ACTIVITY OF NEURONS IN MONKEY SUPERIOR COLLICULUS DURING INTERRUPTED SACCADES

1. Recent studies of the monkey superior colliculus (SC) have identifi ed several types of cells in the intermediate layers (including burst, buildup, and fixation neurons) and the sequence of changes in their a ctivity during the generation of saccadic eye movements. On the basis of these observations, several hypotheses about the organization of th e SC leading to saccade generation have placed the SC in a feedback lo op controlling the amplitude and direction of the impending saccade. W e tested these hypotheses about the organization of the SC by perturbi ng the system while recording the activity of neurons within the SC. 2 . We applied a brief high-frequency train of electrical stimulation am ong the fixation cells in the rostral pole of the SC. This momentarily interrupted the saccade in midflight: after the initial eye accelerat ion, the eye velocity decreased (frequently to 0) and then again accel erated. Despite the break in the saccade, these interrupted saccades w ere of about the same amplitude as normal saccades. The postinterrupti on saccades were usually initiated immediately after the termination o f stimulation and occurred regardless of whether the saccade target wa s visible or not. The velocity-amplitude relationship of the preinterr uption component of the saccade fell slightly above the main sequence for control saccades of that amplitude, whereas postinterruption sacca des fell near the main sequence. 3. Collicular burst neurons are silen t during fixation and discharge a robust burst of action potentials fo r saccades to a restricted region of the visual field that define a cl osed movement field. During the stimulation-induced saccadic interrupt ion, these burst neurons all showed a pause in their high-frequency di scharge. During an interrupted saccade to a visual target, the typical saccade-related burst was broken into two parts: the first part of th e burst began before the initial preinterruption saccade: the second b urst began before the postinterruption saccade, 4. We quantified three aspects of the resumption of activity of burst neurons following sacc ade interruption: I)the total number of spikes in the pre- and postint erruption bursts was very similar to the total number of spikes in the control saccade burst; 2) the increase hi total duration of the burst (preinterruption period + interruption + postinterruption period) was highly correlated with the increase in total saccade duration (preint erruption saccade + interruption;postinterruption saccade); and 3) the time course of the postinterruption saccade and the resumed cell disc harge both followed the same monotonic trajectory as the control sacca de in most cells. 5. The same population of burst neurons was active f or both the preinterruption and the postinterruption saccades, provide d that the stimulation was brief enough to allow the postinterruption saccade to occur immediately. If the postinterruption saccade was dela yed by >100 ms, then burst neurons at a new and more rostral locus rel ated to such smaller saccades became active in association with the sm aller remaining saccade, We interpret this shift in active locations w ithin the SC as a termination of the initial saccadic error command an d the triggering of a new one. 6. Buildup neurons usually had two aspe cts to their discharge a high-frequency burst for saccades of the opti mal amplitude and direction (similar to burst neurons), and a low-freq uency discharge for saccades of optimal direction whose amplitudes wer e equal to or greater than the optimal (different from burst neurons). The stimulation-induced interruption in saccade trajectory differenti ally affected these two components of buildup neuron discharge. The hi gh-frequency burst component was affected in a manner very similar to the burst neurons. However,the low-frequency component was only transi ently affected by the stimulation and resumed immediately after the st imulation, regardless of whether the postinterruption saccade was init iated immediately or delayed beyond 150 ms. These observations indicat e that buildup neurons might carry two independent signals: a high-fre quency burst component that is similar to that in burst neurons, and a low-frequency discharge related to the rostral spread of activity acr oss the SC. 7. The activity of fixation neurons in the rostral pole co ntralateral to the site of stimulation, which typically paused for sac cades and resumed their tonic discharge at the end of the saccade, sho wed a more prolonged pause during the interrupted saccades. The time o f resumption of fixation cell discharge remained highly correlated wit h the termination of the postinterruption saccade, 8. We believe that these observations support the hypotheses that place the SC ina feedba ck loop controlling the amplitude and direction of saccades. In additi on, the observations provide further evidence on the role of the SC in saccade generation: the fixation cells in the rostral SC inhibit the activity of the burst and buildup cells in the caudal SC; the burst ne urons provide the signal for the total desired change in eye position rather than instantaneous motor error; and the activity of burst cells is held at one locus within the SC for a limited time (100-150 ms) fo r each saccade and only then can be released to a new site within the SC.