Neural Dynamics of Saccadic Suppression

Saccadic suppression at the single-cell level

In Figure 2, we illustrate the perisaccadic changes in neural responses with a recording from a single MT neuron. Flashes presented just to the right of the fovea either long before (Fig. 2 A) or long after (Fig. 2 B) a saccade lead to a robust response. The spike density (Fig. 2 E) reaches peaks of ∼60 spikes per second and is comparable for stimuli flashed in the presaccadic (red curve) and postsaccadic (blue curve) window. Figure 2 C shows the response of the same neuron to stimuli flashed in its presaccadic receptive field around the time of saccade onset. The trials in the raster plot are ordered such that trials in which the stimulus was presented long before the saccade are at the top, and trials in which the stimulus was presented long after the saccade are at the bottom. Saccade onset time is indicated by the red triangles.

Reading the raster from top to bottom, we see a robust response for flashes presented 100 ms or more before the saccade. Flashes presented between 75 and 0 ms before the saccade, however, evoke fewer spikes. The spike density for stimuli presented in this perisaccadic window is shown as the solid green curve in Figure 2 E. The peak response does not rise above 35 Hz, a reduction of nearly 50% compared with the response during fixation (red/blue curves). Because the eye has not moved yet when the flash is presented, this suppression of the response must involve an active process of suppression and cannot be caused by changes in the retinal input attributable to the motion of the eye.

Continuing stepping through the trials in Figure 2 C, we reach the trials in which flashes are presented after the eye has started to move. The average response to these flashes (green dashed curve in Fig. 2 E) is also much less than those presented during fixation. This reduction can be caused by active processes, but it almost certainly also involves the (passive) reduction in firing expected from the fact that the receptive field, which is presumed to be yoked to the eye, moves away from the position where the stimulus is flashed.

Figure 2 D shows the response to flashes presented in the future field, i.e., the location on the screen where the receptive field will be after the saccade. For flashes presented before the saccade, responses at this location are small and delayed (solid black curve in Fig. 2 E). This likely includes a passive effect; when these flashes are presented, the receptive field does not yet encompass their location. It also could reflect a memory trace as described, e.g., in area LIP (Duhamel et al., 1992). However, the raster plot shows that, even for flashes presented >50 ms after saccade onset, when the eye has reached its new position and the flashes are again presented within the receptive field, the response is also reduced compared with fixation (dashed black curve in Fig. 2 E).

The single-cell example of Figure 2 demonstrates that it is critical to distinguish between the time of a response relative to the stimulus and the time of the stimulus relative to the saccade. Moreover, it illustrates how active sources of saccadic suppression can be isolated by investigating responses evoked by flashes presented just before or just after an eye movement. We believe, however, that passive sources of saccadic suppression may also play a role in perisaccadic perception. To illustrate this, consider an ideal observer with access to a perfect eye position signal. This observer, when faced with a detection task, always knows which neurons to consult about the presence of a visual stimulus on the screen. Therefore, this observer does not suffer from passive mechanisms of suppression because, as soon as the eye starts to move, the observer will select to read out a different neuron whose receptive field is now in the appropriate position. In contrast, any mechanism for detection that does not have access to a perfect eye position signal would suffer from passive suppression. For instance, if the eye position signal were delayed, the detection mechanism may retrieve information from a neuron whose receptive field no longer encompasses the stimulus (as in the bottom half of Fig. 2 C). The passively reduced signal from this neuron could therefore increase the detection threshold of this mechanism. We believe that it is conceivable, even likely, that perceptual mechanisms have imperfect access to the current eye position and would therefore be expected to suffer from both passive and active suppression. For this reason, the following analysis first investigates the combined effect of passive and active suppression, in an attempt to show the overall reduction in sensitivity during eye movements (data shown in Figs. 3, 4). Subsequent analyses (Figs. 6 ⇑–8) will study active suppression in isolation.

The joint effect of passive and active saccadic suppression

At the coarsest level, we performed a population analysis that simply compared average activity per area in a fixed time window after stimulus onset. Figure 3 shows the average population response separately for the four areas and for stimuli flashed long before (pre), near (peri), and long after (post) a saccade. The response in the pre-period was set to 100%. Responsiveness in motion-sensitive areas MT, MST, and VIP was less during saccades than during steady fixation. In areas MT and MST, perisaccadic activity was reduced to a level of 83% (area MT) and 88% (area MST), whereas responses in area VIP were reduced to 91% of the presaccadic level. This difference was statistically significant in each area (repeated-measures ANOVA on ranks, followed by Tukey–Kramer post hoc tests, p < 0.05). Postsaccadic responses were enhanced to levels of 106% (area MT), 106% (area MST), and 108% (area VIP). This effect reached statistical significance in both VIP and MST but not in MT.

In the LIP population as a whole, the average response did not differ significantly between the three periods (peri, 106%; post, 104%). Within this population of cells, however, some showed a strong increase in firing in the saccade-only condition (i.e., without any flashed visual stimuli), whereas others showed a strong decrease in the saccade-only condition. In other words, the average response shown in Figure 3 D is a mixture of pure saccade responses and visual responses. Given that almost all LIP cells in our population were modulated in the saccade-only condition, we are unable to perfectly isolate a pure visual response in the perisaccadic window. Within the subpopulation of cells in which the saccade alone evoked a response modulation of less than ±10% (LIP-0; see Materials and Methods), however, the responsivity was qualitatively similar (peri, 108%; post, 99%).

Next, we calculated a time-resolved population response, by aligning the response of each neuron to response onset (i.e., we corrected for the individual latency of the cell). We ignored the spatial location of the flashed bars and simply averaged across all cells and trials; as such, this is an estimate of the overall population response. We determined this average separately for flashes presented in three time windows: long before the saccade (pre), long after the saccade (post), and in the time window in which suppression was maximal (peri) (0 ms, 75 ms). In this time window, both active and passive suppression mechanisms can operate. This analysis also allowed us to compare the visual response with the average response of these same neurons in the saccade-only condition (i.e., without any flashed bars). Figure 4 compares these presaccade, perisaccade, postsaccade, and saccade responses for the four populations of neurons. A comparison of the presaccadic and postsaccadic responses across areas shows that our visual stimuli led to clear and qualitatively comparable population responses in each area. Moreover, in each area, the presaccadic and postsaccadic responses are approximately the same, which demonstrates the consistency of the responses, as well as the fact that the coverage of the population receptive field was approximately the same before and after the saccade.

In areas MT, MST, and VIP, the average perisaccadic responses were clearly reduced. The mechanisms underlying this suppression, however, are likely to be different in these areas. In areas MT and VIP, the neural response in the saccade-only condition was essentially unaffected by the saccade; hence, the suppression was specific to visual responses during the saccade. In the MST population, however, we found a clear reduction of activity even in the absence of visual stimuli (black curve). The suppression of visual activity during saccades (green curve) could at least qualitatively be explained as a linear summation of the suppression of activity evoked in the saccade-only condition (black curve) and the response to visual stimuli during fixation (red/blue curves).

The response pattern in LIP was quite different. Not unexpectedly, the saccade-only conditions led to large eye-movement-related activity in LIP (black curve). Visual stimuli presented during the saccade could not drive the LIP population above this saccade-related activity and, at ∼50 ms after stimulus onset, even reduced the average LIP activity below the activity evoked in the saccade-only condition.

Neural suppression matches behavioral suppression

The behavioral phenomenon of saccadic suppression has a well known time course. Our goal in this section is to determine whether changes in neural response in areas of the dorsal stream match this time course. To link neural activity with behavior, we determined what we call the population excitability (see Materials and Methods). This measure can be interpreted as the average neural response to a continuous stream of flashes presented to the retina. To allow a comparison across areas, we scaled the population excitability of each area at ∼100 ms before saccade onset to 100%. Note that changes in this measure of population excitability around saccades include both active and passive mechanisms of suppression.

To relate the population excitability to the behavioral data obtained in humans, we made assumptions about the neural code that are necessarily tentative. We assumed that the neural response corresponds to the visibility of a stimulus that was presented some fixed amount of time earlier. With this assumption, the link between neural response and stimulus perception can be quantified by a single number: the latency. We estimated this latency by cross-correlating the behavioral sensitivity data with the neural activity profiles. We used the behavioral data of Diamond et al. (2000) and found that the temporal shift as obtained from this cross-correlation analysis was very similar but not identical for the three areas MT, MST, and VIP, respectively. In areas MT and MST, neurophysiological data had to be shifted by τ = 98 ms to obtain an optimal match with the behavioral data [maximum of the normalized cross-correlation coefficient: r _Max = 0.6153 (area MST) and r _Max = 0.6073 (area MT)]. Data from area VIP had to be shifted by τ = 112 ms (r _Max = 0.6087). In other words, if perception were based on neural activity ∼100 ms after stimulus onset, then the suppression of neural activity in areas MT, MST, and VIP would be a good predictor of perisaccadic reductions of visibility. In Figure 5, we shifted the ongoing population activity of areas MT and MST by τ = 98 ms and population activity of area VIP by τ = 112 ms and overlaid it with the behavioral sensitivity data of Diamond et al. (2000).

Temporal dynamics of saccadic suppression

Psychophysical studies have investigated the temporal evolution of saccadic suppression by measuring contrast sensitivity for luminance gratings presented shortly before, during, or after saccades (Diamond et al., 2000). The suppression of contrast sensitivity starts for stimuli presented well before saccade onset and is maximal for stimuli presented at the time the eyes start to move. Contrast sensitivity returns back to control level for stimuli presented ∼50–100 ms after saccade offset. Although this shows that presaccadic stimuli are suppressed, this does not by itself imply that the saccadic suppression mechanism must operate before the eye movement starts. The reason for this is that the response of the subject only comes after the saccade; hence, there is ample time for intra-saccadic and postsaccadic mechanisms to change the behavioral response to the presaccadic stimulus. Behavioral methods or imaging methods relying on the slow blood oxygenation level-dependent (BOLD) response (Kleiser et al., 2004; Vallines and Greenlee, 2006) inevitably suffer from this delay between the measurement and the stimulus presentation time. In an electrophysiological recording, this delay is reduced to the response latency of the cell (plus minimal latencies in the recording equipment). This allowed us to address the temporal dynamics of suppression with high fidelity.

In this section, we focus on the perisaccadic time window. First, we quantify suppression on a cell-by-cell basis (Fig. 6), and then we show the average population response for stimuli flashed at different times with respect to saccade onset (see Figs. 7, 8).

Active saccadic suppression

The response of the example cell in Figure 2 was reduced even for flashes that were presented to a stationary retina. This is what we refer to as active suppression. To quantify the strength of active and passive suppression across areas, we determined the peak of the response for stimuli flashed long before a saccade and compared that with the peak response evoked by stimuli flashed (1) just before or (2) during a saccade. Determining the peak response across spatial positions of the flashed bar ensured that we always compared stimuli flashed in the most sensitive part of the receptive field, regardless of when and where the receptive field moved relative to the saccade. We calculated a suppression index as follows: SI = [(perisaccadic response/presaccadic response) − 1] × 100%. An SI of zero corresponds to a cell whose peak firing rate is not affected by the saccade; a negative SI corresponds to saccadic suppression, whereas a positive SI corresponds to saccadic enhancement. We calculated these indices separately for the two perisaccadic time windows. The effects in the first perisaccadic time window (−75 ms, 0 ms) are attributable to pure active suppression; we refer to them as SI_a. The effects in the second perisaccadic time window (0 ms, 75 ms) include both active and passive mechanisms; we refer to them as SI_a&p.

Figure 6 A–D shows histograms of the suppression indices for each of the populations. Overall, the magnitude of saccadic suppression was similar in range across areas, ranging from ∼60% suppression to ∼40% enhancement. The median indices [indicated by blue (before, SI_a) and red (during, SI_a&p) arrows in each panel] were always below zero; hence, perisaccadic peak responses were typically reduced compared with presaccadic peak responses. The median suppression index for stimuli presented just before the saccade (SI_a) was as follows: MT, −26%; MST, −19%; VIP, −20%. The median suppression for combined active and passive mechanisms (SI_a&p) was as follows: MT, −29%; MST, −18%; VIP, −22%. These reductions in peak response compared with the presaccadic peak responses were statistically significant in both perisaccadic time windows and in all areas (p < 0.001, paired sign test). The difference in reduction between the two time windows was not significant in MT, MST, or VIP (p > 0.6, paired sign test).

In LIP, both active and combined active and passive suppression indices were also significantly below zero (SI_a of −22%; SI_a&p of −18%; p < 0.001, paired sign test). Note that these data may appear to contradict the findings shown in Figure 4 in which we showed that the average perisaccadic response in LIP (green curve) is higher than the average presaccadic response (red curve). Here we show that the peak perisaccadic response is lower than the peak presaccadic response. The resolution of this paradox lies in the fact that the LIP response in the perisaccadic windows most likely is a motor response that is independent of the position of the flash; hence, its average over all positions (shown in Fig. 4) is higher than the average taken long before the eye movement when the response is truly visual and restricted to a few locations on the screen. Therefore, a different way of phrasing the LIP results is that visual stimuli drive the cells during fixation but that the same visual stimuli cannot increase the response during or just before a saccade, when the cell is already responding strongly in response to the saccade itself. In fact, if anything, the visual stimuli reduce the saccade response.

Consistent with this, we found that the suppression index during the saccade was slightly less negative than just before the saccade (SI_a&p > SI_a; p < 0.01, paired sign test). This is presumably attributable to the fact that most of our LIP cells increased their firing perisaccadically even in the saccade-only condition. To confirm this, we performed this analysis separately for the subpopulation of LIP cells that had enhanced responses in the saccade-only condition (LIP⁺), those that reduced their responses during saccades (LIP⁻), and those that were only modestly modulated by saccades (LIP-0) (see Materials and Methods). In the LIP⁺ population, the suppression index was −15% (p < 0.01) for both time windows. In the LIP⁻ population, SI_a was increased to −43% (p < 0.01), whereas SI_a&p was −31% (p < 0.01). In the LIP-0 population, SI_a was −23% (p < 0.01) and SI_a&p was −10% (p > 0.05). This shows that, in the perisaccadic time window, the LIP population as a whole but also each of its subpopulations is driven mainly by saccade planning; visual stimuli that arrive around this time are actively suppressed.

To provide additional insight into the detailed temporal dynamics of the population activity around a saccade, Figure 7 displays the full time courses as two-dimensional activity maps. The two dimensions correspond to two important temporal factors that determine the neural response: the time of stimulus presentation relative to saccade onset (horizontal) and the time relative to response onset (vertical). Zero on the horizontal axis corresponds to stimuli that land on the retina when the saccade starts. Positive values indicate that the stimulus was presented after saccade onset. Zero on the vertical axis is the time at which the first response can reliably be detected in a cell (i.e., the response time is corrected for the latency of each cell).

There are two important features to note in this diagram. First, the horizontal yellow–red bands in Figure 7 A–C show that, in areas MT, MST, and VIP, the stimulus triggered a clear response that lasted ∼70 ms. This response, however, was reduced for stimuli presented just before and during the saccade. This reinforces the finding described in Figure 4 and shows that a reduction in visual activity is found for stimuli presented around saccade onset.

The second feature of interest is most notable in MST. A diagonal dark band of suppressed activity aligns with the black line indicating saccade onset. Given that this suppression starts before saccade onset, it cannot be caused by changes in the retinal stimulation but must be attributable to an active process of suppression. Neurons in area LIP show a quite different response pattern: the population shows strong saccade-related activity (yellow–red diagonal band) but responds little if at all to the stimulus (absence of a horizontal band). This occurs although this same population responds quite well to visual stimuli during fixation (not shown in this format, but see Fig. 4).

We performed a statistical analysis (see Materials and Methods) to determine when the perisaccadic neural response (Fig. 7) was different from the response to visual stimuli long before a saccade. Figure 8 shows the results of this analysis in approximately the same format as Figure 7; the main difference is that, in this representation, red shows a statistically significant suppression, and green indicates a significant enhancement of perisaccadic activity (see Materials and Methods). This statistical thresholding reveals a much clearer pattern of suppression. To refer to specific parts of these maps, we use t_x to refer to the time of stimulus presentation relative to saccade onset (x-axis) and t_y to the time after response onset (y-axis).

In area MT, the main features are a saccadic enhancement (green) of stimuli presented 100 to 50 ms before the saccade [t_x = (−100 ms, −50 ms); t_y = ∼250 ms] and a suppression (red) of the response to stimuli presented perisaccadically [t_x = (−20 ms, 100 ms); t_y = ∼80 ms].

In area MST, we see an enhancement (green) of the response to stimuli presented before the saccade [t_x = (−100 ms, 0 ms); both near t_y = ∼0 and ∼250 ms], as well as an enhancement of responses for stimuli presented after the saccade (t_x = >100 ms; t_y = ∼50 ms). The main feature, however, is a trough of suppression (red) that starts before saccade onset and extends well beyond the saccade. The alignment with the diagonal white line of saccade onset and the presence of significant suppression before stimulus response onset (t_y = 0 ms) shows that this suppression is saccade related and an active process that takes place even without the presence of visual responses. Additionally, the fact that this suppression is significant even before the onset of the saccade (white line) shows that this suppression cannot be attributable to the retinal slip caused by the saccades.

In area VIP, all significant suppression (red) was observed after stimulus response onset and never in the absence of visual stimuli. The strongest enhancement (green) was found in the late (t_y = ∼250 ms) response to stimuli presented 100 ms before until 50 ms after saccade onset [t_x = (−100 ms, 50 ms)]. A weaker enhancement appears to precede saccade onset, even before the visual response.

In area LIP, the statistical analysis confirms that cells are typically more strongly driven by (impending) saccades than by visual stimuli. The isolated island of suppression near t_x = 50 ms, t_y = 50 ms corresponds to the reduction in response after a visual stimulus presented during a saccade visible in Figure 4.