Saccade-related Purkinje cell activity in the oculomotor vermis during spontaneous eye movements in light and darkness

Abstract

Saccade-related Purkinje cells (PCs) were recorded in the oculomotor vermis (lobules VI, VII) during spontaneous eye movements and fast phases of optokinetic and vestibular nystagmus in the light and darkness, from two macaque monkeys. All neurons (n=46) were spontaneously active and exhibited a saccade-related change of activity with all saccades and fast phases of nystagmus. Four types of neurons were found: most neurons (n=31) exhibited a saccade-related burst of activity only (VBN); other units (n=7) showed a burst of activity with a subsequent pause (VBPN); some of the units (n=5) paused in relation to the saccadic eye movement (pause units,VPN); a few PCs (n=3) showed a burst of activity in one direction and a pause of activity in the opposite direction. For all neurons, burst activity varied considerably for similar saccades. There were no activity differences between spontaneous saccades and vestibular or optokinetically elicited fast phases of nystagmus. The activity before, during, and after horizontal saccades was quantitatively analyzed. For 24 burst PCs (VBN, VBPN), the burst started before saccade onset in one horizontal direction (preferred direction), on average by 15.3 ms (range 27-5 ms). For all these neurons, burst activity started later in the opposite (non-preferred) direction, on average 4.9 ms (range 20 to -12 ms, P<0.01) before saccade onset. The preferred direction could be either with ipsilateral (42% of neurons) or contralateral (58%) saccades. Nine burst PCs had similar latencies and burst patterns in both horizontal directions. The onset of burst activity of a minority of PCs (n=5) lagged saccade onset in all directions. The pause for VBPN neurons started after the end of the saccade and reached a minimum of activity some 40–50 ms after saccade completion. For all saccades and quick phases of nystagmus, burst duration increased with saccade duration. Peak burst activity was not correlated with saccade amplitude or peak eye velocity. PCs continued to show saccade-related burst activity in the dark. However, in 59% of the PCs (VBN, VBPN), peak burst activity was significantly reduced in the dark (on average 28%, range 15–36%) when saccades with the same amplitude (but longer duration in the dark) were compared. For VBP neurons, the pause component after the saccade disappeared in the dark. The difference in peak burst activity (light vs darkness) is similar to that seen for saccade-related neurons in the fastigial oculomotor region (FOR, the structure receiving direct input from vermal PCs) and suggests that the oculomotor vermis also might affect saccade acceleration and/or deceleration. The findings indicate that in the oculomotor vermis — in contrast to the FOR — several different types of saccade-related neurons (PCs) are found. However, the vast majority of PCs behave qualitatively similar to FOR neurons with regard to the burst activity pattern and a direction-specific burst activity onset starting well before saccade onset. This latency will allow these neurons to influence the initiation of saccades in the saccadic brainstem generator through multisynaptic pathways. At present, it has to be determined how (saccade-related) PC activity determines FOR activity.