Dissecting cortical and subcortical contributions to perception with white noise optogenetic inhibition

During visually guided behaviours, hundreds of milliseconds or more can elapse between stimulus onset and a behavioural response. How spikes occurring at different times and in different brain areas are read out to generate perception and guide behaviour remains elusive. To explore temporal relationships between sensory input, neuronal spiking, and behaviour, we recently adapted reverse correlation approaches for optogenetic inhibition. We delivered white noise pulse trains of optogenetic stimulation to excite ChR2-expressing inhibitory neurons in the primary visual cortex (V1) or superior colliculus (SC) of head-fixed mice while they performed a visual detection task. We computed neuronal-behavioral kernels (NBK) based on a reverse correlation of the optogenetic stimuli aligned to stimulus onset after sorting those stimuli based on task outcomes (hit, miss). The NBK provides an unbiased, temporally-precise estimate of how suppression of spiking at different moments during a trial affects behavioural detection of visual stimuli. Because visual stimulus preferences in V1 and SC differ, we hypothesized that spike weighting dynamics differ between SC and V1 depending on the identity of the visual stimulus (e.g., luminance versus contrast). SC NBKs revealed that spikes in the earliest portion of mouse SC visual responses contribute to detection of visual contrast as well as luminance. However, while early V1 spikes are strongly weighted for detecting contrast stimuli, there is little sign of V1 contributions to luminance detection. Optogenetic perturbations outside of the initial 100 ms after the onset of visual stimuli had little impact on performance in either area or condition. Electrophysiological recordings in SC and V1 revealed no long-lasting circuit level effects in response to white noise optogenetic stimulus trains. These data suggest that V1 and SC make concurrent contributions to detection of visual contrast, while detecting changes in luminance depends more strongly on the SC.