SACCADE-RELATED ACTIVITY IN MONKEY SUPERIOR COLLICULUS .1. CHARACTERISTICS OF BURST AND BUILDUP CELLS

1. In the monkey superior colliculus (SC), the activity of most saccade-related neurons studied so far consists of a burst of activity in a population of cells at one place on the SC movement map. In contrast, recent experiments in the cat have described saccade-related activity as a slow increase in discharge before saccades followed by a hill of activity moving across the SC map. In order to explore this striking difference in the distribution of activity across the SC, we recorded from all saccade-related neurons that we encountered in microelectrode penetrations through the monkey SC and placed them in categories according to their activity during the generation of saccades. 2. When we considered the activity preceding the onset of the saccade, we could divide the cells into two categories. Cells with burst activity had a high-frequency discharge just before saccade onset but little activity between the signal to make a saccade and saccade onset. About two thirds of the saccade-related cells had only a burst of activity. Cells with a buildup of activity began to discharge at a low frequency after the signal to make a saccade and the discharge continued until generation of the saccade. About one third of the saccade-related cells studied had a buildup of activity, and about three fourths of these cells also gave a burst of activity with the saccade in addition to the slow buildup of activity. 3. The buildup of activity seemed to be more closely related to preparation to make a saccade than to the generation of the saccade. The buildup developed even in cases when no saccade occurred. 4. The falling phase of the discharge of these saccade-related cells stopped with the end of the saccade (a clipped discharge), shortly after the end of the saccade (partially clipped), or long after the end of the saccade (unclipped). 5. Some cells had closed movement fields in which saccades that were substantially smaller or larger than the optimal amplitude were not associated with increased activity. Other cells tended to have open-ended movement fields without any peripheral border; they were active for all saccades of optimal direction whose amplitudes were equal to or greater than a given amplitude. We found both types of movement fields at all movement field eccentricities studied within the SC. 6. The activity of cells with open-ended movement fields did not result from the smear of the visual target as it swept across the retina during a saccade because the discharge of the cell was still present when saccades were made in the dark to remembered rather than visual targets. The activity of these cells was also not due to the occurrence of corrective saccades because the activity was visible whether or not there was one. 7. In penetrations through the intermediate layers of the SC, we usually found cells with a burst of activity and those with closed movement fields to Lie more dorsally than those with a buildup of activity and open-ended movement fields. 8. We also compared the activity of the saccade-related cells with the activity of fixation cells located in the rostral pole of the SC. We found transition between saccade-related cells with open-ended movement fields and fixation cells. Cells within this transition zone were tonically active during fixation but also discharged during small contraversive saccades. These fixation cells were encountered deeper in the intermediate layers, at the same level as the cells with open-ended movement fields and buildup of activity. We propose that fixation cells form a rostral extension of the layer of cells with a buildup of activity. 9. We conclude that these characteristics of the saccade-related cells overlap sufficiently to allow us to place the cells into two groups. Burst cells have a high-frequency burst occurring immediately before saccades and no buildup of activity; the majority have clipped activity at the end of the saccade and usually have closed movement fields. In contrast, buildup cells show activity beginning with the signal to make a saccade that continues until the generation of the saccade; the majority have partially clipped activity at the end of the saccade and have open-ended movement fields. Because we encountered the cells with burst activity and closed movement fields more dorsally than we did cells with buildup activity and open-ended movement fields, we hypothesize further that the burst and buildup cells can be regarded as separate functional sublayers with the burst layer on top and the buildup layer below. The buildup cells are similar to the saccade-related cells in the cat SC, but the burst cells may be an added feature of the primate SC.