Retinal outputs depend on behavioural state

The operating mode of the visual system depends on behavioural states such as arousal. This dependence is seen both in primary visual cortex (V1) and in subcortical brain structures receiving direct retinal input. Here we show that this effect arises as early as in the output of the retina. We first measured activity in a region that receives retinal projections, the superficial superior colliculus (sSC), and found that this activity strongly depended on behavioural state. This modulation was not mediated by feedback inputs from V1 as it was immune to V1 inactivation. We then used Neuropixels probes to record activity in the optic tract, and we found some retinal axons whose activity significantly varied with arousal, even in darkness. To characterize these effects on a larger sample of retinal outputs, we imaged the activity of retinal boutons in sSC during behaviour using a calcium indicator. The activity of these boutons correlated with arousal as strongly as that of sSC neurons, and this correlation persisted also during darkness. These results reveal a novel property of retinal function in mice, which could be observed only during behaviour: retinal outputs are modulated by behavioural state before they reach the rest of the brain.