During fixation, the eyes are not still, but often exhibit microsaccadic movements. The function of microsaccades is controversial, largely because the neural mechanisms responsible for their generation are unknown. Here we show that the superior colliculus (SC), a retinotopically organized structure involved in voluntary-saccade target selection, plays a causal role in microsaccade generation. Neurons in the foveal portion of the SC increase their activity before and during microsaccades with sizes of only a few minutes of arc, and exhibit selectivity for the direction and amplitude of these movements. Reversible inactivation of these neurons significantly reduces microsaccade rate without otherwise compromising fixation. These results, coupled with computational modeling of SC activity, demonstrate that microsaccades are controlled by the SC, and explain the link between microsaccades and visual attention.Microsaccades are the very small (typically <12 min arc), involuntary, fast eye movements that occur during fixation (1-3). The behavioral properties and functional significance of microsaccades have been extensively studied -and sometimes vigorously debated -for many years (1-14). However, the neural mechanisms responsible for their generation are unexplored. We now show that the superior colliculus (SC), a retinotopically organized structure known to be important for selecting and initiating voluntary eye movements (15)(16)(17), is also part of the neural mechanism that controls microsaccades.We analyzed SC activity associated with 15,205 microsaccades that occurred while monkeys fixated a small stationary spot (18). Each fixation trial lasted for 3,500 ms resulting in many microsaccades with a variety of directions and amplitudes (Fig. 1A,Supp. Fig. S1). These movements had dynamics like those of larger saccades (3) (Supp. Fig. S1A), consistent with evidence that pre-motor neurons (downstream from the SC) are active during movements as small as 12-15 min arc (19).We targeted neurons in the rostral pole of the SC, which represents foveal goal locations (18,20). Figure 1A shows the spiking activity of a neuron in the left SC during a single trial containing 9 microsaccades (highlighted in green). The neuron exhibited changes in activity that were correlated with microsaccades. For example, the microsaccades labeled 1 and 2 in Fig. 1A were predominantly downward and leftward, respectively, and both were associated with a reduction in the neuron's activity. In contrast, small, predominantly rightward † This manuscript has been accepted for publication in Science. This version has not undergone final editing. Please refer to the complete version of record at http://www.sciencemag.org/. The manuscript may not be reproduced or used in any manner that does not fall within the fair use provisions of the Copyright Act without the prior, written permission of AAAS.*To whom correspondence should be addressed. E-mail: zhafed@salk.edu. NIH Public Access Author ManuscriptScience. Author manuscript; available in P...

Microsaccades, or tiny eye movements that take place during periods of fixation, have long been thought to be random artifacts of the oculomotor system. Here we demonstrate a possible link between microsaccades and covert attention shifts. We designed two psychophysical tasks involving spatial cues that had identical sensory stimuli but differing patterns of attentional benefits and costs. We found that microsaccades, rather than being randomly distributed, had directions that were directly correlated with the directions of covert attention shifts in the two tasks. Our results suggest that microsaccades occur because of subliminal activation of the oculomotor system by covert attention.

Neuronal response gain enhancement is a classic signature of the allocation of covert visual attention without eye movements. However, microsaccades continuously occur during gaze fixation. Because these tiny eye movements are preceded by motor preparatory signals well before they are triggered, it may be the case that a corollary of such signals may cause enhancement, even without attentional cueing. In six different macaque monkeys and two different brain areas previously implicated in covert visual attention (superior colliculus and frontal eye fields), we show neuronal response gain enhancement for peripheral stimuli appearing immediately before microsaccades. This enhancement occurs both during simple fixation with behaviorally irrelevant peripheral stimuli and when the stimuli are relevant for the subsequent allocation of covert visual attention. Moreover, this enhancement occurs in both purely visual neurons and visual-motor neurons, and it is replaced by suppression for stimuli appearing immediately after microsaccades. Our results suggest that there may be an obligatory link between microsaccade occurrence and peripheral selective processing, even though microsaccades can be orders of magnitude smaller than the eccentricities of peripheral stimuli. Because microsaccades occur in a repetitive manner during fixation, and because these eye movements reset neurophysiological rhythms every time they occur, our results highlight a possible mechanism through which oculomotor events may aid periodic sampling of the visual environment for the benefit of perception, even when gaze is prevented from overtly shifting. One functional consequence of such periodic sampling could be the magnification of rhythmic fluctuations of peripheral covert visual attention.

Visually guided behavior in three-dimensional environments entails handling immensely different sensory and motor conditions across retinotopic visual field locations: peri-personal ("near") space is predominantly viewed through the lower retinotopic visual field (LVF), whereas extra-personal ("far") space encompasses the upper visual field (UVF). Thus, when, say, driving a car, orienting toward the instrument cluster below eye level is different from scanning an upcoming intersection, even with similarly sized eye movements. However, an overwhelming assumption about visuomotor circuits for eye-movement exploration, like those in the primate superior colliculus (SC), is that they represent visual space in a purely symmetric fashion across the horizontal meridian. Motivated by ecological constraints on visual exploration of far space, containing small UVF retinal-image features, here we found a large, multi-faceted difference in the SC's representation of the UVF versus LVF. Receptive fields are smaller, more finely tuned to image spatial structure, and more sensitive to image contrast for neurons representing the UVF. Stronger UVF responses also occur faster. Analysis of putative synaptic activity revealed a particularly categorical change when the horizontal meridian is crossed, and our observations correctly predicted novel eye-movement effects. Despite its appearance as a continuous layered sheet of neural tissue, the SC contains functional discontinuities between UVF and LVF representations, paralleling a physical discontinuity present in cortical visual areas. Our results motivate the recasting of structure-function relationships in the visual system from an ecological perspective, and also exemplify strong coherence between brain-circuit organization for visually guided exploration and the nature of the three-dimensional environment in which we function.

Gaze fixation is an active process, with the incessant occurrence of tiny eye movements, including microsaccades. While the retinal consequences of microsaccades may be presumed minimal because of their minute size, a significant perceptual consequence of these movements can also stem from active extraretinal mechanisms associated with corollaries of their motor generation. Here I show that prior to microsaccade onset, spatial perception is altered in a very specific manner: foveal stimuli are erroneously perceived as more eccentric, whereas peripheral stimuli are rendered more foveal. The mechanism for this perceptual "compression of space" is consistent with a spatially specific gain modulation of visual representations caused by the upcoming eye movements, as is hypothesized to happen for much larger saccades. I then demonstrate that this perimicrosaccadic perceptual alteration has at least one important functional consequence: it mediates visual-performance alterations similar to ones classically attributed to the cognitive process of covert visual attention.

Microsaccades during fixation exhibit distinct time courses of frequency and direction modulations after stimulus onsets, but the mechanisms for these modulations are unresolved. On the one hand, microsaccade rate drops within Ͻ100 ms after stimulus onset, a phenomenon described as microsaccadic inhibition. On the other, the directions of the rare microsaccades that do occur during inhibition are, surprisingly, the most highly correlated with stimulus location. Here we show, using a combined computational and experimental approach, that these apparently dichotomous observations can simply result from a single mechanism: the phase resetting by stimulus onsets of ongoing microsaccadic oscillatory rhythms during fixation. Using experiments on monkeys and model simulations, we show that stimulus onsets act as countermanding stimuli, such as those in large saccadic countermanding tasks: they cancel an upcoming movement program and start a competing one, thus implementing phase resetting. We also show that the rare microsaccades occurring during microsaccadic inhibition are simply noncanceled movements in the countermanding framework and that they reflect the instantaneous state of visual representations expected in spatial maps representing stimuli. Remarkably, a dynamic interaction between the efficacy of the countermanding process and the metrics of the microsaccade being countermanded not only explains microsaccade rate changes, but it also predicts the time course patterns of microsaccade directions and amplitudes. Our parsimonious framework for understanding microsaccadic modulations around stimulus onsets allows analyzing microsaccades (and larger saccades) using the extensive toolkit of oscillatory dynamical systems often used for modeling spiking neurons, and it constrains neural models of microsaccade triggering.

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.

Microsaccades exhibit systematic oscillations in direction after spatial cueing, and these oscillations correlate with facilitatory and inhibitory changes in behavioral performance in the same tasks. However, independent of cueing, facilitatory and inhibitory changes in visual sensitivity also arise pre-microsaccadically. Given such pre-microsaccadic modulation, an imperative question to ask becomes: how much of task performance in spatial cueing may be attributable to these peri-movement changes in visual sensitivity? To investigate this question, we adopted a theoretical approach. We developed a minimalist model in which: (1) microsaccades are repetitively generated using a rise-to-threshold mechanism, and (2) pre-microsaccadic target onset is associated with direction-dependent modulation of visual sensitivity, as found experimentally. We asked whether such a model alone is sufficient to account for performance dynamics in spatial cueing. Our model not only explained fine-scale microsaccade frequency and direction modulations after spatial cueing, but it also generated classic facilitatory (i.e., attentional capture) and inhibitory [i.e., inhibition of return (IOR)] effects of the cue on behavioral performance. According to the model, cues reflexively reset the oculomotor system, which unmasks oscillatory processes underlying microsaccade generation; once these oscillatory processes are unmasked, “attentional capture” and “IOR” become direct outcomes of pre-microsaccadic enhancement or suppression, respectively. Interestingly, our model predicted that facilitatory and inhibitory effects on behavior should appear as a function of target onset relative to microsaccades even without prior cues. We experimentally validated this prediction for both saccadic and manual responses. We also established a potential causal mechanism for the microsaccadic oscillatory processes hypothesized by our model. We used retinal-image stabilization to experimentally control instantaneous foveal motor error during the presentation of peripheral cues, and we found that post-cue microsaccadic oscillations were severely disrupted. This suggests that microsaccades in spatial cueing tasks reflect active oculomotor correction of foveal motor error, rather than presumed oscillatory covert attentional processes. Taken together, our results demonstrate that peri-microsaccadic changes in vision can go a long way in accounting for some classic behavioral phenomena.