Abstract
We recently found that inactivation of the macaque superior colliculus (SC) reduces responses to visual objects in temporal cortex neurons, suggesting that visual object processing may be an important component of how the SC contributes to visual attention and orienting. Here, to investigate how SC activity is modulated by visual object stimuli, we recorded visually responsive neurons in the superficial and intermediate layers of the SC of two rhesus macaques while they passively viewed images presented in the neurons’ visual receptive fields. We used 150 grayscale images of objects belonging to 5 categories that have been extensively used to test visual object representation in the temporal cortex: face, body, hand, fruit/vegetable, and human-made objects. Crucially, the 30 images comprising these categories were matched in their distributions of low-level features (RMS contrast, size, power in three spatial frequency bands), allowing us to determine how SC responses varied with object category in a manner that is independent of low-level visual features. We found that many SC neurons exhibited an object category preference – specifically, a preference for faces – within 60ms of stimulus onset. A linear classifier using SC spike counts in the interval of 40 to 80ms after stimulus onset, distinguished faces from each of the other 4 object categories with accuracies well above chance, but could not reliably distinguish amongst the other object categories. Together, our results reveal that the primate SC, the most important subcortical brain structure for controlling where we look, signals the presence of a face with an extremely short latency, providing a plausible neural substrate for the primates’ well-recognized ability to rapidly detect and orient towards faces. By biasing us to look at faces, the SC may also play a crucial role in how cortical face processing operates, especially during development.