Distinct brain states modulate visual cortical processing in mouse

Variations in brain states and behavioral profiles clearly influence neuronal activity in the visual cortex[1,2]. However, the mechanisms behind these influences and their consequent effect on sensory encoding remain to be determined. Here, we address this issue by analyzing simultaneous recordings of spiking activity and local field potentials (LFPs) from visual and subcortical regions of (N = 25) awake mice viewing a naturalistic movie. Applying a hidden Markov model (HMM) to cortical LFPs, we consistently identified three stable states in each mouse: a high-frequency state (dominated by gamma oscillations), a low-frequency state (dominated by beta and theta oscillations), and an intermediate state. These brain states strongly reflected behavioral states and mouse arousal levels, where the high-frequency state was associated with the most pronounced movements and largest pupil sizes. To quantify the contribution of state modulations to neuronal activity, we designed an HMM-regression model where the inclusion of LFPs and state dependency improved the explained variance of population activity by ~14%. In individual neurons, we observed the highest shared variance during low arousal states, whereas higher arousal states induced more irregular firing. Consequently, population spiking demonstrated the highest mutual information (MI) with visual stimuli during high-arousal states, with MI gradually decreasing along the visual hierarchy.

To investigate whether all areas are modulated equally by brain states, we evaluated state transition-triggered population responses in the visual cortical areas, lateral geniculate nucleus (LGN), and hippocampal regions. Across all areas, transitions towards a higher arousal state increased population activity and vice versa. Interestingly, the earliest changes in these neuronal responses preceded the state transitions and reflected a direction of state-dependent influences from the hippocampus, propagating down the visual hierarchy and towards LGN. Overall, we observed a top-down wave of state modulations of the visual cortices, which differentially affected visual processing based on arousal levels.