Ziad M. Hafed

A Neural Mechanism for Microsaccade Generation in the Primate Superior Colliculus

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.

Similarity of superior colliculus involvement in microsaccade and saccade generation

The characteristics of microsaccades, or small fixational saccades, and their influence on visual function have been studied extensively. However, the detailed mechanisms for generating these movements are less understood. We recently found that the superior colliculus (SC), a midbrain structure involved in saccade generation, also plays a role in microsaccade generation. Here we compared the dynamics of neuronal activity in the SC associated with microsaccades to those observed in this structure in association with larger voluntary saccades. We found that microsaccade-related activity in the SC is characterized by a gradual increase in firing rate starting ∼100 ms prior to microsaccade onset, a peak of neuronal discharge just after movement onset, and a subsequent gradual decrease in firing rate until ∼100 ms after movement onset. These properties were shared with saccade-related SC neurons, recorded from the same monkeys but preferring larger eye movements, suggesting that at the level of the SC the neuronal control of microsaccades is similar to that for larger voluntary saccades. We also found that neurons exhibiting microsaccade-related activity often also exhibited saccade-related activity for slightly larger movements of similar direction, suggesting a continuity of the spatial representation in the SC, in both amplitude and direction, down to the smallest movements. Our results indicate that the mechanisms controlling microsaccades may be fundamentally the same as those for larger saccades, and thus shed new light on the functional role of these eye movements and their possible influence on sensory and sensory-motor processes.

Microsaccadic Suppression of Visual Bursts in the Primate Superior Colliculus

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 ∼30% suppression of the bursts. Suppression started ∼70 ms before microsaccade onset and ended ∼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.

Modulation of Microsaccades in Monkey during a Covert Visual Attention Task

The use of awake, fixating monkeys in neuroscience has allowed significant advances in understanding numerous brain functions. However, fixation is an active process, with the occurrence of incessant eye movements, including rapid ones called microsaccades. Even though microsaccades have been shown to be modulated by stimulus and cognitive processes in humans, it is not known to what extent these results are similar in monkeys or why they occur. Here, we analyzed the stimulus-, context-, and attention-related changes in microsaccades while monkeys performed a challenging visual attention task. The distributions of microsaccade times were highly stereotypical across thousands of trials in the task. Moreover, in epochs of the task in which animals anticipated the occurrence of brief stimulus probes, microsaccade frequency decreased to a rate of less than one movement per second even on long multisecond trials. These effects were explained by the observation that microsaccades occurring at the times of the brief probes were sometimes associated with reduced perceptual performance. Microsaccade directions also exhibited temporal modulations related to the attentional demands of the task, like earlier studies in humans, and were more likely to be directed toward an attended location on successfully performed trials than on unsuccessfully completed ones. Our results show that microsaccades in nonhuman primates are correlated with the allocation of stimulus-evoked and sustained covert attention. We hypothesize that involvement of the superior colliculus in microsaccade generation and attentional allocation contributes to these observations. More importantly, our results clarify the potential role of these eye movements in modifying behavior and neural activity.

Superior Colliculus Inactivation Causes Stable Offsets in Eye Position during Tracking

The primate superior colliculus (SC) is often viewed as composed of two distinct motor zones with complementary functions: a peripheral region that helps generate saccades to eccentric targets and a central one that maintains fixation by suppressing saccades. Here, we directly tested the alternative interpretation that topography in the SC is not strictly motor, nor does it form two distinct zones, but instead forms a single map of behaviorally relevant goal locations. Primates tracked the invisible midpoint between two moving stimuli, such that the stimuli guiding tracking were peripheral whereas the inferred movement goal was foveal and parafoveal. Temporary inactivation of neurons in the central portion of the topographic map of the SC, representing the invisible goal, caused stable offsets in eye position during tracking that were directed away from the retinotopic position encoded by the inactivated SC site. Critically, these offsets were not accompanied by a systematic inability to generate or suppress saccades, and they were not fully explained by motor deficits in saccades, smooth pursuit, or fixation. In addition, the magnitude of the offset depended on the eccentricity of the inactivated site as well as the degree of spatial uncertainty associated with the behavioral goal. These results indicate that gaze control depends on the balance of activity across a map of goal locations in the SC, and that by silencing some of the neurons in the normally active population representing the behavioral goal, focal inactivation causes a biased estimate of where to look.

Visual fixation as equilibrium: Evidence from superior colliculus inactivation

During visual fixation, the image of an object is maintained within the fovea. Previous studies have shown that such maintenance involves the deep superior colliculus (dSC). However, the mechanisms by which the dSC supports visual fixation remain controversial. According to one view, activity in the rostral dSC maintains gaze direction by preventing neurons in the caudal dSC from issuing saccade commands. An alternative hypothesis proposes that gaze direction is achieved through equilibrium of target position signals originating from the two dSCs. Here, we show in monkeys that artificially reducing activity in the rostral half of one dSC results in a biased estimate of target position during fixation, consistent with the second hypothesis, rather than an inability to maintain gaze fixation as predicted by the first hypothesis. After injection of muscimol at rostral sites in the dSC, fixation became more stable since microsaccade rate was reduced rather than increased. Moreover, the scatter of eye positions was offset relative to preinactivation baselines. The magnitude and the direction of the offsets depended on both the target size and the injected site in the collicular map. Other oculomotor parameters, such as the accuracy of saccades to peripheral targets and the amplitude and velocity of fixational saccades, were largely unaffected. These results suggest that the rostral half of the dSC supports visual fixation through a distributed representation of behaviorally relevant target position signals. The inactivation-induced fixation offset establishes the foveal visual stimulation that is required to restore the balance of activity between the two dSCs.

Goal Representations Dominate Superior Colliculus Activity during Extrafoveal Tracking

The primate superior colliculus (SC) has long been known to be involved in saccade generation. However, SC neurons also exhibit fixation-related and smooth-pursuit-related activity. A parsimonious explanation for these seemingly disparate findings is that the SC contains a map of behaviorally relevant goal locations, rather than just a motor map for saccades and fixation. This explanation predicts that SC activity should reflect the behavioral goal, even when the behavioral response is not fixation or saccades, and even if the goal does not correspond to a visual stimulus. We tested this prediction by using a tracking task that dissociates the stimulus and goal locations. In this task, monkeys tracked the invisible midpoint between two peripheral bars, such that the visual stimuli were peripheral but the goal was foveal/parafoveal. We recorded from SC neurons representing peripheral locations associated with the stimulus or central locations associated with the goal. Most neurons with peripheral response fields did not respond differently during tracking than during passive viewing of the stimulus under fixation; most neurons with central response fields responded more during tracking than during fixation, despite the lack of a visual stimulus. Moreover, the spatial distribution of activity during tracking was larger than that during fixation or tracking of a foveal stimulus, suggesting that the greater spatial uncertainty about the invisible goal corresponded to more widespread SC activity. These results demonstrate the flexibility with which activity across the SC represents the location, as well as the spatial precision, of behaviorally relevant goals for multiple eye movements.

Ongoing eye movements constrain visual perception

Eye movements markedly change the pattern of retinal stimulation. To maintain stable vision, the brain possesses a variety of mechanisms that compensate for the retinal consequences of eye movements. However, eye movements may also be important for resolving the ambiguities often posed by visual inputs, because motor commands contain additional spatial information that is necessarily absent from retinal signals. To test this possibility, we used a perceptually ambiguous stimulus composed of four line segments, consistent with a shape whose vertices were occluded. In a passive condition, subjects fixated a spot while the shape translated along a certain trajectory. In several active conditions, the spot, occluder and shape translated such that when subjects tracked the spot, they experienced the same retinal stimulus as during fixation. We found that eye movements significantly promoted perceptual coherence compared to fixation. These results indicate that eye movement information constrains the perceptual interpretation of visual inputs.

Neuronal control of fixation and fixational eye movements

Ocular fixation is a dynamic process that is actively controlled by many of the same brain structures involved in the control of eye movements, including the superior colliculus, cerebellum and reticular formation. In this article, we review several aspects of this active control. First, the decision to move the eyes not only depends on target-related signals from the peripheral visual field, but also on signals from the currently fixated target at the fovea, and involves mechanisms that are shared between saccades and smooth pursuit. Second, eye position during fixation is actively controlled and depends on bilateral activity in the superior colliculi and medio-posterior cerebellum; disruption of activity in these circuits causes systematic deviations in eye position during both fixation and smooth pursuit eye movements. Third, the eyes are not completely still during fixation but make continuous miniature movements, including ocular drift and microsaccades, which are controlled by the same neuronal mechanisms that generate larger saccades. Finally, fixational eye movements have large effects on visual perception. Ocular drift transforms the visual input in ways that increase spatial acuity; microsaccades not only improve vision by relocating the fovea but also cause momentary changes in vision analogous to those caused by larger saccades. This article is part of the themed issue ‘Movement suppression: brain mechanisms for stopping and stillness’.

A neural locus for spatial-frequency specific saccadic suppression in visual-motor neurons of the primate superior colliculus

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.NEW & NOTEWORTHY 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.