Visual Feature Tuning Properties of Short-Latency Stimulus-Driven Ocular Position Drift Responses during Gaze Fixation.

Ocular position drifts during gaze fixation are significantly less well understood than microsaccades. We recently identified a short-latency ocular position drift response, of ∼1 min arc amplitude, that is triggered within <100 ms by visual onsets. This systematic eye movement response is feature-tuned and seems to be coordinated with a simultaneous resetting of the saccadic system by visual stimuli. However, much remains to be learned about the drift response, especially for designing better-informed neurophysiological experiments unraveling its mechanistic substrates. Here we systematically tested multiple new feature tuning properties of drift responses. Using highly precise eye tracking in three male rhesus macaque monkeys, we found that drift responses still occur for tiny foveal visual stimuli. Moreover, the responses exhibit size tuning, scaling their amplitude (both up and down) as a function of stimulus size, and they also possess a monotonically increasing contrast sensitivity curve. Importantly, short-latency drift responses still occur for small peripheral visual targets, which additionally introduce spatially directed modulations in drift trajectories toward the appearing peripheral stimuli. Drift responses also remain predominantly upward even for stimuli exclusively located in the lower visual field and even when starting gaze position is upward. When we checked the timing of drift responses, we found it was better synchronized to stimulus-induced saccadic inhibition than to stimulus onset. These results, along with a suppression of drift response amplitudes by peristimulus saccades, suggest that drift responses reflect the rapid impacts of short-latency and feature-tuned visual neural activity on final oculomotor control circuitry in the brain.

Faster Detection of "Darks" than "Brights" by Monkey Superior Colliculus Neurons.

Visual processing is segregated into ON and OFF channels as early as in the retina, and the superficial (output) layers of the primary visual cortex (V1) are dominated by neurons preferring dark stimuli. However, it is not clear how the timing of neural processing differs between "darks" and "brights" in general, especially in light of psychophysical evidence; it is also equally not clear how subcortical visual pathways that are critical for active orienting represent stimuli of positive (luminance increments) and negative (luminance decrements) contrast polarity. Here, we recorded from all visually-responsive neuron types in the superior colliculus (SC) of two male rhesus macaque monkeys. We presented a disk (0.51° radius) within the response fields (RFs) of neurons, and we varied, across trials, stimulus Weber contrast relative to a gray background. We also varied contrast polarity. There was a large diversity of preferences for darks and brights across the population. However, regardless of individual neural sensitivity, most neurons responded significantly earlier to dark than bright stimuli. This resulted in a dissociation between neural preference and visual response onset latency: a neuron could exhibit a weaker response to a dark stimulus than to a bright stimulus of the same contrast, but it would still have an earlier response to the dark stimulus. Our results highlight an additional candidate visual neural pathway for explaining behavioral differences between the processing of darks and brights, and they demonstrate the importance of temporal aspects in the visual neural code for orienting eye movements.SIGNIFICANCE STATEMENT Objects in our environment, such as birds flying across a bright sky, often project shadows (or images darker than the surround) on our retina. We studied how primate superior colliculus (SC) neurons visually process such dark stimuli. We found that the overall population of SC neurons represented both dark and bright stimuli equally well, as evidenced by a relatively equal distribution of neurons that were either more or less sensitive to darks. However, independent of sensitivity, the great majority of neurons detected dark stimuli earlier than bright stimuli, evidenced by a smaller response latency for the dark stimuli. Thus, SC neural response latency can be dissociated from response sensitivity, and it favors the faster detection of dark image contrasts.

Visual feature tuning properties of stimulus-driven saccadic inhibition in macaque monkeys.

Saccadic inhibition refers to a short-latency transient cessation of saccade generation after visual sensory transients. This oculomotor phenomenon occurs with a latency that is consistent with a rapid influence of sensory responses, such as stimulus-induced visual bursts, on oculomotor control circuitry. However, the neural mechanisms underlying saccadic inhibition are not well understood. Here, we exploited the fact that macaque monkeys experience robust saccadic inhibition to test the hypothesis that inhibition time and strength exhibit systematic visual feature tuning properties to a multitude of visual feature dimensions commonly used in vision science. We measured saccades in three monkeys actively controlling their gaze on a target, and we presented visual onset events at random times. Across seven experiments, the visual onsets tested size, spatial frequency, contrast, orientation, motion direction, and motion speed dependencies of saccadic inhibition. We also investigated how inhibition might depend on the behavioral relevance of the appearing stimuli. We found that saccadic inhibition starts earlier, and is stronger, for large stimuli of low spatial frequencies and high contrasts. Moreover, saccadic inhibition timing depends on motion direction and orientation, with earlier inhibition systematically occurring for horizontally drifting vertical gratings. On the other hand, saccadic inhibition is stronger for faster motions and when the appearing stimuli are subsequently foveated. Besides documenting a range of feature tuning dimensions of saccadic inhibition to the properties of exogenous visual stimuli, our results establish macaque monkeys as an ideal model system for unraveling the neural mechanisms underlying a ubiquitous oculomotor phenomenon in visual neuroscience.NEW & NOTEWORTHY Visual onsets dramatically reduce saccade generation likelihood with very short latencies. Such latencies suggest that stimulus-induced visual responses, normally jump-starting perceptual and scene analysis processes, can also directly impact the decision of whether to generate saccades or not, causing saccadic inhibition. Consistent with this, we found that changing the appearance of the visual onsets systematically alters the properties of saccadic inhibition. These results constrain neurally inspired models of coordination between saccade generation and exogenous sensory stimulation.

Dependence of the stimulus-driven microsaccade rate signature in rhesus macaque monkeys on visual stimulus size and polarity.

Microsaccades have a steady rate of occurrence during maintained gaze fixation, which gets transiently modulated by abrupt sensory stimuli. Such modulation, characterized by a rapid reduction in microsaccade frequency followed by a stronger rebound phase of high microsaccade rate, is often described as the microsaccadic rate signature, owing to its stereotyped nature. Here, we investigated the impacts of stimulus polarity (luminance increments or luminance decrements relative to background luminance) and size on the microsaccadic rate signature. We presented brief, behaviorally irrelevant visual flashes consisting of large or small, white or black stimuli over an otherwise gray image background. Both large and small stimuli caused robust early microsaccadic inhibition, but postinhibition microsaccade rate rebound was significantly delayed and weakened for large stimuli when compared with small ones. Critically, small black stimuli were associated with stronger modulations in the microsaccade rate signature than small white stimuli, particularly in the postinhibition rebound phase, and black stimuli also amplified the incidence of early stimulus-directed microsaccades. Our results demonstrate that the microsaccadic rate signature is sensitive to stimulus size and polarity, and they point to dissociable neural mechanisms underlying early microsaccadic inhibition after stimulus onset and later microsaccadic rate rebound at longer times thereafter. These results also demonstrate early access of oculomotor control circuitry to diverse sensory representations, particularly for momentarily inhibiting saccade generation with short latencies.NEW & NOTEWORTHY Microsaccade rate is transiently reduced after sudden stimulus onsets, and then strongly rebounds before returning to baseline. We explored the influence of stimulus polarity (black vs. white) and size on this "rate signature." Large stimuli caused more muted microsaccadic rebound than small ones, and microsaccadic rebound was also differentially affected by black versus white stimuli, particularly with small stimuli. These results suggest dissociated neural mechanisms for microsaccadic inhibition and rebound in the microsaccadic rate signature.

Superior colliculus saccade motor bursts do not dictate movement kinematics.

The primate superior colliculus (SC) contains a topographic map of space, such that the anatomical location of active neurons defines a desired eye movement vector. Complementing such a spatial code, SC neurons also exhibit saccade-related bursts that are tightly synchronized with movement onset. Current models suggest that such bursts constitute a rate code dictating movement kinematics. Here, using two complementary approaches, we demonstrate a dissociation between the SC rate code and saccade kinematics. First, we show that SC burst strength systematically varies depending on whether saccades of the same amplitude are directed towards the upper or lower visual fields, but the movements themselves have similar kinematics. Second, we show that for the same saccade vector, when saccades are significantly slowed down by the absence of a visible saccade target, SC saccade-related burst strengths can be elevated rather than diminished. Thus, SC saccade-related motor bursts do not necessarily dictate movement kinematics.

Dissociable Cortical and Subcortical Mechanisms for Mediating the Influences of Visual Cues on Microsaccadic Eye Movements.

Visual selection in primates is intricately linked to eye movements, which are generated by a network of cortical and subcortical neural circuits. When visual selection is performed covertly, without foveating eye movements toward the selected targets, a class of fixational eye movements, called microsaccades, is still involved. Microsaccades are small saccades that occur when maintaining precise gaze fixation on a stationary point, and they exhibit robust modulations in peripheral cueing paradigms used to investigate covert visual selection mechanisms. These modulations consist of changes in both microsaccade directions and frequencies after cue onsets. Over the past two decades, the properties and functional implications of these modulations have been heavily studied, revealing a potentially important role for microsaccades in mediating covert visual selection effects. However, the neural mechanisms underlying cueing effects on microsaccades are only beginning to be investigated. Here we review the available causal manipulation evidence for these effects' cortical and subcortical substrates. In the superior colliculus (SC), activity representing peripheral visual cues strongly influences microsaccade direction, but not frequency, modulations. In the cortical frontal eye fields (FEF), activity only compensates for early reflexive effects of cues on microsaccades. Using evidence from behavior, theoretical modeling, and preliminary lesion data from the primary visual cortex and microstimulation data from the lower brainstem, we argue that the early reflexive microsaccade effects arise subcortically, downstream of the SC. Overall, studying cueing effects on microsaccades in primates represents an important opportunity to link perception, cognition, and action through unaddressed cortical-subcortical neural interactions. These interactions are also likely relevant in other sensory and motor modalities during other active behaviors.

Rapid stimulus-driven modulation of slow ocular position drifts.

The eyes are never still during maintained gaze fixation. When microsaccades are not occurring, ocular position exhibits continuous slow changes, often referred to as drifts. Unlike microsaccades, drifts remain to be viewed as largely random eye movements. Here we found that ocular position drifts can, instead, be very systematically stimulus-driven, and with very short latencies. We used highly precise eye tracking in three well trained macaque monkeys and found that even fleeting (~8 ms duration) stimulus presentations can robustly trigger transient and stimulus-specific modulations of ocular position drifts, and with only approximately 60 ms latency. Such drift responses are binocular, and they are most effectively elicited with large stimuli of low spatial frequency. Intriguingly, the drift responses exhibit some image pattern selectivity, and they are not explained by convergence responses, pupil constrictions, head movements, or starting eye positions. Ocular position drifts have very rapid access to exogenous visual information.

Vision is a highly complex, active process. As we observe and interact with the world around us, we constantly use eye movements to capture the visual information we need. In fact, our eyes continue to make tiny, unconscious movements even when we try to fix our gaze on something. There are two main types of tiny eye movements. The first kind, so called microsaccades, are fast, microscopic flicks that happen every second or half-second. The other kind, termed drift, is a slower, gradual motion that takes place between microsaccades, or at any time when other eye movements are not happening. However, we know far less about drifts than about any other eye movements: both the reason why they occur and the brain mechanisms controlling them are still unclear. Many scientists think that drifts are largely random movements, without any set direction. However, eye drifts do sometimes align with other behaviours ­ for example, they can help compensate for small, subtle head movements ­ suggesting that drifts may not be completely random after all. Malevich, Buonocore and Hafed therefore set out to test the hypothesis that eye drifts could, under the right circumstances, in fact be highly directed movements. These experiments used precise sensors to track eye movements in macaque monkeys, which had been trained to fix their gaze on images or shapes (stimuli) presented on a screen. This revealed that presenting new stimuli, even for a few thousandths of a second, could repeatedly trigger drifts. This reaction also happened quickly, starting less than one hundredth of a second after presentation of the stimulus. Further tests, using different images, revealed that the drifts were not only simply reacting to any new stimuli but also appeared to be a partially selective response to specific types of images. These tended to have larger features and less fine detail. For example, a picture of a landscape with large swaths of sky or hilltops would much more reliably trigger the eye drifts than a finely detailed checkerboard pattern, with many small squares alternating between black and white. These results suggested that drifts, far from being random movements, could be another tool for the brain to process visual information. This work sheds new light on the potential role of eye movements in vision, and adds another layer of complexity to the question of how we see. Malevich et al. hope that this study will inspire further research into the brain mechanisms behind ocular drifts.

No evidence for an independent retinotopic reference frame for inhibition of return.

Inhibition of return (IOR) represents a delay in responding to a previously inspected location and is viewed as a crucial mechanism that sways attention toward novelty in visual search. Although most visual processing occurs in retinotopic, eye-centered, coordinates, IOR must be coded in spatiotopic, environmental, coordinates to successfully serve its role as a foraging facilitator. Early studies supported this suggestion but recent results have shown that both spatiotopic and retinotopic reference frames of IOR may co-exist. The present study tested possible sources for IOR at the retinotopic location including being part of the spatiotopic IOR gradient, part of hemifield inhibition and being an independent source of IOR. We conducted four experiments that alternated the cue-target spatial distance (discrete and contiguous) and the response modality (manual and saccadic). In all experiments, we tested spatiotopic, retinotopic and neutral (neither spatiotopic nor retinotopic) locations. We did find IOR at both the retinotopic and spatiotopic locations but no evidence for an independent source of retinotopic IOR for either of the response modalities. In fact, we observed the spread of IOR across entire validly cued hemifield including at neutral locations. We conclude that these results indicate a strategy to inhibit the whole cued hemifield or suggest a large horizontal gradient around the spatiotopically cued location. PUBLIC SIGNIFICANCE STATEMENT: We perceive the visual world around us as stable despite constant shifts of the retinal image due to saccadic eye movements. In this study, we explore whether Inhibition of return (IOR), a mechanism preventing us from returning to previously attended locations, operates in spatiotopic, world-centered or in retinal, eye-centered coordinates. We tested both saccadic and manual IOR at spatiotopic, retinotopic, and control locations. We did not find an independent retinotopic source of IOR for either of the response modalities. The results suggest that IOR spreads over the whole previously attended visual hemifield or there is a large horizontal spatiotopic gradient. The current results are in line with the idea of IOR being a foraging facilitator in visual search and contribute to our understanding of spatiotopically organized aspects of visual and attentional systems.

Temporal Limitations of the Standard Leaky Integrate and Fire Model.

Itti and Koch's Saliency Model has been used extensively to simulate fixation selection in a variety of tasks from visual search to simple reaction times. Although the Saliency Model has been tested for its spatial prediction of fixations in visual salience, it has not been well tested for their temporal accuracy. Visual tasks, like search, invariably result in a positively skewed distribution of saccadic reaction times over large numbers of samples, yet we show that the leaky integrate and fire (LIF) neuronal model included in the classic implementation of the model tends to produce a distribution shifted to shorter fixations (in comparison with human data). Further, while parameter optimization using a genetic algorithm and Nelder-Mead method does improve the fit of the resulting distribution, it is still unable to match temporal distributions of human responses in a visual task. Analysis of times for individual images reveal that the LIF algorithm produces initial fixation durations that are fixed instead of a sample from a distribution (as in the human case). Only by aggregating responses over many input images do they result in a distribution, although the form of this distribution still depends on the input images used to create it and not on internal model variability.

Temporal ambiguity of onsets in a cueing task prevents facilitation but not inhibition of return.

Cueing effects, i.e., early facilitation of reaction time and inhibition of return (IOR), are well-established and robust phenomena characterizing exogenous orienting and are widely observed in experiments with a traditional Posner cueing paradigm. Krüger, MacInnes, and Hunt (2014) proposed that facilitatory effects of peripheral cues are the result of a cue-target perceptual merging due to re-entrant visual processing. To test the role and timing of these feedback mechanisms in peripheral cueing effects, we modified the traditional cueing task in Experiments 1-3 by interleaving pre- and post-cue trials at the valid and invalid location and random cue-target onset asynchrony (CTOA) ranging from -300 to +1,000 ms. Analysis of the manual reaction time distribution over CTOA showed well-pronounced IOR in the valid pre-cue condition and a small cost of perceptual merging in the post-cue condition, but no early facilitation of reaction time was observed in the pre-cue condition. In Experiment 4, we tested directly whether temporal ambiguity eliminated facilitation by restricting CTOAs to only the pre-cue time range and including a between-subject manipulation of a) random, b) mixed discrete, and c) blocked discrete CTOAs. Results obtained in the continuous and binned conditions showed no facilitation but robust IOR. We found both early facilitation and IOR in the blocked condition. Overall, the present findings show a small perceptual merging result without accompanying facilitation, suggesting different underlying mechanisms. Second, they demonstrate that early facilitation is likely to be affected by the presence or absence of temporal expectations and that the early onset of IOR might be masked by stronger facilitation in traditional cueing experiments.