In quiet environments, hearing aids improve the perception of low-intensity sounds. However, for high-intensity sounds in background noise, the aids often fail to provide a benefit to the wearer.Here, by using large-scale single-neuron recordings from hearing-impaired gerbils -an established animal model of human hearing -we show that hearing aids restore the sensitivity of neural responses to speech, but not their selectivity. Rather than reflecting a deficit in supra-threshold auditory processing, the low selectivity is a consequence of hearing-aid compression (which decreases the spectral and temporal contrasts of incoming sound) and of amplification (which distorts neural responses, regardless of whether hearing is impaired). Processing strategies that avoid the trade-off between neural sensitivity and selectivity should improve the performance of hearing aids.

Hearing aids are the only available treatment for mild-to-moderate sensorineural hearing loss, but often fail to improve perception in difficult listening conditions. To identify the reasons for this failure, we studied the underlying neural code using large-scale single-neuron recordings in gerbils, a common animal model of human hearing. We found that a hearing aid restored the sensitivity of neural responses, but failed to restore their selectivity. The low selectivity of aided responses was not a direct effect of hearing loss per se, but rather a consequence of the strategies used by hearing aids to restore sensitivity: compression, which decreases the spectral and temporal contrast of incoming sounds, and amplification, which produces high intensities that distort the neural code even with normal hearing. To improve future hearing aids, new processing strategies that avoid this tradeoff between neural sensitivity and selectivity must be developed.

The perceptual salience of a sound depends on the acoustic context in which it appears. Single-neuron correlates of this contextual sensitivity can be estimated from neuronal responses to complex sounds using the nonlinear-linear "context model". Context models provide estimates of both the principal (spectrotemporal) receptive field of a neuron and a "contextual gain field" describing its nonlinear sensitivity to combinations of sound input. Previous studies of contextual gain fields in auditory cortex of anesthetized mice have revealed strong neuron-specific patterns of nonlinear sensitivity to sound context. However, the stability of these patterns over time, especially in awake animals, is unknown. We recorded electrophysiological activity of neurons in the auditory cortex of awake mice over many days using chronically implanted tetrode arrays, while also obtaining continuous measures of the animal's behavioral state (locomotor activity and pupil diameter), during repeated presentations of prolonged complex sounds. Waveform matching identified neurons that were recorded over multiple days. We estimated principal receptive fields and contextual gain fields for each neuron in each recording session, and quantified the stability of these fields within and across days. We also examined the dependence of context model fits on measures of behavioral state. 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, while patterns of contextual sensitivity to sound combinations were qualitatively similar to those previously observed in anesthetized mice, 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 contextual sensitivity is an integral and stable feature of the neural code in the awake auditory cortex, which might be modulated by behavioral state.

In the version of this article initially published, there was an error in Fig. 4b. The light blue upper band, originally labeled "Internal signal, " has been corrected to read "Internal noise. " The changes have been made in the HTML and PDF versions of the article.