Acute and long-term circuit-level effects in the auditory cortex after sound trauma

Abstract

Harmful environmental sounds are a prevailing source for chronic hearing impairments, including noise induced hearing loss, hyperacusis, or tinnitus. How these symptoms are related to pathophysiological damage to the sensory receptor epithelia and its effects along the auditory pathway, such as functional reorganizations in the auditory cortex (ACx), have been documented in numerous studies. An open question concerns the temporal evolution of maladaptive changes after damage and their manifestation in the balance between afferent thalamocortical input and corticocortical input to the ACx. To address this, we investigated the loci of plastic reorganizations across the tonotopic axis of the auditory cortex of male Mongolian gerbils (Meriones unguiculatus) acutely after a sound trauma and after several weeks. We used a laminar residual current-source density analysis to dissociate adaptations of intracolumnar input and horizontally relayed corticocortical input to synaptic populations across cortical layers in ACx. A pure tone-based sound trauma caused acute changes of subcortical inputs and corticocortical inputs at all tonotopic regions, particularly showing a broad elimination of tone-evoked inputs at tonotopic regions with a pre-trauma best frequency between 2-8 kHz. At other cortical sites, the overall columnar activity acutely decreased, while relative contributions of lateral corticocortical inputs increased. After 4-6 weeks, cortical activity to the altered sensory inputs showed a general increase of local thalamocortical input reaching levels higher than before the trauma. Hence, our results suggest a detailed mechanism for overcompensation of altered frequency input in the auditory cortex that relies on a changing balancing of thalamocortical and intracortical input and is confined to the spectral neighborhood of the trauma frequency. Significance statementHarmful noise exposure is a major anthropogenic cause of hearing disorders and is becoming an ever-increasing burden for human health and society. Damage to the sensory epithelia elicited by harmful sounds can subsequently lead to chronic hearing loss, hyperacusis or tinnitus. We still lack an understanding of the pathophysiological plastic processes and their evolution, particularly at the circuit level of the auditory cortex (ACx), which is fundamentally involved in auditory perception. We demonstrate that plastic changes in ACx after noise induced hearing loss (NIHL) occur over several weeks, and that changes in intracortical functional connectivity compensate the acute effects in the deafferentiated subcortical inputs. Such long-term changes may underlie the temporal evolution of hearing impairments or phantom sounds after NIHL.