Temporal weighting of cortical and subcortical spikes reveals stimulus dependent differences in their contributions to behavior.

The primary visual cortex (V1) and the superior colliculus (SC) both occupy stations early in the processing of visual information. They have long been thought to perform distinct functions, with V1 supporting perception of visual features and the SC regulating orienting to visual inputs. However, growing evidence suggests that the SC supports perception of many of the same visual features traditionally associated with V1. To distinguish V1 and SC contributions to visual processing, it is critical to determine whether both areas causally contribute to perception of specific visual stimuli. Here, mice reported changes in visual contrast or luminance near perceptual threshold while we presented white noise patterns of optogenetic stimulation to V1 or SC inhibitory neurons. We then performed a reverse correlation analysis on the optogenetic stimuli to estimate a neuronal-behavioral kernel (NBK), a moment-to-moment estimate of the impact of V1 or SC inhibition on stimulus detection. We show that the earliest moments of stimulus-evoked activity in SC are critical for detection of both luminance or contrast changes. Strikingly, there was a robust stimulus-aligned modulation in the V1 contrast-detection NBK, but no sign of a comparable modulation for luminance detection. The data suggest that perception of visual contrast depends on both V1 and SC spiking, whereas mice preferentially use SC activity to detect changes in luminance. Electrophysiological recordings showed that neurons in both SC and V1 responded strongly to both visual stimulus types, while the reverse correlation analysis reveals when these neuronal signals actually contribute to visually-guided behaviors.