 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
Volume 17, Number 21, Issue of November 1, 1997 pp. 8566-8579
Copyright ©1997 Society for NeuroscienceNeuronal Activity in Monkey Superior Colliculus Related to the Initiation of Saccadic Eye Movements
Michael C. Dorris, Martin Paré, and Douglas P. Munoz Medical Research Council Group in Sensory-Motor Neuroscience, Department of Physiology, Queen's University, Kingston, Ontario, Canada K7L 3N6
ABSTRACT
The introduction of a temporal gap between the disappearance of an initially fixated target and the appearance of an eccentric saccadic target results in a general reduction of saccadic reaction times (SRTs)
Key words: saccade; oculomotor; reaction times; superior colliculus; monkey; fixation; motor preparation; express saccades; gap effect.the gap effect
INTRODUCTION
Saccades are rapid, conjugate eye movements used to look at visual targets. The time required to initiate a saccade to a suddenly appearing target generally exceeds the conduction time of the shortest neural pathways from the retina to the extraocular muscles (Carpenter, 1981
). A portion of this delay can be eliminated if the initially foveated fixation point is extinguished before the target presentation. The reduction in saccadic reaction times (SRTs) afforded by this gap
Two separate mechanisms have been hypothesized to account for the gap effect and express saccade occurrence (for detailed discussion, see Paré and Munoz, 1996
The main goal of this study is to understand the neural basis of SRTs and to distinguish between the two hypotheses of express saccade generation. We used extracellular recording techniques to measure changes in neuronal activity before target appearance in the monkey superior colliculus (SC), a structure hypothesized to be involved in saccade initiation. Collicular saccade-related neurons discharge a discrete high-frequency burst of action potentials for saccades to a restricted region of the visual field and often respond to the presentation of visual stimuli (Wurtz and Goldberg, 1972
Some of these results have been reported in preliminary form elsewhere (Dorris and Munoz, 1995
MATERIALS AND METHODS
Animal preparation. We recorded the extracellular activity of single neurons in the intermediate layers of the SCs of two male rhesus monkeys (Macaca mulatta) weighing 5-6 kg each. All procedures were approved by the Queen's University Animal Care Committee and complied with the guidelines of the Canadian Council on Animal Care. Animals were under the close supervision of the university veterinarian.
Each monkey underwent a single surgical session to prepare for chronic recording of eye position and single neurons (Paré and Munoz, 1996
Experimental procedures. Throughout the duration of the experiments, the monkeys were seated in a primate chair with their heads firmly attached to the chair via a head holder embedded in the explant. The monkeys faced a tangent screen 86 cm away, which spanned ±35° of the central visual field. Behavioral paradigms, visual displays, and storage of both neuronal discharge and eye movement data were under the control of a 486 personal computer running a real-time data acquisition system (REX) (Hays et al., 1982
The single-neuron activity was recorded with tungsten microelectrodes (Frederick Haer; 1-2 M at 1 kHz), which were lowered through 23 gauge stainless steel guide tubes by a hydraulic microdrive (Narishige, Tokyo, Japan) attached to the recording chambers. The guide tubes were held firmly within a Delrin grid inside the recording chambers (Crist et al., 1988
Behavioral paradigms. Monkeys were initially trained to sit and drink water in the primate chair. They received a liquid reward when their eye position entered the invisible computer-controlled window surrounding a spot of light projected on the screen [hereafter referred to as the fixation point (FP)]. Over the ensuing days of training, the length of time of fixation was increased, whereas the size of the computer-controlled window was decreased. After learning to fixate for prolonged periods, the monkeys were trained to make a saccade to the spot of light when it stepped to an eccentric position (hereafter referred to as the target).
The monkeys were trained to perform the gap paradigm (Fig. 1). Trials were preceded by an intertrial interval (varied randomly between 500 and 1000 msec) during which the screen was illuminated with diffuse white light (1.0 cd/m2) to prevent dark adaptation. The onset of a trial was signaled by the removal of this background light and appearance of the central FP. The monkey was required to look at the FP and to maintain fixation for 500-1000 msec. The FP was then extinguished, and there was a period (gap) during which the animal had to maintain fixation in total darkness before an eccentric target was presented. Within a block of trials, the gap duration was set at a constant duration of 200 msec or randomized between 0 (no gap), 100, 200, 300, 400, 600, and 800 msec. The 200 msec gap was chosen, because a significant percentage of express saccades are produced under this condition (Fischer and Boch, 1983 
Fig. 1. Schematic of the gap paradigm. Time is represented on the horizontal axis, and presentation of the visual stimuli (FP, central fixation point; T, eccentric target) are denoted by the horizontal gray bars. As in the following figures, an upward deflection of the horizontal eye trace (E) represents a rightward movement, and downward deflection represents a leftward movement. The visual fixation interval was randomized between 500 and 1000 msec, and the gap duration was either set at 200 msec or randomized between 0 and 800 msec within a block of trials. The discharge rate of neurons during this task was calculated during the final 100 msec of FP presentation (visual fixation epoch, t1) and from 50 msec before to 50 msec after target presentation (end of gap epoch, t2).[View Larger Version of this Image (18K GIF file)]
In a separate block of 50-120 trials, the gap was fixed at 0 msec (no gap), and target eccentricity was randomly interleaved at eight locations in the optimal direction to ascertain the optimal saccadic vector of each neuron and to determine its movement field characteristics using criteria described by Munoz and Wurtz (1995a) 20°), the FP was positioned on one side of the visual screen, and the target appeared on the opposite side. Thus, target steps of up to 70° eccentricity in either the horizontal or the vertical plane were possible. The maximum amplitude tested for each neuron was at least 60°.
Once a neuron was isolated, and until either the isolation was lost or the series of paradigms was completed, the monkey usually performed the paradigms as follows: (1) the gap paradigm was run with a block of 200 msec gap trials in an effort to obtain a sufficient sample of express and regular saccades; (2) the gap duration was randomized between 0 and 800 msec to determine how neuronal activity evolved over longer gap durations; and (3) in the case of saccade-related neurons, 0 msec gap trials with target amplitude randomized along the optimal direction were run to determine the extent of the movement field of the neuron.
Data analysis. A Sun Sparc2 workstation was used to analyze the data. Computer software determined the beginning and end of each saccade using velocity and acceleration threshold and template-matching criteria (Waitzman et al., 1991 . To analyze population responses during the gap, we convolved the spike train of each neuron with a Gaussian pulse width of 10 msec to generate the spike density function for each gap duration. This value was chosen because it provided sufficient smoothing of the envelope of neuronal discharge without losing important details. The use of smaller Gaussian pulse (e.g., 4 msec) added more noise to the shape of the spike density function without altering the overall shape.
To quantify the gap-related changes in neuronal activity, the discharge rate of individual neurons was measured during two different intervals in the gap paradigm: (1) the final 100 msec before the FP was extinguished, while the monkey was fixating the FP (visual fixation epoch; Fig. 1, t1); and (2) the interval from 50 msec before target appearance to 50 msec after target appearance (end of gap epoch; Fig. 1, t2). All SC neurons in our sample that had target-related responses had response latencies >50 msec. Therefore, sampling during the t2 epoch yielded a measure of activity immediately before any change that could be induced by the appearance of the eccentric target. This was a necessary prerequisite to test appropriately the hypotheses that express saccades are caused by changes in neuronal activity before target appearance related to either advanced motor preparation or disengagement of ocular fixation.
Trial-by-trial correlations (Pearson's r) between SRT and the discharge rate during these two epochs were calculated for each neuron. Two statistical methods were used to determine which factors, neuron type, epoch (t1 or t2), or target location (contralateral or ipsilateral), were involved in any correlations. First, the proportion of neurons with statistically significant correlation coefficients was calculated for each condition. Second, comparisons between the cumulative distributions of correlation coefficients were performed for each condition using a one-way ANOVA followed by an all-pair-wise multiple comparison procedure (Student-Newman-Keuls method).
To quantify the changes in activity preceding express and regular saccades, the level of activity during the visual fixation (t1) and end of gap (t2) epochs was computed separately for express and regular saccades. Examples of the SRT distributions during a block of 200 msec gap trials for the two monkeys are shown in Figure 2. Based on the bimodality of the SRT distributions of the two monkeys, express saccades were defined arbitrarily as those initiated 70-120 msec after target appearance, whereas regular saccades were defined as those initiated 130-180 msec after target appearance. This nomenclature is consistent with that developed by Fischer and colleagues (for review, see Fischer and Weber, 1993 
Fig. 2. Typical SRT histograms obtained during a block of 200 msec gap trials. Only the SRT distributions from one of two possible target locations is shown for each monkey. Hatched bars represent express saccades (70-120 msec), and filled bars represent regular latency saccades (130-180 msec).[View Larger Version of this Image (16K GIF file)]
Edelman and Keller (1996)
To determine the magnitude of target- and saccade-related bursts of action potentials exhibited by saccade-related neurons, the maximum value reached by spike density functions constructed from rasters aligned on the time of occurrence of the target and the saccade were used, respectively. The spike density functions were constructed from the average of rasters only from neurons with at least five trials of both express and regular saccades. Specifically, the target-related burst was considered the largest peak in the target-aligned spike density function that occurred between 60 and 120 msec after target presentation. The saccade-related burst was considered the largest peak in the saccade-aligned spike density function that occurred closest to the time of saccade initiation that was not more than ±20 msec from saccade initiation.
Neuron classification. We separated our neurons into three different classes of SC neurons based on the previous descriptions of Munoz and Wurtz (1993a)
RESULTS
Of all the neurons recorded from both SC of two monkeys performing the gap paradigm, only 159 fulfilled our classification criteria and had a significant portion of the testing completed to be analyzed. According to our criteria, 29% (46 of 159) were fixation, 19% (30 of 159) were buildup, and 52% (83 of 159) were burst neurons.Gap-related neuronal activity
The tonic activity of fixation neurons was modulated in a characteristic manner during the gap period (Dorris and Munoz, 1995
Fig. 3. The activity of a single fixation (A, B) and buildup (C, D) neuron during 600 msec gap trials. The fixation neuron was located in the right SC, and the target was presented 10° left (A, contralateral target) or 10° right (B, ipsilateral target). The buildup neuron was located in the left SC, and the target was presented 10° right (C, contralateral target optimal vector for the response field of this neuron) or 10° left (D, ipsilateral target opposite the response field of this neuron). Trials were collected in a block of trials in which gap duration was randomized between 0, 100, 200, 300, 400, 600, and 800 msec, and the target appeared randomly 10° to the right or left. The individual rasters of neuron discharge, the spike density function, and the horizontal eye position traces are aligned on both FP disappearance (left vertical line) and target onset (right vertical line).[View Larger Version of this Image (42K GIF file)]
Fig. 4. Reciprocal pattern of activity for the sample of fixation and buildup neurons during fixed 200 msec (46 fixation and 30 buildup neurons) (A) and randomized 600 msec (B) gap trials (31 fixation and 15 buildup neurons). The thick line represents the mean spike density, and the envelope surrounding each waveform represents the SEM.[View Larger Version of this Image (27K GIF file)]
The activity of a single buildup neuron recorded in the left SC is shown in Figure 3 for 600 msec gap trials and the target presented 10° right (Fig. 3C, contralateral target) and 10° left (Fig. 3D, ipsilateral target). The neuron had very little activity while the monkey was fixating the FP. During the gap, an increase in neuronal activity began slightly more than 100 msec after the FP disappeared. This discharge remained at a tonic level until target appearance, when a burst of activity occurred for saccades of the optimal vector (Fig. 3C), or the activity was truncated for saccades in the opposite direction (Fig. 3D). The pattern of activity of buildup neurons during the gap period was reciprocal to that recorded from fixation neurons (Fig. 4A,B). Before disappearance of the FP, the mean discharge rate of the buildup neurons was low, averaging ~10 spikes/sec. Approximately 100 msec after FP disappearance the activity of buildup neurons began to increase abruptly. After ~250 msec into the gap, buildup neurons reached their peak level of discharge, which decreased slightly with increasing gap duration (Fig. 4B).
The distribution of mean discharge rates of individual fixation and buildup neurons during the visual fixation (t1) and end of gap (t2) epochs is illustrated in Figure 5. Most fixation neurons decreased their discharge during the gap, and greater activity during visual fixation was generally associated with greater activity at the end of the gap (n = 46; slope = 0.51; r = 0.79; p < 0.001) (Fig. 5A). By definition, all buildup neurons increased their discharge during the gap, but the level of activity reached at the end of the gap was also related to that observed during visual fixation (n = 30; slope = 1.62; r = 0.85; p < 0.001) (Fig. 5B). 
Fig. 5. Mean discharge rate of individual fixation (A) and buildup (B) neurons during the visual fixation (t1) and end of gap (t2) epochs during 200 msec gap trials. Each data point represents a single neuron. Lines of equality are represented by dashed lines, and linear regression lines are represented as solid lines.[View Larger Version of this Image (19K GIF file)]
Relationship between SRT and neuronal activity
We investigated whether specific measures of the neuronal activity of fixation and buildup neurons before or during the gap period was predictive of SRT on a trial-by-trial basis. Because the activity of both fixation and buildup neurons was modulated with gap duration (see Fig. 4), randomizing gap duration could act as a confounding variable. In addition, the effects on neuronal activity of the presence of the FP in trials with a short gap duration (i.e., 0 and 100 msec) introduced an uncontrolled variable. This analysis was therefore performed in two ways. First, analysis was performed using data collected from blocks of trials in which the gap was maintained at a constant duration of 200 msec. Second, the effects of different gap durations on data analysis were considered separately by examining the SRT in blocks of trials in which the gap duration was randomized between 0 and 800 msec. The discharge rate was calculated during the t1 and t2 epochs for each trial and was plotted against the corresponding SRT for that trial. A minimum of 12 trials for a neuron was used in this analysis, although the majority of neurons had between 30 and 100 trials. Using linear regression analysis of the relationship between SRT and discharge rate, correlation coefficients were calculated for each individual neuron, for the two epochs, for the contralateral and (when possible) ipsilateral targets.
We first describe the results of the analysis of the data collected from blocks of 200 msec gap duration trials. Examples of the relationships and correlations obtained for one fixation and one buildup neuron for 200 msec gap duration trials are illustrated in Figure 6. No significant relationship existed between SRT and discharge rate during the visual fixation (t1) epoch for any of the conditions in either of the two neurons shown (p > 0.05) (Fig. 6A,C,E,G). Nor did a significant relationship exist between SRT and the discharge rate during the end of the gap (t2) epoch (Fig. 6B,D,H), with the exception of the buildup neuron activity associated with the contralateral target (r = 0.62; p < 0.001) (Fig. 6F). In this case, the greater the activity, the shorter the SRT.
Fig. 6. Linear regression and correlation between SRT and discharge rate of individual fixation and buildup neurons for data collected in blocks of trials with the gap duration fixed at 200 msec. Each data point was obtained from a single trial from either single fixation (A-D) or buildup (E-H) neuron. Neuronal activity was sampled during the visual fixation (t1) and end of gap (t2) epochs before targets presented contralateral and ipsilateral. *Statistically significant correlation (p < 0.05).[View Larger Version of this Image (25K GIF file)]
Table 1 shows the proportion of fixation and buildup neurons that had significant correlations (p < 0.05) between SRT and discharge rate. For the data collected from blocks of trials with a constant gap duration of 200 msec, the neuronal activity of fixation neurons was not well correlated for any of the epochs or target location tested; <15% of the neurons showed significant correlations in any condition. Buildup neuron activity was also poorly correlated with SRT, except at the end of gap (t2) epoch before saccades into their contralateral response field. In this condition, 41% (12 of 29) of the buildup neurons had discharge rates that were significantly correlated to SRT. A factor that may have limited the proportion of neurons showing a significant correlation between SRT and mean discharge rate was the limited distribution of SRTs obtained during many recordings. For some neurons, the distribution of SRTs obtained was unimodal with very little variance. Also summarized in Table 1 is the percentage of fixation and buildup neurons having significant correlations between SRT and discharge rate in the t1 and t2 epochs with the data set obtained from randomized gap trials of 0-800 msec. This data set usually contained a wider range of SRTs and a greater number of trials. The neuronal activity of fixation neurons was not well correlated for any of the epochs or target locations tested. Although the percentage of significant correlations increased with respect to the results of the analysis restricted to the 200 msec gap trials, it never reached 25% in any condition. Buildup neuron activity was also poorly correlated with SRT, except before saccades into their contralateral response field. In this condition, 33% (5 of 15) of the buildup neurons had discharge rates that were significantly correlated to SRT for the t1 epoch, and 53% (8 of 15) had significant correlations for the t2 epoch.
Table 1. Percentage of neurons with significant correlation coefficients between SRT and neuronal discharge
Neuron Gap (msec) Contralateral target Ipsilateral target t1 t2 t1 t2 Fixation 200 msec 11% (5/44) 14% (6/44) 5% (2/40) 10% (4/40) Random 16% (5/31) 13% (4/31) 23% (7/31) 16% (5/31) Buildup 200 msec 14% (4/29) 41% (12/29) 11% (2/19) 11% (2/19) Random 33% (5/15) 53% (8/15) 18% (2/11) 23% (3/11)
Another method to isolate which, if any, of the combinations of neuron types, target locations, and epoch discharge rates are most related to SRT compares distributions of cumulative correlation coefficients (adapted from Riehle and Requin, 1993 
Fig. 7. Correlation coefficients between SRT and discharge rate of individual neurons plotted as a cumulative distribution. All data were collected from blocks of trials with the gap duration fixed at 200 msec. Each data point represents the correlation coefficient from one neuron when the activity was sampled during different epochs or target locations. A, The fixation neuron distributions were centered around zero and did not differ from each other (ANOVA, p > 0.05). B, The distribution made from buildup neuron activity during the t2 epoch and for the contralateral target was shifted to the left of zero and differed from the other buildup neuron distributions (ANOVA, Student-Newman-Keuls method, p < 0.05). C, The distribution composed from the correlation coefficients of the t2 contralateral target buildup neurons differed significantly from the distribution composed of the t2 contralateral target fixation neuron distribution (t test, p < 0.01).[View Larger Version of this Image (27K GIF file)]
Figure 7A shows the cumulative correlation coefficient distributions for fixation neurons for two epochs (t1 or t2) and two target locations (contralateral or ipsilateral). All four curves closely overlap, suggesting that neither direction of the target nor the epoch influenced the correlation between SRT and the discharge rate of these neurons. There was no significant difference among these fixation neuron curves (ANOVA, p > 0.05). Furthermore, the four mean values of these fixation neuron distributions varied little from zero (Table 2), further demonstrating the lack of predictive value of fixation neuron activity for SRT. The cumulative correlation coefficient distributions constructed for buildup neurons (Fig. 7B) did not differ from one another (Student-Newman-Keuls method, p > 0.05) with the exception of the buildup neuron curve for the t2 epoch when the target was presented at the contralateral location (Student-Newman-Keuls method, p < 0.05). For the three conditions in which the distributions did not differ, the three mean values did not vary much from zero (Table 2), whereas the curve constructed from the buildup neuron correlation coefficients from the t2 epoch and the contralateral target had a mean correlation value of
Table 2. Means of correlation coefficients between SRT and neuronal discharge rate
Neuron Gap (msec) Contralateral target Ipsilateral target t1 t2 t1 t2 Fixation 200 0.01 Buildup 200 0.02
It is not surprising that the most important epoch in which neuronal activity can influence SRT is the end of gap (t2) epoch just before target presentation. This epoch represents the level of neuronal activity just before visual target information reaching the SC. Figure 7C compares the correlation values of buildup and fixation neurons during the t2 epoch when the target is presented in the contralateral direction. This further exemplifies the degree to which buildup activity is a better predictor of upcoming SRT with its curve being clearly shifted from zero compared with that of fixation neurons (t test, df = 71; t = 3.59; p < 0.001). Neuronal activity and express saccades
We have shown that the activity of fixation neurons and buildup neurons was modulated during the gap period. However, SRT was best reflected by the activity of buildup neurons during the end of gap (t2) epoch before saccades into the response field of the neuron. We now ask the more specific question of whether, before the appearance of the target, the activity of either of these neuron populations is related to the occurrence of express saccades produced in the gap paradigm. According to the fixation disengagement and oculomotor preparation hypotheses, the activity of fixation and buildup neurons, respectively, should be correlated to the generation of express saccades through their effect on the saccade-generating circuit before target presentation. To test these hypotheses, the activity of individual neurons recorded during the constant 200 msec gap trials was segregated on the basis of whether the SRTs were of express or regular latency.
Target-aligned rasters and spike density functions of the activity of a fixation neuron are shown in Figure 8A for the generation of express (top) and regular saccades (middle). The typical gap-related decrease in fixation neuron activity beginning ~100 msec into the gap was observed for both types of saccades. The two spike density functions are superimposed at the bottom of Figure 8A, and, except for the earlier pause in activity associated with the shorter latency express saccades, there was little difference between them at either the t1 or t2 epoch (t test, p > 0.05). In contrast, the gap-related discharge rate of the buildup neuron was much higher before express saccades than before regular saccades, as shown by the superposition of spike density functions (Fig. 8B). This was quantified by measuring the activity at the end of the gap (t2) epoch (t test, df = 18; t = 3.56; p < 0.005). In addition, after target appearance, the buildup neuron discharged only one burst of action potentials for express saccades but two bursts for regular saccades. During regular saccade trials, the first burst began ~70 msec after target appearance, whereas the second burst was aligned with the occurrence of the saccade. During express saccade trials, the single burst was aligned with both target appearance and saccade occurrence. The merging of the two bursts during express saccades was also observed for those burst neurons showing two bursts of action potentials for regular saccades (Fig. 9A). This latter finding corroborates observations of visuomotor burst neurons previously reported by Edelman and Keller (1996) 
Fig. 8. Comparison of neuronal discharge during the generation of express and regular saccades in 200 msec gap trials. The spike density functions generated from express (top, solid line) and regular (middle, dashed line) trials are aligned on target appearance and superimposed at the bottom. A, The spike density functions constructed from a fixation neuron did not differ (t test, p > 0.05). B, The end of gap (t2) discharge rate of the buildup neuron was greater before express saccade generation compared with the generation of regular saccades (t test, p < 0.005). When the scale is expanded to 300 spikes/sec, the spike density function generated for regular saccades displayed two peaks: one burst time locked to the appearance of the visual stimulus and a later burst time locked to the generation of the saccade. The spike density function for express saccades had only one robust peak time locked to both target and saccade onsets.[View Larger Version of this Image (41K GIF file)]
Fig. 9. Comparison of neuronal discharge during the generation of express and regular saccades in 200 msec gap trials for burst neurons. The spike density functions generated from express (top, solid line) and regular (middle, dashed line) trials are aligned on target appearance and superimposed at the bottom. A, Spike density functions constructed from a burst neuron with target-related activity. B, Spike density functions constructed from a burst neuron without target-related activity.[View Larger Version of this Image (35K GIF file)]
From our sample, 24 fixation neurons and 17 buildup neurons could be analyzed quantitatively (minimum of five trials of both express and regular saccades). Figure 10 shows the individual discharge rates of these neurons associated with express and regular saccades during visual fixation (t1) and end of gap (t2) epochs. Figure 11 contrasts the mean discharge rates for the sample of neurons. Data obtained from 41 burst neurons, the gap-related discharges of which were usually minimal (Fig. 9), are also presented in Figure 11. During the visual fixation (t1) epoch, discharge rates of most fixation and buildup neurons preceding express and regular saccades were similar, being distributed around the line of equality (Fig. 10A). The mean discharge rate ± SEM of fixation neurons (Fig. 11A) was 55 ± 6 (range, 17-138) spikes/sec before express saccades and 55 ± 5 (range, 17-114) spikes/sec before regular saccades (paired t test, df = 23; t = 0.164; p = 0.87). Furthermore, no individual fixation neuron had significantly different discharge rates preceding express and regular saccades (t test, p > 0.05). The mean discharge rate of buildup neurons (Fig. 11C) was 22 ± 4 (range, 1-50) spikes/sec before express saccades and 16 ± 3 (range, 0-43) spikes/sec before regular saccades. This small difference was statistically significant (paired t test, df = 16; t = 5.10; p < 0.0001). Among individual buildup neurons, 3 of 17 had a significantly higher rate of discharge preceding express saccades (t test, p < 0.05). The mean discharge rate of burst neurons during the visual fixation (t1) epoch (Fig. 11E) was 8 ± 2 (range, 0-33) spikes/sec before express saccades and 6 ± 1 (range, 0-26) spikes/sec before regular saccades. This small difference was statistically significant (Wilcoxon signed rank test, p < 0.01). Thus, during the visual fixation (t1) epoch, the mode of saccade initiation could not be predicted on the basis of activity of fixation neurons, and the predictive capability of buildup and burst neurons in terms of absolute changes in mean discharge rate was minimal. 
Fig. 10. Mean discharge rate before express and regular saccades of 17 buildup neurons and 24 fixation neurons during the visual fixation (t1; A) and the end of gap (t2; B) epochs. The dotted line represents the equality line.[View Larger Version of this Image (21K GIF file)]
Fig. 11. Mean discharge rate before express and regular saccades for the population of fixation (A, B), buildup (C, D), and burst (E, F) neurons during visual fixation (t1) (A, C, E) and the end of gap epochs (t2) (B, D, F).Significant difference between visual fixation (t1) and end of gap (t2) epochs. *Significant difference between express and regular saccades within a sampling period.
[View Larger Version of this Image (36K GIF file)]
During the end of the gap (t2) epoch, the mean discharge rate of fixation neurons for both express and regular saccades was significantly lower compared with that during visual fixation (t1) epoch (paired t test, p < 0.05), whereas the mean discharge rate of buildup and burst neurons during t2 was significantly increased over t1 (paired t test, p < 0.05). The mean discharge rate of fixation neurons (Fig. 11B) was 39 ± 4 (range, 15-74) spikes/sec before express saccades and 41 ± 3 (range, 18-80) spikes/sec before regular saccades (paired t test, df = 23; t =
If the hypothesis that the level of buildup neuron activity before target appearance is predictive of the mode of saccade initiation, then the level of activity should be higher for express saccades regardless of gap duration. We therefore also used a second method to analyze the activity level of both fixation and buildup neurons for those blocks of trials in which the gap duration was randomized between 0 and 800 msec. The number of neurons yielding data sufficient for analysis (17 fixation neurons and 6 buildup neurons) was lower than for the obtained from the constant 200 msec gap trials, because not all neurons were tested in this condition, and often the number of trials yielding express saccades was reduced. Nevertheless, the same pattern of neuronal activity with respect to mode of saccade latency was manifest; during the end of gap (t2) epoch, buildup neuron activity best predicted the mode of saccade latency. During the visual fixation (t1) epoch there was no difference in the mean discharge rate of either class of neuron before express or regular latency saccades. The mean discharge rate ± SEM of fixation neurons was 58 ± 6 (range, 22-114) spikes/sec before express saccades and 63 ± 7 (range, 25-134) spikes/sec before regular saccades (paired t test, df = 16; t = Timing of target-related responses
We have shown that buildup and burst neurons had a higher level of activity at the time of target presentation before the generation of express saccades. Because buildup and burst neurons with both target- and saccade-related responses for regular saccades show only one burst of action potentials for express saccades (Figs. 8B, 9A; also see Edelman and Keller, 1996
Fig. 12. Difference in the target-related burst onset between express and regular saccades of buildup (A) and burst (B) neurons. The majority of burst and buildup neurons showed positive differences, thereby indicating that the burst occurred later after target appearance for regular than express saccades.[View Larger Version of this Image (26K GIF file)]
Magnitude of target- and saccade-related responses
It has been hypothesized that express saccades result from target-related responses of SC saccade-related neurons becoming the saccadic trigger signal (Sommer 1994
Fig. 13. Comparison between express (abscissa) and regular (ordinate) saccades in the magnitude of the peak of the target-aligned burst of activity (A) and saccade-aligned burst of activity (B) of buildup (filled squares) and burst (open triangles) neurons. C, Comparison between the magnitude of the peak of the target-aligned (abscissa) and saccade-aligned (ordinate) bursts for regular saccades. The dotted line represents the equality line.[View Larger Version of this Image (31K GIF file)]
Despite the significant difference in the magnitude of the target-aligned burst for express and regular saccades, there was no difference in the magnitude of the saccade-aligned bursts. Figure 13B contrasts for express and regular saccades the magnitude of the saccade-aligned burst for the same burst and buildup neurons. Note that most data points scatter along the equality line, indicating that the saccade-aligned burst of express and regular saccades was of similar magnitude. For buildup neurons, the mean peak burst rate was 446 ± 44 spikes/sec before express saccades and 447 ± 41 spikes/sec before regular saccades (paired t test, df = 10; t =
DISCUSSION
We have shown that neuronal activity within the SC is modulated in the gap period of the gap paradigm before target presentation in a manner that could account for variation in SRT, including both the gap-related reduction in SRTs and the occurrence of express saccades. The attenuation of fixation neuron activity during the gap may represent a disengagement of ocular fixation (Reuter-Lorenz et al., 1991Collicular role in the gap effect and express saccade generation
The activity of SC neurons is likely shaped by sensory, motor, and cognitive inputs (for review, see Sparks and Hartwich-Young, 1989
While the FP is present, both sensory (foveal visual inputs) and cognitive (the monkey's reward is contingent on foveation of the FP) signals are at their highest level, centered on fixation neurons on the SC saccadic motor map. This results in vigorous activation of fixation neurons and inhibition of saccade-related neurons in the rest of the SC through hypothesized lateral interactions (Munoz and Guitton, 1991
Disappearance of the FP during the gap removes sensory inputs to fixation neurons, leading to a disinhibition of saccade-related neurons. In this case, when the target is presented, less time is required for saccade-related neurons to generate the saccade motor command, and the SRT is reduced, the gap effect. In addition, the onset of the gap may be associated with the impending target appearance (Ross and Ross, 1981
Although we propose that the generation of express saccades is facilitated by the reduced inhibition afforded by attenuated fixation neurons, we have shown that fixation neuron attenuation is, by itself, insufficient to account for express saccade generation. Rather, our data suggest that the increase in the activity of buildup neurons coding for the upcoming target location is necessary for express saccade generation. This localized increase in activity may be caused by inputs related to the monkey's expectation or familiarity of where the target is most likely to be presented after the gap (Paré and Munoz, 1996
Earlier studies by Munoz and Wurtz (1992 Target-related responses and SRT bimodality
The excitability levels of fixation and buildup neurons established by sensory and cognitive inputs before target presentation fulfill predictions of mathematical models of SRT reductions during the gap paradigm (Carpenter and Williams, 1995
The necessity of the transient target-related burst of saccade-related neurons for the generation of express saccades explains other findings particular to this class of saccades. For example, express saccades cannot be generated to targets illuminated continuously, as in the delayed saccade paradigm in which the FP disappearance is the cue to initiate the saccade (Boch and Fischer, 1986 Early increase in activity and preparation for action
Saccadic eye movements are not the only motor responses for which early changes in neuronal activity can be related to preparatory processes. For instance, Requin and colleagues (Lecas et al., 1986
FOOTNOTES
Received June 3, 1997; revised Aug. 11, 1997; accepted Aug. 18, 1997.
This work was supported by the Medical Research Council of Canada. D.P.M. is a research scholar of the EJLB Foundation. We thank D. Hamburger and A. Lablans for technical assistance, P. Istvan, who participated in some of these experiments, and D. Hanes for supplying the algorithm for the Poisson spike train analysis.
Correspondence should be addressed to Douglas P. Munoz, Department of Physiology, Queen's University, Kingston, Ontario, Canada K7L 3N6.
REFERENCES
- Becker W (1989) Metrics. In: The neurobiology of saccadic eye movements (Wurtz RH, Goldberg ME, eds), pp 13-67. Amsterdam: Elsevier.
- Boch R, Fischer B (1986) Further observations on the occurrence of express-saccades in the monkey. Exp Brain Res 63:487-494[ISI][Medline].
- Carpenter RHS (1981) Oculomotor procrastination. In: Eye movements: cognition and visual perception (Fischer DF, Monty RA, eds), pp 237-246. Hillsdale, NJ: Erlbaum.
- Carpenter RHS, Williams MLL (1995) Neural computation of log likelihood in control of saccadic eye movements. Nature 377:59-62[Medline].
- Chou I, Sommer MA, Schiller PH (1994) Bimodal latency distribution of averaging saccades in monkey. Soc Neurosci Abstr 20:1401.
- Crist CF, Yamasaki DSG, Komatsu H, Wurtz RH (1988) A grid system and a microsyringe for single cell recording. J Neurosci Methods 26:117-122[ISI][Medline].
- Dias EC, Bruce CJ (1994) Physiological correlate of fixation disengagement in the primate's frontal eye field. J Neurophysiol 72:2532-2537
[Abstract/Free Full Text] .- Dorris MC, Munoz DP (1995) A neural correlate for the gap effect on saccadic reaction times in monkey. J Neurophysiol 73:2558-2562
[Abstract/Free Full Text] .- Dorris MC, Paré M, Istvan PJ, Lablans A, Munoz DP (1995) Saccadic reaction times in the monkey. II. Neural correlates in the superior colliculus. Soc Neurosci Abstr 21:1193.
- Edelman JA, Keller EL (1996) Activity of visuomotor burst neurons in the superior colliculus accompanying express saccades. J Neurophysiol 76:908-926
[Abstract/Free Full Text] .- Evarts EV, Shinoda Y, Wise SP (1984) In: Neurophysiological approaches to higher brain functions. New York: Wiley.
- Everling S, Krappmann P, Spantekow A, Flohr H (1996) Cortical potentials during the gap before express saccades and fast regular saccades. Exp Brain Res 111:139-143[ISI][Medline].
- Fischer B, Boch R (1983) Saccadic eye movements after extremely short reaction times in the monkey. Brain Res 260:21-26[ISI][Medline].
- Fischer B, Ramsperger E (1984) Human express saccades: extremely short reaction times of goal directed eye movements. Exp Brain Res 57:191-195[ISI][Medline].
ABSTRACT
