Genetic and functional diversity of primary auditory afferents

Petitpré, Charles; Bourien, Jérôme; Wu, Haohao; Diuba, Artem V.; Puel, Jean‐Luc; Lallemend, François

doi:10.1016/j.cophys.2020.09.011

Cited by 14 publications

(12 citation statements)

References 78 publications

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“…The recent demonstration of diverse molecular types of SGNs has provided a solid basis for the distinct anatomical and physiological properties of auditory afferents 1 – 3 , 76 , yet how these neuronal identities are generated has remained unexplored. Using scRNAseq-based analysis of developing sensorineural cells of the cochlea, we demonstrate a continuous representation of changes in gene expression that define the course of SGN diversification.…”

Section: Discussionmentioning

confidence: 99%

Single-cell RNA-sequencing analysis of the developing mouse inner ear identifies molecular logic of auditory neuron diversification

et al. 2022

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Different types of spiral ganglion neurons (SGNs) are essential for auditory perception by transmitting complex auditory information from hair cells (HCs) to the brain. Here, we use deep, single cell transcriptomics to study the molecular mechanisms that govern their identity and organization in mice. We identify a core set of temporally patterned genes and gene regulatory networks that may contribute to the diversification of SGNs through sequential binary decisions and demonstrate a role for NEUROD1 in driving specification of a Ic-SGN phenotype. We also find that each trajectory of the decision tree is defined by initial co-expression of alternative subtype molecular controls followed by gradual shifts toward cell fate resolution. Finally, analysis of both developing SGN and HC types reveals cell-cell signaling potentially playing a role in the differentiation of SGNs. Our results indicate that SGN identities are drafted prior to birth and reveal molecular principles that shape their differentiation and will facilitate studies of their development, physiology, and dysfunction.

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Section: Discussionmentioning

confidence: 99%

Single-cell RNA-sequencing analysis of the developing mouse inner ear identifies molecular logic of auditory neuron diversification

et al. 2022

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“…The possible mechanisms include but are not limited to: i) partial depletion of the "standing" RRP (i.e. the occupancy of the RRP release sites with a fusion-competent SV (Moser, 2020;Pangrsic et al, 2010)) at high SR synapses; ii) differences in SGN excitability (Crozier & Davis, 2014;Markowitz & Kalluri, 2020;Smith et al, 2015) due to heterogenous molecular (Petitpré et al, 2018(Petitpré et al, , 2020Shrestha et al, 2018;Sun et al, 2018) and morphological profiles (M. C. Liberman, 1980;Merchan-Perez & Liberman, 1996;Tsuji & Liberman, 1997); and iii) differences in efferent innervation of SGNs (Hua et al, 2021;M. C. Liberman, 1990;Ruel et al, 2001;Wu et al, 2020;Yin et al, 2014).…”

Section: Challenges For Relating Synaptic and Neural Response Propertiesmentioning

confidence: 99%

“…SGNs with low SR have a higher sound thresholds, shallower spike rate rise and saturate at higher sound intensities (Ohlemiller et al, 1991; Winter et al, 1990). Additionally, SGNs show differences in their excitability (Crozier & Davis, 2014; Markowitz & Kalluri, 2020; Smith et al, 2015), morphological features (M. C. Liberman, 1980; Merchan-Perez & Liberman, 1996; Tsuji & Liberman, 1997) and heterogeneous molecular profiles (C. Li et al, 2020; Petitpré et al, 2018, 2020; Shrestha et al, 2018; Sun et al, 2018). Yet, it has remained challenging to demonstrate a causal link of a candidate mechanism to the physiological SGN diversity.…”

Section: Introductionmentioning

confidence: 99%

Bridging the gap between presynaptic hair cell function and neural sound encoding

Tobón

Moser

2022

Preprint

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Neural diversity can expand the encoding capacity of a circuitry. A striking example of diverse structure and function is presented by the afferent synapses between inner hair cells (IHCs) and spiral ganglion neurons (SGNs) in the cochlea. Synapses at the pillar IHC-side activate at lower voltages than those of the modiolar side, which show larger active zones and Ca2+-channel clusters. At the postsynapse, SGNs differ in their spontaneous firing rates, sound thresholds and operating ranges. While it is tempting to speculate about a causal relationship between synaptic heterogeneity and neural response diversity, direct experimental evidence is lacking. Here, we bridged this gap by ex-vivo paired recordings of IHCs and postsynaptic boutons with stimuli and conditions aimed to mimic those of in-vivo SGN-characterization. Synapses with high spontaneous rate (SR) were found predominantly on the pillar side of the IHC. These high SR synapses had larger spontaneous EPSCs, lower voltage-thresholds, shorter response latencies and higher initial release rates. This study indicates that synaptic heterogeneity in IHCs can account for functional response diversity of spontaneous and sound-evoked SGN.

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“…Compared to other sensory pathways, such as the sensory neurons involved pain or touch [ 35 , 36 ] or the auditory system [ 147 ], our understanding of the genetic subclasses of the proprioceptive and vestibular pathways is relatively limited. However, important progress is being made in these pathways.…”

Section: Future Perspective In the Age Of Molecular Sciencesmentioning

confidence: 99%

Relative Contribution of Proprioceptive and Vestibular Sensory Systems to Locomotion: Opportunities for Discovery in the Age of Molecular Science

Akay

Murray

2021

IJMS

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Locomotion is a fundamental animal behavior required for survival and has been the subject of neuroscience research for centuries. In terrestrial mammals, the rhythmic and coordinated leg movements during locomotion are controlled by a combination of interconnected neurons in the spinal cord, referred as to the central pattern generator, and sensory feedback from the segmental somatosensory system and supraspinal centers such as the vestibular system. How segmental somatosensory and the vestibular systems work in parallel to enable terrestrial mammals to locomote in a natural environment is still relatively obscure. In this review, we first briefly describe what is known about how the two sensory systems control locomotion and use this information to formulate a hypothesis that the weight of the role of segmental feedback is less important at slower speeds but increases at higher speeds, whereas the weight of the role of vestibular system has the opposite relation. The new avenues presented by the latest developments in molecular sciences using the mouse as the model system allow the direct testing of the hypothesis.

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Genetic and functional diversity of primary auditory afferents

Cited by 14 publications

References 78 publications

Single-cell RNA-sequencing analysis of the developing mouse inner ear identifies molecular logic of auditory neuron diversification

Single-cell RNA-sequencing analysis of the developing mouse inner ear identifies molecular logic of auditory neuron diversification

Bridging the gap between presynaptic hair cell function and neural sound encoding

Relative Contribution of Proprioceptive and Vestibular Sensory Systems to Locomotion: Opportunities for Discovery in the Age of Molecular Science

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