Pupil-associated states modulate excitability but not stimulus selectivity in primary auditory cortex

Abstract

Recent research indicates that luminance-independent fluctuations in pupil size predict variability in spontaneous and evoked activity of single neurons in auditory and visual cortex. These findings suggest that pupil is an indicator of large-scale changes in arousal state that affect sensory processing. It is not known whether pupil-related state also influences the selectivity of auditory neurons. We recorded pupil size and single-unit spiking activity in the primary auditory cortex (A1) of ferrets during presentation of vocalizations and tone stimuli. Neurons showed a systematic increase in both spontaneous and sound-evoked activity when pupil was large, as well as a decrease in trial-to-trial variability. Relationships between pupil size and firing rate were non-monotonic in some cells. In most neurons, several measurements of tuning, including acoustic threshold, spectral bandwidth, and best frequency, remained stable across large changes in pupil size. Across the population, however, there was a small but significant decrease in acoustic threshold when pupil was dilated. In some recordings, we observed rapid, saccade-like eye movements during sustained pupil constriction, which may indicate episodes of rapid eye movement sleep. Including the presence of this state as a separate variable in a regression model of neural variability accounted for some, but not all, of the variability associated with changes in pupil size.Recent research indicates that luminance-independent fluctuations in pupil size predict variability in spontaneous and evoked activity of single neurons in auditory and visual cortex. These findings suggest that pupil is an indicator of large-scale changes in arousal state that affect sensory processing. It is not known whether pupil-related state also influences the selectivity of auditory neurons. We recorded pupil size and single-unit spiking activity in the primary auditory cortex (A1) of ferrets during presentation of vocalizations and tone stimuli. Neurons showed a systematic increase in both spontaneous and sound-evoked activity when pupil was large, as well as a decrease in trial-to-trial variability. Relationships between pupil size and firing rate were non-monotonic in some cells. In most neurons, several measurements of tuning, including acoustic threshold, spectral bandwidth, and best frequency, remained stable across large changes in pupil size. Across the population, however, there was a sma...