Visual fixation (i.e., holding gaze on a specific visual object or location of interest) has been shown to be influenced by activity in the rostral pole of the intermediate layers of the superior colliculus (SCi)—a sensory–motor integration nucleus in the midbrain involved in visual fixation and saccadic eye movement generation. Neurons in the rostral SCi discharge tonically during visual fixation and pause during saccades to locations beyond their foveal visual-sensory or saccadic-motor response fields. Injection of muscimol to deactivate rostral SCi neurons also leads to an increase in fixation instability. However, the precise role of rostral SCi activity for controlling visual fixation has not been established and is actively debated. Here, we address whether this activity reflects signals related to task demands (i.e., maintaining visual fixation) or foveal visual stimulus properties. Two non-human primates performed an oculomotor task that required fixation of a central fixation point (FP) of varying luminance at the start of each trial. During this fixation period, we measured fixational saccades (≤ 2° of the FP, including microsaccades) and fixation-error saccades (> 2° from the FP) in combination with activity from the rostral SCi. Fixation of the lowest FP luminance increased the latency (onset time relative to initial FP foveation) for both fixational and fixation-error saccades. Fifty percent of the rostral SCi neurons exhibited activity that opposed the change in FP luminance and correlated with delayed fixational saccades and increased fixation-error saccades. Twenty-two percent of rostral SCi neurons exhibited activity that followed the change in FP luminance and correlated with earlier fixational saccades and decreased fixation-error saccades. This suggests the rostral SCi contains both sensory-driven and task-related motor signals related to foveal sensory stimuli and visual fixation. This evidence supports a role for the rostral SCi in gaze stabilization and can help inform artificial computational models of vision.

The mechanisms that underlie the integration of visual and goal-related signals for the production of saccades remain poorly understood. Here, we examined how spatial proximity of competing stimuli shapes goal-directed responses in the superior colliculus (SC), a midbrain structure closely associated with the control of visual attention and eye movements. Monkeys were trained to perform an oculomotor-capture task [Theeuwes, J., Kramer, A. F., Hahn, S., Irwin, D. E., & Zelinsky, G. J. Influence of attentional capture on oculomotor control. Journal of Experimental Psychology. Human Perception and Performance, 25, 1595–1608, 1999], in which a target singleton was revealed via an isoluminant color change in all but one item. On a portion of the trials, an additional salient item abruptly appeared near or far from the target. We quantified how spatial proximity between the abrupt-onset and the target shaped the goal-directed response. We found that the appearance of an abrupt-onset near the target induced a transient decrease in goal-directed discharge of SC visuomotor neurons. Although this was indicative of spatial competition, it was immediately followed by a rebound in presaccadic activation, which facilitated the saccadic response (i.e., it induced shorter saccadic RT). A similar suppression also occurred at most nontarget locations even in the absence of the abrupt-onset. This is indicative of a mechanism that enabled monkeys to quickly discount stimuli that shared the common nontarget feature. These results reveal a pattern of excitation/inhibition across the SC visuomotor map that acted to facilitate optimal behavior—the short duration suppression minimized the probability of capture by salient distractors, whereas a subsequent boost in accumulation rate ensured a fast goal-directed response. Such nonlinear dynamics should be incorporated into future biologically plausible models of saccade behavior.

During natural vision, eye movements are dynamically controlled by the combinations of goal-related top–down (TD) and stimulus-related bottom–up (BU) neural signals that map onto objects or locations of interest in the visual world. In primates, both BU and TD signals converge in many areas of the brain, including the intermediate layers of the superior colliculus (SCi), a midbrain structure that contains a retinotopically coded map for saccades. How TD and BU signals combine or interact within the SCi map to influence saccades remains poorly understood and actively debated. It has been proposed that winner-take-all competition between these signals occurs dynamically within this map to determine the next location for gaze. Here, we examine how TD and BU signals interact spatially within an artificial two-dimensional dynamic winner-take-all neural field model of the SCi to influence saccadic RT (SRT). We measured point images (spatially organized population activity on the SC map) physiologically to inform the TD and BU model parameters. In this model, TD and BU signals interacted nonlinearly within the SCi map to influence SRT via changes to the (1) spatial size or extent of individual signals, (2) peak magnitude of individual signals, (3) total number of competing signals, and (4) the total spatial separation between signals in the visual field. This model reproduced previous behavioral studies of TD and BU influences on SRT and accounted for multiple inconsistencies between them. This is achieved by demonstrating how, under different experimental conditions, the spatial interactions of TD and BU signals can lead to either increases or decreases in SRT. Our results suggest that dynamic winner-take-all modeling with local excitation and distal inhibition in two dimensions accurately reflects both the physiological activity within the SCi map and the behavioral changes in SRT that result from BU and TD manipulations.