Precerebellar Hindbrain Neurons Encoding Eye Velocity During Vestibular and Optokinetic Behavior in the Goldfish

1 Department of Physiology and Neuroscience, New York University School of Medicine, New York; 2 The Center for Biomathematical Sciences, Mount Sinai School of Medicine, New York, New York; 3 Laboratoire de Neurobiologie des Réseaux Sensorimoteurs, Centre National de la Recherche Scientifique Unité Mixte de Recherche 7060, Université Paris 5, Paris, France; and 4 Fishberg Department of Neuroscience, Mount Sinai School of Medicine, New York, New York Submitted 30 March 2006; accepted in final form 10 June 2006 Elucidating the causal role of head and eye movement signaling during cerebellar-dependent oculomotor behavior and plasticity is contingent on knowledge of precerebellar structure and function. To address this question, single-unit extracellular recordings were made from hindbrain Area II neurons that provide a major mossy fiber projection to the goldfish vestibulolateral cerebellum. During spontaneous behavior, Area II neurons exhibited minimal eye position and saccadic sensitivity. Sinusoidal visual and vestibular stimulation over a broad frequency range (0.1–4.0 Hz) demonstrated that firing rate mirrored the amplitude and phase of eye or head velocity, respectively. Table frequencies >1.0 Hz resulted in decreased firing rate relative to eye velocity gain, while phase was unchanged. During visual steps, neuronal discharge paralleled eye velocity latency ( 90 ms) and matched both the build-up and the time course of the decay ( 19 s) in eye velocity storage. Latency of neuronal discharge to table steps (40 ms) was significantly longer than for eye movement (17 ms), but firing rate rose faster than eye velocity to steady-state levels. The velocity sensitivity of Area II neurons was shown to equal (±10%) the sum of eye- and head-velocity firing rates as has been observed in cerebellar Purkinje cells. These results demonstrate that Area II neuronal firing closely emulates oculomotor performance. Conjoint signaling of head and eye velocity together with the termination pattern of each Area II neuron in the vestibulolateral lobe presents a unique eye-velocity brain stem-cerebellar pathway, eliminating the conceptual requirement of motor error signaling. Address for reprint requests and other correspondence: J. C. Beck, Dept. of Physiology and Neuroscience, NYU School of Medicine, 550 First Ave., New York, NY 10016 (E-mail: james.beck{at}med.nyu.edu )