Internally Noisy Cortical Processing Underlies Failures to Perceive Sounds in External Noise

SUMMARYCorrelational evidence in humans suggests that specific difficulties hearing in noisy, social settings may reflect premature auditory nerve degeneration. Here, we partially eliminated cochlear afferent neurons in mice and found direct behavioral evidence for selective detection deficits in background noise. To identify central determinants for this perceptual disorder, we tracked daily changes in ensembles of auditory cortex parvalbumin-expressing inhibitory neurons and surrounding pyramidal neurons with chronic two-photon calcium imaging. Primary auditory neuropathy (PAN) tipped the cortical excitatory-inhibitory balance towards net hyperactivity, elevated correlated activity, and disrupted adaptation to background noise. In control conditions, layer 2/3 ensemble encoding of the target sound could accurately classify hit or miss trials in background noise. After PAN, miss trials in background noise were instead predicted from random surges of synchronized activity occurring prior to target onset. These data reveal sources of internal cortical noise underlying failures to perceive sounds in external noise.