Spontaneous Variations in Arousal Modulate Subsequent Visual Processing and Local Field Potential Dynamics in the Ferret during Quiet Wakefulness

Abstract

Behavioral states affect neuronal responses throughout the cortex and influence visual processing. Quiet wakefulness (QW) is a behavioral state during which subjects are quiescent, but awake and connected to the environment. Here, we examined the effects of pre-stimulus arousal variability on post-stimulus neural activity in primary visual cortex (V1) and posterior parietal cortex (PPc) in awake ferrets, using the pupil diameter as an indicator of arousal. We observed that during low arousal, low- frequency power increases during visual stimulation, and that the peak alpha frequency shifted depending on the arousal state. High arousal increased gamma power as well as low-frequency inter- and intra-areal coherence. Using a simplified model of laminar circuits, we show that this connectivity pattern is compatible with feedback signals targeting infragranular layers in area PPc and supragranular layers in V1. Neurons in V1 displayed higher firing rates at their preferred orientations on high-arousal trials. Broad-spiking cells in V1 entrained to high-frequency oscillations (>80 Hz), whereas narrow-spiking neurons phase-locked to low (12-18 Hz) and high-frequency (>80 Hz) rhythms. These results indicate that the variability and sensitivity of post-stimulus cortical responses and coherence depend on the pre-stimulus behavioral state and account for the neuronal response variability observed during repeated stimulation.