Orientation and Contrast Tuning Properties and Temporal Flicker Fusion Characteristics of Primate Superior Colliculus Neurons

The primate superior colliculus is traditionally studied from the perspectives of gaze control, target selection, and selective attention. However, this structure is also visually responsive, and it is the primary visual structure in several species. Thus, understanding the visual tuning properties of the primate superior colliculus is important, especially given that the superior colliculus is part of an alternative visual pathway running in parallel to the predominant geniculo-cortical pathway. In recent previous studies, we have characterized receptive field organization and spatial frequency tuning properties in the primate (rhesus macaque) superior colliculus. Here, we explored additional aspects like orientation tuning, putative center-surround interactions, and temporal frequency tuning characteristics of visually-responsive superior colliculus neurons. We found that orientation tuning exists in the primate superior colliculus, but that such tuning is relatively moderate in strength. We also used stimuli of different sizes to explore contrast sensitivity and center-surround interactions. We found that stimulus size within a visual receptive field primarily affects the slope of contrast sensitivity curves without altering maximal firing rate. Additionally, sustained firing rates, long after stimulus onset, strongly depend on stimulus size, and this is also reflected in local field potentials. This suggests the presence of inhibitory interactions within and around classical receptive fields. Finally, primate superior colliculus neurons exhibit temporal frequency tuning for frequencies lower than 30 Hz, with critical flicker fusion frequencies of <20 Hz. These results support the hypothesis that the primate superior colliculus might contribute to visual performance, likely by mediating coarse, but rapid, object detection and identification capabilities for the purpose of facilitating or inhibiting orienting responses. Such mediation may be particularly amplified in blindsight subjects who lose portions of their primary visual cortex and therefore rely on alternative visual pathways including the pathway through the superior colliculus

Peri-saccadic orientation identification performance and visual neural sensitivity are higher in the upper visual field

Visual neural processing is distributed among a multitude of sensory and sensory-motor brain areas exhibiting varying degrees of functional specializations and spatial representational anisotropies. Such diversity raises the question of how perceptual performance is determined, at any one moment in time, during natural active visual behavior. Here, exploiting a known dichotomy between the primary visual cortex (V1) and superior colliculus (SC) in representing either the upper or lower visual fields, we asked whether peri-saccadic orientation identification performance is dominated by one or the other spatial anisotropy. Humans (48 participants, 29 females) reported the orientation of peri-saccadic upper visual field stimuli significantly better than lower visual field stimuli, unlike their performance during steady-state gaze fixation, and contrary to expected perceptual superiority in the lower visual field in the absence of saccades. Consistent with this, peri-saccadic superior colliculus visual neural responses in two male rhesus macaque monkeys were also significantly stronger in the upper visual field than in the lower visual field. Thus, peri-saccadic orientation identification performance is more in line with oculomotor, rather than visual, map spatial anisotropies

A Model of Repetitive Microsaccades, Coupled with Pre-microsaccadic Changes in Vision, is Sufficient to Account for Both Attentional Capture and Inhibition of Return in Posner Cueing

When a cue is presented at a location, orienting efficacy towards that location is improved relative to other locations (“attentional capture”), but only briefly; a mere few hundred milliseconds later, orienting incurs large costs. These costs have been classically termed “inhibition of return” (IOR), alluding to voluntary, cognitive strategies avoiding perseverance at one location. However, despite this popular hypothesis, the origins of both attentional capture and IOR remain elusive. Here we show that both of these phenomena can be accounted for by a single concept of oculomotor rhythmicity, and one that involves the entire gamut of saccadic activity including microsaccades. Our model posits that cues reset the phase of ongoing 1.5-3 Hz microsaccadic temporal frequency rhythms; attentional capture and IOR simply depend on the post-cue phase of the reset rhythms at which subsequent targets appear. We conclude that “attentional capture” and “IOR” may surprisingly be simple emergent properties of motor rhythmicity. More broadly, the strong explanatory power of phase modulation in our model suggests that attentional alterations may be manifestations of existing oscillatory brain fluctuations, which are merely uncovered when cues reset them

Alteration of Visual Perception prior to Microsaccades

SummaryGaze 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

A Neural Network Model Of The Primate Saccadic System

A new, distributed model of the primate oculomotor system is presented. This model generates saccades (rapid eye movements) of various amplitudes, and it is able to exhibit various saccade-related phenomena, including multiple and interrupted saccades. The model differs from those in the literature in some of its hypotheses about the roles of the classes of neurons investigated here, but it remains largely in line with the current knowledge about saccade generation. The Superior Colliculus (a layered structure in the midbrain) plays a particularly important role in the model, and it is represented by three different layers: visual, burst, and buildup. The burst layer includes neurons that encode initial motor error, while the buildup layer houses cells whose shifting activity during a saccade provides an estimate for dynamic motor error. Collicular fixation neurons are also modeled, and they are characterized by a Winner-Take-All competition with burst neurons. Such a competition dicta..

Motor theories of attention : how action serves perception in the visual system

In this dissertation, we investigate the relationship between visual attention and eye movement programming mechanisms in the brain. As a first step in this investigation, we demonstrate a link between microsaccades, or tiny eye movements that occur during periods of fixation, and covert attention shifts. Specifically, we employ psychophysical tasks that involve covert spatial attention shifts to peripheral cues, and we correlate the time courses of microsaccade occurrences in these tasks with the time courses of attention shifts, as revealed by the effects of these shifts on behavioral performance. Our results suggest that microsaccades, rather than being randomly distributed, have directions that are directly correlated with the directions of covert attention shifts. These results therefore suggest that microsaccades occur because of subliminal activation of the oculomotor system by covert attention.Besides providing a plausible explanation for much of the known phenomenology associated with microsaccades, the above link between microsaccades and covert attention means that the first may be used to track the latter. We demonstrate an example of such tracking by using microsaccades as a psychophysical tool to analyze the patterns of covert attention shifts that take place in typical visual tasks. In addition to revealing expected covert attention shifts in our tasks, microsaccade analysis reveals shifts that were previously unreported, including ones that are tightly synchronized with manual response execution. This analysis also shows that the patterns of attention shifts to task-relevant stimuli that are observed in visual tasks are identical whether overt saccades are allowed during task execution or not.The above results lead to an investigation of the implications of overt and covert spatial attention shifts on feature processing. We present a post-motor theory of attention whose main thesis is that feature salience is modified in anticipation of the sensory consequences of a motor act, even if this act is eventually suppressed. We provide psychophysical evidence for such salience modification and show that a spatial attention shift to a location gives rise to a feature-based attention shift to the features at that location. We also show that such a feature-based attention shift outlasts a saccade and therefore aids the visual system in handling the consequences of such a saccade on target appearance