Persistent impairment of spatial hearing and neural binaural interaction after “temporary” noise-induced hearing loss

Many people have suprathreshold auditory processing difficulties despite normal audiometric thresholds, referred to as “hidden hearing loss.” Such difficulties are widely thought to originate from pathology of the inner hair cell ribbon synapse (cochlear synaptopathy) following noise-exposure-induced temporary threshold shifts. This pathology impairs the temporally-precise sound encoding necessary for spatial hearing, but direct evidence in primates, human or nonhuman, is lacking. Here, we show in macaques of both sexes that noise-exposure-induced temporary threshold shifts produced long-lasting alterations in synaptic morphology without synapse loss, and persistent spatial hearing deficits up to 11 months post-exposure, despite recovery of audiometric thresholds. These deficits were accompanied by a reduction in a neurophysiological measure of binaural processing - the binaural interaction component of the auditory brainstem response. Together, these findings provide evidence, in primates, that noise exposure disrupts spatial hearing and binaural neural circuit function without loss of hair cells or synapses.