Saccadic modulation of neural responses: possible roles in saccadic suppression, enhancement, and time compression

Abstract

Humans use saccadic eye movements to make frequent gaze changes, yet the associated full-field image motion is not perceived. The theory of saccadic suppression has been proposed to account for this phenomenon, but it is not clear whether suppression originates from a retinal signal at saccade onset or from the brain before saccade onset. Perceptually, visual sensitivity is reduced before saccades and enhanced afterward. Over the same time period, the perception of time is compressed and even inverted. We explore the origins and neural basis of these effects by recording from neurons in the dorsal medial superior temporal area (MSTd) of alert macaque monkeys. Neuronal responses to flashed presentations of a textured pattern presented at random times relative to saccades exhibit a stereotypical pattern of modulation. Response amplitudes are strongly suppressed for flashes presented up to 90 ms before saccades. Immediately after the suppression, there is a period of 200-450 ms in which flashes generate enhanced response amplitudes. Our results show that (1) MSTd is not directly suppressed, rather suppression is inherited from earlier visual areas; (2) early suppression of the visual system must be of extra-retinal origin; (3) postsaccadic enhancement of neural activity occurs in MSTd; and (4) the enhanced responses have reduced latencies. As a whole, these observations reveal response properties that could account for perceptual observations relating to presaccadic suppression, postsaccadic enhancement and time compression.

Figure 1.

Recording site. Location of MST and medial-lateral range of electrode tracks in MSTd (top). Recoding sites of visual motion neurons in right MSTd verified by structural MRI (T1-weighted, fast spin-echo; Siemens; 3T magnet). Line drawing indicates representative recording tracks run in the coronal plane (bottom). Penetrations and unit depths were reconstructed by MRI and micro-drive readings taken from visual motion sensitive neurons. IPS, Intraparietal sulcus; STS, superior temporal sulcus. Some shadow artifacts from titanium bolts used to secure the recording chamber are evident on the upper right side. Scale bar, 5 mm.

Figure 2.

Methodology and spike trains. A, The stimulus consisted of a random checkerboard pattern, 77 × 77° with a check size of 0.8 × 0.8° (diagram not to scale) briefly presented (duration 10 ms) at random intervals relative to saccades. Trained monkeys made directed saccades to fixation points presented alternately, separated by 10° centered about the midline. Dashed lines show the time of flash presentations relative to the mean eye position trace (actual times are marked in milliseconds) of five such trials. At the bottom of the figure are 100 ms sections of the spike trains recorded from a single MSTd neuron. The beginning of each spike train shows the time of flash onset. B, The spike trains are shown aligned vertically relative to flash onset. Flashes presented before saccade onset lead to a single time-locked spike 67 ms after flash onset. Flashes presented after saccade onset elicited a larger response (4 spikes). The spikes also arrive earlier than in the presaccadic phase, as illustrated by the vertical gray line that marks the presaccade latency.

Figure 3.

Spiking activity around the time of saccades. Responses of an MSTd neuron to 10 ms flashed stimulus presentations presented as SDFs aligned at flash onset. The black boxes show the duration of the flash. The lowest trace shows the control response (no saccades within ±500 ms). The y-axis shows time of stimulus presentation relative to saccade onset. Each SDF represents the mean of all responses generated by flashes within a 20 ms time window centered on the indicated time relative to saccade onset. The yellow area shows the mean saccade duration. The black dots show measured response latency (vertical dashed line indicates the latency of the control).

Figure 4.

Time course of neural modulation. A, Response amplitude normalized to the control condition (no saccades) for a single cell, plotted as a function of stimulus time relative to saccade onset (zero). The yellow bar shows the mean duration of the saccades. Error bars indicate SEs within each 20 ms bin. From left to right, arrows indicate the five markers used to quantify the start of suppression, maximum suppression, start of enhancement, peak of enhancement and end of enhancement, respectively. B–F, Histograms showing the distributions of these five markers for 67 cells. The yellow bar in each histogram shows the mean duration of the saccades.

Figure 5.

Latency changes after saccades. A, Mean responses generated by stimulus flashes presented under control conditions (black) and 50 ms after (blue) saccade onset. The horizontal line shows the threshold, defined as the 99% cutoff of the Poisson distribution fitted to the spontaneous rate, used to determine response latency. Horizontal error bars indicate SEs. The reduction in latency for this cell was 7.6 ms. B, Cell-by-cell comparison of neuronal response latencies for visual stimuli delivered under control conditions (no saccades) and for stimuli delivered 50 ms after saccade onset. The dashed line shows the line of equality for the two measures. Black dots: not significantly different; blue dots: significantly different (t test, p < 0.05); red dots: significantly different (t test, p < 0.01). C, Histogram showing the distribution of cells based on their latency reduction. The red arrow indicates the mean latency reduction (−16.78 ± 2.22 ms, mean ± SE, n = 45) for the population. D, Normalized response latency as a function of stimulus delivery time relative to saccade onset for the cell population (n = 26–46, not all cells were included in every point, see Materials and Methods). It is apparent that significant latency reductions occur for flashes delivered +30 to +250 ms after saccade onset. Asterisks indicate whether the reduction in population mean compared with controls is significant (color code as in A). Error bars indicate SEs.

Figure 6.

Origins of saccadic modulation. A, Mean spontaneous activity in each 20 ms bin plotted as a function of time relative to the onset of saccades performed while viewing a bright, blank screen. Spontaneous rates for each cell were normalized to the control condition (no saccades). Gray band shows saccade duration. B, Mean spontaneous activity as a function of time relative to the onset of saccades in total darkness. Again, spontaneous rates were normalized to the control condition for each cell. The gray band shows the maximum saccade duration (saccades varied from 15 to 62 ms). In A and B, asterisks indicate significant enhancement of spontaneous activity relative to the control condition (*p < 0.05, **p < 0.01, t test). Error bars indicate SEs for the cell population (n = 67).

Figure 7.

Response latency versus time of suppression (relative to saccade onset). Cell-by-cell comparison of control latency and the time of first suppression, defined as the earliest time of stimulus delivery relative to saccade onset for which the observed response was significantly suppressed relative to the control condition (n = 46). Note that some points are plotted on top of each other. The dashed diagonal line denotes the time of saccade onset. Seven cells showed significant suppression only for stimuli delivered after saccade onset (small filled circles). The remainder of the cells showed significant suppression of visual responses for stimuli delivered before saccade onset (large circles). Of these, 14 cells showed significant suppression of responses expected to arrive in MSTd within 16 ms after saccade onset (shown in gray shaded area). The gray areas in A and B show those cells in which the suppression could not have arisen from retinal mechanisms.