USE OF INTERRUPTED SACCADE PARADIGM TO STUDY SPATIAL AND TEMPORAL DYNAMICS OF SACCADIC BURST CELLS IN SUPERIOR COLLICULUS IN MONKEY

1. We recorded the spatial and temporal dynamics of saccade-related burst neurons( SRBNs) found in the intermediate layers of the superior colliculus (SC) in the alert, behaving monkey. These burst cells are normally the first neurons recorded during radially directed microelectrode penetrations of the SC after the electrode has left the more dorsally situated visual layers. They have spatially delimited movement fields whose centers describe the well-studied motor map of the SC. They have a rather sharp, saccade-locked burst of activity that peaks just before saccade onset and then declines steeply during the saccade. Many of these cells, when recorded during saccade trials, also have an early, transient visual response and an irregular prelude of presaccadic activity. 2. Because saccadic eye movements normally have very stereotyped durations and velocity trajectories that vary systematically with saccade size, it has been difficult in the past to establish quantitatively whether the activity of SRBNs temporally codes dynamic saccadic control signals, e.g., dynamic motor error or eye velocity, where dynamic motor error is defined as a signal proportional to the instantaneous difference between desired final eye position and the actual eye position during a saccade. It has also not been unequivocally established whether SRBNs participate in an organized spatial shift of ensemble activity in the intermediate layers of the SC during saccadic eye movements. 3. To address these issues, we studied the activity of SRBNs using an interrupted saccade paradigm. Saccades were interrupted with pulsatile electrical stimulation through a microelectrode implanted in the omnipauser region of the brain stem while recordings were made simultaneously from single SRBNs in the SC. 4. Shortly after the beginning of the stimulation (which was electronically triggered at saccade onset), the eyes decelerated rapidly and stopped completely. When the high-frequency (typically 300-400 pulses per second) stimulation was terminated (average duration 12 ms), the eye movement was reinitiated and a resumed saccade was made accurately to the location of the target. 5. When we recorded from SRBNs in the more caudal colliculus, which were active for large saccades, cell discharge was powerfully and rapidly suppressed by the stimulation (average latency = 3.8 ms). Activity in the same cells started again just before the onset of the resumed saccade and continued during this saccade even though it had a much smaller amplitude than would normally be associated with significant discharge for caudal SC cells. The resumption of discharge in caudal SRBNs during the resumed saccades suggests that the colliculus is inside a dynamic local feedback loop from brain stem circuits controlling saccades (i.e., they are part of a network that sensed the braking of the saccade in midflight and participated in the resumed saccade). Therefore the sharp decline in the discharge of SRBNs during saccades is not an intrinsic property of intracollicular networks by themselves. 6. In contrast, when we recorded from SRBNs with less eccentric movement fields that are located anatomically near the middle of the SC (along its rostral-to-caudal axis), we found no or only minimal activity during resumed saccades. Intense activity was recorded in the same cells during unstimulated saccades with similar amplitudes to the resumed saccades. Taken together, conclusions 5 and 6 provide unequivocal evidence that the population of active SRBNs does not shift on the colliculus during a saccadic eye movement. 7. We attempted to relate the magnitude of the second burst of activity in SRBNs during the resumed saccade to presumed motor error relationships calculated from data gathered during uninterrupted saccades from the same block of trials. The average renewed discharge measured just before the start of the resumed saccade was 42% greater than that measured at similar values of motor error during uninterrupted movements. In contrast, peak saccadic eye velocity during the resumed saccade was lower than the normal saccadic velocity measured in the same animals. The eyes were undergoing maximum acceleration at the onset of the resumed saccade, which suggests that the higher discharge of SRBNs might be correlated with this dynamic signal. Overall, the results suggest that the discharge of SRBNs does not quantitatively code dynamic motor error, at least during the initial phase of the resumed saccades. Nevertheless, the averaged SRBN activity did return very rapidly (in similar to 10 ms) to the relationship between discharge and motor error established during the single, large uninterrupted saccades.