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For this purpose, IHCs utilize highly specialized sensory synapses. During development, these so-called \u2018ribbon\u2019 synapses and their postsynaptic counterparts undergo extensive structural and functional refinement\u2014a process driven by pre-sensory spontaneous activity. The underlying molecular mechanisms remain incompletely understood to date. Interestingly, little is known about the involvement of retrograde feedback provided by postsynaptic SGN terminals to transsynaptically instruct ribbon morphology and presynaptic active zone organization. This review therefore aims to shed light on this phenomenon and assess a potential role of retrograde signaling during IHC ribbon synapse maturation. We first summarize the main mechanisms established for conventional CNS synapses before discussing the current evidence regarding these pathways at IHC-SGN synapses. In particular, we focus on the gasotransmitter nitric oxide, lipid-derived endocannabinoid signaling, and cell adhesion molecules as the most promising candidate pathways. In summary, we propose that differential retrograde signaling may contribute to IHC synaptogenesis, SGN subtype diversification as well as the pruning of afferent contacts during development and might even play an extended functional role in auditory ribbon synapse regulation after hearing onset.<\/jats:p>","DOI":"10.3390\/cells15191779","type":"journal-article","created":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T16:33:12Z","timestamp":1790699592000},"page":"1779","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Listening in Reverse: A Case for Retrograde Signaling During Auditory Inner Hair Cell Ribbon Synapse Maturation"],"prefix":"10.3390","volume":"15","author":[{"given":"Roos A.","family":"Voorn","sequence":"first","affiliation":[{"name":"Auditory Neuroscience Group, Institute of Physiology, Medical University Innsbruck, 6020 Innsbruck, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0001-4754-182X","authenticated-orcid":false,"given":"Louisa S.","family":"Kuenkel","sequence":"additional","affiliation":[{"name":"Auditory Neuroscience Group, Institute of Physiology, Medical University Innsbruck, 6020 Innsbruck, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-7837-1714","authenticated-orcid":false,"given":"Jan F.","family":"Ahrend","sequence":"additional","affiliation":[{"name":"Auditory Neuroscience Group, Institute of Physiology, Medical University Innsbruck, 6020 Innsbruck, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christian","family":"Vogl","sequence":"additional","affiliation":[{"name":"Auditory Neuroscience Group, Institute of Physiology, Medical University Innsbruck, 6020 Innsbruck, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,9,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"e22087","DOI":"10.1002\/syn.22087","article-title":"Current Concepts in Cochlear Ribbon Synapse Formation","volume":"73","author":"Coate","year":"2019","journal-title":"Synapse"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Voorn, R.A., and Vogl, C. (2020). Molecular Assembly and Structural Plasticity of Sensory Ribbon Synapses\u2014A Presynaptic Perspective. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21228758"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1016\/S0896-6273(00)00159-8","article-title":"RIBEYE, a Component of Synaptic Ribbons: A Protein\u2019s Journey through Evolution Provides Insight into Synaptic Ribbon Function","volume":"28","author":"Schmitz","year":"2000","journal-title":"Neuron"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1229","DOI":"10.1016\/j.cell.2018.07.007","article-title":"Sensory Neuron Diversity in the Inner Ear Is Shaped by Activity","volume":"174","author":"Shrestha","year":"2018","journal-title":"Cell"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1247","DOI":"10.1016\/j.cell.2018.07.008","article-title":"Hair Cell Mechanotransduction Regulates Spontaneous Activity and Spiral Ganglion Subtype Specification in the Auditory System","volume":"174","author":"Sun","year":"2018","journal-title":"Cell"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1239","DOI":"10.1126\/science.7079757","article-title":"Single-Neuron Labeling in the Cat Auditory Nerve","volume":"216","author":"Liberman","year":"1982","journal-title":"Science"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1523\/JNEUROSCI.3389-10.2011","article-title":"Opposing Gradients of Ribbon Size and AMPA Receptor Expression Underlie Sensitivity Differences among Cochlear-Nerve\/Hair-Cell Synapses","volume":"31","author":"Liberman","year":"2011","journal-title":"J. Neurosci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1016\/j.devcel.2023.01.008","article-title":"Runx1 Controls Auditory Sensory Neuron Diversity in Mice","volume":"58","author":"Shrestha","year":"2023","journal-title":"Dev. Cell"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"5284","DOI":"10.1523\/JNEUROSCI.2728-18.2019","article-title":"Pou4f1 Defines a Subgroup of Type I Spiral Ganglion Neurons and Is Necessary for Normal Inner Hair Cell Presynaptic Ca2+ Signaling","volume":"39","author":"Sherrill","year":"2019","journal-title":"J. Neurosci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e50491","DOI":"10.7554\/eLife.50491","article-title":"Comprehensive Transcriptome Analysis of Cochlear Spiral Ganglion Neurons at Multiple Ages","volume":"9","author":"Li","year":"2020","journal-title":"eLife"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"2366","DOI":"10.1126\/science.288.5475.2366","article-title":"Cholinergic Synaptic Inhibition of Inner Hair Cells in the Neonatal Mammalian Cochlea","volume":"288","author":"Glowatzki","year":"2000","journal-title":"Science"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"7814","DOI":"10.1523\/JNEUROSCI.2102-04.2004","article-title":"Developmental Regulation of Nicotinic Synapses on Cochlear Inner Hair Cells","volume":"24","author":"Katz","year":"2004","journal-title":"J. Neurosci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e1653242025","DOI":"10.1523\/JNEUROSCI.1653-24.2025","article-title":"Co-Release of GABA and ACh from Medial Olivocochlear Neurons as a Fine Regulatory Mechanism of Cochlear Efferent Inhibition","volume":"45","author":"Castagnola","year":"2025","journal-title":"J. Neurosci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"981","DOI":"10.1111\/j.1460-9568.1992.tb00124.x","article-title":"Triple Immunofluorescence Evidence for the Coexistence of Acetylcholine, Enkephalins and Calcitonin Gene-Related Peptide Within Efferent (Olivocochlear) Neurons of Rats and Guinea-Pigs","volume":"4","author":"Safieddine","year":"1992","journal-title":"Eur. J. Neurosci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1523\/JNEUROSCI.4720-11.2012","article-title":"Dopaminergic Signaling in the Cochlea: Receptor Expression Patterns and Deletion Phenotypes","volume":"32","author":"Maison","year":"2012","journal-title":"J. Neurosci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"e83855","DOI":"10.7554\/eLife.83855","article-title":"Experience-Dependent Flexibility in a Molecularly Diverse Central-to-Peripheral Auditory Feedback System","volume":"12","author":"Frank","year":"2023","journal-title":"eLife"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1007\/s00441-015-2158-z","article-title":"Cochlear Efferents in Developing Adult and Pathological Conditions","volume":"361","author":"Nouvian","year":"2015","journal-title":"Cell Tissue Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"e324","DOI":"10.1002\/wdev.324","article-title":"Talking Back: Development of the Olivocochlear Efferent System","volume":"7","author":"Frank","year":"2018","journal-title":"Wiley Interdiscip. Rev. Dev. Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"108278","DOI":"10.1016\/j.heares.2021.108278","article-title":"Diverse Identities and Sites of Action of Cochlear Neurotransmitters","volume":"419","author":"Kitcher","year":"2022","journal-title":"Hear. Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"11009","DOI":"10.1073\/pnas.191351698","article-title":"Retrograde Signaling at Central Synapses","volume":"98","author":"Tao","year":"2001","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1038\/nrn1727","article-title":"Functions and Mechanisms of Retrograde Neurotrophin Signalling","volume":"6","author":"Zweifel","year":"2005","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"2783","DOI":"10.1111\/j.1460-9568.2008.06285.x","article-title":"Concepts of Neural Nitric Oxide-Mediated Transmission","volume":"27","author":"Garthwaite","year":"2008","journal-title":"Eur. J. Neurosci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1016\/j.neuron.2009.06.021","article-title":"Activity-Dependent Regulation of Synapses by Retrograde Messengers","volume":"63","author":"Regehr","year":"2009","journal-title":"Neuron"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Zou, S., and Kumar, U. (2018). Cannabinoid Receptors and the Endocannabinoid System: Signaling and Function in the Central Nervous System. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19030833"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Hardingham, N., Dachtler, J., and Fox, K. (2013). The Role of Nitric Oxide in Pre-Synaptic Plasticity and Homeostasis. Front. Cell. Neurosci., 7.","DOI":"10.3389\/fncel.2013.00190"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1016\/S0092-8674(00)81053-3","article-title":"Interaction of Nitric Oxide Synthase with the Postsynaptic Density Protein PSD-95 and Alpha1-Syntrophin Mediated by PDZ Domains","volume":"84","author":"Brenman","year":"1996","journal-title":"Cell"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"7407","DOI":"10.1523\/JNEUROSCI.16-23-07407.1996","article-title":"Cloning and Characterization of Postsynaptic Density 93, a Nitric Oxide Synthase Interacting Protein","volume":"16","author":"Brenman","year":"1996","journal-title":"J. Neurosci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1845","DOI":"10.1126\/science.284.5421.1845","article-title":"Specific Coupling of NMDA Receptor Activation to Nitric Oxide Neurotoxicity by PSD-95 Protein","volume":"284","author":"Sattler","year":"1999","journal-title":"Science"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"666","DOI":"10.1080\/19336950.2021.2002594","article-title":"Nitrergic Modulation of Ion Channel Function in Regulating Neuronal Excitability","volume":"15","author":"Spiers","year":"2021","journal-title":"Channels"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1016\/j.neuron.2005.01.011","article-title":"Presynaptic and Postsynaptic Roles of NO, cGK, and RhoA in Long-Lasting Potentiation and Aggregation of Synaptic Proteins","volume":"45","author":"Wang","year":"2005","journal-title":"Neuron"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Pigott, B.M., and Garthwaite, J. (2016). Nitric Oxide Is Required for L-Type Ca2+ Channel-Dependent Long-Term Potentiation in the Hippocampus. Front. Synaptic Neurosci., 8.","DOI":"10.3389\/fnsyn.2016.00017"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"6211","DOI":"10.1523\/JNEUROSCI.0666-22.2022","article-title":"Induction of Activity-Dependent Plasticity at Auditory Nerve Synapses","volume":"42","author":"Wong","year":"2022","journal-title":"J. Neurosci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2065","DOI":"10.1093\/cercor\/bhq281","article-title":"Nitric Oxide Signaling Modulates Synaptic Transmission during Early Postnatal Development","volume":"21","author":"Veres","year":"2011","journal-title":"Cereb. Cortex"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"E4142","DOI":"10.1073\/pnas.1311927110","article-title":"Nitric Oxide Mediates Local Activity-Dependent Excitatory Synapse Development","volume":"110","author":"Nikonenko","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"6520","DOI":"10.1523\/JNEUROSCI.1264-05.2005","article-title":"Modeling Cooperative Volume Signaling in a Plexus of Nitric Oxide Synthase-Expressing Neurons","volume":"25","author":"Philippides","year":"2005","journal-title":"J. Neurosci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1824713","DOI":"10.1155\/2018\/1824713","article-title":"Roles of Gasotransmitters in Synaptic Plasticity and Neuropsychiatric Conditions","volume":"2018","author":"Shefa","year":"2018","journal-title":"Neural Plast."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1152\/jn.1997.78.1.43","article-title":"Cannabinoids Inhibit N- and P\/Q-Type Calcium Channels in Cultured Rat Hippocampal Neurons","volume":"78","author":"Twitchell","year":"1997","journal-title":"J. Neurophysiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1523\/JNEUROSCI.21-01-00109.2001","article-title":"Localization and Mechanisms of Action of Cannabinoid Receptors at the Glutamatergic Synapses of the Mouse Nucleus Accumbens","volume":"21","author":"Robbe","year":"2001","journal-title":"J. Neurosci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"5623","DOI":"10.1523\/JNEUROSCI.0918-04.2004","article-title":"Endocannabinoids Inhibit Transmission at Granule Cell to Purkinje Cell Synapses by Modulating Three Types of Presynaptic Calcium Channels","volume":"24","author":"Brown","year":"2004","journal-title":"J. Neurosci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"665","DOI":"10.1124\/mol.65.3.665","article-title":"Endocannabinoids Modulate N-Type Calcium Channels and G-Protein-Coupled Inwardly Rectifying Potassium Channels via CB1 Cannabinoid Receptors Heterologously Expressed in Mammalian Neurons","volume":"65","author":"Guo","year":"2004","journal-title":"Mol. Pharmacol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1267","DOI":"10.1152\/jn.01227.2005","article-title":"Cannabinoids Modulate the P-Type High-Voltage-Activated Calcium Currents in Purkinje Neurons","volume":"96","author":"Fisyunov","year":"2006","journal-title":"J. Neurophysiol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Kim, O., Okamoto, Y., Kaufmann, W.A., Brose, N., Shigemoto, R., and Jonas, P. (2024). Presynaptic cAMP-PKA-Mediated Potentiation Induces Reconfiguration of Synaptic Vesicle Pools and Channel-Vesicle Coupling at Hippocampal Mossy Fiber Boutons. PLoS Biol., 22.","DOI":"10.1371\/journal.pbio.3002879"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"686","DOI":"10.1038\/372686a0","article-title":"Formation and Inactivation of Endogenous Cannabinoid Anandamide in Central Neurons","volume":"372","author":"Fontana","year":"1994","journal-title":"Nature"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1016\/S0896-6273(01)00246-X","article-title":"Retrograde Inhibition of Presynaptic Calcium Influx by Endogenous Cannabinoids at Excitatory Synapses onto Purkinje Cells","volume":"29","author":"Kreitzer","year":"2001","journal-title":"Neuron"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1016\/S0896-6273(01)00247-1","article-title":"Endogenous Cannabinoids Mediate Retrograde Signals from Depolarized Postsynaptic Neurons to Presynaptic Terminals","volume":"29","author":"Maejima","year":"2001","journal-title":"Neuron"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"588","DOI":"10.1038\/35069076","article-title":"Endogenous Cannabinoids Mediate Retrograde Signalling at Hippocampal Synapses","volume":"410","author":"Wilson","year":"2001","journal-title":"Nature"},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Piette, C., Cui, Y., Gervasi, N., and Venance, L. (2020). Lights on Endocannabinoid-Mediated Synaptic Potentiation. Front. Mol. Neurosci., 13.","DOI":"10.3389\/fnmol.2020.00132"},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Boczek, T., and Zylinska, L. (2021). Receptor-Dependent and Independent Regulation of Voltage-Gated Ca2+ Channels and Ca2+-Permeable Channels by Endocannabinoids in the Brain. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22158168"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"41362","DOI":"10.1038\/srep41362","article-title":"Membrane-Mediated Action of the Endocannabinoid Anandamide on Membrane Proteins: Implications for Understanding the Receptor-Independent Mechanism","volume":"7","author":"Medeiros","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"861","DOI":"10.1016\/0306-4522(94)00450-J","article-title":"Galanin Induces a Hyperpolarization of Norepinephrine-Containing Locus Coeruleus Neurons in the Brainstem Slice","volume":"64","author":"Pieribone","year":"1995","journal-title":"Neuroscience"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1002\/cne.22105","article-title":"Dendritic Synthesis and Release of the Neuropeptide Galanin: Morphological Evidence from Studies on Rat Locus Coeruleus Neurons","volume":"516","author":"Xu","year":"2009","journal-title":"J. Comp. Neurol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1265","DOI":"10.1016\/0896-6273(95)90273-2","article-title":"L-Type Calcium Channels Mediate Dynorphin Neuropeptide Release from Dendrites but Not Axons of Hippocampal Granule Cells","volume":"14","author":"Simmons","year":"1995","journal-title":"Neuron"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"e74107","DOI":"10.7554\/eLife.74107","article-title":"Common Coupling Map Advances GPCR-G Protein Selectivity","volume":"11","author":"Hauser","year":"2022","journal-title":"eLife"},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Owczarek, A., and Blecharz-Klin, K. (2026). Galanin Receptors in the Central Nervous System: Exploring Ligand Interactions, Signal Transduction, and Potential Clinical Implications. Molecules, 31.","DOI":"10.3390\/molecules31050792"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"979","DOI":"10.1016\/S0896-6273(00)81044-2","article-title":"Dendritic GABA Release Depresses Excitatory Transmission between Layer 2\/3 Pyramidal and Bitufted Neurons in Rat Neocortex","volume":"24","author":"Zilberter","year":"1999","journal-title":"Neuron"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1111","DOI":"10.1016\/j.celrep.2017.07.013","article-title":"A Cooperative Mechanism Involving Ca2+-Permeable AMPA Receptors and Retrograde Activation of GABAB Receptors in Interpeduncular Nucleus Plasticity","volume":"20","author":"Koppensteiner","year":"2017","journal-title":"Cell Rep."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1111\/j.1469-7793.2000.00489.x","article-title":"Dendritic Release of Glutamate Suppresses Synaptic Inhibition of Pyramidal Neurons in Rat Neocortex","volume":"528","author":"Zilberter","year":"2000","journal-title":"J. Physiol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1111\/j.1469-7793.2001.0125k.x","article-title":"Retrograde Modulation of Transmitter Release by Postsynaptic Subtype 1 Metabotropic Glutamate Receptors in the Rat Cerebellum","volume":"537","author":"Levenes","year":"2001","journal-title":"J. Physiol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"4978","DOI":"10.1523\/JNEUROSCI.4884-03.2004","article-title":"Endocannabinoid-Independent Retrograde Signaling at Inhibitory Synapses in Layer 2\/3 of Neocortex: Involvement of Vesicular Glutamate Transporter 3","volume":"24","author":"Harkany","year":"2004","journal-title":"J. Neurosci."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"12464","DOI":"10.1523\/JNEUROSCI.0178-07.2007","article-title":"Somatodendritic Release of Glutamate Regulates Synaptic Inhibition in Cerebellar Purkinje Cells via Autocrine mGluR1 Activation","volume":"27","author":"Duguid","year":"2007","journal-title":"J. Neurosci."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"5887","DOI":"10.1093\/emboj\/20.21.5887","article-title":"Synaptic Secretion of BDNF after High-Frequency Stimulation of Glutamatergic Synapses","volume":"20","author":"Hartmann","year":"2001","journal-title":"EMBO J."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"4249","DOI":"10.1523\/JNEUROSCI.21-12-04249.2001","article-title":"BDNF Enhances Quantal Neurotransmitter Release and Increases the Number of Docked Vesicles at the Active Zones of Hippocampal Excitatory Synapses","volume":"21","author":"Tyler","year":"2001","journal-title":"J. Neurosci."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"878","DOI":"10.1038\/nature02618","article-title":"Rapid BDNF-Induced Retrograde Synaptic Modification in a Developing Retinotectal System","volume":"429","author":"Du","year":"2004","journal-title":"Nature"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"13531","DOI":"10.1523\/JNEUROSCI.4576-06.2006","article-title":"Single-Cell Characterization of Retrograde Signaling by Brain-Derived Neurotrophic Factor","volume":"26","author":"Magby","year":"2006","journal-title":"J. Neurosci."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"3358","DOI":"10.1523\/JNEUROSCI.4227-04.2005","article-title":"Brain-Derived Neurotrophic Factor Enhances GABA Release Probability and Nonuniform Distribution of N- and P\/Q-Type Channels on Release Sites of Hippocampal Inhibitory Synapses","volume":"25","author":"Baldelli","year":"2005","journal-title":"J. Neurosci."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1016\/j.mcn.2005.09.002","article-title":"Brain-Derived Neurotrophic Factor-Induced Potentiation of Glutamate and GABA Release: Different Dependency on Signaling Pathways and Neuronal Activity","volume":"31","author":"Matsumoto","year":"2006","journal-title":"Mol. Cell. Neurosci."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"114382","DOI":"10.1016\/j.celrep.2024.114382","article-title":"Retrograde Adenosine\/A2A Receptor Signaling Facilitates Excitatory Synaptic Transmission and Seizures","volume":"43","author":"Nasrallah","year":"2024","journal-title":"Cell Rep."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"975","DOI":"10.1016\/S0896-6273(03)00543-9","article-title":"Presynaptic BDNF Required for a Presynaptic but Not Postsynaptic Component of LTP at Hippocampal CA1-CA3 Synapses","volume":"39","author":"Zakharenko","year":"2003","journal-title":"Neuron"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1038\/nrn.2015.3","article-title":"Specification of Synaptic Connectivity by Cell Surface Interactions","volume":"17","author":"Ghosh","year":"2016","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1007\/978-3-031-34229-5_13","article-title":"Regulation of Presynaptic Release Machinery by Cell Adhesion Molecules","volume":"33","author":"Uchigashima","year":"2023","journal-title":"Adv. Neurobiol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/j.mcn.2012.03.004","article-title":"Ephrin Regulation of Synapse Formation, Function and Plasticity","volume":"50","author":"Hruska","year":"2012","journal-title":"Mol. Cell. Neurosci."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1016\/j.neuron.2017.10.006","article-title":"Transcellular Nanoalignment of Synaptic Function","volume":"96","author":"Biederer","year":"2017","journal-title":"Neuron"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1016\/j.cell.2017.10.024","article-title":"Synaptic Neurexin Complexes: A Molecular Code for the Logic of Neural Circuits","volume":"171","year":"2017","journal-title":"Cell"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1016\/S0092-8674(00)80877-6","article-title":"Neuroligin Expressed in Nonneuronal Cells Triggers Presynaptic Development in Contacting Axons","volume":"101","author":"Scheiffele","year":"2000","journal-title":"Cell"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1525","DOI":"10.1126\/science.1072356","article-title":"SynCAM, a Synaptic Adhesion Molecule That Drives Synapse Assembly","volume":"297","author":"Biederer","year":"2002","journal-title":"Science"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"708","DOI":"10.1038\/nn1074","article-title":"Neurexin Mediates the Assembly of Presynaptic Terminals","volume":"6","author":"Dean","year":"2003","journal-title":"Nat. Neurosci."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1016\/j.neuron.2009.12.019","article-title":"LRRTM2 Interacts with Neurexin1 and Regulates Excitatory Synapse Formation","volume":"64","author":"Sylwestrak","year":"2009","journal-title":"Neuron"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1016\/j.neuron.2009.12.012","article-title":"LRRTM2 Functions as a Neurexin Ligand in Promoting Excitatory Synapse Formation","volume":"64","author":"Ko","year":"2009","journal-title":"Neuron"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1038\/nature19058","article-title":"A Trans-Synaptic Nanocolumn Aligns Neurotransmitter Release to Receptors","volume":"536","author":"Tang","year":"2016","journal-title":"Nature"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"e31755","DOI":"10.7554\/eLife.31755","article-title":"Pre-Post Synaptic Alignment through Neuroligin-1 Tunes Synaptic Transmission Efficiency","volume":"7","author":"Haas","year":"2018","journal-title":"eLife"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1038\/s41593-021-00843-3","article-title":"CaMKII Activation Persistently Segregates Postsynaptic Proteins via Liquid Phase Separation","volume":"24","author":"Hosokawa","year":"2021","journal-title":"Nat. Neurosci."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1902","DOI":"10.1038\/s41380-019-0512-3","article-title":"ELFN2 Is a Postsynaptic Cell Adhesion Molecule with Essential Roles in Controlling Group III mGluRs in the Brain and Neuropsychiatric Behavior","volume":"24","author":"Dunn","year":"2019","journal-title":"Mol. Psychiatry"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"1848","DOI":"10.1038\/s41467-021-22059-6","article-title":"Canonical versus Non-Canonical Transsynaptic Signaling of Neuroligin 3 Tunes Development of Sociality in Mice","volume":"12","author":"Yoshida","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1016\/j.cell.2015.06.056","article-title":"\u03b2-Neurexins Control Neural Circuits by Regulating Synaptic Endocannabinoid Signaling","volume":"162","author":"Anderson","year":"2015","journal-title":"Cell"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1038\/nn.4471","article-title":"Modulation of Excitation on Parvalbumin Interneurons by Neuroligin-3 Regulates the Hippocampal Network","volume":"20","author":"Polepalli","year":"2017","journal-title":"Nat. Neurosci."},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"Innocenzi, E., Sciamanna, G., Zucchi, A., Medici, V., Cesari, E., Farini, D., Elliott, D.J., Sette, C., and Grimaldi, P. (2025). Modulation of Neurexins Alternative Splicing by Cannabinoid Receptors 1 (CB1) Signaling. Cells, 14.","DOI":"10.3390\/cells14130972"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"2488","DOI":"10.1523\/JNEUROSCI.16-08-02488.1996","article-title":"CASK: A Novel Dlg\/PSD95 Homolog with an N-Terminal Calmodulin-Dependent Protein Kinase Domain Identified by Interaction with Neurexins","volume":"16","author":"Hata","year":"1996","journal-title":"J. Neurosci."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"939","DOI":"10.1038\/nature01755","article-title":"\u03b1-Neurexins Couple Ca2+ Channels to Synaptic Vesicle Exocytosis","volume":"423","author":"Missler","year":"2003","journal-title":"Nature"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"4330","DOI":"10.1523\/JNEUROSCI.0497-05.2005","article-title":"Extracellular Domains of \u03b1-Neurexins Participate in Regulating Synaptic Transmission by Selectively Affecting N- and P\/Q-Type Ca2+ Channels","volume":"25","author":"Zhang","year":"2005","journal-title":"J. Neurosci."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"8277","DOI":"10.1523\/JNEUROSCI.0511-18.2018","article-title":"\u03b1-Neurexins Together with A2\u03b4-1 Auxiliary Subunits Regulate Ca2+ Influx through Cav2.1 Channels","volume":"38","author":"Brockhaus","year":"2018","journal-title":"J. Neurosci."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"EMBJ2019103208","DOI":"10.15252\/embj.2019103208","article-title":"Neurexins Cluster Ca2+ Channels within the Presynaptic Active Zone","volume":"39","author":"Luo","year":"2020","journal-title":"EMBO J."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"919","DOI":"10.1016\/j.neuron.2007.05.029","article-title":"Activity-Dependent Validation of Excitatory versus Inhibitory Synapses by Neuroligin-1 versus Neuroligin-2","volume":"54","author":"Chubykin","year":"2007","journal-title":"Neuron"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1038\/nn1837","article-title":"Retrograde Modulation of Presynaptic Release Probability through Signaling Mediated by PSD-95\u2013Neuroligin","volume":"10","author":"Futai","year":"2007","journal-title":"Nat. Neurosci."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"4483","DOI":"10.1073\/pnas.0813213106","article-title":"Mechanisms Contributing to Synaptic Ca2+ Signals and Their Heterogeneity in Hair Cells","volume":"106","author":"Frank","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"E4716","DOI":"10.1073\/pnas.1605737113","article-title":"Hair Cells Use Active Zones with Different Voltage Dependence of Ca2+ Influx to Decompose Sounds into Complementary Neural Codes","volume":"113","author":"Ohn","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"1877","DOI":"10.1002\/ar.22587","article-title":"The Trk A, B, C\u2019s of Neurotrophins in the Cochlea","volume":"295","author":"Green","year":"2012","journal-title":"Anat. Rec."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"876","DOI":"10.1523\/JNEUROSCI.1918-18.2018","article-title":"Puncta of Neuronal Nitric Oxide Synthase (nNOS) Mediate NMDA Receptor Signaling in the Auditory Midbrain","volume":"39","author":"Olthof","year":"2019","journal-title":"J. Neurosci."},{"key":"ref_98","doi-asserted-by":"crossref","unstructured":"Kopp-Scheinpflug, C., and Forsythe, I.D. (2021). Nitric Oxide Signaling in the Auditory Pathway. Front. Neural Circuits, 15.","DOI":"10.3389\/fncir.2021.759342"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1016\/0378-5955(91)90042-8","article-title":"Electrophysiological Evidence for the Presence of NMDA Receptors in the Guinea Pig Cochlea","volume":"51","author":"Puel","year":"1991","journal-title":"Hear. Res."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"1161","DOI":"10.1097\/00001756-199505300-00022","article-title":"NMDA (NMDAR1) and AMPA-Type (GluR2\/3) Receptor Subunits Are Expressed in the Inner Ear","volume":"6","author":"Usami","year":"1995","journal-title":"NeuroReport"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"726","DOI":"10.3109\/00016489609137914","article-title":"Localization of Nitric Oxide Synthase I and III in the Cochlea","volume":"116","author":"Franz","year":"1996","journal-title":"Acta Otolaryngol."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1007\/s004410050729","article-title":"Transient Expression of NMDA Receptors during Rearrangement of AMPA-Receptor-Expressing Fibers in the Developing Inner Ear","volume":"287","author":"Knipper","year":"1996","journal-title":"Cell Tissue Res."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1016\/S0378-5955(98)00027-6","article-title":"The Nitric Oxide\/Cyclic GMP Pathway: A Potential Major Regulator of Cochlear Physiology","volume":"118","author":"Fessenden","year":"1998","journal-title":"Hear. Res."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1002\/(SICI)1096-9861(19990201)404:1<52::AID-CNE4>3.0.CO;2-W","article-title":"Nitric Oxide\/Cyclic Guanosine Monophosphate Pathway in the Peripheral and Central Auditory System of the Rat","volume":"404","author":"Fessenden","year":"1999","journal-title":"J. Comp. Neurol."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"7313","DOI":"10.1523\/JNEUROSCI.5335-07.2008","article-title":"Salicylate Enables Cochlear Arachidonic-Acid-Sensitive NMDA Receptor Responses","volume":"28","author":"Ruel","year":"2008","journal-title":"J. Neurosci."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"5549","DOI":"10.1038\/s41598-019-41770-5","article-title":"Characterization of Transgenic Mouse Lines for Labeling Type I and Type II Afferent Neurons in the Cochlea","volume":"9","author":"Vyas","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/j.neuron.2015.12.016","article-title":"NMDA Receptors Enhance Spontaneous Activity and Promote Neuronal Survival in the Developing Cochlea","volume":"89","author":"Agarwal","year":"2016","journal-title":"Neuron"},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1016\/j.neuron.2018.07.004","article-title":"Homeostatic Control of Spontaneous Activity in the Developing Auditory System","volume":"99","author":"Babola","year":"2018","journal-title":"Neuron"},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1523\/JNEUROSCI.2178-20.2020","article-title":"Purinergic Signaling Controls Spontaneous Activity in the Auditory System throughout Early Development","volume":"41","author":"Babola","year":"2021","journal-title":"J. Neurosci."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"1715","DOI":"10.1113\/jphysiol.2009.168542","article-title":"Functional Maturation of the Exocytotic Machinery at Gerbil Hair Cell Ribbon Synapses","volume":"587","author":"Johnson","year":"2009","journal-title":"J. Physiol."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"8720","DOI":"10.1073\/pnas.1219578110","article-title":"Presynaptic Maturation in Auditory Hair Cells Requires a Critical Period of Sensory-Independent Spiking Activity","volume":"110","author":"Johnson","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"822","DOI":"10.1016\/j.neuron.2014.04.001","article-title":"The Precise Temporal Pattern of Prehearing Spontaneous Activity Is Necessary for Tonotopic Map Refinement","volume":"82","author":"Clause","year":"2014","journal-title":"Neuron"},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"1188","DOI":"10.1152\/jn.00849.2006","article-title":"Modulation of Voltage-Gated Ca2+ Current in Vestibular Hair Cells by Nitric Oxide","volume":"97","author":"Almanza","year":"2007","journal-title":"J. Neurophysiol."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"2494","DOI":"10.1152\/jn.00017.2010","article-title":"Release and Elementary Mechanisms of Nitric Oxide in Hair Cells","volume":"103","author":"Lv","year":"2010","journal-title":"J. Neurophysiol."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ceca.2017.05.008","article-title":"Regulation of L-Type CaV1.3 Channel Activity and Insulin Secretion by the cGMP-PKG Signaling Pathway","volume":"66","author":"Sandoval","year":"2017","journal-title":"Cell Calcium"},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"3333","DOI":"10.1111\/j.1460-9568.2012.08260.x","article-title":"Nitric Oxide as Intracellular Modulator: Internal Production of NO Increases Neuronal Excitability via Modulation of Several Ionic Conductances","volume":"36","author":"Artinian","year":"2012","journal-title":"Eur. J. Neurosci."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1113\/jphysiol.2004.072868","article-title":"A Transiently Expressed SK Current Sustains and Modulates Action Potential Activity in Immature Mouse Inner Hair Cells","volume":"560","author":"Marcotti","year":"2004","journal-title":"J. Physiol."},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1038\/71090","article-title":"Molecular Basis of NMDA Receptor-Coupled Ion Channel Modulation by S-Nitrosylation","volume":"3","author":"Choi","year":"2000","journal-title":"Nat. Neurosci."},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1016\/j.neuron.2005.03.028","article-title":"S-Nitrosylation of N-Ethylmaleimide Sensitive Factor Mediates Surface Expression of AMPA Receptors","volume":"46","author":"Huang","year":"2005","journal-title":"Neuron"},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1016\/0896-6273(94)90349-2","article-title":"Modulation of Ion Channels in Rod Photoreceptors by Nitric Oxide","volume":"13","author":"Kurenny","year":"1994","journal-title":"Neuron"},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"19176","DOI":"10.1523\/JNEUROSCI.2792-13.2013","article-title":"Nitric Oxide Mediates Activity-Dependent Plasticity of Retinal Bipolar Cell Output via S-Nitrosylation","volume":"33","author":"Tooker","year":"2013","journal-title":"J. Neurosci."},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"6621","DOI":"10.1523\/JNEUROSCI.1474-04.2004","article-title":"cGMP-Dependent Kinase Regulates Response Sensitivity of the Mouse On Bipolar Cell","volume":"24","author":"Snellman","year":"2004","journal-title":"J. Neurosci."},{"key":"ref_123","first-page":"e106010","article-title":"A Sensory Cell Diversifies Its Output by Varying Ca2+ Influx-Release Coupling among Active Zones","volume":"40","author":"Moser","year":"2021","journal-title":"EMBO J."},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"e79494","DOI":"10.7554\/eLife.79494","article-title":"Optogenetics and Electron Tomography for Structure-Function Analysis of Cochlear Ribbon Synapses","volume":"11","author":"Chakrabarti","year":"2022","journal-title":"eLife"},{"key":"ref_125","doi-asserted-by":"crossref","unstructured":"Halim, V.C., Hallbrucker, L., Ahrend, J.F., Setz, C., Voorn, R.A., Franke, S., Konrad, V., Seiler, A., Pangr\u0161i\u010d, T., and Roesler, S. (2026). Patterned Pre-Sensory Spontaneous Activity Drives the Structural Refinement of Developing Cochlear Ribbon Synapses. Front. Synaptic Neurosci., 18.","DOI":"10.3389\/fnsyn.2026.1730181"},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"5955","DOI":"10.1523\/JNEUROSCI.0768-04.2004","article-title":"Retroinhibition of Presynaptic Ca2+ Currents by Endocannabinoids Released via Postsynaptic mGluR Activation at a Calyx Synapse","volume":"24","author":"Kushmerick","year":"2004","journal-title":"J. Neurosci."},{"key":"ref_127","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1097\/00001756-199512000-00046","article-title":"Expression of mGluR1 Alpha mRNA Receptor in Rat and Guinea Pig Cochlear Neurons","volume":"7","author":"Safieddine","year":"1995","journal-title":"Neuroreport"},{"key":"ref_128","doi-asserted-by":"crossref","first-page":"1879","DOI":"10.1097\/00001756-199906230-00015","article-title":"Metabotropic Glutamate Receptors Group I Are Involved in Cochlear Neurotransmission","volume":"10","author":"Kleinlogel","year":"1999","journal-title":"Neuroreport"},{"key":"ref_129","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1016\/j.neuroscience.2003.09.010","article-title":"Group i Metabotropic Glutamate Receptors in Spiral Ganglion Neurons Contribute to Excitatory Neurotransmissions in the Cochlea","volume":"123","author":"Peng","year":"2004","journal-title":"Neuroscience"},{"key":"ref_130","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1159\/000259232","article-title":"Molecular Analysis of Excitatory Amino Acid Receptor Expression in the Cochlea","volume":"2","author":"Niedzielski","year":"2009","journal-title":"Audiol. Neurotol."},{"key":"ref_131","doi-asserted-by":"crossref","first-page":"3483","DOI":"10.1113\/JP272604","article-title":"mGluR1 Enhances Efferent Inhibition of Inner Hair Cells in the Developing Rat Cochlea","volume":"595","author":"Ye","year":"2017","journal-title":"J. Physiol."},{"key":"ref_132","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/j.neuron.2005.01.004","article-title":"Phospholipase C\u03b2 Serves as a Coincidence Detector through Its Ca2+ Dependency for Triggering Retrograde Endocannabinoid Signal","volume":"45","author":"Hashimotodani","year":"2005","journal-title":"Neuron"},{"key":"ref_133","doi-asserted-by":"crossref","unstructured":"Mart\u00edn-Salda\u00f1a, S., Trinidad, A., Ramil, E., S\u00e1nchez-L\u00f3pez, A.J., Coronado, M.J., Mart\u00ednez-Mart\u00ednez, E., Garc\u00eda, J.M., Garc\u00eda-Berrocal, J.R., and Ram\u00edrez-Camacho, R. (2016). Spontaneous Cannabinoid Receptor 2 (CB2) Expression in the Cochlea of Adult Albino Rat and Its Up-Regulation after Cisplatin Treatment. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0161954"},{"key":"ref_134","doi-asserted-by":"crossref","unstructured":"Ghosh, S., Sheth, S., Sheehan, K., Mukherjea, D., Dhukhwa, A., Borse, V., Rybak, L.P., and Ramkumar, V. (2018). The Endocannabinoid\/Cannabinoid Receptor 2 System Protects Against Cisplatin-Induced Hearing Loss. Front. Cell. Neurosci., 12.","DOI":"10.3389\/fncel.2018.00271"},{"key":"ref_135","doi-asserted-by":"crossref","first-page":"4131","DOI":"10.1038\/s41598-019-40425-9","article-title":"Capsaicin Protects Against Cisplatin Ototoxicity by Changing the STAT3\/STAT1 Ratio and Activating Cannabinoid (CB2) Receptors in the Cochlea","volume":"9","author":"Bhatta","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_136","doi-asserted-by":"crossref","unstructured":"Col\u00f3n-Cruz, L., Rodriguez-Morales, R., Santana-Cruz, A., Cantres-Velez, J., Torrado-Tapias, A., Lin, S.-J., Yudowski, G., Kensler, R., Marie, B., and Burgess, S.M. (2021). Cnr2 Is Important for Ribbon Synapse Maturation and Function in Hair Cells and Photoreceptors. Front. Mol. Neurosci., 14.","DOI":"10.3389\/fnmol.2021.624265"},{"key":"ref_137","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1017\/S095252380320208X","article-title":"Biphasic Modulation of Voltage-Dependent Currents of Retinal Cones by Cannabinoid CB1 Receptor Agonist WIN 55212-2","volume":"20","author":"Fan","year":"2003","journal-title":"Vis. Neurosci."},{"key":"ref_138","doi-asserted-by":"crossref","first-page":"2647","DOI":"10.1152\/jn.00268.2002","article-title":"Cannabinoid Receptor Activation Differentially Modulates Ion Channels in Photoreceptors of the Tiger Salamander","volume":"89","author":"Straiker","year":"2003","journal-title":"J. Neurophysiol."},{"key":"ref_139","doi-asserted-by":"crossref","first-page":"109920","DOI":"10.1016\/j.isci.2024.109920","article-title":"Non-Canonical Type 1 Cannabinoid Receptor Signaling Regulates Night Visual Processing in the Inner Rat Retina","volume":"27","author":"Estay","year":"2024","journal-title":"iScience"},{"key":"ref_140","doi-asserted-by":"crossref","first-page":"e2277242025","DOI":"10.1523\/JNEUROSCI.2277-24.2025","article-title":"The Retinal Light Response Is Modulated by an mGluR5-Mediated Retrograde Signal from ON-Bipolar Cells to Photoreceptors","volume":"46","author":"Morgans","year":"2026","journal-title":"J. Neurosci."},{"key":"ref_141","doi-asserted-by":"crossref","first-page":"934","DOI":"10.1002\/dvdy.24629","article-title":"Neuronal Cell Adhesion Molecule (NrCAM) Is Expressed by Sensory Cells in the Cochlea and Is Necessary for Proper Cochlear Innervation and Sensory Domain Patterning during Development","volume":"247","author":"Harley","year":"2018","journal-title":"Dev. Dyn."},{"key":"ref_142","doi-asserted-by":"crossref","first-page":"e07830","DOI":"10.7554\/eLife.07830","article-title":"Neuropilin-2\/Semaphorin-3F-Mediated Repulsion Promotes Inner Hair Cell Innervation by Spiral Ganglion Neurons","volume":"4","author":"Coate","year":"2015","journal-title":"eLife"},{"key":"ref_143","doi-asserted-by":"crossref","first-page":"6425","DOI":"10.1523\/JNEUROSCI.0113-19.2019","article-title":"Semaphorin-5B Controls Spiral Ganglion Neuron Branch Refinement during Development","volume":"39","author":"Jung","year":"2019","journal-title":"J. Neurosci."},{"key":"ref_144","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1002\/dvdy.548","article-title":"Cochlear Hair Cell Innervation Is Dependent on a Modulatory Function of Semaphorin-3A","volume":"252","author":"Papazian","year":"2023","journal-title":"Dev. Dyn."},{"key":"ref_145","doi-asserted-by":"crossref","first-page":"1438","DOI":"10.1038\/ncomms2445","article-title":"Ephrin-A5\/EphA4 Signalling Controls Specific Afferent Targeting to Cochlear Hair Cells","volume":"4","author":"Defourny","year":"2013","journal-title":"Nat. Commun."},{"key":"ref_146","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/j.ydbio.2019.02.004","article-title":"Eph\/Ephrin Signalling in the Development and Function of the Mammalian Cochlea","volume":"449","author":"Defourny","year":"2019","journal-title":"Dev. Biol."},{"key":"ref_147","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1016\/0092-8674(95)90396-8","article-title":"Neuroligin 1: A Splice Site-Specific Ligand for \u03b2-Neurexins","volume":"81","author":"Ichtchenko","year":"1995","journal-title":"Cell"},{"key":"ref_148","doi-asserted-by":"crossref","first-page":"2676","DOI":"10.1074\/jbc.271.5.2676","article-title":"Structures, Alternative Splicing, and Neurexin Binding of Multiple Neuroligins (*)","volume":"271","author":"Ichtchenko","year":"1996","journal-title":"J. Biol. Chem."},{"key":"ref_149","doi-asserted-by":"crossref","first-page":"752","DOI":"10.1016\/j.neuron.2016.04.001","article-title":"Transsynaptic Modulation of Kainate Receptor Functions by C1q-like Proteins","volume":"90","author":"Matsuda","year":"2016","journal-title":"Neuron"},{"key":"ref_150","doi-asserted-by":"crossref","first-page":"dev202723","DOI":"10.1242\/dev.202723","article-title":"Presynaptic Nrxn3 Is Essential for Ribbon-Synapse Maturation in Hair Cells","volume":"151","author":"Jukic","year":"2024","journal-title":"Development"},{"key":"ref_151","doi-asserted-by":"crossref","first-page":"104803","DOI":"10.1016\/j.isci.2022.104803","article-title":"Cochlear Ribbon Synapse Maturation Requires Nlgn1 and Nlgn3","volume":"25","author":"Ramirez","year":"2022","journal-title":"iScience"},{"key":"ref_152","doi-asserted-by":"crossref","first-page":"1007","DOI":"10.1016\/j.neuron.2019.12.028","article-title":"LRRTM4: A Novel Regulator of Presynaptic Inhibition and Ribbon Synapse Arrangements of Retinal Bipolar Cells","volume":"105","author":"Sinha","year":"2020","journal-title":"Neuron"},{"key":"ref_153","doi-asserted-by":"crossref","unstructured":"Biswas, J., Pijewski, R.S., Makol, R., Miramontes, T.G., Thompson, B.L., Kresic, L.C., Burghard, A.L., Oliver, D.L., and Martinelli, D.C. (2021). C1ql1 Is Expressed in Adult Outer Hair Cells of the Cochlea in a Tonotopic Gradient. PLoS ONE, 16, Correction in PLoS ONE\u00a02025, 20, e0333506. https:\/\/doi.org\/10.1371\/journal.pone.0333506.","DOI":"10.1371\/journal.pone.0333506"},{"key":"ref_154","doi-asserted-by":"crossref","unstructured":"Qi, Y., Xiong, W., Yu, S., Du, Z., Qu, T., He, L., Wei, W., Zhang, L., Liu, K., and Li, Y. (2021). Deletion of C1ql1 Causes Hearing Loss and Abnormal Auditory Nerve Fibers in the Mouse Cochlea. Front. Cell. Neurosci., 15.","DOI":"10.3389\/fncel.2021.713651"},{"key":"ref_155","doi-asserted-by":"crossref","first-page":"11116","DOI":"10.1073\/pnas.0914233107","article-title":"Essential Cooperation of N-Cadherin and Neuroligin-1 in the Transsynaptic Control of Vesicle Accumulation","volume":"107","author":"Stan","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_156","doi-asserted-by":"crossref","unstructured":"Klotz-Weigand, L., and Enz, R. (2022). Metabotropic Glutamate Receptors at Ribbon Synapses in the Retina and Cochlea. Cells, 11.","DOI":"10.3390\/cells11071097"},{"key":"ref_157","doi-asserted-by":"crossref","first-page":"1165","DOI":"10.1016\/j.neuron.2015.11.011","article-title":"Topographic Mapping of the Synaptic Cleft into Adhesive Nanodomains","volume":"88","author":"Schrod","year":"2015","journal-title":"Neuron"},{"key":"ref_158","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1083\/jcb.201205041","article-title":"The Novel Synaptogenic Protein Farp1 Links Postsynaptic Cytoskeletal Dynamics and Transsynaptic Organization","volume":"199","author":"Cheadle","year":"2012","journal-title":"J. Cell Biol."},{"key":"ref_159","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.mcn.2016.08.012","article-title":"SynCAMs\u2014From Axon Guidance to Neurodevelopmental Disorders","volume":"81","author":"Frei","year":"2017","journal-title":"Mol. Cell. Neurosci."},{"key":"ref_160","doi-asserted-by":"crossref","first-page":"1864","DOI":"10.1126\/science.1069081","article-title":"Trans-Synaptic Eph Receptor-Ephrin Signaling in Hippocampal Mossy Fiber LTP","volume":"296","author":"Contractor","year":"2002","journal-title":"Science"},{"key":"ref_161","doi-asserted-by":"crossref","first-page":"3474","DOI":"10.1523\/JNEUROSCI.4338-05.2006","article-title":"B-Ephrin Reverse Signaling Is Required for NMDA-Independent Long-Term Potentiation of Mossy Fibers in the Hippocampus","volume":"26","author":"Armstrong","year":"2006","journal-title":"J. Neurosci."},{"key":"ref_162","doi-asserted-by":"crossref","first-page":"RP103481","DOI":"10.7554\/eLife.103481","article-title":"Probing the Role of Synaptic Adhesion Molecule RTN4RL2 in Setting up Cochlear Connectivity","volume":"14","author":"Karagulyan","year":"2025","journal-title":"eLife"},{"key":"ref_163","doi-asserted-by":"crossref","first-page":"e80950","DOI":"10.7554\/eLife.80950","article-title":"GluA3 Subunits Are Required for Appropriate Assembly of AMPAR GluA2 and GluA4 Subunits on Cochlear Afferent Synapses and for Presynaptic Ribbon Modiolar-Pillar Morphology","volume":"12","author":"Rutherford","year":"2023","journal-title":"eLife"},{"key":"ref_164","doi-asserted-by":"crossref","first-page":"e70069","DOI":"10.1111\/ejn.70069","article-title":"Conditional Deletion of CB1 Receptor in Parvalbumin-Expressing GABAergic Neurons Results in Hearing Loss and Abnormal Auditory Brainstem Response in Mice","volume":"61","author":"Wu","year":"2025","journal-title":"Eur. J. Neurosci."},{"key":"ref_165","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1186\/s13023-024-03418-0","article-title":"PHARC Syndrome: An Overview","volume":"19","author":"Harutyunyan","year":"2024","journal-title":"Orphanet J. Rare Dis."},{"key":"ref_166","doi-asserted-by":"crossref","first-page":"1500","DOI":"10.1073\/pnas.1217121110","article-title":"ABHD12 Controls Brain Lysophosphatidylserine Pathways That Are Deregulated in a Murine Model of the Neurodegenerative Disease PHARC","volume":"110","author":"Blankman","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_167","doi-asserted-by":"crossref","unstructured":"Alvarado, J.C., Fuentes-Santamar\u00eda, V., Gabald\u00f3n-Ull, M.C., Jare\u00f1o-Flores, T., Miller, J.M., and Juiz, J.M. (2016). Noise-Induced \u201cToughening\u201d Effect in Wistar Rats: Enhanced Auditory Brainstem Responses Are Related to Calretinin and Nitric Oxide Synthase Upregulation. Front. Neuroanat., 10.","DOI":"10.3389\/fnana.2016.00019"},{"key":"ref_168","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/S0378-5955(01)00409-9","article-title":"The Electrochemical and Fluorescence Detection of Nitric Oxide in the Cochlea and Its Increase Following Loud Sound","volume":"164","author":"Shi","year":"2002","journal-title":"Hear. Res."},{"key":"ref_169","doi-asserted-by":"crossref","first-page":"eabh2369","DOI":"10.1126\/scitranslmed.abh2369","article-title":"NOS1 Mutations Cause Hypogonadotropic Hypogonadism with Sensory and Cognitive Deficits That Can Be Reversed in Infantile Mice","volume":"14","author":"Chachlaki","year":"2022","journal-title":"Sci. Transl. Med."},{"key":"ref_170","doi-asserted-by":"crossref","first-page":"e192090","DOI":"10.1172\/JCI192090","article-title":"Carboxypeptidase D Deficiency Causes Hearing Loss Amenable to Treatment","volume":"135","author":"Ramzan","year":"2025","journal-title":"J. Clin. Investig."},{"key":"ref_171","doi-asserted-by":"crossref","first-page":"720","DOI":"10.1093\/hmg\/ddac223","article-title":"A Non-Coding Variant in 5\u2019 Untranslated Region Drove up-Regulation of Pseudo-Kinase EPHA10 and Caused Non-Syndromic Hearing Loss in Humans","volume":"32","author":"Huang","year":"2023","journal-title":"Hum. Mol. Genet."},{"key":"ref_172","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1016\/j.ydbio.2025.05.002","article-title":"EPHRIN-A1 and -A2 Act as Positive Growth Factors for Developing Spiral Ganglion Radial Bundles","volume":"524","author":"Gurjar","year":"2025","journal-title":"Dev. Biol."},{"key":"ref_173","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/j.neuroscience.2025.02.006","article-title":"Endocannabinoid and Nitric Oxide Interactions in the Brain","volume":"569","author":"From","year":"2025","journal-title":"Neuroscience"},{"key":"ref_174","doi-asserted-by":"crossref","first-page":"8070","DOI":"10.1523\/JNEUROSCI.2838-19.2020","article-title":"BDNF Activates Postsynaptic TrkB Receptors to Induce Endocannabinoid Release and Inhibit Presynaptic Calcium Influx at a Calyx-Type Synapse","volume":"40","author":"Wu","year":"2020","journal-title":"J. Neurosci."},{"key":"ref_175","doi-asserted-by":"crossref","first-page":"843","DOI":"10.1038\/s41592-021-01200-9","article-title":"gEAR: Gene Expression Analysis Resource Portal for Community-Driven, Multi-Omic Data Exploration","volume":"18","author":"Orvis","year":"2021","journal-title":"Nat. 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