Laminar organization of the superior colliculus priority map

The superior colliculus (SC) is a multilayered midbrain structure with depth-dependent cortical/subcortical connectivity, and a longstanding role in the control of attention/gaze. While the superficial layers (SCs) have been associated with a bottom-up saliency map, the intermediate layers (SCi) have been described as a priority map, where neuronal signals related to visual salience and behavioral relevance combine to determine attention/gaze. However, the use of single electrodes to understand SC laminar function has been a major limitation due to inaccurate depth estimates. Here, we examined depth-dependent processing of stimuli of different salience/relevance across the intermediate and deeper SC layers using a linear microelectrode (LMA; 16ch, 200 μm inter-contact spacing). Rhesus monkeys were presented with an array of oriented color stimuli (~200 items) with two salient but feature-distinct oddballs. One oddball was goal-relevant (salient/relevant), the other goal-irrelevant (salient/non-relevant), and both were embedded in a feature-homogenous array of ‘distractors’ (non-salient/non-relevant). Following array onset, the animals maintained fixation for 0.5–0.7s allowing temporal separation between visual- and saccade- processes. The fixation stimulus then disappeared, instructing the animal to saccade to the goal-relevant oddball for a reward. We examined multiunit activity (MUA), local field potential activity (LFP), and current source density (CSD). We observed a depth-specific change from net inward-to-outward current flow in the saccade-evoked LFP, and corresponding CSD, indicating a depth-dependent functional distinction. We also observed depth-dependent oddball selectivity corresponding roughly to the upper window (~1600 μm) defined by the CSD cutoff, consistent with SCi. This oddball response was maximal at the center of the window and systematically attenuated dorsal and ventral from this. The deepest sites showed visual and saccadic responses, yet were not oddball selective. These results are consistent with a depth-dependent priority map in the SCi that combines information about stimulus saliency and relevancy to systematically rank order map locations for attention/gaze control.