Macromolecular and electrical coupling between inner hair cells in the rodent cochlea

Philippe Jean, Tommi Anttonen, Susann Michanski, Antonio M. G. Diego, Anna M. Steyer, Andreas Neef, David Oestreicher, Jana Kroll, Christos Nardis, Tina Pangršič, Wiebke Möbius, Jonathan Ashmore, Carolin Wichmann () and Tobias Moser ()
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Philippe Jean: University Medical Center Göttingen
Tommi Anttonen: University Medical Center Göttingen
Susann Michanski: University of Göttingen
Antonio M. G. Diego: Physiology and Pharmacology, University College London
Anna M. Steyer: Max Planck Institute of Experimental Medicine
Andreas Neef: University of Göttingen
David Oestreicher: University Medical Center Göttingen
Jana Kroll: University of Göttingen
Christos Nardis: Max Planck Institute of Experimental Medicine
Tina Pangršič: University of Göttingen
Wiebke Möbius: Max Planck Institute of Experimental Medicine
Jonathan Ashmore: Physiology and Pharmacology, University College London
Carolin Wichmann: University of Göttingen
Tobias Moser: University Medical Center Göttingen

Nature Communications, 2020, vol. 11, issue 1, 1-14

Abstract: Abstract 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, Ca2+-current, and resting current increase with the number of dye-coupled IHCs. Dual voltage-clamp experiments substantiate low resistance electrical coupling. Pharmacology and tracer permeability rule out coupling by gap junctions and purinoceptors. 3D electron microscopy indicates instead that IHCs are coupled by membrane fusion sites. Consequently, depolarization of one IHC triggers presynaptic Ca2+-influx at active zones in the entire mini-syncytium. Based on our findings and modeling, we propose that IHC-mini-syncytia enhance sensitivity and reliability of cochlear sound encoding.

Date: 2020
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DOI: 10.1038/s41467-020-17003-z

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