Vertical purkinje cells of the monkey floccular lobe: Simple-spike activity during pursuit and passive whole body rotation

To understand how the simian floccular lobe is involved in vertical smooth pursuit eye movements and the vertical vestibuloocular reflex (VOR), we examined simple-spike activity of 70 Purkinje (P) cells during pursuit eye movements and passive whole body rotation. Fifty-eight cells responded during vertical and 12 during horizontal pursuit. We classified P cells as vertical gaze velocity (V(G) over dot ) if their modulation occurred for movements of both the eye (during vertical pursuit) and head (during pitch VOR suppression) with the modulation during one less than twice that of the other and was less during the target-fixed-in-space condition (pitch VOR X1) than during pitch VOR suppression. V(G) over dot P cells constituted only a minority of vertical P cells (19%). Other vertical P cells that responded during pitch VOR suppression were classified as vertical eye and head velocity (V(E) over dot/(H) over dot) P cells (48%), regardless of the synergy of their response direction during smooth pursuit and VOR suppression. Vertical P cells that did not respond during pitch VOR suppression but did respond during rotation in vertical planes other than pitch were classified as off-pitch V(E) over dot/(H) over dot P cells (33%). The:mean eye-velocity and eye-position sensitivities of the three types of vertical P cells were similar. One-third (2/7 V(G) over dot, 2/11 V(E) over dot/(H) over dot, 6/13 off-pitch V(E) over dot/(H) over dot). in addition, showed eye position sensitivity during saccade-free fixations. Maximal vestibular activation directions (MADs) were examined during VOR suppression by applying vertical whole body rotation with the monkeys oriented in different vertical planes. The MADs for V(G) over dot P calls and V(E) over dot/(H) over dot P cells with eye and vestibular sensitivity in the same direction were distributed near the pitch plane, suggesting convergence of bilateral anterior canal inputs. In contrast, MADs of off-pitch V(E) over dot/(H) over dot P cells and V(E) over dot/(H) over dot P cells with oppositely directed eye and vestibular sensitivity were shifted toward the roll plane, suggesting convergence of anterior and posterior canal inputs of the same side. Unlike horizontal (G) over dot P cells, the modulation of many V(G) over dot and V(E) over dot/(H) over dot P cells when the target was fixed in space (pitch VOR X1) was not well predicted by the linear addition of their modulations during vertical pursuit and pitch VOR suppression. These results indicate that the populations of vertical and horizontal eye-movement P cells in the floccular lobe have markedly different discharge properties and therefore may be involved in different kinds of processing of vestibular-oculomotor interactions.