Pooled versus structured inhibition drives stimulus competition across distinct spatial scales in the superior colliculus

Competitive stimulus interactions across the space map of the midbrain superior colliculus (SC) are critical for spatial decision-making among multiple options. Here, using electrophysiological recordings from the intermediate and deep layers of the SC (SCid) in mice of either sex, we discovered that the rules and spatial profiles of these competitive interactions are different between local within-receptive field (RF), versus global across-RF-boundary, spatial scales. When one visual stimulus was centered in the RF and a second one was located within the RF’s classical inhibitory surround, we found that stimulus interactions followed an averaging rule. This classical surround was spatially restricted, and the strength of inhibition underlying these within-RF interactions decreased with distance from the RF center. By contrast, when the second stimulus was located outside the RF, stimulus interactions followed a divisive rule. Strikingly, this extra-classical inhibitory surround was spatially global, and the strength of competitive inhibition underlying these across-RF-boundary interactions was distance-invariant while being dependent on the relative strengths of the competing stimuli. Computational modeling revealed that whereas within-RF interactions are well-explained by a normalization-like mechanism driven by pooled inhibition, across-RF-boundary interactions are not, and instead, are well-explained by a winner-take-all-like mechanism driven by structured, donut-like inhibition. Combined, our results reveal the mechanistic logic of stimulus competition across the space-map of mammalian SCid. Significance statement Selecting one target among many is essential for diverse cognitive functions, and requires neural circuits to compare priorities of competing stimuli. Using electrophysiological recordings in the mouse superior colliculus, a critical brain area for spatial decision-making, we show that stimulus competition follows fundamentally different rules at local versus distant spatial scales. Nearby stimuli within a receptive field (RF) engage spatially restricted, decaying inhibition, enacting an averaging rule. By contrast, distant stimuli separated by the RF boundary engage spatially global, distance-invariant inhibition, enacting a divisive, relative strength-dependent rule. Computational modeling reveals that local interactions are explained by a pooling normalization mechanism, whereas global interactions are explained by a donut-like winner-take-all mechanism. Results resolve long open questions about stimulus competition in the SC.