Skip to main content
Top
Published in: Journal of the Association for Research in Otolaryngology 1/2017

01-02-2017 | Research Article

Tyrosine Hydroxylase Expression in Type II Cochlear Afferents in Mice

Authors: Pankhuri Vyas, Jingjing Sherry Wu, Amanda Zimmerman, Paul Fuchs, Elisabeth Glowatzki

Published in: Journal of the Association for Research in Otolaryngology | Issue 1/2017

Login to get access

Abstract

Acoustic information propagates from the ear to the brain via spiral ganglion neurons that innervate hair cells in the cochlea. These afferents include unmyelinated type II fibers that constitute 5 % of the total, the majority being myelinated type I neurons. Lack of specific genetic markers of type II afferents in the cochlea has been a roadblock in studying their functional role. Unexpectedly, type II afferents were visualized by reporter proteins induced by tyrosine hydroxylase (TH)-driven Cre recombinase. The present study was designed to determine whether TH-driven Cre recombinase (TH-2A-CreER) provides a selective and reliable tool for identification and genetic manipulation of type II rather than type I cochlear afferents. The “TH-2A-CreER neurons” radiated from the spiral lamina, crossed the tunnel of Corti, turned towards the base of the cochlea, and traveled beneath the rows of outer hair cells. Neither the processes nor the somata of TH-2A-CreER neurons were labeled by antibodies that specifically labeled type I afferents and medial efferents. TH-2A-CreER-positive processes partially co-labeled with antibodies to peripherin, a known marker of type II afferents. Individual TH-2A-CreER neurons gave off short branches contacting 7–25 outer hair cells (OHCs). Only a fraction of TH-2A-CreER boutons were associated with CtBP2-immunopositive ribbons. These results show that TH-2A-CreER provides a selective marker for type II versus type I afferents and can be used to describe the morphology and arborization pattern of type II cochlear afferents in the mouse cochlea.
Literature
go back to reference Adamson CL, Reid MA, Mo ZL, Bowne-English J, Davis RL (2002) Firing features and potassium channel content of murine spiral ganglion neurons vary with cochlear location. J Comp Neurol 447:331–350CrossRefPubMed Adamson CL, Reid MA, Mo ZL, Bowne-English J, Davis RL (2002) Firing features and potassium channel content of murine spiral ganglion neurons vary with cochlear location. J Comp Neurol 447:331–350CrossRefPubMed
go back to reference Berglund AM, Brown MC (1994) Central trajectories of type II spiral ganglion cells from various cochlear regions in mice. Hear Res 75:121–130CrossRefPubMed Berglund AM, Brown MC (1994) Central trajectories of type II spiral ganglion cells from various cochlear regions in mice. Hear Res 75:121–130CrossRefPubMed
go back to reference Berglund AM, Ryugo DK (1987) Hair cell innervation by spiral ganglion neurons in the mouse. J Comp Neurol 255:560–570CrossRefPubMed Berglund AM, Ryugo DK (1987) Hair cell innervation by spiral ganglion neurons in the mouse. J Comp Neurol 255:560–570CrossRefPubMed
go back to reference Brown MC (1987) Morphology of labeled efferent fibers in the guinea pig cochlea. J Comp Neurol 260:605–618CrossRefPubMed Brown MC (1987) Morphology of labeled efferent fibers in the guinea pig cochlea. J Comp Neurol 260:605–618CrossRefPubMed
go back to reference Brown MC (1994) Antidromic responses of single units from the spiral ganglion. J Neurophysiol 71:1835–1847PubMed Brown MC (1994) Antidromic responses of single units from the spiral ganglion. J Neurophysiol 71:1835–1847PubMed
go back to reference Brown MC, Berglund AM, Kiang NY, Ryugo DK (1988) Central trajectories of type II spiral ganglion neurons. J Comp Neurol 278:581–590CrossRefPubMed Brown MC, Berglund AM, Kiang NY, Ryugo DK (1988) Central trajectories of type II spiral ganglion neurons. J Comp Neurol 278:581–590CrossRefPubMed
go back to reference Brown MC, Ledwith JV 3rd (1990) Projections of thin (type-II) and thick (type-I) auditory-nerve fibers into the cochlear nucleus of the mouse. Hear Res 49:105–118CrossRefPubMed Brown MC, Ledwith JV 3rd (1990) Projections of thin (type-II) and thick (type-I) auditory-nerve fibers into the cochlear nucleus of the mouse. Hear Res 49:105–118CrossRefPubMed
go back to reference Darrow KN, Simons EJ, Dodds L, Liberman MC (2006) Dopaminergic innervation of the mouse inner ear: evidence for a separate cytochemical group of cochlear efferent fibers. J Comp Neurol 498:403–414CrossRefPubMedPubMedCentral Darrow KN, Simons EJ, Dodds L, Liberman MC (2006) Dopaminergic innervation of the mouse inner ear: evidence for a separate cytochemical group of cochlear efferent fibers. J Comp Neurol 498:403–414CrossRefPubMedPubMedCentral
go back to reference Escurat M, Djabali K, Gumpel M, Gros F, Portier MM (1990) Differential expression of two neuronal intermediate-filament proteins, peripherin and the low-molecular-mass neurofilament protein (NF-L), during the development of the rat. J Neurosci 10:764–784PubMed Escurat M, Djabali K, Gumpel M, Gros F, Portier MM (1990) Differential expression of two neuronal intermediate-filament proteins, peripherin and the low-molecular-mass neurofilament protein (NF-L), during the development of the rat. J Neurosci 10:764–784PubMed
go back to reference Eybalin M, Charachon G, Renard N (1993) Dopaminergic lateral efferent innervation of the guinea-pig cochlea: immunoelectron microscopy of catecholamine-synthesizing enzymes and effect of 6-hydroxydopamine. Neuroscience 54:133–142CrossRefPubMed Eybalin M, Charachon G, Renard N (1993) Dopaminergic lateral efferent innervation of the guinea-pig cochlea: immunoelectron microscopy of catecholamine-synthesizing enzymes and effect of 6-hydroxydopamine. Neuroscience 54:133–142CrossRefPubMed
go back to reference Flores-Otero J, Davis RL (2011) Synaptic proteins are tonotopically graded in postnatal and adult type I and type II spiral ganglion neurons. J Comp Neurol 519:1455–1475CrossRefPubMedPubMedCentral Flores-Otero J, Davis RL (2011) Synaptic proteins are tonotopically graded in postnatal and adult type I and type II spiral ganglion neurons. J Comp Neurol 519:1455–1475CrossRefPubMedPubMedCentral
go back to reference Flores EN, Duggan A, Madathany T, Hogan AK, Marquez FG, Kumar G, Seal RP, Edwards RH, Liberman MC, Garcia-Anoveros J (2015) A non-canonical pathway from cochlea to brain signals tissue-damaging noise. Curr Biol 25:606–612CrossRefPubMedPubMedCentral Flores EN, Duggan A, Madathany T, Hogan AK, Marquez FG, Kumar G, Seal RP, Edwards RH, Liberman MC, Garcia-Anoveros J (2015) A non-canonical pathway from cochlea to brain signals tissue-damaging noise. Curr Biol 25:606–612CrossRefPubMedPubMedCentral
go back to reference Francis HW, Nadol JB Jr (1993) Patterns of innervation of outer hair cells in a chimpanzee: I. Afferent and reciprocal synapses. Hear Res 64:184–190CrossRefPubMed Francis HW, Nadol JB Jr (1993) Patterns of innervation of outer hair cells in a chimpanzee: I. Afferent and reciprocal synapses. Hear Res 64:184–190CrossRefPubMed
go back to reference Froud KE, Wong AC, Cederholm JM, Klugmann M, Sandow SL, Julien JP, Ryan AF, Housley GD (2015) Type II spiral ganglion afferent neurons drive medial olivocochlear reflex suppression of the cochlear amplifier. Nat Commun 6:7115CrossRefPubMedPubMedCentral Froud KE, Wong AC, Cederholm JM, Klugmann M, Sandow SL, Julien JP, Ryan AF, Housley GD (2015) Type II spiral ganglion afferent neurons drive medial olivocochlear reflex suppression of the cochlear amplifier. Nat Commun 6:7115CrossRefPubMedPubMedCentral
go back to reference Ginzberg RD, Morest DK (1983) A study of cochlear innervation in the young cat with the Golgi method. Hear Res 10:227–246CrossRefPubMed Ginzberg RD, Morest DK (1983) A study of cochlear innervation in the young cat with the Golgi method. Hear Res 10:227–246CrossRefPubMed
go back to reference Gorham JD, Baker H, Kegler D, Ziff EB (1990) The expression of the neuronal intermediate filament protein peripherin in the rat embryo. Brain Res Dev Brain Res 57:235–248CrossRefPubMed Gorham JD, Baker H, Kegler D, Ziff EB (1990) The expression of the neuronal intermediate filament protein peripherin in the rat embryo. Brain Res Dev Brain Res 57:235–248CrossRefPubMed
go back to reference Hafidi A (1998) Peripherin-like immunoreactivity in type II spiral ganglion cell body and projections. Brain Res 805:181–190CrossRefPubMed Hafidi A (1998) Peripherin-like immunoreactivity in type II spiral ganglion cell body and projections. Brain Res 805:181–190CrossRefPubMed
go back to reference Hafidi A, Despres G, Romand R (1993) Ontogenesis of type II spiral ganglion neurons during development: peripherin immunohistochemistry. Int J Dev Neurosci 11:507–512CrossRefPubMed Hafidi A, Despres G, Romand R (1993) Ontogenesis of type II spiral ganglion neurons during development: peripherin immunohistochemistry. Int J Dev Neurosci 11:507–512CrossRefPubMed
go back to reference Holloway BB, Stornetta RL, Bochorishvili G, Erisir A, Viar KE, Guyenet PG (2013) Monosynaptic glutamatergic activation of locus coeruleus and other lower brainstem noradrenergic neurons by the C1 cells in mice. J Neurosci 33:18792–18805CrossRefPubMedPubMedCentral Holloway BB, Stornetta RL, Bochorishvili G, Erisir A, Viar KE, Guyenet PG (2013) Monosynaptic glutamatergic activation of locus coeruleus and other lower brainstem noradrenergic neurons by the C1 cells in mice. J Neurosci 33:18792–18805CrossRefPubMedPubMedCentral
go back to reference Huang LC, Thorne PR, Housley GD, Montgomery JM (2007a) Spatiotemporal definition of neurite outgrowth, refinement and retraction in the developing mouse cochlea. Development Huang LC, Thorne PR, Housley GD, Montgomery JM (2007a) Spatiotemporal definition of neurite outgrowth, refinement and retraction in the developing mouse cochlea. Development
go back to reference Huang LC, Thorne PR, Housley GD, Montgomery JM (2007b) Spatiotemporal definition of neurite outgrowth, refinement and retraction in the developing mouse cochlea. Development 134:2925–2933CrossRefPubMed Huang LC, Thorne PR, Housley GD, Montgomery JM (2007b) Spatiotemporal definition of neurite outgrowth, refinement and retraction in the developing mouse cochlea. Development 134:2925–2933CrossRefPubMed
go back to reference Jagger DJ, Housley GD (2003) Membrane properties of type II spiral ganglion neurones identified in a neonatal rat cochlear slice. J Physiol 552:525–533CrossRefPubMedPubMedCentral Jagger DJ, Housley GD (2003) Membrane properties of type II spiral ganglion neurones identified in a neonatal rat cochlear slice. J Physiol 552:525–533CrossRefPubMedPubMedCentral
go back to reference 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 301:443–460CrossRefPubMed 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 301:443–460CrossRefPubMed
go back to reference Martinez-Monedero, R. 2016. GluA2-containing AMPA receptors distinguish ribbon-associated from ribbonless afferent contacts on rat cochlear hair cells. 3. Martinez-Monedero, R. 2016. GluA2-containing AMPA receptors distinguish ribbon-associated from ribbonless afferent contacts on rat cochlear hair cells. 3.
go back to reference Martinez-Monedero R, Liu C, Weisz C, Vyas P, Fuchs PA, Glowatzki E (2016) GluA2-containing AMPA receptors distinguish ribbon-associated from ribbonless afferent contacts on rat cochlear hair cells. eNeuro 3 Martinez-Monedero R, Liu C, Weisz C, Vyas P, Fuchs PA, Glowatzki E (2016) GluA2-containing AMPA receptors distinguish ribbon-associated from ribbonless afferent contacts on rat cochlear hair cells. eNeuro 3
go back to reference McLean WJ, Smith KA, Glowatzki E, Pyott SJ (2009) Distribution of the Na, K-ATPase alpha subunit in the rat spiral ganglion and organ of corti. J Assoc Res Otolaryngol 10:37–49CrossRefPubMed McLean WJ, Smith KA, Glowatzki E, Pyott SJ (2009) Distribution of the Na, K-ATPase alpha subunit in the rat spiral ganglion and organ of corti. J Assoc Res Otolaryngol 10:37–49CrossRefPubMed
go back to reference Morgan YV, Ryugo DK, Brown MC (1994) Central trajectories of type II (thin) fibers of the auditory nerve in cats. Hear Res 79:74–82CrossRefPubMed Morgan YV, Ryugo DK, Brown MC (1994) Central trajectories of type II (thin) fibers of the auditory nerve in cats. Hear Res 79:74–82CrossRefPubMed
go back to reference Mou K, Adamson CL, Davis RL (1998) Time-dependence and cell-type specificity of synergistic neurotrophin actions on spiral ganglion neurons. J Comp Neurol 402:129–139CrossRefPubMed Mou K, Adamson CL, Davis RL (1998) Time-dependence and cell-type specificity of synergistic neurotrophin actions on spiral ganglion neurons. J Comp Neurol 402:129–139CrossRefPubMed
go back to reference Nadol JB Jr (1983) Serial section reconstruction of the neural poles of hair cells in the human organ of Corti. II. outer hair cells. Laryngoscope 93:780–791CrossRefPubMed Nadol JB Jr (1983) Serial section reconstruction of the neural poles of hair cells in the human organ of Corti. II. outer hair cells. Laryngoscope 93:780–791CrossRefPubMed
go back to reference Perkins RE, Morest DK (1975) A study of cochlear innervation patterns in cats and rats with the Golgi method and Nomarkski Optics. J Comp Neurol 163:129–158CrossRefPubMed Perkins RE, Morest DK (1975) A study of cochlear innervation patterns in cats and rats with the Golgi method and Nomarkski Optics. J Comp Neurol 163:129–158CrossRefPubMed
go back to reference Reid MA, Flores-Otero J, Davis RL (2004) Firing patterns of type II spiral ganglion neurons in vitro. J Neurosci 24:733–742CrossRefPubMed Reid MA, Flores-Otero J, Davis RL (2004) Firing patterns of type II spiral ganglion neurons in vitro. J Neurosci 24:733–742CrossRefPubMed
go back to reference Robertson D (1984) Horseradish peroxidase injection of physiologically characterized afferent and efferent neurones in the guinea pig spiral ganglion. Hear Res 15:113–121CrossRefPubMed Robertson D (1984) Horseradish peroxidase injection of physiologically characterized afferent and efferent neurones in the guinea pig spiral ganglion. Hear Res 15:113–121CrossRefPubMed
go back to reference Robertson D, Sellick PM, Patuzzi R (1999) The continuing search for outer hair cell afferents in the guinea pig spiral ganglion. Hear Res 136:151–158CrossRefPubMed Robertson D, Sellick PM, Patuzzi R (1999) The continuing search for outer hair cell afferents in the guinea pig spiral ganglion. Hear Res 136:151–158CrossRefPubMed
go back to reference Rusznak Z, Szucs G (2009) Spiral ganglion neurones: an overview of morphology, firing behaviour, ionic channels and function. Pflugers Arch 457:1303–1325CrossRefPubMed Rusznak Z, Szucs G (2009) Spiral ganglion neurones: an overview of morphology, firing behaviour, ionic channels and function. Pflugers Arch 457:1303–1325CrossRefPubMed
go back to reference Ryugo DK, Dodds LW, Benson TE, Kiang NY (1991) Unmyelinated axons of the auditory nerve in cats. J Comp Neurol 308:209–223CrossRefPubMed Ryugo DK, Dodds LW, Benson TE, Kiang NY (1991) Unmyelinated axons of the auditory nerve in cats. J Comp Neurol 308:209–223CrossRefPubMed
go back to reference Simmons DD, Liberman MC (1988) Afferent innervation of outer hair cells in adult cats: II. Electron microscopic analysis of fibers labeled with horseradish peroxidase. J Comp Neurol 270:145–154CrossRefPubMed Simmons DD, Liberman MC (1988) Afferent innervation of outer hair cells in adult cats: II. Electron microscopic analysis of fibers labeled with horseradish peroxidase. J Comp Neurol 270:145–154CrossRefPubMed
go back to reference Sobkowicz HM, Rose JE, Scott GL, Levenick CV (1986) Distribution of synaptic ribbons in the developing organ of Corti. J Neurocytol 15:693–714CrossRefPubMed Sobkowicz HM, Rose JE, Scott GL, Levenick CV (1986) Distribution of synaptic ribbons in the developing organ of Corti. J Neurocytol 15:693–714CrossRefPubMed
go back to reference Sundaresan S, Kong JH, Fang Q, Salles FT, Wangsawihardja F, Ricci AJ, Mustapha M (2016) Thyroid hormone is required for pruning, functioning and long-term maintenance of afferent inner hair cell synapses. Eur J Neurosci 43:148–161CrossRefPubMed Sundaresan S, Kong JH, Fang Q, Salles FT, Wangsawihardja F, Ricci AJ, Mustapha M (2016) Thyroid hormone is required for pruning, functioning and long-term maintenance of afferent inner hair cell synapses. Eur J Neurosci 43:148–161CrossRefPubMed
go back to reference Trigueiros-Cunha N, Renard N, Humbert G, Tavares MA, Eybalin M (2003) Catecholamine-independent transient expression of tyrosine hydroxylase in primary auditory neurons is coincident with the onset of hearing in the rat cochlea. Eur J Neurosci 18:2653–2662CrossRefPubMed Trigueiros-Cunha N, Renard N, Humbert G, Tavares MA, Eybalin M (2003) Catecholamine-independent transient expression of tyrosine hydroxylase in primary auditory neurons is coincident with the onset of hearing in the rat cochlea. Eur J Neurosci 18:2653–2662CrossRefPubMed
go back to reference Ugrumov MV (2009) Non-dopaminergic neurons partly expressing dopaminergic phenotype: distribution in the brain, development and functional significance. J Chem Neuroanat 38:241–256CrossRefPubMed Ugrumov MV (2009) Non-dopaminergic neurons partly expressing dopaminergic phenotype: distribution in the brain, development and functional significance. J Chem Neuroanat 38:241–256CrossRefPubMed
go back to reference Wang Q, Green SH (2011) Functional role of neurotrophin-3 in synapse regeneration by spiral ganglion neurons on inner hair cells after excitotoxic trauma in vitro. J Neurosci 31:7938–7949CrossRefPubMedPubMedCentral Wang Q, Green SH (2011) Functional role of neurotrophin-3 in synapse regeneration by spiral ganglion neurons on inner hair cells after excitotoxic trauma in vitro. J Neurosci 31:7938–7949CrossRefPubMedPubMedCentral
go back to reference Weisz CJ, Lehar M, Hiel H, Glowatzki E, Fuchs PA (2012) Synaptic transfer from outer hair cells to type II afferent fibers in the rat cochlea. J Neurosci 32:9528–9536CrossRefPubMedPubMedCentral Weisz CJ, Lehar M, Hiel H, Glowatzki E, Fuchs PA (2012) Synaptic transfer from outer hair cells to type II afferent fibers in the rat cochlea. J Neurosci 32:9528–9536CrossRefPubMedPubMedCentral
go back to reference Xing Y, Samuvel DJ, Stevens SM, Dubno JR, Schulte BA, Lang H (2012) Age-related changes of myelin basic protein in mouse and human auditory nerve. PLoS One 7, e34500CrossRefPubMedPubMedCentral Xing Y, Samuvel DJ, Stevens SM, Dubno JR, Schulte BA, Lang H (2012) Age-related changes of myelin basic protein in mouse and human auditory nerve. PLoS One 7, e34500CrossRefPubMedPubMedCentral
go back to reference Zhou L, Nepote V, Rowley DL, Levacher B, Zvara A, Santha M, Mi QS, Simonneau M, Donovan DM (2002) Murine peripherin gene sequences direct Cre recombinase expression to peripheral neurons in transgenic mice. FEBS Lett 523:68–72CrossRefPubMed Zhou L, Nepote V, Rowley DL, Levacher B, Zvara A, Santha M, Mi QS, Simonneau M, Donovan DM (2002) Murine peripherin gene sequences direct Cre recombinase expression to peripheral neurons in transgenic mice. FEBS Lett 523:68–72CrossRefPubMed
Metadata
Title
Tyrosine Hydroxylase Expression in Type II Cochlear Afferents in Mice
Authors
Pankhuri Vyas
Jingjing Sherry Wu
Amanda Zimmerman
Paul Fuchs
Elisabeth Glowatzki
Publication date
01-02-2017
Publisher
Springer US
Published in
Journal of the Association for Research in Otolaryngology / Issue 1/2017
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI
https://doi.org/10.1007/s10162-016-0591-7

Other articles of this Issue 1/2017

Journal of the Association for Research in Otolaryngology 1/2017 Go to the issue