgical and experimental procedures conformed to the National Institutes of Health guidelines and were approved by the Animal Care and Use Committee at Washington University.…”

Effect of unilateral vestibular deafferentation on the initial human vestibulo-ocular reflex to surge translation

“…In contrast, the LVOR is dominated by excitatory ipsilateral connections from the otoliths to ipsilateral abducens neurons with inhibitory connections to contralateral abducens neurons (Imagawa et al 1995;Schwindt et al 1973;Uchino et al 1994Uchino et al , 1996Uchino et al , 1997b. Most eyemovement related secondary vestibular neurons are activated not only by the semi-circular canals but also the otoliths (Angelaki et al 2001;Chen-Huang and McCrea 1999;King et al 2003;McConville et al 1996). Most secondary vestibular neurons projecting ipsilaterally to the abducens neurons exhibit a clear modulation during LVOR suppression (Angelaki et al 2001;King et al 2003;Meng and Angelaki 2003).…”

“…Most eyemovement related secondary vestibular neurons are activated not only by the semi-circular canals but also the otoliths (Angelaki et al 2001;Chen-Huang and McCrea 1999;King et al 2003;McConville et al 1996). Most secondary vestibular neurons projecting ipsilaterally to the abducens neurons exhibit a clear modulation during LVOR suppression (Angelaki et al 2001;King et al 2003;Meng and Angelaki 2003).…”