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 bu rst neurons( SRBNs) found in the intermediate layers of the superior c olliculus (SC) in the alert, behaving monkey. These burst cells are no rmally the first neurons recorded during radially directed microelectr ode penetrations of the SC after the electrode has left the more dorsa lly situated visual layers. They have spatially delimited movement fie lds 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. Man y of these cells, when recorded during saccade trials, also have an ea rly, transient visual response and an irregular prelude of presaccadic activity.2. Because saccadic eye movements normally have very stereot yped durations and velocity trajectories that vary systematically with saccade size, it has been difficult in the past to establish quantita tively whether the activity of SRBNs temporally codes dynamic saccadic control signals, e.g., dynamic motor error or eye velocity, where dyn amic motor error is defined as a signal proportional to the instantane ous difference between desired final eye position and the actual eye p osition during a saccade. It has also not been unequivocally establish ed whether SRBNs participate in an organized spatial shift of ensemble activity in the intermediate layers of the SC during saccadic eye mov ements. 3. To address these issues, we studied the activity of SRBNs u sing an interrupted saccade paradigm. Saccades were interrupted with p ulsatile electrical stimulation through a microelectrode implanted in the omnipauser region of the brain stem while recordings were made sim ultaneously from single SRBNs in the SC.4. Shortly after the beginning of the stimulation (which was electronically triggered at saccade ons et), the eyes decelerated rapidly and stopped completely. When the hig h-frequency (typically 300-400 pulses per second) stimulation was term inated (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 wer e 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 sac cade and continued during this saccade even though it had a much small er amplitude than would normally be associated with significant discha rge for caudal SC cells. The resumption of discharge in caudal SRBNs d uring the resumed saccades suggests that the colliculus is inside a dy namic local feedback loop from brain stem circuits controlling saccade s (i.e., they are part of a network that sensed the braking of the sac cade 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 co ntrast, when we recorded from SRBNs with less eccentric movement field s that are located anatomically near the middle of the SC (along its r ostral-to-caudal axis), we found no or only minimal activity during re sumed 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 tha t the population of active SRBNs does not shift on the colliculus duri ng a saccadic eye movement. 7. We attempted to relate the magnitude of the second burst of activity in SRBNs during the resumed saccade to p resumed motor error relationships calculated from data gathered during uninterrupted saccades from the same block of trials. The average ren ewed discharge measured just before the start of the resumed saccade w as 42% greater than that measured at similar values of motor error dur ing uninterrupted movements. In contrast, peak saccadic eye velocity d uring the resumed saccade was lower than the normal saccadic velocity measured in the same animals. The eyes were undergoing maximum acceler ation at the onset of the resumed saccade, which suggests that the hig her discharge of SRBNs might be correlated with this dynamic signal. O verall, the results suggest that the discharge of SRBNs does not quant itatively 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 uninter rupted saccades.