RT Journal Article
SR Electronic
T1 Pupil-associated states modulate excitability but not stimulus selectivity in primary auditory cortex
JF bioRxiv
FD Cold Spring Harbor Laboratory
SP 619619
DO 10.1101/619619
A1 Zachary P. Schwartz
A1 Brad N. Buran
A1 Stephen V. David
YR 2019
UL http://biorxiv.org/content/early/2019/04/26/619619.abstract
AB Recent research in mice 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. However, 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 non-anesthetized male and female ferrets during presentation of vocalizations and tone stimuli that allow measurement of frequency and level tuning. 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 and non-monotonicity associated with changes in pupil size.Significance Statement Cortical neurons vary in their response to repeated stimuli, and some portion of the variability is due to fluctuations in network state. By simultaneously recording pupil and single-neuron activity in primary auditory cortex of ferrets, we provide new evidence that that network state affects the overall excitability of auditory neurons, but sensory selectivity remains stable. During high-arousal states – indicated by dilated pupil – baseline activity, neuronal gain, and reliability increase, and there is a decrease in acoustic threshold. In addition, we report the occurrence of possible rapid eye movement sleep states, adding to evidence that pupil provides an index of both sleep and physiological arousal.