Integration of Vestibular and Head Movement Signals in the Vestibular Nuclei During Whole-Body Rotation

Abstract

Single-unit recordings were obtained from 107 horizontal semicircular canal-related central vestibular neurons in three alert squirrel monkeys during passive sinusoidal whole-body rotation (WBR) while the head was free to move in the yaw plane (2.3 Hz, 20 degrees /s). Most of the units were identified as secondary vestibular neurons by electrical stimulation of the ipsilateral vestibular nerve (61/80 tested). Both non-eye-movement (n = 52) and eye-movement-related (n = 55) units were studied. Unit responses recorded when the head was free to move were compared with responses recorded when the head was restrained from moving. WBR in the absence of a visual target evoked a compensatory vestibulocollic reflex (VCR) that effectively reduced the head velocity in space by an average of 33 +/- 14%. In 73 units, the compensatory head movements were sufficiently large to permit the effect of the VCR on vestibular signal processing to be assessed quantitatively. The VCR affected the rotational responses of different vestibular neurons in different ways. Approximately one-half of the units (34/73, 47%) had responses that decreased as head velocity decreased. However, the responses of many other units (24/73) showed little change. These cells had signals that were better correlated with trunk velocity than with head velocity. The remaining units had responses that were significantly larger (15/73, 21%) when the VCR produced a decrease in head velocity. Eye-movement-related units tended to have rotational responses that were correlated with head velocity. On the other hand, non-eye-movement units tended to have rotational responses that were better correlated with trunk velocity. We conclude that sensory vestibular signals are transformed from head-in-space coordinates to trunk-in-space coordinates on many secondary vestibular neurons in the vestibular nuclei by the addition of inputs related to head rotation on the trunk. This coordinate transformation is presumably important for controlling postural reflexes and constructing a central percept of body orientation and movement in space.

Responses of caudal vestibular nucleus neurons of conscious cats to rotations in vertical planes, before and after a bilateral vestibular neurectomy

“…Although a variety of studies have considered the responses of vestibular nucleus neurons to rotations and translations of the head (e.g., Chubb et al 1984;Kasper et al 1988;Gdowski and McCrea 1999;Dickman and Angelaki 2002;Zhou et al 2006), virtually all of these experiments have focused on units in the rostral or middle portions of the nuclear complex. With the exception of a small GABAergic cell population that comprises the parasolitary nucleus (Barmack and Yakhnitsa 2000), the caudal vestibular nuclei (CVN) have not been extensively studied, particularly in conscious animals.…”

Stabilization and mobility of the head and trunk in vervet monkeys(Cercopithecus aethiops) during treadmill walks and gallops

“…gravity vertical or gravito-inertial acceleration vector). During gallops, a stabilized head in a face-forward, downwardly pitched orientation that aligns the horizontal semicircular canals near earth-horizontal allows the eyes and vestibular apparatus to provide the brain with redundant reference frames for gaze Clément et al, 1988;Grossman et al, 1988;Owen and Lee, 1986;Pozzo et al, 1990), and spatial orientation and heading (Gdowski and McCrea, 1999;Mayne, 1974;Pozzo et al, 1990). Evidence continues to accumulate that the vestibular apparatus functions as an inertial navigational system (Berthoz and Pozzo, 1994;Dunbar et al, 2004;Mayne, 1974;Pozzo et al, 1990) within the stable platform of the head (Pozzo et al, 1990), and is sensitive to the gravito-inertial acceleration vector (Imai et al, 2001).…”

Squirrel Monkeys and Space Motion Sickness

“…Floccular Purkinje cell activity was also studied in the Japanese monkey in relation to a pursuit of eye movements and WBR [106]. Neuronal activity in relation to active head movements were also studied in the vestibular nuclei of squirrel monkeys [107][108][109].…”