Anisomorphic cortical reorganization in asymmetric sensorineural hearing loss

Abstract

Acoustic trauma or inner ear disease may predominantly injure one ear, causing asymmetric sensorineural hearing loss (SNHL). While characteristic frequency (CF) map plasticity of primary auditory cortex (AI) contralateral to the injured ear has been detailed, there is no study that also evaluates ipsilateral AI to compare cortical reorganization across both hemispheres. We assess whether the normal isomorphic mirror-image relationship between the two hemispheres is maintained or disrupted in mild-to-moderate asymmetric SNHL of adult squirrel monkeys. At week 24 after induction of acoustic injury to the right ear, functional organization of the two hemispheres differs in direction and magnitude of interaural CF difference, percentage of recording sites with spectrally nonoverlapping binaural activation, and the concurrence of peripheral and central activation thresholds. The emergence of this anisomorphic cortical reorganization of the two hemispheres is replicated by simulation based on spike timing-dependent plasticity, where 1) AI input from the contralateral ear is dominant, 2) reestablishment of relatively shorter contralateral ear input timing drives reorganization, and 3) only AI contralateral to the injured ear undergoes major realignment of interaural frequency maps that evolve over months. Asymmetric SNHL disrupts isomorphic organization between the two hemispheres and results in relative local hemispheric autonomy, potentially impairing performance of tasks that require binaural input alignment or interhemispheric processing.NEW & NOTEWORTHY Mild-to-moderate hearing loss in one ear and essentially normal hearing in the other triggers cortical reorganization that is different in the two hemispheres. Asymmetry of cochlea sensitivities does not simply propagate to the two auditory cortices in mirror-image fashion. The resulting anisomorphic cortical reorganization may be a neurophysiological basis of clinical deficits in asymmetric hearing loss, such as difficulty with hearing in noise, impaired spatial hearing, and accelerated decline of the poorer ear.

Keywords: auditory cortex; frequency map alignment; interaural latency; plasticity; spike timing-dependent plasticity.