Abstract
Visual responses in primate superior colliculus (SC) are strongly modulated by salient low-level features. Higher-order salience, such as the presence of a distinct form, may also modulate SC neurons independent of low-level features. Here we tested whether SC visual activity was higher when a stimulus in the receptive field (RF) was distinct from, rather than part of, a background while holding low-level salience fixed. We compared the visual responses of neurons in macaque SC to orientation-filtered white noise textures presented either as full-field stimuli (“background” condition) or including an orthogonally oriented patch placed in the neurons’ RF (“patch+background”). To further probe the interactions between the RF and the background, we also included isolated patches on blank backgrounds and full-field textures with blank RF patches (“hole”). All textures had the same average luminance, contrast, and spatial frequency. SC neurons (n = 65) were modulated by higher-order salience already in their earliest response phase. Activity in the patch+background condition was 65% higher compared to the background 40-60ms after stimulus onset (p<0.01, Wilcoxon rank-sum test), and increased to being 2.7 times higher in a later phase (70-120ms: p<0.0001). Early responses to the isolated patch were almost twice as high as the uniform background (p<0.0001) and 20% higher than the patch+background (p<0.05), reflecting rapid surround inhibition from the background. Responses to the hole were lower than to the background in the early phase (p<0.05), but 22% higher in the later phase (p<0.05), suggesting a second-order discrepancy detection process even in the absence of inputs to the RF. Our results show that the primate SC rapidly detects stimuli that are distinct from the background even when their low-level features are the same. This suggests that the SC may be involved in aspects of figure-ground segmentation, an intermediate step between low-level salience and higher-order object processing.