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Olivocochlear Innervation Maintains the Normal Modiolar-Pillar and Habenular-Cuticular Gradients in Cochlear Synaptic Morphology

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Abstract

Morphological studies of inner hair cell (IHC) synapses with cochlear nerve terminals have suggested that high- and low-threshold fibers differ in the sizes of their pre- and postsynaptic elements as well as the position of their synapses around the hair cell circumference. Here, using high-power confocal microscopy, we measured sizes and spatial positions of presynaptic ribbons, postsynaptic glutamate receptor (GluR) patches, and olivocochlear efferent terminals at eight locations along the cochlear spiral in normal and surgically de-efferented mice. Results confirm a prior report suggesting a modiolar > pillar gradient in ribbon size and a complementary pillar > modiolar gradient in GluR-patch size. We document a novel habenular < cuticular gradient in GluR patch size and a complementary cuticular < habenular gradient in olivocochlear innervation density. All spatial gradients in synaptic elements collapse after cochlear de-efferentation, suggesting a major role of olivocochlear efferents in maintaining functional heterogeneity among cochlear nerve fibers. Our spatial analysis also suggests that adjacent IHCs may contain a different synaptic mix, depending on whether their tilt in the radial plane places their synaptic pole closer to the pillar cells or to the modiolus.

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References

  • Bohne BA, Kenworthy A, Carr CD (1982) Density of myelinated nerve fibers in the chinchilla cochlea. J Acoust Soc Am 72:102–107

    Article  CAS  PubMed  Google Scholar 

  • Borg E, Engstrom B, Linde G, Marklund K (1988) Eighth nerve fiber firing features in normal-hearing rabbits. Hear Res 36:191–201

    Article  CAS  PubMed  Google Scholar 

  • Fujioka M, Tokano H, Fujioka KS, Okano H, Edge AS (2011) Generating mouse models of degenerative diseases using Cre/lox-mediated in vivo mosaic cell ablation. J Clin Investig 121:2462–2469

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Furman AC, Kujawa SG, Liberman MC (2013) Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates. J Neurophysiol 110:577–586

    Article  PubMed  Google Scholar 

  • Khimich D, Nouvian R, Pujol R, Tom Dieck S, Egner A, Gundelfinger ED, Moser T (2005) Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434:889–894

    Article  CAS  PubMed  Google Scholar 

  • Kujawa SG, Liberman MC (2009) Adding insult to injury: cochlear nerve degeneration after "temporary" noise-induced hearing loss. J Neurosci 29:14077–14085

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liberman MC (1978) Auditory-nerve response from cats raised in a low-noise chamber. J Acoust Soc Am 63:442–455

    Article  CAS  PubMed  Google Scholar 

  • Liberman MC (1980a) Morphological differences among radial afferent fibers in the cat cochlea: an electron-microscopic study of serial sections. Hear Res 3:45–63

    Article  CAS  PubMed  Google Scholar 

  • Liberman MC (1980b) Efferent synapses in the inner hair cell area of the cat cochlea: an electron microscopic study of serial sections. Hear Res 3:189–204

    Article  CAS  PubMed  Google Scholar 

  • Liberman MC (1982) Single-neuron labeling in the cat auditory nerve. Science 216:1239–1241

    Article  CAS  PubMed  Google Scholar 

  • Liberman MC (1990) Effects of chronic cochlear de-efferentation on auditory-nerve response. Hear Res 49:209–223

    Article  CAS  PubMed  Google Scholar 

  • Liberman MC, Dodds LW, Pierce S (1990) Afferent and efferent innervation of the cat cochlea: quantitative analysis with light and electron microscopy. J Comp Neurol 301:443–460

    Article  CAS  PubMed  Google Scholar 

  • Liberman LD, Wang H, Liberman MC (2011) Opposing gradients of ribbon size and AMPA receptor expression underlie sensitivity differences among cochlear-nerve/hair-cell synapses. J Neurosci Off J Soc Neurosci 31:801–808

    Article  CAS  Google Scholar 

  • Maison SF, Adams JC, Liberman MC (2003) Olivocochlear innervation in the mouse: immunocytochemical maps, crossed versus uncrossed contributions, and transmitter colocalization. J Comp Neurol 455:406–416

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Matsubara A, Laake JH, Davanger S, Usami S, Ottersen OP (1996) Organization of AMPA receptor subunits at a glutamate synapse: a quantitative immunogold analysis of hair cell synapses in the rat organ of Corti. J Neurosci Off J Soc Neurosci 16:4457–4467

    CAS  Google Scholar 

  • Merchan-Perez A, Liberman MC (1996) Ultrastructural differences among afferent synapses on cochlear hair cells: correlations with spontaneous discharge rate. J Comp Neurol 371:208–221

    Article  CAS  PubMed  Google Scholar 

  • Meyer AC, Frank T, Khimich D, Hoch G, Riedel D, Chapochnikov NM, Yarin YM, Harke B, Hell SW, Egner A, Moser T (2009) Tuning of synapse number, structure and function in the cochlea. Nat Neurosci 12:444–453

    Article  CAS  PubMed  Google Scholar 

  • Muller M, von Hunerbein K, Hoidis S, Smolders JW (2005) A physiological place-frequency map of the cochlea in the CBA/J mouse. Hear Res 202:63–73

    Article  PubMed  Google Scholar 

  • Osen KK, Roth K (1969) Histochemical localization of cholinesterases in the cochlear nuclei of the cat, with notes on the origin of acetylcholinesterase positive afferents and the superior olive. Brain Res 16:165–185

  • Pujol R, Marty R (1970) Postnatal maturation in the cochlea of the cat. J Comp Neurol 139:115–118

    Article  CAS  PubMed  Google Scholar 

  • Sachs MB, Abbas PJ (1974) Rate versus level functions for auditory-nerve fibers in cats: tone-burst stimuli. J Acous Soc Am 56:1835–1847

    Article  CAS  Google Scholar 

  • Schmiedt RA (1989) Spontaneous rates, thresholds and tuning of auditory-nerve fibers in the gerbil: comparisons to cat data. Hear Res 42:23–36

    Article  CAS  PubMed  Google Scholar 

  • Schmitz F, Konigstorfer A, Sudhof TC (2000) RIBEYE, a component of synaptic ribbons: a protein's journey through evolution provides insight into synaptic ribbon function. Neuron 28:857–872

    Article  CAS  PubMed  Google Scholar 

  • Sergeyenko Y, Lall K, Liberman MC, Kujawa SG (2013) Age-related cochlear synaptopathy: an early-onset contributor to auditory functional decline. J Neurosci Off J Soc Neurosci 33:13686–13694

    Article  CAS  Google Scholar 

  • Sheets L, Kindt KS, Nicolson T (2012) Presynaptic CaV1.3 channels regulate synaptic ribbon size and are required for synaptic maintenance in sensory hair cells. J Neurosci 32:17273–17286

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stamataki S, Francis HW, Lehar M, May BJ, Ryugo DK (2006) Synaptic alterations at inner hair cells precede spiral ganglion cell loss in aging C57BL/6J mice. Hear Res 221:104–118

    Article  PubMed  Google Scholar 

  • Taberner AM, Liberman MC (2005) Response properties of single auditory nerve fibers in the mouse. J Neurophysiol 93:557–569

    Article  PubMed  Google Scholar 

  • Tsuji J, Liberman MC (1997) Intracellular labeling of auditory nerve fibers in guinea pig: central and peripheral projections. J Comp Neurol 381:188–202

    Article  CAS  PubMed  Google Scholar 

  • Vetter DE, Li C, Zhao L, Contarino A, Liberman MC, Smith GW, Marchuk Y, Koob GF, Heinemann SF, Vale W, Lee KF (2002) Urocortin-deficient mice show hearing impairment and increased anxiety-like behavior. Nat Genet 31:363–369

    CAS  PubMed  Google Scholar 

  • Walsh EJ, McGee J (1987) Postnatal development of auditory nerve and cochlear nucleus neuronal responses in kittens. Hear Res 28:97–116

    Article  CAS  PubMed  Google Scholar 

  • Winter IM, Robertson D, Yates GK (1990) Diversity of characteristic frequency rate-intensity functions in guinea pig auditory nerve fibres. Hear Res 45:191–202

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Research supported by grants from the NIDCD: R01 DC 0188 and P30 DC 05209.

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The authors have no financial conflicts of interest to declare.

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Correspondence to M. Charles Liberman.

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Yin, Y., Liberman, L.D., Maison, S.F. et al. Olivocochlear Innervation Maintains the Normal Modiolar-Pillar and Habenular-Cuticular Gradients in Cochlear Synaptic Morphology. JARO 15, 571–583 (2014). https://doi.org/10.1007/s10162-014-0462-z

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  • DOI: https://doi.org/10.1007/s10162-014-0462-z

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