Macromolecular and electrical coupling between inner hair cells in the rodent cochlea.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
25 06 2020
25 06 2020
Historique:
received:
17
12
2019
accepted:
30
05
2020
entrez:
27
6
2020
pubmed:
27
6
2020
medline:
29
8
2020
Statut:
epublish
Résumé
Inner hair cells (IHCs) are the primary receptors for hearing. They are housed in the cochlea and convey sound information to the brain via synapses with the auditory nerve. IHCs have been thought to be electrically and metabolically independent from each other. We report that, upon developmental maturation, in mice 30% of the IHCs are electrochemically coupled in 'mini-syncytia'. This coupling permits transfer of fluorescently-labeled metabolites and macromolecular tracers. The membrane capacitance, Ca
Identifiants
pubmed: 32587250
doi: 10.1038/s41467-020-17003-z
pii: 10.1038/s41467-020-17003-z
pmc: PMC7316811
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3208Subventions
Organisme : Wellcome Trust
Pays : United Kingdom
Références
Shepherd, G. M. Foundations of the Neuron Doctrine: 25th Anniversary Edition. (Oxford University Press, 2015).
Oren-Suissa, M., Hall, D. H., Treinin, M., Shemer, G. & Podbilewicz, B. The Fusogen EFF-1 controls sculpting of mechanosensory dendrites. Science 328, 1285–1288 (2010).
doi: 10.1126/science.1189095
Giordano-Santini, R., Linton, C. & Hilliard, M. A. Cell-cell fusion in the nervous system: alternative mechanisms of development, injury, and repair. Semin. Cell Dev. Biol. 60, 146–154 (2016).
doi: 10.1016/j.semcdb.2016.06.019
Alcamí, P. & Pereda, A. E. Beyond plasticity: the dynamic impact of electrical synapses on neural circuits. Nat. Rev. Neurosci. 20, 253–271 (2019).
doi: 10.1038/s41583-019-0133-5
Harris, A. L. Electrical coupling and its channels. J. Gen. Physiol. 150, 1606–1639 (2018).
doi: 10.1085/jgp.201812203
Connors, B. W. & Long, M. A. Electrical synapses in the mammalian brain. Annu. Rev. Neurosci. 27, 393–418 (2004).
doi: 10.1146/annurev.neuro.26.041002.131128
Bloomfield, S. A. & Völgyi, B. The diverse functional roles and regulation of neuronal gap junctions in the retina. Nat. Rev. Neurosci. 10, 495–506 (2009).
doi: 10.1038/nrn2636
Christie, J. M. & Westbrook, G. L. Lateral excitation within the olfactory bulb. J. Neurosci. 26, 2269–2277 (2006).
doi: 10.1523/JNEUROSCI.4791-05.2006
Mammano, F. Inner ear connexin channels: roles in development and maintenance of cochlear function. Cold Spring Harb. Perspect. Med. https://doi.org/10.1101/cshperspect.a033233 (2018).
Kiang, N. Y., Rho, J. M., Northrop, C. C., Liberman, M. C. & Ryugo, D. K. Hair-cell innervation by spiral ganglion cells in adult cats. Science 217, 175–177 (1982).
doi: 10.1126/science.7089553
Fettiplace, R. Hair cell transduction, tuning, and synaptic transmission in the mammalian cochlea. Compr. Physiol. 7, 1197–1227 (2017).
doi: 10.1002/cphy.c160049
Mikaelian, D. & Ruben, R. J. Development of hearing in the normal cba-j mouse: correlation of physiological observations with behavioral responses and with cochlear anatomy. Acta Otolaryngol. (Stockh.) 59, 451–461 (1965).
doi: 10.3109/00016486509124579
Juszczak, G. R. & Swiergiel, A. H. Properties of gap junction blockers and their behavioural, cognitive and electrophysiological effects: animal and human studies. Prog. Neuropsychopharmacol. Biol. Psychiatry 33, 181–198 (2009).
doi: 10.1016/j.pnpbp.2008.12.014
Shimamura, K. et al. Effects of flufenamic acid on smooth muscle of the carotid artery isolated from spontaneously hypertensive rats. J. Smooth Muscle Res. Nihon Heikatsukin Gakkai Kikanshi 38, 39–50 (2002).
doi: 10.1540/jsmr.38.39
Squecco, R., Bencini, C., Piperio, C. & Francini, F. L-type Ca2+ channel and ryanodine receptor cross-talk in frog skeletal muscle. J. Physiol. 555, 137–152 (2004).
doi: 10.1113/jphysiol.2003.051730
Vessey, J. P. et al. Carbenoxolone inhibition of voltage-gated ca channels and synaptic transmission in the retina. J. Neurophysiol. 92, 1252–1256 (2004).
doi: 10.1152/jn.00148.2004
Qiu, F. & Dahl, G. A permeant regulating its permeation pore: inhibition of pannexin 1 channels by ATP. Am. J. Physiol. - Cell Physiol. 296, C250–C255 (2009).
doi: 10.1152/ajpcell.00433.2008
Rustom, A., Saffrich, R., Markovic, I., Walther, P. & Gerdes, H.-H. Nanotubular highways for intercellular organelle transport. Science 303, 1007–1010 (2004).
doi: 10.1126/science.1093133
Jean, P. et al. The synaptic ribbon is critical for sound encoding at high rates and with temporal precision. eLife 7, 1–39 (2018).
Neef, J. et al. Quantitative optical nanophysiology of Ca 2
doi: 10.1038/s41467-017-02612-y
Ohn, T.-L. et al. Hair cells use active zones with different voltage dependence of Ca2+ influx to decompose sounds into complementary neural codes. Proc. Natl Acad. Sci. 113, 201605737 (2016).
doi: 10.1073/pnas.1605737113
Joris, P. X., Carney, L. H., Smith, P. H. & Yin, T. C. Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. Responses to tones at the characteristic frequency. J. Neurophysiol. 71, 1022–1036 (1994).
doi: 10.1152/jn.1994.71.3.1022
Lukashkina, V. A., Levic, S., Lukashkin, A. N., Strenzke, N. & Russell, I. J. A connexin30 mutation rescues hearing and reveals roles for gap junctions in cochlear amplification and micromechanics. Nat. Commun. 8, 14530 (2017).
doi: 10.1038/ncomms14530
Taberner, A. M. & Liberman, M. C. Response properties of single auditory nerve fibers in the mouse. J. Neurophysiol. 93, 557–569 (2005).
doi: 10.1152/jn.00574.2004
He, N., Dubno, J. R. & Mills, J. H. Frequency and intensity discrimination measured in a maximum-likelihood procedure from young and aged normal-hearing subjects. J. Acoust. Soc. Am. 103, 553–565 (1998).
doi: 10.1121/1.421127
Gousset, K., Marzo, L., Commere, P.-H. & Zurzolo, C. Myo10 is a key regulator of TNT formation in neuronal cells. J. Cell Sci. 126, 4424–4435 (2013).
doi: 10.1242/jcs.129239
Liu, H. et al. Characterization of transcriptomes of cochlear inner and outer hair cells. J. Neurosci. J. Soc. Neurosci. 34, 11085–11095 (2014).
doi: 10.1523/JNEUROSCI.1690-14.2014
Müller, M., Laube, B., Burda, H. & Bruns, V. Structure and function of the cochlea in the African mole rat (Cryptomys hottentotus): evidence for a low frequency acoustic fovea. J. Comp. Physiol. [A] 171, 469–476 (1992).
Köppl, C., Gleich, O. & Manley, G. A. An auditory fovea in the barn owl cochlea. J. Comp. Physiol. A 171, 695–704 (1993).
doi: 10.1007/BF00213066
Bruns, V. & Schmieszek, E. Cochlear innervation in the greater horseshoe bat: demonstration of an acoustic fovea. Hear. Res. 3, 27–43 (1980).
doi: 10.1016/0378-5955(80)90006-4