Abstract

BackgroundThe auditory efferent system has unique neuroanatomical pathways that connect the cerebral cortex with sensory receptor cells. Pyramidal neurons located in layers V and VI of the primary auditory cortex constitute descending projections to the thalamus, inferior colliculus, and even directly to the superior olivary complex and to the cochlear nucleus. Efferent pathways are connected to the cochlear receptor by the olivocochlear system, which innervates outer hair cells and auditory nerve fibers. The functional role of the cortico-olivocochlear efferent system remains debated. We hypothesized that auditory cortex basal activity modulates cochlear and auditory-nerve afferent responses through the efferent system.Methodology/Principal FindingsCochlear microphonics (CM), auditory-nerve compound action potentials (CAP) and auditory cortex evoked potentials (ACEP) were recorded in twenty anesthetized chinchillas, before, during and after auditory cortex deactivation by two methods: lidocaine microinjections or cortical cooling with cryoloops. Auditory cortex deactivation induced a transient reduction in ACEP amplitudes in fifteen animals (deactivation experiments) and a permanent reduction in five chinchillas (lesion experiments). We found significant changes in the amplitude of CM in both types of experiments, being the most common effect a CM decrease found in fifteen animals. Concomitantly to CM amplitude changes, we found CAP increases in seven chinchillas and CAP reductions in thirteen animals. Although ACEP amplitudes were completely recovered after ninety minutes in deactivation experiments, only partial recovery was observed in the magnitudes of cochlear responses.Conclusions/SignificanceThese results show that blocking ongoing auditory cortex activity modulates CM and CAP responses, demonstrating that cortico-olivocochlear circuits regulate auditory nerve and cochlear responses through a basal efferent tone. The diversity of the obtained effects suggests that there are at least two functional pathways from the auditory cortex to the cochlea.

Highlights

  • Sensory systems are usually thought as biological receptors that transduce external energy into bioelectrical signals, which are conducted through ascending pathways from sensory epithelia to the brain

  • Conclusions/Significance: These results show that blocking ongoing auditory cortex activity modulates Cochlear microphonics (CM) and compound action potentials (CAP) responses, demonstrating that cortico-olivocochlear circuits regulate auditory nerve and cochlear responses through a basal efferent tone

  • The majority of MOC fibers cross to the contralateral cochlea and contact outer hair cells (OHC) by cholinergic synapses mediated via exclusive nicotinic receptors constituted of alpha-9/alpha-10 subunits [9,10]

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Summary

Introduction

Sensory systems are usually thought as biological receptors that transduce external energy into bioelectrical signals, which are conducted through ascending pathways from sensory epithelia to the brain. The corticofugal descending auditory system is a complex neuronal network that comprises the primary auditory cortex, thalamus, inferior colliculus (IC), cochlear nucleus (CN), superior olivary complex, and reaches cochlear receptor cells by olivocochlear fibers [5,6,7]. According to their anatomic origin, olivocochlear neurons are classified into the medial (MOC) and lateral (LOC) olivocochlear systems [8]. We hypothesized that auditory cortex basal activity modulates cochlear and auditory-nerve afferent responses through the efferent system

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