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Molecular Aspects of the Development and Function of Auditory Neurons

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Molecular Aspects of the Development and Function of Auditory Neurons International Journal of Molecular Sciences Review Molecular Aspects of the Development and Function of Auditory Neurons Gabriela Pavlinkova BIOCEV, Institute of Biotechnology of the Czech Academy of Sciences, 25250 Vestec, Czech Republic; [email protected] Abstract: This review provides an up-to-date source of information on the primary auditory neurons or spiral ganglion neurons in the cochlea. These neurons transmit auditory information in the form of electric signals from sensory hair cells to the first auditory nuclei of the brain stem, the cochlear nuclei. Congenital and acquired neurosensory hearing loss affects millions of people worldwide. An increasing body of evidence suggest that the primary auditory neurons degenerate due to noise exposure and aging more readily than sensory cells, and thus, auditory neurons are a primary target for regenerative therapy. A better understanding of the development and function of these neurons is the ultimate goal for long-term maintenance, regeneration, and stem cell replacement therapy. In this review, we provide an overview of the key molecular factors responsible for the function and neurogenesis of the primary auditory neurons, as well as a brief introduction to stem cell research focused on the replacement and generation of auditory neurons. Keywords: cochlea; single-cell RNAseq; transcription factor; auditory pathways; genetic mutations 1. Introduction According to the World Health Organization, hearing impairment, the partial or total inability to hear sounds, is among the top 10 disabilities of today’s society and affects approximately 6% of the world’s population. Neurosensory hearing loss is permanent and Citation: Pavlinkova, G. Molecular results from the death of neurons or sensory cells that have no ability to regenerate. Audi- Aspects of the Development and tory neurons are a critical component of the auditory pathway, as they transmit auditory Function of Auditory Neurons. Int. J. information from sensory hair cells to the cochlear nucleus in the brainstem. The current Mol. Sci. 2021, 22, 131. https://dx. effective therapies for hearing impairment utilize either hearing aids to increase hair cell doi.org/10.3390/ijms22010131 stimulation or cochlear implants as a substitute for hair cells. These medical devices require the presence of functional auditory neurons in the inner ear. Therefore, recent studies focus Received: 23 November 2020 on possibilities for neuronal replacement, including exogenous stem cell transplantation Accepted: 22 December 2020 and endogenous cell source replacement. Transcriptional networks are key in controlling Published: 24 December 2020 the regeneration or replacement of auditory neurons from stem cells. Understanding and identifying individual transcription factors involved in the development and survival of Publisher’s Note: MDPI stays neu- auditory neurons are crucial for future more effective treatments for hearing loss [1]. This tral with regard to jurisdictional claims in published maps and institutional review focuses on the latest advances in the research on auditory neurons and new per- affiliations. spectives on future directions of this research, particularly on molecular factors important for the development and maintenance of auditory neurons. 2. Functional Diversity of Auditory Neurons Copyright: © 2020 by the author. Li- Two distinguishable systems of neurons exist within the mammalian inner ear, known censee MDPI, Basel, Switzerland. This as the descending neuronal pathway and ascending neuronal pathway. article is an open access article distributed The pathway descending from the cortex is called the efferent system or the olivo- under the terms and conditions of the cochlear system [2]. While being unique to the auditory region, it consists of efferent Creative Commons Attribution (CC BY) neurons subdivided into medial olivocochlear efferents and lateral olivocochlear efferents. license (https://creativecommons.org/ The efferents are derived from facial branchial motor neurons. The groups differ in the licenses/by/4.0/). Int. J. Mol. Sci. 2021, 22, 131. https://dx.doi.org/10.3390/ijms22010131 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 2 of 13 The pathway descending from the cortex is called the efferent system or the olivo- Int. J. Mol. Sci. 2021, 22, 131 cochlear system [2]. While being unique to the auditory region, it consists of efferent 2neu- of 13 rons subdivided into medial olivocochlear efferents and lateral olivocochlear efferents. The efferents are derived from facial branchial motor neurons. The groups differ in the neuronneuron bodies’ bodies’ location locationss and and degree degree of of myelination. myelination. Thicker Thicker myelinated myelinated medial medial efferents efferents formform synapses synapses with with outer outer hair hair cells cells of of the the organ organ of of Corti Corti in in the the cochlea cochlea (Figure (Figure 1A).1A). Thin Thin,, unmyelinatedunmyelinated lateral lateral efferents efferents innervate innervate the the dendrites dendrites of of nerve nerve fibers fibers connecting connecting inner inner hairhair cells cells [2] [2.]. The The pathway pathway uses uses acetylcholine acetylcholine as asthe the major major neurotransmitter neurotransmitter [3,4] [3., 4The]. The ef- ferentefferent system system is isinvolved involved in in the the improvement improvement of of signal signal detection, detection, the the functioning functioning of of the the outerouter hair hair cells, cells, and and protection protection of of the the cochlea cochlea from from acoustic acoustic damage. damage. The The difference difference in the in olivocochlearthe olivocochlear system system efficiency efficiency is an is anessential essential factor factor of of the the vulnerability vulnerability to to permanent permanent acousticacoustic in injuryjury [5] [5].. Figure 1. Auditory neuronsFigure form the1. Auditory spiral ganglion neurons in form the cochlea the spiral and ganglion connect hairin the cells cochlea in the and organ connect of Corti hair to cells cochlear in the nuclei in the brain stem. (Aorgan) Diagram of Corti shows to cochlear innervation nuclei of thein the organ brain of stem. Corti. ( TypeA) Diagram I neurons shows extend innervation radial fibers of the toward organ of Corti. Type I neurons extend radial fibers toward the inner hair cells (5–30 type I neurons inner- the inner hair cells (5–30 type I neurons innervate one inner hair cell), and type II neurons provide diffuse innervations to the vate one inner hair cell), and type II neurons provide diffuse innervations to the outer hair cells outer hair cells and supporting cells within the cochlea. Efferent axons from superior olivary complex innervate the outer and supporting cells within the cochlea. Efferent axons from superior olivary complex innervate hair cells. (B) Whole-mountthe immunolabeling outer hair cells. of(B the) Whole mouse-mount cochlea immunolabeling shows outer hair of the cells mouse (OHC, cochlea labeled shows by anti-prestin) outer hair cells and inner hair cells (IHC, labeled(OHC, by labeled anti-calretinin) by anti-prestin) forming and the inner organ hair of Corticells (IHC, (OC). labeled (C) Whole-mount by anti-calretinin) immunostaining forming the of the spiral ganglion (SG) neuronsorgan (anti-NeuN,of Corti (OC). a neuronal(C) Whol somae-mount marker) immunostaining shows the dendrites of the spiral extending ganglion in the(SG) periphery neurons (anti to - the organ of Corti (OC) andNeuN, the axons a neuronal traveling soma to the marker) central shows nervous the system dendrites (anti-acetylated extending in alpha-tubulin-labeledthe periphery to the organ nerve of fibers). Scale bars, 50 µm. ConfocalCorti (OC) images and (theB) takenaxons from traveling [6] and to (theC) unpublishedcentral nervous data. system (D) Schematic (anti-acetylated drawing alpha of synapses-tubulin- of molecular subtypes of typelabeled I neurons nerve fibers). on the innerScale hairbars, cell.50 μ Typem. Confocal I neurons images are segregated (B) taken from into [6] three and distinct (C) unpublished groups: types Ia (blue), Ib (magenta),data. and ( IcD) (green-blue) Schematic drawing of the spiral of synapses auditory of neurons, molecular which subtypes extend of peripheral type I neurons processes on the that inner are hair cell. Type I neurons are segregated into three distinct groups: types Ia (blue), Ib (magenta), and Ic spatially segregated on the surface of the IHC. HS: Hoechst nuclear staining. Neurons forming the ascending neuronal pathway innervate the sensory epithelia of the organ of Corti in the cochlea and transmit auditory information in the form of electrical signals to the brain (Figure1A). The somata of auditory neurons form the spiral ganglion Int. J. Mol. Sci. 2021, 22, 131 3 of 13 that twists within a coiled cochlear duct. Peripheral neuronal processes innervating hair cells of the organ of Corti are referred to as the dendrites, whereas the central processes are the axons (Figure1B,C). Most of them are myelinated, which is considered to be a charac- teristic of the axons. The axons of the afferent neurons merge into the vestibulocochlear nerve, also known as the VIII cranial nerve, relaying acoustic information further to the central nervous system. Two types of auditory neurons have been described in the cochlea (Figure1A; [ 7]). Large, myelinated, bipolar type I neurons connect the inner hair cells in the organ of Corti to the cochlear nuclei
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