Color-Change Detection Activity in the Primate Superior Colliculus

Abstract

The primate superior colliculus (SC) is a midbrain structure that participates in the control of spatial attention. Previous studies examining the role of the SC in attention have mostly used luminance-based visual features (e.g., motion, contrast) as the stimuli and saccadic eye movements as the behavioral response – both of which are known to modulate the activity of SC neurons. To explore the limits of the SC’s involvement in the control of spatial attention, we recorded SC neuronal activity during a task using color, a visual feature dimension not traditionally associated with the SC, and required monkeys to detect threshold-level changes in the saturation of a cued stimulus by releasing a joystick during maintained fixation. Using this color-based spatial attention task, we found substantial cue-related modulation in all categories of visually responsive neurons in the intermediate layers of the SC. Notably, near-threshold changes in color saturation – both increases and decreases – evoked phasic bursts of activity with magnitudes as large as those evoked by stimulus onset. This change-detection activity had two distinctive features: activity for hits was larger than for misses, and the timing of change-detection activity accounted for 67% of joystick release latency, even though it preceded the release by at least 200 milliseconds. We conclude that during attention tasks, SC activity denotes the behavioral relevance of the stimulus regardless of feature dimension, and that phasic event-related SC activity is suitable to guide the selection of manual responses as well as saccadic eye movements.

Significance Statement Control of spatial attention by primate SC is traditionally viewed as supporting orienting or targeting behaviors, and has been tested with a limited set of visual features. Additionally, despite SC’s characterization as a novel event detector, analysis of SC neuronal activity has been limited to stimulus onset or delay periods. Here, we document change-detection activity in SC: large phasic bursts shortly after threshold-level isoluminant color saturation changes during a task requiring maintained fixation and manual joystick response. Change-detection activity is modulated by spatial cueing, but is also predictive of response choice and accounts for a substantial proportion of response latency. Activity in SC may thus guide the selection of motor responses to visual events regardless of effector or feature dimension.