RESPONSES OF PIGEON VESTIBULOCEREBELLAR NEURONS TO OPTOKINETIC STIMULATION .2. THE 3-DIMENSIONAL REFERENCE FRAME OF ROTATION NEURONS IN THEFLOCCULUS

1. The complex spike activity Of Purkinje cells in the flocculus in re sponse to rotational flowfields was recorded extracellularly in anesth etized 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 mo tor oscillated the cylinder about its long axis. This apparatus was pl aced above the bird's head and the resultant rotational flowfield 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: ver tical axis (VA: n = 43) neurons responded best to visual rotation abou t the vertical axis, and H-135i neurons (n = 34) responded best to rot ation about a horizontal axis. The preferred orientation of the horizo ntal axis was at approximately 135-degrees ipsilateral azimuth. VA neu rons were excited by rotation about the vertical axis producing forwar d (temporal to nasal) and backward motion in the ipsilateral and contr alateral eyes, respectively, and were inhibited by rotation in the opp osite 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 ro tations stimulating the ipsilateral horizontal and ipsilateral anterio r semicircular canals. 4. Sixty-seven percent of VA and 80% of H-135i neurons had binocular receptive fields, although for most binocular ce lls the ipsilateral eye was dominant. Binocular stimulation resulted i n 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 tilt ed back 11-degrees, on average, to the best axis for ipsilateral stimu lation. For the H-135i neurons, the best axes for monocular stimulatio n of the two eyes were approximately the same. 6. By stimulating circu mscribed portions of the monocular receptive fields of the H-135i neur ons with alternating upward and downward largefield motion, it was rev ealed that the contralateral receptive fields were bipartite. Upward m otion was preferred in the anterior 45-degrees of the contralateral fi eld, and downward motion was preferred in the central 90-degrees of th e contralateral visual field. Stimulation of the ipsilateral field rev ealed that upward motion was preferred in both the anterior 45-degrees and central 90-degrees. Stimulation restricted to the posterior 45-de grees of either visual field did not affect the cells' firing rates. 7 . These results suggest that the three-dimensional reference frame of the optokinetic system for self-rotation in the flocculus is similar t o those of the semicircular canals and eye muscles.