Retinal Inputs to the Thalamus Are Selectively Gated by Arousal

The brain can flexibly filter out sensory information in a manner that depends on behavioral state. In the visual thalamus and cortex, arousal and locomotion are associated with changes in the magnitude of responses to visual stimuli. Here, we asked whether such modulation of visual responses might already occur at an earlier stage in this visual pathway. We measured neural activity of retinal axons using wide-field and two-photon calcium imaging in awake mouse thalamus across arousal states associated with different pupil sizes. Surprisingly, visual responses to drifting gratings in retinal axonal boutons were robustly modulated by arousal level in a manner that varied across stimulus dimensions and across functionally distinct subsets of boutons. At low and intermediate spatial frequencies, the majority of boutons were suppressed by arousal. In contrast, at high spatial frequencies, boutons tuned to regions of visual space ahead of the mouse showed enhancement of responses. Arousal-related modulation also varied with a bouton's preference for luminance changes and direction or axis of motion, with greater response suppression in boutons tuned to luminance decrements versus increments, and in boutons preferring motion along directions or axes of optic flow. Together, our results suggest that differential modulation of distinct visual information channels by arousal state occurs at very early stages of visual processing, before the information is transmitted to neurons in visual thalamus. Such early filtering may provide an efficient means of optimizing central visual processing and perception across behavioral contexts.