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.

Active sensation poses unique challenges to sensory systems because moving the sensor necessarily alters the input sensory stream. Sensory input quality is additionally compromised if the sensor moves rapidly, as during rapid eye movements, making the period immediately after the movement critical for recovering reliable sensation. Here, we studied this immediate postmovement interval for the case of microsaccades during fixation, which rapidly jitter the "sensor" exactly when it is being voluntarily stabilized to maintain clear vision. We characterized retinal-image slip in monkeys immediately after microsaccades by analyzing postmovement ocular drifts. We observed enhanced ocular drifts by up to ϳ28% relative to premicrosaccade levels, and for up to ϳ50 ms after movement end. Moreover, we used a technique to trigger full-field image motion contingent on real-time microsaccade detection, and we used the initial ocular following response to this motion as a proxy for changes in early visual motion processing caused by microsaccades. When the full-field image motion started during microsaccades, ocular following was strongly suppressed, consistent with detrimental retinal effects of the movements. However, when the motion started after microsaccades, there was up to ϳ73% increase in ocular following speed, suggesting an enhanced motion sensitivity. These results suggest that the interface between even the smallest possible saccades and "fixation" includes a period of faster than usual image slip, as well as an enhanced responsiveness to image motion, and that both of these phenomena need to be considered when interpreting the pervasive neural and perceptual modulations frequently observed around the time of microsaccades.

Microsaccades are small saccades. Neurophysiologically, microsaccades are generated using similar brainstem mechanisms as larger saccades. This suggests that peri-saccadic changes in vision that accompany large saccades might also be expected to accompany microsaccades. In this review, we highlight recent evidence demonstrating this. Microsaccades are not only associated with suppressed visual sensitivity and perception, as in the phenomenon of saccadic suppression, but they are also associated with distorted spatial representations, as in the phenomenon of saccadic compression, and pre-movement response gain enhancement, as in the phenomenon of pre-saccadic attention. Surprisingly, the impacts of peri-microsaccadic changes in vision are far reaching, both in time relative to movement onset as well as spatial extent relative to movement size. Periods of ~100 ms before and ~100 ms after microsaccades exhibit significant changes in neuronal activity and behavior, and this happens at eccentricities much larger than the eccentricities targeted by the microsaccades themselves. Because microsaccades occur during experiments enforcing fixation, these effects create a need to consider the impacts of microsaccades when interpreting a variety of experiments on vision, perception, and cognition using awake, behaving subjects. The clearest example of this idea to date has been on the links between microsaccades and covert visual attention. Recent results have demonstrated that peri-microsaccadic changes in vision play a significant role in both neuronal and behavioral signatures of covert visual attention, so much so that in at least some attentional cueing paradigms, there is very tight synchrony between microsaccades and the emergence of attentional effects. Just like large saccades, microsaccades are genuine motor outputs, and their impacts can be substantial even during perceptual and cognitive experiments not concerned with overt motor generation per se.

Saccades cause rapid retinal-image shifts that go perceptually unnoticed several times per second. The mechanisms for saccadic suppression have been controversial, in part because of sparse understanding of neural substrates. In this study we uncovered an unexpectedly specific neural locus for spatial frequency-specific saccadic suppression in the superior colliculus (SC). We first developed a sensitive behavioral measure of suppression in two macaque monkeys, demonstrating selectivity to low spatial frequencies similar to that observed in earlier behavioral studies. We then investigated visual responses in either purely visual SC neurons or anatomically deeper visual motor neurons, which are also involved in saccade generation commands. Surprisingly, visual motor neurons showed the strongest visual suppression, and the suppression was dependent on spatial frequency, as in behavior. Most importantly, suppression selectivity for spatial frequency in visual motor neurons was highly predictive of behavioral suppression effects in each individual animal, with our recorded population explaining up to ~74% of behavioral variance even on completely different experimental sessions. Visual SC neurons had mild suppression, which was unselective for spatial frequency and thus only explained up to ~48% of behavioral variance. In terms of spatial frequency-specific saccadic suppression, our results run contrary to predictions that may be associated with a hypothesized SC saccadic suppression mechanism, in which a motor command in the visual motor and motor neurons is first relayed to the more superficial purely visual neurons, to suppress them and to then potentially be fed back to cortex. Instead, an extraretinal modulatory signal mediating spatial-frequency-specific suppression may already be established in visual motor neurons. Saccades, which repeatedly realign the line of sight, introduce spurious signals in retinal images that normally go unnoticed. In part, this happens because of perisaccadic suppression of visual sensitivity, which is known to depend on spatial frequency. We discovered that a specific subtype of superior colliculus (SC) neurons demonstrates spatial-frequency-dependent suppression. Curiously, it is the neurons that help mediate the saccadic command itself that exhibit such suppression, and not the purely visual ones.

No abstract

Visual brain areas exhibit tuning characteristics well suited for image statistics present in our natural environment. However, visual sensation is an active process, and if there are any brain areas that ought to be particularly in tune with natural scene statistics, it would be sensory-motor areas critical for guiding behavior. Here we found that the rhesus macaque superior colliculus, a structure instrumental for rapid visual exploration with saccades, detects low spatial frequencies, which are the most prevalent in natural scenes, much more rapidly than high spatial frequencies. Importantly, this accelerated detection happens independently of whether a neuron is more or less sensitive to low spatial frequencies to begin with. At the population level, the superior colliculus additionally over-represents low spatial frequencies in neural response sensitivity, even at near-foveal eccentricities. Thus, the superior colliculus possesses both temporal and response gain mechanisms for efficient gaze realignment in low-spatial-frequency-dominated natural environments.

Microsaccades are tiny saccades that occur during gaze fixation. Even though visual processing has been shown to be strongly modulated close to the time of microsaccades, both at central and peripheral eccentricities, it is not clear how these eye movements might influence longer term fluctuations in brain activity and behavior. Here we found that visual processing is significantly affected and, in a rhythmic manner, even several hundreds of milliseconds after a microsaccade. Human visual detection efficiency, as measured by reaction time, exhibited coherent rhythmic oscillations in the α- and β-frequency bands for up to ~650-700 ms after a microsaccade. Surprisingly, the oscillations were sequentially pulsed across visual hemifields relative to microsaccade direction, first occurring in the same hemifield as the movement vector for ~400 ms and then the opposite. Such pulsing also affected perceptual detection performance. Our results suggest that visual processing is subject to long-lasting oscillations that are phase locked to microsaccade generation, and that these oscillations are dependent on microsaccade direction. We investigated long-term microsaccadic influences on visual processing and found rhythmic oscillations in behavioral performance at α- and β-frequencies (~8-20 Hz). These oscillations were pulsed at a much lower frequency across visual hemifields, first occurring in the same hemifield as the microsaccade direction vector for ~400 ms before switching to the opposite hemifield for a similar interval. Our results suggest that saccades temporally organize visual processing and that such organization can sequentially switch hemifields.