Effects of saccades on visual processing in primate MSTd

Abstract

In surveying their visual environment, primates, including humans make frequent rapid eye movements known as saccades. Saccades result in rapid motion of the retinal image and yet this motion is not perceived. We recorded saccade-related changes in neural activity in the dorsal medial superior temporal area (MSTd) of alert macaque monkeys. We show that the spontaneous activity of neurons in MSTd is modulated around the time of saccades. Some cells show considerable suppression of spontaneous activity, while most show early and significant enhancement. While this modulation of spontaneous activity is variable, the concomitant modulation of neural responses evoked by flashed visual stimuli is uniform and stereotypical - visual responses are suppressed for stimuli presented around the time of saccades and enhanced for stimuli presented afterwards. The combined modulation of spontaneous activity and evoked visual responses likely serves to reduce the detectability of peri-saccadic stimuli and promote the perceptual awareness of visual stimuli between saccades.

Fig. 1

Methods. (A) Neural response of a single neuron in MSTd following briefly presented stimuli delivered more than 500 ms before or after a saccade (the control condition). The upper panel shows the raw spike arrival times as a raster plot (n = 938). The lower panel shows the mean spike rate as a spike density function (see Methods). All trials are aligned at the time of stimulus onset. The onset and duration of the flashed stimulus is indicated by the solid black bar. The spontaneous firing rate (dashed line) in the absence of saccades was estimated from the mean spike rate in the first 25 ms after presentation of the stimulus as shown by the shaded region. Visual response amplitude in the absence of saccades was defined as the increase in spike rate above the estimated spontaneous rate. (B) Neural response from the same cell to the same flashed stimuli delivered 20–40 ms after saccade onset, i.e., within a 20 ms time bin centred 30 ms after saccade onset. The upper panel shows the eye position traces. The lower panel shows the mean spike rate as a spike density function (n = 12). All trials are aligned with respect to stimulus onset and the mean response then aligned 30 ms after saccade onset. The onset and duration of the flashed stimulus is indicated by the solid black bar. The prevailing spontaneous rate within each 20 ms time bin (defined relative to saccade onset) was estimated from the mean spike rate in the first 25 ms after presentation of the flashes within that bin. Visual response amplitude was calculated as the amplitude of the evoked response minus the prevailing spontaneous rate within the time bin containing the response. In the example shown, this spontaneous rate (indicated by the dash line) was estimated from the 25 ms period after flashes presented (during other trials) within the shaded region.

Fig. 2

Modulation of visual response amplitude around the time of saccades. (A–C). Normalized visual response amplitude of three neurons as functions of time relative to saccade onset. The visual response amplitude in each 20 ms bin was calculated by subtracting the prevailing spontaneous rate from the peak amplitude of the mean response within that bin. Visual response amplitude was then normalized to the visual response amplitude observed in the control condition (horizontal line). In (A) the cell shows suppression of responses arriving in MSTd at saccade onset and strong post-saccadic enhancement of responses arriving 100–400 ms after saccade onset. Example spike density functions from three different time bins are shown inset for flashes that occurred at −170 ms, −110 ms and +130 ms relative to saccade onset. (B) An example cell showing little in the way of early suppression but exhibiting substantial post-saccadic enhancement. (C) A cell showing strong suppression for flashes presented before saccades but no subsequent post-saccadic enhancement. The grey shaded region shows the mean duration of the saccades. Error bars indicate the standard error of the estimate of the mean response amplitudes. In some time bins, particularly those exhibiting substantial suppression, subtraction of the spontaneous rate resulted in response amplitudes close to or even less than zero. These cannot be represented on the log scale and so are shown in grey below the axes. These points show times at which extreme suppression occurred.

Fig. 3

Maximum influence of post-saccadic enhancement. Normalized visual response amplitude as a function of time relative to saccade onset. This cell exhibits only weak responses to visual stimulation during fixation and robust responses after saccades. (Inset, top left) Evidence for a visual response is weak, with the mean response failing to reach the 99% Poisson threshold (dashed line) used to determine response onset (n = 772). (Inset, top right) Mean spike density function showing the response to flashed stimuli presented 120 ms after saccade onset: the visual response is robust (n = 16). The grey shaded region shows the mean duration of the saccades. Time bins exhibiting extreme suppression, resulting in response amplitudes close to or even less than zero, are shown as grey symbols outside the limits of the axes. Error bars indicate the standard error of the estimate of the mean response amplitudes.

Fig. 4

Saccade-related modulation of visual responses for 72 neurons in MSTd. The scatter plot shows the mean normalized visual response amplitude in the early response window (0–100 ms after saccade onset) plotted against that in the late response window (100–250 ms) for 72 cells. The majority of cells (n = 39) are clustered in the lower right quadrant of the scatter plot, indicative of early suppression followed by late enhancement of visual responses. Cells for which the mean response amplitude was very close to or even less than zero, thus preventing plotting on a log scale, are shown as grey symbols outside the limits of the axes. These points show cells exhibiting extreme suppression of visual responses.

Fig. 5

Modulation of spontaneous activity around the time of saccades. (A–D) Normalized spontaneous firing rate of three neurons as functions of time relative to saccade onset. Spontaneous firing rate was estimated within each 20 ms bin and normalized by dividing by the mean spontaneous rate of each cell in the absence of saccades (as represented by the horizontal line). The cells in (A) and (B) show substantial enhancement of spontaneous rate from 0 to 100 ms after saccade onset. (C) An example cell showing substantial enhancement in the early window (0–100 ms) followed by suppression of spontaneous firing until approximately 300 ms after saccade onset. Early enhancement of spontaneous firing as shown by these cells was observed in more than half the cells (47 cells, 65%). Error bars indicate the standard error of the estimate of the mean response amplitudes. The grey shaded region shows the mean duration of the saccades. Grey symbols indicate periods of extreme suppression (see Fig. 2; caption).

Fig. 6

Saccade-related modulation of spontaneous activity for 72 neurons in MSTd. The scatter plot shows the mean normalized spontaneous rate in the early window (0–100 ms after saccade onset) plotted against that in the late response window (100–250 ms). In contrast to the modulation of visual responses shown in Fig. 4, it is evident from the lack of clustering that cells in MSTd exhibit considerable variability in saccade-related modulation of spontaneous activity. Cells for which the mean spontaneous rate was very low or even completely suppressed in either window are shown as grey symbols outside the limits of the axes. These points show cells exhibiting extreme suppression of spontaneous activity.

Fig. 7

Population averages. (A) Normalized total response amplitude as a function of time relative to saccade onset, averaged across 72 cells. The total response is measured as the peak spike rate, including the evoked visual response and the ongoing spontaneous activity. On average, peak spike rate exhibits a biphasic modulation: responses arriving in MSTd immediately after saccades are suppressed while later responses are enhanced. (B) Normalized spontaneous activity over the same time period, averaged across 72 cells. It is evident that on average cells in MSTd exhibit a significant increase in spontaneous activity immediately after saccades. (C) Normalized visual response amplitude (i.e., total response amplitude minus the prevailing spontaneous rate) normalized and averaged across 72 cells. On average, neurons in MSTd exhibit significant suppression followed by enhancement of visual response amplitudes beginning immediately after saccades. Note that the level of suppression is far greater (more than 80% compared to the control condition) than that seen for the total response (30–50% compared to the control condition). This is because spontaneous activity in MSTd is enhanced immediately after saccades, precisely when the suppressed visual signals are arriving in MSTd. In each panel, the level of significance of the modulation in each 20 ms bin is indicated by stars (t-tests; *, p < 0.05; **, p < 0.01). Error bars indicate the standard error of the estimate of the mean. The grey shaded region shows the mean duration of the saccades.

Fig 8

Detectability of visual responses in MSTd around the time of saccades. (A) Variation in the evoked-to-spontaneous ratio as a function of time relative to saccade onset, averaged across 72 cells. The evoked-to-spontaneous ratio, an indicator of detectability of the evoked visual response, is transiently reduced immediately following a saccade and is then subsequently enhanced. (B) Variation in the evoked-to-spontaneous ratio over the same time period averaged only across those cells which exhibited suppression of their spontaneous activity 100–250 ms after saccade onset (35 cells, 49% of the population). It is evident that this suppression of spontaneous activity produces a substantial increase in the evoked-to-spontaneous ratio in this window. Notably, these cells also show a substantial reduction in the evoked-to-spontaneous ratio during and immediately following saccades. (C) Variation in the evoked-to-spontaneous ratio averaged only across those cells which exhibited an enhancement of their spontaneous activity 100–250 ms after saccade onset (37 cells, 51% of the population). These cells also exhibit a transient reduction in the evoked-to-spontaneous ratio immediately after saccades. However, despite the subsequent increase in spontaneous rate these cells also show a substantial post-saccadic increase in their evoked-to-spontaneous ratio. In each panel, the level of significance of the modulation in each 20 ms bin is indicated by stars (t-tests; *, p < 0.05; **, p < 0.01). The grey shaded region shows the mean duration of the saccades.