Responses of pigeon vestibulocerebellar neurons to optokinetic stimulation. I. Functional organization of neurons discriminating between translational and rotational visual flow.

1. Extracellular recordings were made from 235 neurons in the vestibulocerebellum (VbC), including the flocculus (lateral VbC), nodulus (folium X), and ventral uvula (ventral folium IXc,d), of the anesthetized pigeon, in response to an optokinetic stimulus. 2. The optokinetic stimuli consisted of two black and white random-dot patterns that were back-projected onto two large tangent screens. The screens were oriented parallel to each other and placed on either side of the bird's head. The resultant stimulus covered the central 100 degrees x 100 degrees of each hemifield. The directional tuning characteristics of each unit were assessed by moving the largefield stimulus in 12 different directions, 30 degrees apart. The directional tuning curves were performed monocularly or binocularly. The binocular directional tuning curves were performed with the direction of motion the same in both eyes (in-phase; e.g., ipsi = upward, contra = upward) or with the direction of motion opposite in either eye (antiphase; e.g., ipsi = upward, contra = downward). 3. Mossy fiber units (n = 17) found throughout folia IXa,b and IXc,d had monocular receptive fields and exhibited direction selectivity in response to stimulation of either the ipsilateral (n = 12) or contralateral (n = 5) eye. None had binocular receptive fields. 4. The complex spike (CS) activity of 218 Purkinje cells in folia IXc,d and X exhibited direction selectivity in response to the large-field visual stimulus moving in one or both visual fields. Ninety-one percent of the cells had binocular receptive fields that could be classified into four groups: descent neurons (n = 112) preferred upward motion in both eyes; ascent neurons (n = 14) preferred downward motion in both eyes; roll neurons (n = 33) preferred upward and downward motion in the ipsilateral and contralateral eyes, respectively; and yaw neurons (n = 40) preferred forward and backward motion in the ipsilateral and contralateral eyes, respectively. Within all groups, most neurons (70%) showed an ipsilateral dominance. 5. For most binocular neurons (91%), the maximum depth of modulation occurred with simultaneous stimulation of both eyes, compared with monocular stimulation of the dominant eye alone. For the translation neurons (descent and ascent), binocular inphase stimulation produced the maximum depth of modulation, whereas for the rotation neurons (roll and yaw), binocular antiphase stimulation produced the maximum depth of modulation. 6. There was a clear functional segregation of the translation and rotation neurons.(ABSTRACT TRUNCATED AT 400 WORDS)