Responses of pigeon vestibulocerebellar neurons to optokinetic stimulation. II. The 3-dimensional reference frame of rotation neurons in the flocculus.

1. The complex spike activity of Purkinje cells in the flocculus in response to rotational flowfields was recorded extracellularly in anesthetized pigeons. 2. The optokinetic stimulus was produced by a rotating "planetarium projector." A light source was placed in the center of a tin cylinder, which was pierced with numerous small holes. A pen motor oscillated the cylinder about its long axis. This apparatus was placed above the bird's head and the resultant rotational flow-field was projected onto screens that surrounded the bird on all four sides. The axis of rotation of the planetarium could be oriented to any position in three-dimensional space. 3. Two types of responses were found: vertical axis (VA; n = 43) neurons responded best to visual rotation about the vertical axis, and H-135i neurons (n = 34) responded best to rotation about a horizontal axis. The preferred orientation of the horizontal axis was at approximately 135 degrees ipsilateral azimuth. VA neurons were excited by rotation about the vertical axis producing forward (temporal to nasal) and backward motion in the ipsilateral and contralateral eyes, respectively, and were inhibited by rotation in the opposite direction. H-135i neurons in the left flocculus were excited by counterclockwise rotation about the 135 degrees ipsilateral horizontal axis and were inhibited by clockwise motion. Thus, the VA and H-135i neurons, respectively, encode visual flowfields resulting from head rotations stimulating the ipsilateral horizontal and ipsilateral anterior semicircular canals. 4. Sixty-seven percent of VA and 80% of H-135i neurons had binocular receptive fields, although for most binocular cells the ipsilateral eye was dominant. Binocular stimulation resulted in a greater depth of modulation than did monocular stimulation of the dominant eye for 69% of the cells. 5. Monocular stimulation of the VA neurons revealed that the best axis for the contralateral eye was tilted back 11 degrees, on average, to the best axis for ipsilateral stimulation. For the H-135i neurons, the best axes for monocular stimulation of the two eyes were approximately the same. 6. By stimulating circumscribed portions of the monocular receptive fields of the H-135i neurons with alternating upward and downward largefield motion, it was revealed that the contralateral receptive fields were bipartite. Upward motion was preferred in the anterior 45 degrees of the contralateral field, and downward motion, was preferred in the central 90 degrees of the contralateral visual field.(ABSTRACT TRUNCATED AT 400 WORDS)