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According to this simulation, the chance levels of trial success rates are When inhibition of return was imposed, the chance levels were higher at Events in this task were the same as in the MEM task above, except one feature that the red targets remained visible throughout the trial. Therefore, the animals did not need to rely on short-term memory to reach the second target and onwards. In both tasks, saccade targets were selected based on salient color contrast. While VIS did not require memory of the targets, the planning and execution of sequential saccades was comparable with MEM.

Other details, such as constraints on the response period and behavioral measures were the same in both. Markers were set for all experimental events for off-line analysis. This was performed on-line to control the events in the behavioral tasks, such as detecting the first saccade and hiding targets in MEM. Correct detection of saccade onsets was confirmed during off-line data analysis. Given the matrix arrangement of the visual stimuli, saccades were judged as directed to the nearest disc, regardless of the absolute distance from the disc to the saccade end-point.

In other words, a saccade was judged as directed to a disc if it ended within a square window of degree width and height centered at the disc. A cortical sites of electrode penetration was regarded as within the FEF if a saccade was evoked with a probability greater than 0. For each track of penetration, the electrode was slowly lowered by a electrical microdrive NAN Instruments Ltd, Nazareth, Israel and responses to ES were checked at every 0.

The depth with the lowest threshold of ES-evoked saccades was marked on the way into the cortex and confirmed again on the way out. A The multi-target visual short-term memory and pop-out search tasks. After fixation at the central square, a set of discs were shown in either red or green. The red discs were saccade targets defined by the color contrast. In the multi-target memory-guided saccade task MEM, upper panel , the targets were rendered indistinguishable from non-targets as soon as the first saccade was initiated.

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The animal therefore had to rely on short-term memory for subsequent saccades. In the visually-guided saccade task VIS, lower panel , the targets were visible while the animal made a series of saccades to each target, obviating the need for memory. B Sites in the FEF are shown where saccades were evoked by electrical stimulation black circles. Red and blue arrowheads mark the penetrations with injection of muscimol red or normal saline blue , whereas a circular head indicates sites that were tested but not infused.

Each arrow coming from a circle represents the vector of saccades evoked at the site and depth of injections. Some sites were penetrated more than once, and the lines were slightly shifted for clarity.

An injectrode constructed using a gauge hypodermic cannula was inserted at the same site as the electrode, and lowered slowly until its tip was located at the depth marked as having the minimal ES threshold. Following the injection, the cannula was left in place for about five minutes before it was withdrawn.

Data collection began immediately before the injection and continued up to three hours. Data were also collected in the following day, and full recovery was always noted. The injection experiments including the saline control were separated by at least two days. In order to obtain homogenous behavioral effects, muscimol injections were made at FEF sites where ES-evoked saccades were directed to the left either horizontally or with an upward component and the current threshold was lower than or equal to 50 microampere penetrations marked by red arrows shown in Figure 1B , five sites in M9, and six in M For control experiments, two sites in each monkey were tested by injecting saline penetrations marked by blue arrows in Figure 1B.

Two behavioral measures were assessed from the eye traces: 1 the trial success rate, or the proportion of trials rewarded, reflecting the overall performance in the tasks, and 2 the saccade proportion rate to each target location, i. This measure was used to assess the spatial distribution of effects by FEF inactivation. Two-way analysis-of-variance ANOVA was used to test statistical significance of the main effects of time after an injection and task type i. Interactions between post-injection time and task type or between post-injection time and target number were also tested. Since the animals often got frustrated with the low yield of reward and refused to work, MEM was tested only up to three targets in inactivation experiments.

To use the reward sparingly, the VIS task was administered only with one or three targets, skipping the two-target condition. The trial success rate, i. Data were pooled over five and six experiments with M9 and M10, respectively. The bar graphs on the right represent the TSR more than one hour after muscimol black bars or saline injections white bars. Horizontal dashed lines indicate the pre-injection TSR levels. T: number of targets. The specificity of muscimol injection was demonstrated in comparison with saline injection Bar graphs on the right side in Figure 2 : The performance after saline injection remained at the same level as before the injection not different from the pre-injection levels indicated by horizontal lines in the figure , while it declined after muscimol injections.

TSR more than one hour after muscimol black bars and saline injections white bars were statistically significantly different in the two- and three-target MEM conditions in both monkeys p values given in the figure by the Kruskal-Wallis test. Minor changes in saccade latency and end-point accuracy were observed during FEF inactivation Figures 3 and 4.

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There was an appreciable increase in dispersion of saccade endpoints around discs during the inactivation Figure 3A , and the latency of first saccades in a series was delayed during inactivation by about 30 ms when they were directed contralesionally Figure 3B. While consistent with previous observations [14] , [15] , [21] , the slight increase in saccade inaccuracy and latency would not account for the decline in TSR in the MEM tasks, because the saccade dispersions were within the window boundaries set for detecting correctly targeted saccades Figure 3A.

A The effect of FEF inactivation on the accuracy of saccades. End-points are shown of all saccades in three-target MEM sessions, before muscimol infusion into the right FEF upper panels and more than one hour after lower panels. The post-muscimol data are pooled from multiple sessions to show approximately equal number of saccades to the contralesional locations.

B FEF inactivation effect on saccade latency. The latency of the first, presumably visually-driven saccades are plotted in histograms, with the solid and broken curves representing data before and during inactivation, respectively. In each panel, the x axis indicates the latency in milliseconds, and the y axis the saccade count. Twelve panels in a set are arranged according to the target locations.

The first number in a pair above each panel indicate the difference of median saccade latency in ms between pre- and post-injection data and the second the p value of the difference by the Kruskal-Wallis test. The latency increased by about 30 ms for contralesionally-directed visually-guided saccades during FEF inactivation. The first and later saccades of the saccade sequence in the trials were separately displayed. The data for M9 and M10 are shown in upper and lower sections, respectively.

Both monkeys made downward saccades more often as the first saccade in the series. Note that later saccades driven by short-term memory tended to be multiples of 15 degrees in amplitude in both horizontal and vertical directions, which corresponded to the separation of discs in the matrix array. No obvious changes occurred during FEF inactivation, other than slight reduction in saccade frequency and increase in saccade vector variability when the saccade were directed contralesionally.

To delve into the reasons underlying the worse performance of MEM during FEF inactivation, saccade behavior was examined in detail. Specifically three aspects were considered as possible explanations for the TSR decline: overall frequency of generating saccades, relative frequency of saccades during rewarded and error trials, and target discriminability by individual saccades Table 1. First, we hypothesized that perhaps the animals became less prudent in saccade generation during FEF inactivation.

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Too many non-discriminatory saccades would have negatively affected the task performance, resulting in lower TSR. However, this hypothesis was not supported by the data: Both animals actually made significantly fewer saccades per trial when the FEF on one side was inactivated. The data also showed that the reduction was more prominent with saccades directed contralateral to the inactivated FEF for both animals the second column in Table 1. Therefore, the decrease in TSR did not appear to result from less prudent saccade behavior, but rather from a reduction of contralesionally-directed saccades.

Now, the reduction in saccade counts occurred only in situations requiring a high-load of short-term memory, i. Thus, it appeared that FEF inactivation specifically affected the memory of saccade targets, rather than visual or oculomotor aspects in saccade behavior.

Second, we compared the number of saccades between rewarded and unrewarded trials. If indiscriminate saccade behavior was responsible for the failure in unrewarded trails, the saccade count would be higher in these trials.

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To the contrary, there was fewer saccades in unrewarded in both animals, consistent with our impression that the animals were skilled enough on the tasks to refrain from making unnecessary saccades when unsure of where the targets had been. The animal apparently maintained this strategy during FEF inactivation, making fewer saccades in unrewarded trials. Presumably, the mnemonic representation of saccade targets was weakened by the inactivation. Third, target discrimination by saccades was unaffected by FEF inactivation.

As given in Table 1 , there was no change in the target discrimination index TDI , or the ratio of on-target saccades over all saccades. Even when the overall performance was impaired by FEF inactivation, the animals made saccades very selectively to the targets, and avoided non-targets as successfully as before the inactivation.

Therefore, the decline in TSR was not attributable to indiscriminate saccade behavior. By the same token, increased scatter in saccade end-points during inactivation Figure 3 could not account for the TSR decline either. Despite the saccade motor errors, TDI remained high Table 1 , i. The above analyses on saccade behavior together made it rather unlikely that abnormalities in saccade execution could account for the impairment in MEM during FEF inactivation.

To explore the relationship between spatial coding in the inactivated FEF sites and the memory impairment, we measured the saccade proportion to each target location, i. Therefore, the denominator of the saccade proportion varied depending on the target number in the tasks. On the other hand, the numerator in the saccade proportion was trials in which at least one saccade was made to a location on each trial.

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For this calculation, even if multiple saccades was made to a location on a single trial, the trial was counted only once. In this way, the saccade proportion was designed to quantify the saccade responses as a function of target location, normalizing the saccade behavior with respect to the target appearance in multi-target search and memory. To evaluate the effect of FEF inactivation, the saccade proportion was compared before versus during FEF inactivation by a ratio i. Now, SPR close to one indicated no change in the saccade proportion, while zero meant complete disruption of memory saccades to a specific target location by the inactivation. However, no such case was observed in our experiments, likely because of the near-perfect performance before the inactivation. A Effects of FEF inactivation on the saccade behavior on each target location. The saccade proportion ratio SPR before and during inactivation is shown by grayscale images representing the layout of target locations.

The saccade proportion is the proportion of trials in which a saccade was made to a target location over those where the target had appeared therein.