Cortical and subcortical neurons discriminate sounds in noise on the sole basis of acoustic amplitude modulations

Humans and animals maintain accurate sound discrimination in the presence of loud sources of background noise. It is commonly assumed that this ability relies on the robustness of auditory cortex responses. However, no attempt has been made to characterize neural discrimination of sounds masked by noise at each stage of the auditory system and disentangle the sub-effects of noise, namely the distortion of temporal cues conveyed by modulations in instantaneous amplitude and frequency, and the introduction of randomness (stochastic fluctuations in amplitude). Here, we measured neural discrimination between communication sounds masked by steady noise in the cochlear nucleus, inferior colliculus, auditory thalamus, primary and secondary auditory cortex at several signal-to-noise ratios. Sound discrimination by neuronal populations markedly decreased in each auditory structure, but collicular and thalamic populations showed better performance than cortical populations at each signal-to-noise ratio. Comparison with neural responses to tone-vocoded sounds revealed that the reduction in neural discrimination caused by noise was mainly driven by the attenuation of slow amplitude modulation cues, with the exception of the cochlear nucleus that showed a dramatic drop in discrimination caused by the randomness of noise. These results shed new light on the specific contributions of subcortical structures to robust sound encoding, and demonstrate that neural discrimination in the presence of background noise is mainly determined by the distortion of the slow temporal cues conveyed by communication sounds.