Changes in the response rate and response variability of area V4 neurons during the preparation of saccadic eye movements

Abstract

The visually driven responses of macaque area V4 neurons are modulated during the preparation of saccadic eye movements, but the relationship between presaccadic modulation in area V4 and saccade preparation is poorly understood. Recent neurophysiological studies suggest that the variability across trials of spiking responses provides a more reliable signature of motor preparation than mean firing rate across trials. We compared the dynamics of the response rate and the variability in the rate across trials for area V4 neurons during the preparation of visually guided saccades. As in previous reports, we found that the mean firing rate of V4 neurons was enhanced when saccades were prepared to stimuli within a neuron's receptive field (RF) in comparison with saccades to a non-RF location. Further, we found robust decreases in response variability prior to saccades and found that these decreases predicted saccadic reaction times for saccades both to RF and non-RF stimuli. Importantly, response variability predicted reaction time whether or not there were any accompanying changes in mean firing rate. In addition to predicting saccade direction, the mean firing rate could also predict reaction time, but only for saccades directed to the RF stimuli. These results demonstrate that response variability of area V4 neurons, like mean response rate, provides a signature of saccade preparation. However, the two signatures reflect complementary aspects of that preparation.

Fig. 1.

The visually guided delayed saccade task. In the task, the monkey fixates a central dot while an oriented bar is displayed in the receptive field (RF; dashed circle) of a single V4 neuron. After a delay, the monkey is cued (by fixation spot offset) to make a saccade in 1 of 3 directions. On 2/3 of the trials, a target dot appears in 1 of 2 locations, conditions up (left) and opposite (middle), and the monkey is rewarded for making a saccade to that dot. If no target appears, the monkey is rewarded for executing a saccade to the RF stimulus (right).

Fig. 2.

Effects of RF stimulation and saccade preparation on the mean firing rate and response variability for the population of area V4 neurons. Left: mean firing rate (A) and Fano factor (FF; B) aligned to the time of RF stimulus onset and divided into responses to preferred vs. nonpreferred visual stimuli. These traces, as well as those in C–F, are all smoothed with an 80-ms box filter (see methods). C and D: mean firing rate and FF aligned to movement cue onset (i.e., fixation offset) and split by direction of saccade. E and F: the same but aligned to saccade onset. In all traces, means (dark lines) and SE (shading) are shown. In E and F, horizontal bars indicate significant difference from delay period. In E, translucent plots above traces show distributions of cue onset times relative to saccade onset. G: data from individual neuron-conditions for 2 time points: baseline and immediately prior to saccade onset. Each dot represents the mean and variance of spike counts within an 80-ms window for just 1 neuron-condition (those trials corresponding to a particular neuron, stimulus, and saccade direction). Black dots represent variance/mean pairs taken from windows during the baseline period of each saccade condition (1st arrow in F). Colored dots represent variance/mean pairs taken from windows just prior to saccade onset (2nd arrow in F). Thick lines are linear regressions on the data.

Fig. 3.

Presaccadic changes in FF for “mean-matched” conditions. The mean-matching algorithm was applied to presaccadic spike trains from the population of recorded V4 neurons to equalize firing rate distributions across time for each of the saccade directions. A: mean-matched firing rates for each of the saccade directions (toward, left; up, middle; opposite, right), which no longer vary over time. B: FF of the mean-matched data, which still declines presaccadically despite removing variation in firing rate. C: the magnitude of FF decline in the final 80-ms period before the saccade for each of the 3 saccade directions. The FF decline plotted corresponds to the component of the FF decline independent of the presaccadic change in mean firing rate, computed in an ANCOVA. Error bars represent 95% confidence intervals from ANCOVA.

Fig. 4.

Relationship of presaccadic mean firing rate and FF to saccadic RT for the population of V4 neurons. A, left: traces show percent difference in mean firing rate between short and long reaction time (RT) trials for each saccade condition. Right: percent differences in FF. B: differences in mean firing rate and FF for short and long RT trials in each saccade condition at the time of the movement cue (t = 0). C: same data as in A but collapsed across the 3 saccade conditions. Horizontal bar indicates a significant difference between long and short RT traces.