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.

Agency
National Institute of Health (NIH)
Institute
National Institute of Neurological Disorders and Stroke (NINDS)
Type
Research Project (R01)
Project #
5R01NS027050-03
Application #
3413214
Study Section
Hearing Research Study Section (HAR)
Project Start
1991-01-01
Project End
1993-12-31
Budget Start
1993-01-01
Budget End
1993-12-31
Support Year
3
Fiscal Year
1993
Total Cost
Indirect Cost
Name
Oregon Health and Science University
Department
Type
Schools of Medicine
DUNS #
009584210
City
Portland
State
OR
Country
United States
Zip Code
97239
Boyle, R; Bush, G; Ehsanian, R (2004) Input/output properties of the lateral vestibular nucleus. Arch Ital Biol 142:133-53
Lewis, Richard F; Gong, Wangsong; Ramsey, Mitchell et al. (2002) Vestibular adaptation studied with a prosthetic semicircular canal. J Vestib Res 12:87-94
Boyle, Richard; Highstein, Stephen M; Carey, John P et al. (2002) Functional recovery of anterior semicircular canal afferents following hair cell regeneration in birds. J Assoc Res Otolaryngol 3:149-66
Boyle, R (2001) Vestibulospinal control of reflex and voluntary head movement. Ann N Y Acad Sci 942:364-80
McCollum, G; Boyle, R (2001) Conditional transitions in gaze dynamics: role of vestibular nuclei in eye-only and eye/head gaze behaviors. Biol Cybern 85:423-36
Boyle, R (2000) Morphology of lumbar-projecting lateral vestibulospinal neurons in the brainstem and cervical spinal cord in the squirrel monkey. Arch Ital Biol 138:107-22
Gdowski, G T; Boyle, R; McCrea, R A (2000) Sensory processing in the vestibular nuclei during active head movements. Arch Ital Biol 138:15-28
McCrea, R A; Gdowski, G T; Boyle, R et al. (1999) Firing behavior of vestibular neurons during active and passive head movements: vestibulo-spinal and other non-eye-movement related neurons. J Neurophysiol 82:416-28
Holly, J E; McCollum, G; Boyle, R (1999) Identification of head motions by central vestibular neurons receiving linear and angular input. Biol Cybern 81:177-88
Rabbitt, R D; Boyle, R; Highstein, S M (1994) Sensory transduction of head velocity and acceleration in the toadfish horizontal semicircular canal. J Neurophysiol 72:1041-8

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