Anatomical and physiological characteristics of vestibular neurons mediating the horizontal vestibulo‐ocular reflex of the squirrel monkey

Abstract

The anatomical characteristics of vestibular neurons, which are involved in controlling the horizontal vestibulo-ocular reflex, were studied by injecting horseradish peroxidase (HRP) into neurons whose response during spontaneous eye movements had been characterized in alert squirrel monkeys. Most of the vestibular neurons injected with HRP that had axons projecting to the abducens nucleus or the medial rectus subdivision of the oculomotor nucleus had discharge rates related to eye position and eye velocity. Three morphological types of cells were injected whose firing rates were related to horizontal eye movements. Two of the cell types were located in the ventral lateral vestibular nucleus and the ventral part of the medial vestibular nucleus (MV). These vestibular neurons could be activated at monosynaptic latencies following electrical stimulation of the vestibular nerve; increased their firing rate when the eye moved in the direction contralateral to the soma; had tonic firing rates that increased when the eye was held in contralateral positions; and had a pause in their firing rate during saccadic eye movements in the ipsilateral or vertical directions. Eleven of the above cells had axons that arborized exclusively on the contralateral side of the brainstem, terminating in the contralateral abducens nucleus, the dorsal paramedian pontine reticular formation, the prepositus nucleus, medial vestibular nucleus, dorsal medullary reticular formation, caudal interstitial nucleus of the medial longitudinal fasciculus, and raphé obscurus. Eight of the cells had axons that projected rostrally in the ascending tract of Deiters and arborized exclusively on the ipsilateral side of the brainstem, terminating in the ipsilateral medial rectus subdivision of the oculomotor nucleus and, in some cases, the dorsal paramedian pontine reticular formation or the caudal interstitial nucleus of the medial longitudinal fasciculus. Two MV neurons were injected that had discharge rates related to ipsilateral eye position, generated bursts of spikes during saccades in the ipsilateral direction, and paused during saccades in the contralateral direction. The axons of those cells arborized ipsilaterally, and terminated in the ipsilateral abducens nucleus, MV, prepositus nucleus, and the dorsal medullary reticular formation. The morphology of vestibular neurons that projected to the abducens nucleus whose discharge rate was not related to eye movements, or was related primarily to vertical eye movements, is also briefly presented.

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

“…Subsequent penetrations were concentrated in a relatively small area in the rostral part of the vestibular nucleus extending 3 mm posterior and 4 mm lateral from the center of the abducens nuclei. These areas, consisting mainly of the rostral medial vestibular nuclei (with a few penetrations extending into the caudal aspects of the superior vestibular nucleus), have been shown to contain eye movement-sensitive cells, many of which project directly to the abducens and oculomotor nuclei (McCrea et al, 1987;Scudder and Fuchs, 1992;Cullen and McCrea, 1993). In the animals that were implanted with bilateral labyrinthine stimulating electrodes, localization of the vestibular nuclei was also guided by vestibular field potentials evoked with electrical stimulation of the ipsilateral vestibular nerve (0.1 msec monophasic pulses; 50 -400 A).…”

“…(4) Vestibular-only (VO) neurons included all cells that did not exhibit any slow eye movement sensitivity but modulated during either rotational or translational head movements. The present analysis focuses specifically on the translational responses of those neuron types the firing rates of which exhibited some form of correlation with the slow component of the eye movement (i.e., PV/ PV P, BT, and E-H cells), because it is a subset of these cell groups that has been shown to be the premotor neurons in the RVOR pathways (McCrea et al, 1987;Scudder and Fuchs, 1992).…”

“…In contrast, the shortest latency excitatory utriculoabducens pathway is a weak ipsilateral projection, whereas the contralateral projections are at least trisynaptic and inhibitory (Schwindt et al, 1973;Uchino et al, 1994Uchino et al, , 1996, 1997; Imagawa et al, 1995). Because it is known that the large majority of type I PVP neurons make direct excitatory connections to the contralateral abducens (McCrea et al, 1987;Scudder and Fuchs, 1992), one must conclude that primary otolith afferents do not make monosynaptic projections to type I PVP neurons (Fig. 13).…”

“…However, the feedback realization is more realistic in terms of the highly interconnected nature of the premotor circuitry (cf. McCrea et al, 1981McCrea et al, , 1987. Furthermore, the neural integration relies on distributed positive feedback loops around a neural filter with a relatively small time constant (i.e., equal to the dominant eye plant time constant of ϳ0.25 sec), as opposed to a localized integrator with a large time constant.…”

“…In the case of the RVOR, it has been well established that the most direct vestibulo-ocular connections are disynaptic, involving second-order neurons in the rostral vestibular nuclei (Richter and Precht, 1968;Baker et al, 1969;Precht et al, 1969;Schwindt et al, 1973;McCrea et al, 1987;Scudder and Fuchs, 1992). The majority of these premotor neurons carry a combination of signals that are correlated with both vestibular canal inputs (i.e., "sensory" signals) and eye movement-related activity (i.e., "motor-like" signals).…”