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 ϳ30% suppression of the bursts. Suppression started ϳ70 ms before microsaccade onset and ended ϳ70 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.

Similarity of superior colliculus involvement in microsaccade and saccade generation

“…Moreover, by virtue of the similarity between microsaccade and saccade generation, our results also suggest that microsaccadic influences on sensory processing (Bair and O'Keefe 1998;Bosman et al 2009;Herrington et al 2009;Kagan et al 2008;Leopold and Logothetis 1998;MartinezConde et al 2000;Snodderly et al 2001) extend beyond retinal image refreshing and may include additional functions such as saccadic suppression (Hafed and Krauzlis 2010) and perisaccadic spatial updating.…”

“…Saccades (and microsaccades) were detected with velocity and acceleration thresholds (Krauzlis and Miles 1996), also described in detail for microsaccades (Hafed et al 2009;Hafed and Krauzlis 2010). We used a velocity threshold of 30°/s for the movements collected from our saccade tasks and a threshold of 8°/s for the significantly smaller (and therefore slower) movements collected in our fixation tasks; similarly, we used an acceleration threshold of 800°·s Ϫ1 ·s Ϫ1 for the movements of our saccade tasks and 550°·s…”

“…Even though neurophysiological studies of microsaccade generation (Guerrasio et al 2010;Hafed 2011;Hafed et al 2009;Van Gisbergen et al 1981) are scarce relative to studies of these movements' sensory consequences (Bair and O'Keefe 1998;Bosman et al 2009;Hafed and Krauzlis 2010;Herrington et al 2009;Kagan et al 2008;Leopold and Logothetis 1998;Martinez-Conde et al 2000;Snodderly et al 2001), the existing evidence supports the hypothesis of a common mechanism. For example, preliminary results show that brainstem omnipause neurons (OPNs) pause during microsaccades just as they do during larger saccades (Brien et al 2009;Van Gisbergen et al 1981).…”

Coding of Microsaccades in Three-Dimensional Space by Premotor Saccadic Neurons

“…There is accumulating evidence that the analysis of the timing, rate, and direction of microsaccades provide information about the neural mechanisms underlying vision and certain higher-order cognitive behaviors. For example, microsaccades, which modulate neural activity in visual areas (Martinez-Conde et al, 2000Snodderly et al, 2001;Herrington et al, 2009;Hafed and Krauzlis, 2010;Hass and Horwitz, 2011), have also been shown to be correlated with visual awareness and visuospatial attention (Hafed and Clark, 2002;Engbert and Kliegl, 2003;Laubrock et al, 2005;Betta and Turatto, 2006;Engbert, 2006;Otero-Millan et al, 2008;Cui et al, 2009;Herrington et al, 2009;Kliegl et al, 2009;Pastukhov and Braun, 2010). Given that the temporal dynamics of each eye can differ throughout a given microsaccade, our results suggest that the knowledge of the motion of both eyes could improve the correlation observed between microsaccades and neural activity (or behavior).…”

Computational Modeling of Collicular Integration of Perceptual Responses and Attention in Microsaccades

“…Solutions to the problem of integration of low-level perceptual signals (Martinez-Conde et al, 2000;Rucci and Casile, 2004;Hafed and Krauzlis, 2010) and top-down attention (Posner, 1980;Hafed et al, 2011) studied here in the context of microsaccades might contribute to other aspects of this long-standing issue in active vision (Findlay and Walker, 1999) and scene perception (Itti and Koch, 2001). …”