Ribbon Synapse Reformation: A Key Role for the Hearing Restoration; A Review
Journal of Otorhinolaryngology and Facial Plastic Surgery,
Vol. 5 No. 2 (2019),
1 December 2019
,
Page 1-6
https://doi.org/10.22037/orlfps.v5i2.27999
Abstract
Background: Auditory sensory epithelium of mammals has two types of mechanosensory cells including the inner hair cells (IHC) and outer hair cells (OHC). IHC in the mammalian inner ear is an important component for the sound perception. Information about the frequency, intensity, and timingof acoustic signals is transmitted rapidly and precisely via ribbon synapses of the IHCs to the type 1 spiral ganglion neurons (SGNs). Even in the absence of stimulation, these synapses drive spontaneous spiking into the afferent neuron. Evidence has shown that cochlear neuropathy leading to hearing loss may be a result of the damage to ribbon synapses
Aim:Here, we review how these synapses promote the rapid neurotransmitter release and sustained signal transmission. We also discuss the mechanisms involved in ribbon synapse reformation for hearing restoration.
Conclusion:Although cochlear ribbon synapses fail to regenerate spontaneously when injured, recent studies have provided evidence for cochlear synaptogenesis that will be relevant to regenerative methods for cochlear neural loss. A better understanding of mechanisms underlying synaptic reformation would be helpful in achieving reversal of sensorineural hearing loss.
- Ribbon Synapse
- Inner Hair Cells
- Spiral Ganglion Neurons
- Hearing Restoration
How to Cite
References
Murakoshi M, Suzuki S, Wada H. All three rows of outer hair cells are required for cochlear amplification. BioMed research international. 2015;2015.
Raphael Y, Altschuler RA. Structure and innervation of the cochlea. Brain research bulletin. 2003;60(5-6):397-422.
Ashmore JF, Kolston PJ. Hair cell based amplification in the cochlea. Current opinion in neurobiology. 1994;4(4):503-8.
Barclay M, Ryan AF, Housley GD. Type I vs type II spiral ganglion neurons exhibit differential survival and neuritogenesis during cochlear development. Neural development. 2011;6(1):33.
Yu W-M, Goodrich LV. Morphological and physiological development of auditory synapses. Hearing research. 2014;311:3-16.
Roberts WM, Jacobs R, Hudspeth A. Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. Journal of Neuroscience. 1990;10(11):3664-84.
Fuchs PA. Time and intensity coding at the hair cell's ribbon synapse. The Journal of physiology. 2005;566(1):7-12.
Khimich D, Nouvian R, Pujol R, Tom Dieck S, Egner A, Gundelfinger ED, et al. Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature. 2005;434(7035):889.
Nouvian R, Beutner D, Parsons TD, Moser T. Structure and function of the hair cell ribbon synapse. The Journal of membrane biology. 2006;209(2-3):153-65.
Fremeau Jr RT, Voglmaier S, Seal RP, Edwards RH. VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends in neurosciences. 2004;27(2):98-103.
Wan G, Gómez-Casati ME, Gigliello AR, Liberman MC, Corfas G. Neurotrophin-3 regulates ribbon synapse density in the cochlea and induces synapse regeneration after acoustic trauma. Elife. 2014;3:e03564.
Lu X, Shu Y, Tang M, Li H. Mammalian cochlear hair cell regeneration and ribbon synapse reformation. Neural plasticity. 2016.
Moser T, Brandt A, Lysakowski A. Hair cell ribbon synapses. Cell and tissue research. 2006;326(2):347-59.
Meyer AC, Frank T, Khimich D, Hoch G, Riedel D, Chapochnikov NM, et al. Tuning of synapse number, structure and function in the cochlea. Nature neuroscience. 2009;12(4):444.
Brandt A, Khimich D, Moser T. Few CaV1. 3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. Journal of Neuroscience. 2005;25(50):11577-85.
Marrs GS, Spirou GA. Embryonic assembly of auditory circuits: spiral ganglion and brainstem. The Journal of physiology. 2012;590(10):2391-408.
Johnson SL, Kuhn S, Franz C, Ingham N, Furness DN, Knipper M, et al. Presynaptic maturation in auditory hair cells requires a critical period of sensory-independent spiking activity. Proceedings of the National Academy of Sciences. 2013;110(21):8720-5.
Tritsch NX, Bergles DE. Developmental regulation of spontaneous activity in the Mammalian cochlea. Journal of Neuroscience. 2010;30(4):1539-50.
Sobkowicz H, Slapnick S. The efferents interconnecting auditory inner hair cells. Hearing research. 1994;75(1-2):81-92.
Sobkowicz H, Rose J, Scott G, Levenick C. Distribution of synaptic ribbons in the developing organ of Corti. Journal of neurocytology. 1986;15(6):693-714.
Pfenninger K, Sandri C, Akert K, Eugster C. Contribution to the problem of structural organization of the presynaptic area. Brain research. 1969;12(1):10-8.
Sobkowicz HM, Rose JE, Scott GE, Slapnick SM. Ribbon synapses in the developing intact and cultured organ of Corti in the mouse. Journal of Neuroscience. 1982;2(7):942-57.
Daniel E. Noise and hearing loss: a review. Journal of School Health. 2007;77(5):225-31.
Lee K-Y. Pathophysiology of age-related hearing loss (peripheral and central). Korean journal of audiology. 2013;17(2):45.
Liberman MC, Dodds LW. Single-neuron labeling and chronic cochlear pathology. III. Stereocilia damage and alterations of threshold tuning curves. Hearing research. 1984;16(1):55-74.
Robertson D. Effects of acoustic trauma on stereocilia structure and spiral ganglion cell tuning properties in the guinea pig cochlea. Hearing research. 1982;7(1):55-74.
Walton JP. Timing is everything: temporal processing deficits in the aged auditory brainstem. Hearing research. 2010;264(1-2):63-9.
Stone MA, Moore BC, Greenish H. Discrimination of envelope statistics reveals evidence of sub-clinical hearing damage in a noise-exposed population with ‘normal’hearing thresholds. International journal of audiology. 2008;47(12):737-50.
Ruggles D, Bharadwaj H, Shinn-Cunningham BG. Why middle-aged listeners have trouble hearing in everyday settings. Current Biology. 2012;22(15):1417-22.
Canlon B, Schacht J. Acoustic stimulation alters deoxyglucose uptake in the mouse cochlea and inferior colliculus. Hearing research. 1983;10(2):217-26.
Nakai Y, Masutani H. Noise-induced vasoconstriction in the cochlea. Acta Oto-Laryngologica. 1988;105(sup447):23-7.
Cassandro E, Sequino L, Mondola P, Attanasio G, Barbara M, Filipo R. Effect of superoxide dismutase and allopurinol on impulse noise-exposed guinea pigs--electrophysiological and biochemical study. Acta oto-laryngologica. 2003;123(7):802-7.
Nordmann AS, Bohne BA, Harding GW. Histopathological differences between temporary and permanent threshold shift. Hearing research. 2000;139(1-2):13-30.
Robertson D. Functional significance of dendritic swelling after loud sounds in the guinea pig cochlea. Hearing research. 1983;9(3):263-78.
Chen Z, Ulfendahl M, Ruan R, Tan L, Duan M. Protection of auditory function against noise trauma with local caroverine administration in guinea pigs. Hearing research. 2004;197(1-2):131-6.
Weisz CJ, Glowatzki E, Fuchs PA. Excitability of type II cochlear afferents. Journal of Neuroscience. 2014;34(6):2365-73.
Kujawa SG, Liberman MC. Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. Journal of Neuroscience. 2009;29(45):14077-85.
Bartolomé MV, López LM, Gil-Loyzaga P. Galectine-1 expression in cochleae of C57BL/6 mice during aging. Neuroreport. 2001;12(14):3107-10.
Bartolome M, Ibanez-Olias M, Gil-Loyzaga P. Transitional expression of OX-2 and GAP-43 glycoproteins in developing rat cochlear nerve fibers. Histology and histopathology. 2002.
Chen MA, Webster P, Yang E, Linthicum Jr FH. Presbycusic neuritic degeneration within the osseous spiral lamina. Otology & Neurotology. 2006;27(3):316-22.
Liberman MC, Liberman LD, Maison SF. Efferent feedback slows cochlear aging. Journal of Neuroscience. 2014;34(13):4599-607.
Sergeyenko Y, Lall K, Liberman MC, Kujawa SG. Age-related cochlear synaptopathy: an early-onset contributor to auditory functional decline. Journal of Neuroscience. 2013;33(34):13686-94.
Stamataki S, Francis HW, Lehar M, May BJ, Ryugo DK. Synaptic alterations at inner hair cells precede spiral ganglion cell loss in aging C57BL/6J mice. Hearing research. 2006;221(1-2):104-18.
Lin HW, Furman AC, Kujawa SG, Liberman MC. Primary neural degeneration in the Guinea pig cochlea after reversible noise-induced threshold shift. Journal of the Association for Research in Otolaryngology. 2011;12(5):605-16.
Chen W, Jongkamonwiwat N, Abbas L, Eshtan SJ, Johnson SL, Kuhn S, et al. Restoration of auditory evoked responses by human ES-cell-derived otic progenitors. Nature. 2012;490(7419):278.
Liu K, Jiang X, Shi C, Shi L, Yang B, Shi L, et al. Cochlear inner hair cell ribbon synapse is the primary target of ototoxic aminoglycoside stimuli. Molecular neurobiology. 2013;48(3):647-54.
Maison SF, Usubuchi H, Liberman MC. Efferent feedback minimizes cochlear neuropathy from moderate noise exposure. Journal of Neuroscience. 2013;33(13):5542-52.
Shi L, Liu L, He T, Guo X, Yu Z, Yin S, et al. Ribbon synapse plasticity in the cochleae of Guinea pigs after noise-induced silent damage. PloS one. 2013;8(12):e81566.
Tong M, Brugeaud A, Edge AS. Regenerated synapses between postnatal hair cells and auditory neurons. Journal of the Association for Research in Otolaryngology. 2013;14(3):321-9.
Hardie NA, Shepherd RK. Sensorineural hearing loss during development: morphological and physiological response of the cochlea and auditory brainstem. Hearing research. 1999;128(1-2):147-65.
Matsumoto M, Nakagawa T, Kojima K, Sakamoto T, Fujiyama F, Ito J. Potential of embryonic stem cell‐derived neurons for synapse formation with auditory hair cells. Journal of neuroscience research. 2008;86(14):3075-85.
Liu Z, Owen T, Fang J, Zuo J. Overactivation of Notch1 signaling induces ectopic hair cells in the mouse inner ear in an age-dependent manner. PloS one. 2012;7(3):e34123.
Park H, Poo M-m. Neurotrophin regulation of neural circuit development and function. Nature Reviews Neuroscience. 2013;14(1):7.
Alto LT, Havton LA, Conner JM, Hollis II ER, Blesch A, Tuszynski MH. Chemotropic guidance facilitates axonal regeneration and synapse formation after spinal cord injury. Nature neuroscience. 2009;12(9):1106.
Deng L-X, Deng P, Ruan Y, Xu ZC, Liu N-K, Wen X, et al. A novel growth-promoting pathway formed by GDNF-overexpressing Schwann cells promotes propriospinal axonal regeneration, synapse formation, and partial recovery of function after spinal cord injury. Journal of Neuroscience. 2013;33(13):5655-67.
Fritzsch B, Tessarollo L, Coppola E, Reichardt LF. Neurotrophins in the ear: their roles in sensory neuron survival and fiber guidance. Progress in brain research. 2004;146:265-78.
Martinez‐Monedero R, Corrales CE, Cuajungco MP, Heller S, Edge AS. Reinnervation of hair cells by auditory neurons after selective removal of spiral ganglion neurons. Journal of neurobiology. 2006;66(4):319-31.
Liu Z, Dearman JA, Cox BC, Walters BJ, Zhang L, Ayrault O, et al. Age-dependent in vivo conversion of mouse cochlear pillar and Deiters' cells to immature hair cells by Atoh1 ectopic expression. Journal of Neuroscience. 2012;32(19):6600-10.
Shi F, Corrales CE, Liberman MC, Edge AS. BMP4 induction of sensory neurons from human embryonic stem cells and reinnervation of sensory epithelium. European Journal of Neuroscience. 2007;26(11):3016-23.
Nayagam BA, Edge AS, Needham K, Hyakumura T, Leung J, Nayagam DA, et al. An in vitro model of developmental synaptogenesis using cocultures of human neural progenitors and cochlear explants. Stem cells and development. 2012;22(6):901-12.
Nayagam B, Edge A, Dottori M. Stem cellderived sensory progenitors can innervate the early post-natal sensory epithelium in vitro. Proceedings of the Association for Research in Otolaryngology. 2011;8.
Wang Q, Green SH. Functional role of neurotrophin-3 in synapse regeneration by spiral ganglion neurons on inner hair cells after excitotoxic trauma in vitro. Journal of Neuroscience. 2011;31(21):7938-49.
- Abstract Viewed: 216 times
- PDF Downloaded: 251 times