O. G. DEBOWY, R. BAKER
Department Physiology & Neuroscience, NYU Medical School, New York, NY.
Goldfish present an excellent model system to explore the extent to which neuronal monocularity underlies conjugate horizontal eye movement. Naturally occurring oculomotor behaviors such as the optokinetic and vestibuloocular reflexes (OKR & VOR) and saccades/fixation are conjugate in timing, direction and, in most viewing conditions, amplitude; however, monocular eye motion can be readily induced by visual (OKR) stimuli. Two independent, servo-controlled planetariums subtending 150° of the visual field (30° central null) of each eye were used to implement monocular OKR performance during 1) VOR plasticity training and 2) the tuning of separate (left vs. right eye) eye position integrator time constants (t). In both paradigms, learning and short-term memory of monocular eye movement (2-6hrs) was bidirectional (e.g. leak or instability) and reversible. Neuronal activity recorded from the downstream premotor horizontal eye velocity-to-position neural integrator (PNI) revealed distinct ipsilateral, conjugate and contralateral eye position sensitive populations. Since acquisition of integrator tuning (t) and VOR changes (gain of each eye) were dependent on cerebellar integrity, monocular eye movement learning and plasticity must be entrained and relayed through separate cerebellar-vestibular-PNI channels for each eye. Complementary firing rate analysis of Area II precerebellar/vestibular neurons during monocular performance and plasticity clearly distinguished two different populations exhibiting either ipsilateral or conjugate eye velocity sensitivity. Modeling these results with current structure/function understanding of hindbrain and cerebellar pathways indicated that specific vestibular commissural connections are necessary, and likely sufficient, for eye movement monocularity. We conclude that the conspicuously conjugate oculomotor behaviors in the goldfish are actually produced by predominantly monocular brainstem/cerebellar neurons and circuits that can be distinguished with monocular stimuli. More generally, this finding implies that obligatory conjugacy likely evolved by linking circuitry ancestrally-specific for monocular eye movements.