Nonlinear sensitivity to acoustic context is a stable feature of neuronal responses to complex sounds in auditory cortex of awake mice

Abstract

The perceptual salience of a sound depends on the acoustic context in which it appears, and can vary on a timescale of milliseconds. At the level of single neurons in the auditory cortex, spectrotemporal tuning for particular sounds is shaped by a similarly fast and systematic nonlinear sensitivity to acoustic context. Does this neuronal context sensitivity “drift” over time in awake animals, or is it a stable feature of sound representation in the auditory cortex? We used chronically implanted tetrode arrays in awake mice to measure the electrophysiological responses of auditory cortical neurons to spectrotemporally complex, rapidly varying sounds across many days. For each neuron in each recording session, we applied the nonlinear-linear “context model” to estimate both a principal (spectrotemporal) receptive field and a “contextual gain field” describing the neuron’s nonlinear sensitivity to acoustic context. We then quantified the stability of these fields within and across days, using spike waveforms to match neurons recorded in multiple sessions. Contextual gain fields of auditory cortical neurons in awake mice were remarkably stable across many days of recording, and comparable in stability to principal receptive fields. Interestingly, there were small but significant effects of changes in locomotion or pupil size on the ability of the context model to fit temporal fluctuations in the neuronal response.We conclude that both spectrotemporal tuning and nonlinear sensitivity to acoustic context are stable features of neuronal sound representation in the awake auditory cortex, which can be modulated by behavioral state.