Properties of superior vestibular nucleus flocculus target neurons in the squirrel monkey. II. Signal components revealed by reversible flocculus inactivation

Abstract

1. Seven upward eye velocity flocculus target neurons (FTNs) and two flocculus projecting neurons (FPNs) were studied before and after ipsilateral flocculus inactivation by injection of muscimol in the alert squirrel monkey. An additional seven FTNs and seven FPNs recorded from the corresponding FTN and FPN areas were recorded after injection. Response properties of FTNs and FPNs were characterized by visual-vestibular interaction paradigms and were compared before and after flocculus inactivation. 2. In FTNs the mean firing rate increased within 2-5 min after muscimol injection in the flocculus and reached a plateau level in approximately 10-20 min. The average mean firing rate for seven FTNs increased from 117 to 174 spikes/s, a net increase of 57 spikes/s (49%). Accompanying the large increase of the mean firing rate, a spontaneous nystagmus in the darkness developed with the slow phase directed upward and contralateral. 3. The firing rate modulation during visual following of a sinusoidal optokinetic drum (0.5 Hz) decreased within 2-5 min after muscimol injection in the flocculus and reached a level of 0 in approximately 10-20 min for all FTNs. After that, some cells remained unmodulated for the period of recording; other cells gradually reversed their phase and developed a modulation out of phase with drum velocity. The depletion of the visual following eye velocity signal on superior vestibular nucleus (SVN) FTNs accompanied a small but consistent decrease of visual following eye velocity amplitude. The average maximum decrease of eye velocity was 26 +/- 9% (mean +/- SD). 4. After flocculus inactivation, even though the modulation response at 0.5 Hz during visual following was abolished, a slow-component eye velocity signal with the same on direction was revealed by a constant-velocity optokinetic stimulus. It is concluded that there are at least two kinds of eye velocity signals during the optokinetic response. These signals are combined at the FTNs and are subsequently relayed to the oculomotor neurons. The source of the fast component is the flocculus, and the source of the slow component is another, as yet unidentified brain structure. 5. The effect of flocculus inactivation on the modulation amplitude during the vestibuloocular reflex (VOR) in darkness was variable: two cells did not change, two cells decreased, and three cells increased their amplitude. The response phase tended to move toward a phase lead, but the change was small. The effect on VOR suppression was more prominent.(ABSTRACT TRUNCATED AT 400 WORDS)

Neural Correlates of Forward and Inverse Models for Eye Movements: Evidence from Three-Dimensional Kinematics

“…The cerebellum has long been implicated in eye movement adaptation and internal models (Shidara et al, 1993;Wolpert et al, 1995;Glasauer, 2003). EH neurons are the recipients of direct inhibition from Purkinje cells in the cerebellar flocculus and ventral paraflocculus and are shown to participate in motor learning (Lisberger et al, 1994;Zhang et al, 1995). Therefore, the present findings and those of Angelaki and Dickman (2003), showing that EH responses might be consistent with coding the half-angle rule during pursuit, provide strong support that the cerebellum might be constructing a forward model for slow eye movements.…”

Eyes on Target: What Neurons Must do for the Vestibuloocular Reflex During Linear Motion

“…Even though FTN response behavior during saccades and VOR suppression could vary greatly, their unique characteristics include a strong eye-velocity sensitivity with a small and often non-linear eye-position sensitivity. FPNs, on the other hand, have been described as cells with small eye-movement sensitivity and represent distinctly different and nonoverlapping populations from FTNs (Nagao et al 1997;Zhang et al 1993Zhang et al , 1995a. Neuroanatomical and electrophysiological studies have identified FTNs in the rostral medial and ventrolateral vestibular nuclei (Langer et al 1985a;Lisberger et al 1994;Nagao et al 1997;Sato et al 1988).…”

Histamine Excites Rat Superior Vestibular Nuclear Neurons via Postsynaptic H1and H2Receptors in vitro

“…Among the four major vestibular nuclei, the SVN receives inputs predominantly from the semicircular canals and sends axons to the oculomotor nucleus, the cerebellar nodulus, uvula and flocculus, and the ventral posterior nuclear complex of the thalamus, which in turn projects to the cortical areas relevant to vestibular sensations [12]. Consequently, slightly different from the other vestibular nuclei which are also essential for posture adjustments of the head and/or body, the SVN primarily participates in vertical vestibulo-ocular reflexes and holds a key position in gaze control [12,14,15,16], together with the MVN. Therefore, the present results that histamine directly excites the SVN neurons suggest that the histaminergic innervation from the hypothalamus on vestibular nuclei may actively participate in stabilizing not only head and posture through the MVN and LVN, but also gaze through the MVN as well as the SVN.…”

“…Among the four nuclei in the central vestibular nuclear complex, the SVN, together with the MVN, receives fibers predominantly from the semicircular canals and sends fibers through the medial longitudinal fasciculus rostrally to oculomotor centers and caudally to the spinal cord [12,13]. Both of these two nuclei actually hold a key position in vestibulo-ocular reflexes and gaze control [12,14,15,16], and are closely related to nystagmus [17,18]. …”