Spiking activity in the visual thalamus is coupled to pupil dynamics across temporal scales

Abstract

The processing of sensory information, even at early processing stages, is influenced by the internal state of the animal. Internal states, such as arousal, are often characterized by relating neural activity to a single "level" of arousal, defined by a behavioral indicator such as pupil size. In this study, we expand the understanding of arousal-related modulations in sensory systems by uncovering multiple timescales of pupil dynamics and their relationship to neural activity. Specifically, we observed coupling between spiking activity in the mouse dorsal lateral geniculate nucleus (dLGN) of the thalamus and pupil dynamics across timescales spanning three orders of magnitude, from seconds to minutes. Throughout all of these timescales, two distinct spiking patterns - tonic spikes and bursts - preferred opposing phases of pupil dynamics. This multi-scale coupling captures modulations distinct from those captured by pupil size per se, transitions between locomotion and quiescence, or saccadic eye movements. Furthermore, coupling persisted even during viewing of a naturalistic movie, where it contributed to differences in how visual information was encoded. We conclude that dLGN spiking activity is influenced by arousal processes associated with pupil dynamics occurring simultaneously across a broad range of timescales, with implications for the transfer of sensory information to the cortex.