Abstract
The cochlear inner hair cells synapse onto type I afferent terminal dendrites, constituting the main afferent pathway for auditory information flow. This pathway receives central control input from the lateral olivocochlear efferent neurons that release various neurotransmitters, among which dopamine (DA) plays a salient role. DA receptors activation exert a protective role in the over activation of the afferent glutamatergic synapses, which occurs when an animal is exposed to intense sound stimuli or during hypoxic events. However, the mechanism of action of DA at the cellular level is still not completely understood. In this work, we studied the actions of DA and its receptor agonists and antagonists on the voltage-gated sodium current (INa) in isolated cochlear afferent neurons of the rat to define the mechanisms of dopaminergic control of the afferent input in the cochlear pathway. Experiments were performed using the voltage and current clamp techniques in the whole-cell configuration in primary cultures of cochlear spiral ganglion neurons (SGNs). Recordings of the INa showed that DA receptor activation induced a significant inhibition of the peak current amplitude, leading to a significant decrease in cell excitability. Inhibition of the INa was produced by a phosphorylation of the sodium channels as shown by the use of phosphatase inhibitor that produced an inhibition analogous to that caused by DA receptor activation. Use of specific agonists and antagonists showed that inhibitory action of DA was mediated both by activation of D1- and D2-like DA receptors. The action of the D1- and D2-like receptors was shown to be mediated by a Gαs/AC/cAMP/PKA and Gαq/PLC/PKC pathways respectively. These results showed that DA receptor activation constitutes a significant modulatory input to SGNs, effectively modulating their excitability and information flow in the auditory pathway.
Highlights
The organ of Corti consists of several cells types that perform auditory functions harmoniously
The inner hair cells (IHC) receive afferent innervation from type I spiral ganglion neurons (SGNs), which comprise approximately 95% of the cochlear afferents [1], while the outer hair cells (OHC) receive afferent innervation through the type II SGNs, which correspond to approximately 5% of the cochlear afferents
The efferent neurons originating from the lateral superior olivary complex (LOC) make synaptic contacts with the afferent neurons innervating the IHC [2]
Summary
The organ of Corti consists of several cells types that perform auditory functions harmoniously. The efferent neurons originating from the lateral superior olivary complex (LOC) make synaptic contacts with the afferent neurons innervating the IHC [2] These neurons have been found to release various neurotransmitters including acetylcholine, dynorphin [3], encephalin [4], calcitonin gene-related peptide (CGRP) [5], GABA [6], adenylate cyclase-activating polypeptide [7], and dopamine (DA) [8]. Another group of efferent neurons originates from the medial superior olivary complex (MOC) and synapse directly onto the OHC [9]. A particular case consists of a group of neurons originating from the periolivary nucleus, which form part of the efferent system innervating both the OHC and IHC that release serotonin as a neurotransmitter [11]
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