Visual loom caused by self-movement or object-movement elicits distinct responses in mouse superior colliculus

Abstract

The meaning of a visual image depends on context—a mouse sees an expanding visual stimulus when approaching a dark refuge or when a cat approaches them, and distinguishing between the two is a matter of life and death. The superior colliculus (SC) is an evolutionarily ancient hub essential for survival behaviors like approach and avoidance of threats.1,2 We therefore combined virtual reality and neural recordings to ask whether matching visual stimuli to self-motion alters behavior and neural activity in SC. We first measured locomotion behavior and neural activity while animals approached an object in virtual reality or while the same object loomed at them. In both contexts, vision dominated activity in the superficial layers of SC (SCs), whereas locomotion had more influence on activity in the intermediate layers (SCim). In addition, animals instinctively slowed their locomotion when nearing the object or when the object neared them. To directly test animals’ ability to distinguish self from object motion, we replayed the visual images generated during object approach. Locomotion behavior often changed during replay, showing animals can determine whether visual motion is matched to their self-movement. Further, decoders trained on locomotion behavior or on population activity in SC, particularly in SCim, were able to reliably discriminate self-movement and object movement contexts. We conclude that both mouse behavior and SC activity distinguish the context of visual motion and can thus discriminate motion arising from an animal’s own movement and that of an external agent.