The structure and function of vestibulo-collic, vestibulo-ocular, and vestibulo-ocular-collic (VOC) neurons are studied in adult squirrel monkeys to specify their roles in the vestibular control of neck-eye coordination in relation to gaze. These neurons, and particularly the VOC cells, represent the possible interfaces between the eyes and the head and neck. The immediate aim is to understand the information content, vis-a-vis head movement, supplied by primary vestibular afferents to these secondary neurons. Specifically, using an electrophysiological paradigm (27) and intrasomatic labeling with biocytin, the short-latency synaptic input profile of irregular and regular afferents, which have distinct response dynamics to head acceleration, to neurons participating in the different vestibular relay pathways is determined in the anesthetized and paralyzed monkey. The vestibular neurons contributing to the spinal reflex pathways are further characterized by identifying the axis of head rotation, viz. the semicircular canal, that influences the cell and intra-axonally labeled with biocytin to resolve their exact brainstem and intraspinal collateral arborizations. The motoneuronal pools supplying selected neck muscles are retrogradely labeled to specify the cervical organization of these muscle groups, and to evaluate the contribution of vestibular neurons to intrinsic and extrinsic spinal circuits controlling specific reflex and dynamic regulation of head movement. Finally, in the trained, alert monkey the diverse classes of vestibular neurons are identified by ortho- and antidromic stimulation, and their discharge studied during sinusoidal head rotation to determine the transfer of head movement dynamics from afferent to cell. The cells are further characterized by identifying their eye movement-related signals during spontaneous scanning, pursuit tracking, and optokinetic-induced eye movements. Preliminary data show, unexpectedly, that vestibulospinal neurons are differentially affected by volitional and reflex-induced eye movements. Because of their differential afferent input, collateral arborizations and gaze signals, it is hypothesized that the vestibular cells participate in dissimilar operations of neck-eye coordination and gaze control. The long-term goal of these studies is to understand the precise role of the vestibular and neck proprioceptive systems in the achievement of final gaze orientation in man, and the disorders affecting neck-eye coordination seen in the clinical practices of Otolaryngology and related services.
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