1. The locus of activity within the superior colliculus (SC) is related to the desired displacement of the eye. Current hypotheses suggest that the location of this locus of activity determines the amplitude of the saccade and that the level of activity at this locus determines eye velocity. We present evidence that suggests that, although the locus determines the amplitude of the saccade, the level of activity in the colliculus encodes dynamic motor error (the difference between desired and current eye displacement). 2. We categorized 86 neurons in the intermediate and deep layers of the superior colliculus of two rhesus monkeys by their activity in relation to the end of saccadic eye movements. In 36% of the cells (n = 31), activity was completely cut off by the end of the saccade (clipped cells). For 53% of cells (n = 46), the major burst of activity ceased by the end of the saccade, but activity continued for 30-100 ms after the end of the movement (partially clipped cells). The remaining 10% of the cells (n = 9) had no clear burst of activity (unclipped cells) but rather had activity that increased gradually before the saccade and then slowly decreased for up to 100 ms after the saccade. These categories were part of a continuum of cell types rather than discrete classes of cells. 3. We first determined whether this new categorization of cells revealed a special relation between the discharge of clipped and partially clipped cells and saccadic amplitude and peak velocity. As expected, we found a steady increase in spike count as saccadic amplitude increased up to the center of the movement field, and an increase in peak spike discharge as peak velocity increased up to a maximum radial eye velocity. Variability in the cell discharge was substantially greater than the variability of saccadic amplitude or peak velocity. We concluded that these single point or averaged measures did not reveal any new functional relationship of these cells. 4. We then examined the relationship of the temporal pattern of discharge of clipped and partially clipped cells to instantaneous changes in radial error and radial velocity. There was a monotonic decay in spike discharge with declining radial error. In contrast, there was a complex, multivalued relationship between spike discharge and radial velocity; collicular cells produced two different values of spike discharge for the same velocity, one during acceleration and the other during deceleration of the eye during a saccade.(ABSTRACT TRUNCATED AT 400 WORDS)
1. One hundred twenty neurons were recorded in the central mesencephalic reticular formation (cMRF) of four rhesus monkeys, trained to make visually guided and targeted saccadic eye movements. Eye movements were recorded with the head fixed, using electrooculography (EOG) or subconjunctival scleral search coils. Seventy-six percent (92/120) of cells discharged before and during contraversive visually guided or targeted rapid eye movements, and 76% of these (70/92) responded during contraversive spontaneous saccades in the dark. cMRF neurons had large contraversive movement fields and either a high (> 10 spikes/s) or low background level of spontaneous activity in the dark. The optimal movement vectors (i.e., saccades with greatest response) were predominantly horizontal, although many had a vertical component. Cells with optimal movement vectors within +/- 25 degrees of pure vertical were more rostral in the MRF and were excluded from the analysis. 2. A subgroup of cMRF neurons (31 of 92) that discharged before and during visually guided saccades were examined for visual sensitivity. Slightly less than one-half of these cells (42%, 13/31) were visuomotor units, i.e., they responded to visual targets in the absence of eye movement. The other 58% (n = 18) did not discharge during the visual probe trial; they were movement-related cells. 3. Microstimulation (threshold 40-60 microA at 333 Hz) at the sites of many of these cMRF neurons produced contraversive saccadic eye movements at short latency (< 40 ms). The amplitude and direction of the elicited saccades were similar to the optimal movement vector determined from single-unit recording. This suggested that cMRF cells recorded at the same locus of electrical microstimulation participated in the network responsible for the production and control of rapid eye movements. 4. The 92 saccade-related neurons were divided into two groups on the basis of their background discharge rate. Firing rates for both low background (28%, n = 26) and high background (72%, n = 66) cells increased approximately 30 ms before contraversive saccades and reached a peak discharge just before saccade onset. The low background neurons had either no activity or generated a few spikes just before the end of ipsiversive saccades. The steady rate of discharge (> 10 spikes/s) of high background neurons was inhibited from approximately 20 ms before ipsiversive saccades until just before saccade end. 5. Cells were also subdivided on the basis of how their discharge rates fell at the end of saccades. Clipped cells (38%, n = 35) had activity that fell sharply with saccade offset. Partially clipped cells (62%, n = 57) had persistent firing in the 100 ms following the saccade that was > 20% higher than the firing during the 100 ms before the saccade. 6. Latencies between the 90% point on the rising edge of the peak discharge and the start of the saccade were < or = 5.3 ms for eye movement-related cells in two monkeys. Longer latencies (11-19 ms) were found when measured between the 10% point on the ris...
1. Recent studies of the monkey superior colliculus (SC) have identified several types of cells in the intermediate layers (including burst, buildup, and fixation neurons) and the sequence of changes in their activity during the generation of saccadic eye movements. On the basis of these observations, several hypotheses about the organization of the SC leading to saccade generation have placed the SC in a feedback loop controlling the amplitude and direction of the impending saccade. We tested these hypotheses about the organization of the SC by perturbing the system while recording the activity of neurons within the SC. 2. We applied a brief high-frequency train of electrical stimulation among the fixation cells in the rostral pole of the SC. This momentarily interrupted the saccade in midflight: after the initial eye acceleration, the eye velocity decreased (frequently to 0) and then again accelerated. Despite the break in the saccade, these interrupted saccades were of about the same amplitude as normal saccades. The postinterruption saccades were usually initiated immediately after the termination of stimulation and occurred regardless of whether the saccade target was visible or not. The velocity-amplitude relationship of the preinterruption component of the saccade fell slightly above the main sequence for control saccades of that amplitude, whereas postinterruption saccades fell near the main sequence. 3. Collicular burst neurons are silent during fixation and discharge a robust burst of action potentials for saccades to a restricted region of the visual field that define a closed movement field. During the stimulation-induced saccadic interruption, these burst neurons all showed a pause in their high-frequency discharge. During an interrupted saccade to a visual target, the typical saccade-related burst was broken into two parts: the first part of the burst began before the initial preinterruption saccade; the second burst began before the postinterruption saccade. 4. We quantified three aspects of the resumption of activity of burst neurons following saccade interruption: 1) the total number of spikes in the pre- and postinterruption bursts, was very similar to the total number of spikes in the control saccade burst; 2) the increase in total duration of the burst (preinterruption period + interruption + postinterruption period) was highly correlated with the increase in total saccade duration (preinterruption saccade + interruption + postinterruption saccade); and 3) the time course of the postinterruption saccade and the resumed cell discharge both followed the same monotonic trajectory as the control saccade in most cells. 5. The same population of burst neurons was active for both the preinterruption and the postinterruption saccades, provided that the stimulation was brief enough to allow the postinterruption saccade to occur immediately. If the postinterruption saccade was delayed by > 100 ms, then burst neurons at a new and more rostral locus related to such smaller saccades became active in associ...
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