Microsaccadic suppression of visual bursts in the primate superior colliculus

Abstract

Saccadic suppression, a behavioral phenomenon in which perceptual thresholds are elevated before, during, and after saccadic eye movements, is an important mechanism for maintaining perceptual stability. However, even during fixation, the eyes never remain still, but undergo movements including microsaccades, drift, and tremor. The neural mechanisms for mediating perceptual stability in the face of these "fixational" movements are not fully understood. Here, we investigated one component of such mechanisms: a neural correlate of microsaccadic suppression. We measured the size of short-latency, stimulus-induced visual bursts in superior colliculus neurons of adult, male rhesus macaques. We found that microsaccades caused approximately 30% suppression of the bursts. Suppression started approximately 70 ms before microsaccade onset and ended approximately 70 ms after microsaccade end, a time course similar to behavioral measures of this phenomenon in humans. We also identified a new behavioral effect of microsaccadic suppression on saccadic reaction times, even for continuously presented, suprathreshold visual stimuli. These results provide evidence that the superior colliculus is part of the mechanism for suppressing self-generated visual signals during microsaccades that might otherwise disrupt perceptual stability.

Figure 1.

Microsaccadic suppression of SC visual bursts. A, Visual RF of an SC neuron preferring eccentricities of ∼16°. The red blip at the origin shows the extent of microsaccades. This is magnified in the inset, with the red curve showing average microsaccade size (in 24 equally spaced angular bins) and the dashed curve showing the mean + SD contour. B, Bottom, Raw activity of the neuron around stimulus onset, with trials sorted by visual burst size (red, 10 strongest trials; blue, 10 weakest trials). Top, Each row represents a trial (same sorting as the rasters), and each cross indicates the onset of a microsaccade. Weak visual bursts were associated with more microsaccades around stimulus onset. C, Across all trials from the same neuron as in A and B, we plotted the magnitude of the neuron's stimulus-induced visual bursts as a function of when microsaccades occurred relative to stimulus onset. Microsaccade onsets near stimulus onset were associated with ∼50% suppression of visual bursts. Error bars denote SEM. D, The suppressive effect was consistent across the population. The inset shows population results from monkey W and monkey J individually. Thin lines indicate SEM. Average microsaccade duration: 23 ± 6.5 ms SD (25 ± 6.6 ms SD for the sample session of B, C).

Figure 2.

Suppression precedes movement onset and outlasts movement end. A, Visual burst suppression data, plotted as a function of when the stimulus appeared relative to microsaccade onset. Results are shown for the sample neuron of Figure 1 (top) and the neuronal population (bottom). Suppression preceded microsaccade onset by ∼70 ms. B, Same data aligned on microsaccade end. Suppression outlasted movement end by ∼70 ms.

Figure 3.

Behavioral correlate of microsaccadic suppression in reaction times. A, B, RT as a function of stimulus onset relative to microsaccade onset. RTs increased when microsaccade and stimulus onsets coincided. For monkey W (A), we also plot the time course of neural suppression effects in the SC (dashed, arbitrary y-axis), which shows a similar time course.