LOCOMOTION MODULATES VISUAL ADAPTATION IN THE MOUSE RETINO-COLLICULAR CIRCUIT

Visual processing adapts not only to sensory input but also to internal and behavioural states. While locomotion is known to modulate the magnitude of visually evoked responses as early as the retina, its impact on the temporal dynamics of neural activity, specifically spike-rate adaptation, remains poorly understood.
We used Neuropixels probes to record retinal ganglion cell axons and neurons across superficial and deep layers of the mouse superior colliculus (SC), a layered midbrain structure integrating visual and motor signals. We presented drifting gratings of 2 s duration, while head-fixed mice were free to run on a wheel.
Neural responses were classified by fitting exponential functions, yielding four response types: depressing, sensitising, biphasic, and non-adapting. From these fits, we quantified adaptation strength (relative change in firing rate) and adaptation speed (exponential time constant, τ). More than 85% of visually responsive retinal axons and SC neurons exhibited adapting responses, most commonly depressing (80%). From stimulus onset to offset, firing rate dropped by 17% in retinal axons, 44% in superficial and 48% in deep SC neurons. Locomotion further increased adaptation strength in all populations, with the largest effect in deep SC (20%). During stationary periods, adaptation slowed progressively along the pathway (from 0.20 s in retinal axons to 0.26 s in deep SC). During locomotion, adaptation speeds converged across populations (0.20 s). These effects could not be explained by variations in mean firing rate.
Together, locomotion modulates spike-rate adaptation from the retina onward and may optimize visual processing during movement.