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Published in: Journal of the Association for Research in Otolaryngology 3/2008

01-09-2008

Diverse Synaptic Terminals on Rat Stapedius Motoneurons

Authors: Daniel J. Lee, Thane E. Benson, M. Christian Brown

Published in: Journal of the Association for Research in Otolaryngology | Issue 3/2008

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Abstract

Stapedius motoneurons (SMN) mediate the contraction of the stapedius muscle, which protects the inner ear from injury and reduces the masking effects of background noise. A variety of inputs to SMNs are known to exist, but their terminal ultrastructure has not been investigated. We characterized the synaptic terminals on retrogradely labeled SMNs found just ventromedial to the facial motor nucleus. About 80% of the terminals contained round synaptic vesicles. One type (Sm Rnd) had small, round vesicles filling the terminal with occasional dense core vesicles and formed an asymmetric synapse. Sm Rnd terminals were small with lengths of apposition to the SMN less than 3 μm. Partial reconstructions from serial sections demonstrated that these terminals formed up to three synapses per terminal. Another terminal type (Lg Rnd) had large, round vesicles and asymmetric synapses. Most Lg Rnd terminals were small but some were extensive, e.g., abutting the SMN for up to 10 μm. One of these terminals formed at least seven synapses. Another terminal type (Pleo) had pleomorphic vesicles and symmetric active zones that, in some cases, were invaginated by spines from the SMN. A fourth uncommon terminal type (Het Rnd) had round vesicles of heterogeneous sizes and asymmetric synapses. A fifth rare terminal type (Cist) had large, round vesicles and an accompanying subsurface cistern in the SMN. These were generally the same kinds of terminals found on other motoneurons, but the high proportion of round vesicle synapses indicate that SMNs receive mostly excitatory inputs.
Literature
go back to reference Benson TE, Brown MC. Ultrastructure of synaptic input to medial olivocochlear neurons. J. Comp. Neurol 499:244–257, 2006.PubMedCrossRef Benson TE, Brown MC. Ultrastructure of synaptic input to medial olivocochlear neurons. J. Comp. Neurol 499:244–257, 2006.PubMedCrossRef
go back to reference Benson TE, Berglund AM, Brown MC. Synaptic input to cochlear nucleus dendrites that receive medial olivocochlear synapses. J. Comp. Neurol 365:27–41, 1996.PubMedCrossRef Benson TE, Berglund AM, Brown MC. Synaptic input to cochlear nucleus dendrites that receive medial olivocochlear synapses. J. Comp. Neurol 365:27–41, 1996.PubMedCrossRef
go back to reference Blok BF, De Weerd H, Holstege G. Ultrastructural evidence for a paucity of projections from the lumbosacral cord to the pontine micturition center or M-region in the cat: A new concept for the organization of the micturition reflex with the periaqueductal gray as central relay. J. Comp. Neurol 359:300–309, 1995.PubMedCrossRef Blok BF, De Weerd H, Holstege G. Ultrastructural evidence for a paucity of projections from the lumbosacral cord to the pontine micturition center or M-region in the cat: A new concept for the organization of the micturition reflex with the periaqueductal gray as central relay. J. Comp. Neurol 359:300–309, 1995.PubMedCrossRef
go back to reference Borg E. On the neuronal organization of the acoustic middle ear reflex: A physiological and anatomical study. Brain Res 49:101–123, 1973.PubMedCrossRef Borg E. On the neuronal organization of the acoustic middle ear reflex: A physiological and anatomical study. Brain Res 49:101–123, 1973.PubMedCrossRef
go back to reference Borg E, Zakrisson JE. The activity of the stapedius muscle in man during vocalization. Acta Otolaryngol 79:325–333, 1975.PubMedCrossRef Borg E, Zakrisson JE. The activity of the stapedius muscle in man during vocalization. Acta Otolaryngol 79:325–333, 1975.PubMedCrossRef
go back to reference Borg E, Counter SA, Rosler G. Theories of middle ear muscle functions. In: Silman S (ed) The Acoustic Reflex: Basic Principles and Clinical Applications. Orlando, Academic, pp. 63–101, 1984. Borg E, Counter SA, Rosler G. Theories of middle ear muscle functions. In: Silman S (ed) The Acoustic Reflex: Basic Principles and Clinical Applications. Orlando, Academic, pp. 63–101, 1984.
go back to reference Brannstrom T. Quantitative synaptology of functionally different types of cat medial gastrocnemius alpha-motoneurons. J. Comp. Neurol 330:439–454, 1993.PubMedCrossRef Brannstrom T. Quantitative synaptology of functionally different types of cat medial gastrocnemius alpha-motoneurons. J. Comp. Neurol 330:439–454, 1993.PubMedCrossRef
go back to reference Brask T. The noise protection effect of the stapedius reflex. Acta Otolaryngol. Suppl 360:116–117, 1979.PubMed Brask T. The noise protection effect of the stapedius reflex. Acta Otolaryngol. Suppl 360:116–117, 1979.PubMed
go back to reference Cant NB. The synaptic organization of the ventral cochlear nucleus of the cat: The peripheral cap of small cells. In: Merchan MA, Juiz JM, Godfrey DA, Mugnaini E (eds) The Mammalian Cochlear Nuclei: Organization and Function. New York, Plenum, pp. 91–106, 1993. Cant NB. The synaptic organization of the ventral cochlear nucleus of the cat: The peripheral cap of small cells. In: Merchan MA, Juiz JM, Godfrey DA, Mugnaini E (eds) The Mammalian Cochlear Nuclei: Organization and Function. New York, Plenum, pp. 91–106, 1993.
go back to reference Cant NB, Morest DK. The bushy cells in the anteroventral cochlear nucleus of the cat. A study with the electron microscope. Neuroscience 4:1924–1945, 1979. Cant NB, Morest DK. The bushy cells in the anteroventral cochlear nucleus of the cat. A study with the electron microscope. Neuroscience 4:1924–1945, 1979.
go back to reference Conradi S, Kellerth JO, Berthold CH. Electron microscopic studies of serially sectioned cat spinal alpha-motoneurons. II. A method for the description of architecture and synaptology of the cell body and proximal dendritic segments. J. Comp. Neurol 184:741–754, 1979.PubMedCrossRef Conradi S, Kellerth JO, Berthold CH. Electron microscopic studies of serially sectioned cat spinal alpha-motoneurons. II. A method for the description of architecture and synaptology of the cell body and proximal dendritic segments. J. Comp. Neurol 184:741–754, 1979.PubMedCrossRef
go back to reference Fernand VS, Hess A. The occurrence, structure and innervation of slow and twitch muscle fibres in the tensor tympani and stapedius of the cat. J. Physiol 200:547–554, 1969.PubMed Fernand VS, Hess A. The occurrence, structure and innervation of slow and twitch muscle fibres in the tensor tympani and stapedius of the cat. J. Physiol 200:547–554, 1969.PubMed
go back to reference Fornal CA, Metzler CW, Marrosu F, Ribiero-do-Valle LE, Jacobs BL. A subgroup of dorsal raphe serotonergic neurons in the cat is strongly activated during oral-buccal movements. Brain Res 716:123–133, 1996.PubMedCrossRef Fornal CA, Metzler CW, Marrosu F, Ribiero-do-Valle LE, Jacobs BL. A subgroup of dorsal raphe serotonergic neurons in the cat is strongly activated during oral-buccal movements. Brain Res 716:123–133, 1996.PubMedCrossRef
go back to reference Gelfand SA. The contralateral acoustic reflex. In: Silman S (ed) The Acoustic Reflex: Basic Principles and Clinical Applications. Orlando, Academic, pp. 137–186, 1984. Gelfand SA. The contralateral acoustic reflex. In: Silman S (ed) The Acoustic Reflex: Basic Principles and Clinical Applications. Orlando, Academic, pp. 137–186, 1984.
go back to reference Gelfand SA. Hearing: An Introduction to Psychological and Physiological Acoustics. New York, Marcel Dekker, 1998. Gelfand SA. Hearing: An Introduction to Psychological and Physiological Acoustics. New York, Marcel Dekker, 1998.
go back to reference Gelfand SA. The Acoustic Reflex. In: Katz J (ed) Handbook of Clinical Audiology. Lippincott Williams & Wilkins, Baltimore, pp. 206–232, 2002. Gelfand SA. The Acoustic Reflex. In: Katz J (ed) Handbook of Clinical Audiology. Lippincott Williams & Wilkins, Baltimore, pp. 206–232, 2002.
go back to reference Gentschev T, Sotelo C. Degenerative patterns in the ventral cochlear nucleus of the rat after primary deafferentation. An ultrastructural study. Brain Res 62:37–60, 1973.PubMedCrossRef Gentschev T, Sotelo C. Degenerative patterns in the ventral cochlear nucleus of the rat after primary deafferentation. An ultrastructural study. Brain Res 62:37–60, 1973.PubMedCrossRef
go back to reference Guinan JJ, Jr., Joseph MP, Norris BE. Brainstem facial–motor pathways from two distinct groups of stapedius motoneurons in the cat. J. Comp. Neurol 287:134–144, 1989.PubMedCrossRef Guinan JJ, Jr., Joseph MP, Norris BE. Brainstem facial–motor pathways from two distinct groups of stapedius motoneurons in the cat. J. Comp. Neurol 287:134–144, 1989.PubMedCrossRef
go back to reference Hayakawa T, Zheng JQ, Maeda S, Ito H, Seki M, Yajima Y. Synaptology and ultrastructural characteristics of laryngeal cricothyroid and posterior cricoarytenoid motoneurons in the nucleus ambiguus of the rat. Anat. Embryol. (Berl) 200:301–311, 1999.CrossRef Hayakawa T, Zheng JQ, Maeda S, Ito H, Seki M, Yajima Y. Synaptology and ultrastructural characteristics of laryngeal cricothyroid and posterior cricoarytenoid motoneurons in the nucleus ambiguus of the rat. Anat. Embryol. (Berl) 200:301–311, 1999.CrossRef
go back to reference Helfert RH, Schwartz IR, Ryan AF. Ultrastructural characterization of gerbil olivocochlear neurons based on differential uptake of 3H-D-Aspartic acid and a wheatgerm agglutinin-horseradish peroxidase conjugate from the cochlea. J. Neurosci 8:3111–3123, 1988.PubMed Helfert RH, Schwartz IR, Ryan AF. Ultrastructural characterization of gerbil olivocochlear neurons based on differential uptake of 3H-D-Aspartic acid and a wheatgerm agglutinin-horseradish peroxidase conjugate from the cochlea. J. Neurosci 8:3111–3123, 1988.PubMed
go back to reference Henry MA, Westrum LE, Johnson LR. Enhanced ultrastructural visualization of the horseradish peroxidase-tetramethylbenzidine reaction product. J. Histochem. Cytochem 33:1256–1259, 1985.PubMed Henry MA, Westrum LE, Johnson LR. Enhanced ultrastructural visualization of the horseradish peroxidase-tetramethylbenzidine reaction product. J. Histochem. Cytochem 33:1256–1259, 1985.PubMed
go back to reference Hilding DA. The intratympanic muscle reflex as a protective mechanism against loud impulsive noise. Ann. Otol. Rhinol. Laryngol 69:51–60, 1960.PubMed Hilding DA. The intratympanic muscle reflex as a protective mechanism against loud impulsive noise. Ann. Otol. Rhinol. Laryngol 69:51–60, 1960.PubMed
go back to reference Holstein GR, Martinelli GP, Boyle R, Rabbitt RD, Highstein SM. Ultrastructural observations of efferent terminals in the crista ampullaris of the toadfish, Opsanus tau. Exp. Brain Res 155:265–273, 2004.PubMedCrossRef Holstein GR, Martinelli GP, Boyle R, Rabbitt RD, Highstein SM. Ultrastructural observations of efferent terminals in the crista ampullaris of the toadfish, Opsanus tau. Exp. Brain Res 155:265–273, 2004.PubMedCrossRef
go back to reference Ichiyama RM, Broman J, Edgerton VR, Havton LA. Ultrastructural synaptic features differ between alpha- and gamma-motoneurons innervating the tibialis anterior muscle in the rat. J. Comp. Neurol 499:306–315, 2006.PubMedCrossRef Ichiyama RM, Broman J, Edgerton VR, Havton LA. Ultrastructural synaptic features differ between alpha- and gamma-motoneurons innervating the tibialis anterior muscle in the rat. J. Comp. Neurol 499:306–315, 2006.PubMedCrossRef
go back to reference Jones DG, Eslami H. An ultrastructural study of the development of afferent and efferent synapses on outer hair cells of the guinea pig organ of Corti. Cell Tissue Res 231:533–549, 1983.PubMedCrossRef Jones DG, Eslami H. An ultrastructural study of the development of afferent and efferent synapses on outer hair cells of the guinea pig organ of Corti. Cell Tissue Res 231:533–549, 1983.PubMedCrossRef
go back to reference Joseph MP, Guinan JJ, Jr., Fullerton BC, Norris BE, Kiang NY. Number and distribution of stapedius motoneurons in cats. J. Comp. Neurol 232:43–54, 1985.PubMedCrossRef Joseph MP, Guinan JJ, Jr., Fullerton BC, Norris BE, Kiang NY. Number and distribution of stapedius motoneurons in cats. J. Comp. Neurol 232:43–54, 1985.PubMedCrossRef
go back to reference Kellerth JO, Berthold CH, Conradi S. Electron microscopic studies of serially sectioned cat spinal alpha-motoneurons. III. Motoneurons innervating fast-twitch (type FR) units of the gastrocnemius muscle. J. Comp. Neurol 184:755–767, 1979.PubMedCrossRef Kellerth JO, Berthold CH, Conradi S. Electron microscopic studies of serially sectioned cat spinal alpha-motoneurons. III. Motoneurons innervating fast-twitch (type FR) units of the gastrocnemius muscle. J. Comp. Neurol 184:755–767, 1979.PubMedCrossRef
go back to reference Kobler JB, Vacher SR, Guinan JJ, Jr. The recruitment order of stapedius motoneurons in the acoustic reflex varies with sound laterality. Brain Res 425:372–375, 1987.PubMedCrossRef Kobler JB, Vacher SR, Guinan JJ, Jr. The recruitment order of stapedius motoneurons in the acoustic reflex varies with sound laterality. Brain Res 425:372–375, 1987.PubMedCrossRef
go back to reference Kobler JB, Guinan JJ, Jr., Vacher SR, Norris BE. Acoustic reflex frequency selectivity in single stapedius motoneurons of the cat. J. Neurophysiol 68:807–817, 1992.PubMed Kobler JB, Guinan JJ, Jr., Vacher SR, Norris BE. Acoustic reflex frequency selectivity in single stapedius motoneurons of the cat. J. Neurophysiol 68:807–817, 1992.PubMed
go back to reference Lee DJ, de Venecia RK, Guinan JJ, Jr., Brown MC. Central auditory pathways mediating the rat middle ear muscle reflexes. Anat. Rec 288:358–369, 2006.CrossRef Lee DJ, de Venecia RK, Guinan JJ, Jr., Brown MC. Central auditory pathways mediating the rat middle ear muscle reflexes. Anat. Rec 288:358–369, 2006.CrossRef
go back to reference Liberman MC, Brown MC. Physiology and anatomy of single olivocochlear neurons in the cat. Hear. Res 24:17–36, 1986.PubMedCrossRef Liberman MC, Brown MC. Physiology and anatomy of single olivocochlear neurons in the cat. Hear. Res 24:17–36, 1986.PubMedCrossRef
go back to reference Lyon MJ. The central location of the motor neurons to the stapedius muscle in the cat. Brain Res 143:437–444, 1978.PubMedCrossRef Lyon MJ. The central location of the motor neurons to the stapedius muscle in the cat. Brain Res 143:437–444, 1978.PubMedCrossRef
go back to reference Mahoney T, Vernon J, Meikle M. Function of the acoustic reflex in discrimination of intense speech. Arch. Otolaryngol 105:119–123, 1979.PubMed Mahoney T, Vernon J, Meikle M. Function of the acoustic reflex in discrimination of intense speech. Arch. Otolaryngol 105:119–123, 1979.PubMed
go back to reference Maxwell DJ, Kerr R, Rashid S, Anderson E. Characterisation of axon terminals in the rat dorsal horn that are immunoreactive for serotonin 5-HT3A receptor subunits. Exp. Brain Res 149:114–124, 2003.PubMed Maxwell DJ, Kerr R, Rashid S, Anderson E. Characterisation of axon terminals in the rat dorsal horn that are immunoreactive for serotonin 5-HT3A receptor subunits. Exp. Brain Res 149:114–124, 2003.PubMed
go back to reference McCue MP, Guinan JJ, Jr. Anatomical and functional segregation in the stapedius motoneuron pool of the cat. J. Neurophysiol 60:1160–1180, 1988.PubMed McCue MP, Guinan JJ, Jr. Anatomical and functional segregation in the stapedius motoneuron pool of the cat. J. Neurophysiol 60:1160–1180, 1988.PubMed
go back to reference McLaughlin BJ. The fine structure of neurons and synapses in the motor nuclei of the cat spinal cord. J. Comp. Neurol 144:429–60, 1972.CrossRef McLaughlin BJ. The fine structure of neurons and synapses in the motor nuclei of the cat spinal cord. J. Comp. Neurol 144:429–60, 1972.CrossRef
go back to reference Moller AR. Neurophysiological basis of the acoustic middle-ear reflex. In: Silman S (ed) The Acoustic Reflex: Basic Principles and Clinical Applications. Orlando, Academic, pp. 1–35, 1984. Moller AR. Neurophysiological basis of the acoustic middle-ear reflex. In: Silman S (ed) The Acoustic Reflex: Basic Principles and Clinical Applications. Orlando, Academic, pp. 1–35, 1984.
go back to reference Nomura Y, Harada T, Fukaya T. Dynamic tympanometry. J. Am. Audit. Soc 4:190–194, 1979. Nomura Y, Harada T, Fukaya T. Dynamic tympanometry. J. Am. Audit. Soc 4:190–194, 1979.
go back to reference Ochi K, Ohashi T, Kinoshita H. Acoustic tensor tympani response and vestibular-evoked myogenic potential. Laryngoscope 112:2225–2229, 2002.PubMedCrossRef Ochi K, Ohashi T, Kinoshita H. Acoustic tensor tympani response and vestibular-evoked myogenic potential. Laryngoscope 112:2225–2229, 2002.PubMedCrossRef
go back to reference Oliver DL. Projections to the inferior colliculus from the anteroventral cochlear nucleus in the cat: Possible substrates for binaural interaction. J. Comp. Neurol 264:24–46, 1987.PubMedCrossRef Oliver DL. Projections to the inferior colliculus from the anteroventral cochlear nucleus in the cat: Possible substrates for binaural interaction. J. Comp. Neurol 264:24–46, 1987.PubMedCrossRef
go back to reference Olucha F, Martinez-Garcia F, Lopez-Garcia C. A new stabilizing agent for the tetramethyl benzidine (TMB) reaction product in the histochemical detection of horseradish peroxidase (HRP). J. Neurosci. Methods 13:131–138, 1985.PubMedCrossRef Olucha F, Martinez-Garcia F, Lopez-Garcia C. A new stabilizing agent for the tetramethyl benzidine (TMB) reaction product in the histochemical detection of horseradish peroxidase (HRP). J. Neurosci. Methods 13:131–138, 1985.PubMedCrossRef
go back to reference Peters A, Palay SF, Webster Hd. The Fine Structure of the Nervous System: Neurons and their Supporting Cells. New York, Oxford University Press, 1991. Peters A, Palay SF, Webster Hd. The Fine Structure of the Nervous System: Neurons and their Supporting Cells. New York, Oxford University Press, 1991.
go back to reference Robertson D, Gummer M. Physiological and morphological characterization of efferent neurons in the guinea pig cochlea. Hear. Res 20:63–77, 1985.PubMedCrossRef Robertson D, Gummer M. Physiological and morphological characterization of efferent neurons in the guinea pig cochlea. Hear. Res 20:63–77, 1985.PubMedCrossRef
go back to reference Rouiller EM, Capt M, Dolivo M, De Ribaupierre F. Neuronal organization of the stapedius reflex pathways in the rat: A retrograde HRP and viral transneuronal tracing study. Brain Res 476:21–28, 1989.PubMedCrossRef Rouiller EM, Capt M, Dolivo M, De Ribaupierre F. Neuronal organization of the stapedius reflex pathways in the rat: A retrograde HRP and viral transneuronal tracing study. Brain Res 476:21–28, 1989.PubMedCrossRef
go back to reference Saxon DW, Robertson GN, Hopkins DA. Ultrastructure and synaptology of the nucleus ambiguus in the rat: The semicompact and loose formations. J. Comp. Neurol 375:109–27, 1996.PubMedCrossRef Saxon DW, Robertson GN, Hopkins DA. Ultrastructure and synaptology of the nucleus ambiguus in the rat: The semicompact and loose formations. J. Comp. Neurol 375:109–27, 1996.PubMedCrossRef
go back to reference Schwartz AM, Gulley RL. Non-primary afferents to the principal cells of the rostral anteroventral cochlear nucleus of the guinea-pig. Am. J. Anat 153:489–508, 1978.PubMedCrossRef Schwartz AM, Gulley RL. Non-primary afferents to the principal cells of the rostral anteroventral cochlear nucleus of the guinea-pig. Am. J. Anat 153:489–508, 1978.PubMedCrossRef
go back to reference Smith PH, Joris PX, Carney LH, Yin TC. Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat. J. Comp. Neurol 304:387–407, 1991.PubMedCrossRef Smith PH, Joris PX, Carney LH, Yin TC. Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat. J. Comp. Neurol 304:387–407, 1991.PubMedCrossRef
go back to reference Smith PH, Joris PX, Banks MI, Yin TJ. Responses of cochlear nucleus cells and projections of their axons. In: Merchán MA, Juiz JM, Godfrey DA, Mugnaini E (eds) The Mammalian Cochlear Nuclei: Organization and Function. New York, Plenum, pp. 349–371, 1993a. Smith PH, Joris PX, Banks MI, Yin TJ. Responses of cochlear nucleus cells and projections of their axons. In: Merchán MA, Juiz JM, Godfrey DA, Mugnaini E (eds) The Mammalian Cochlear Nuclei: Organization and Function. New York, Plenum, pp. 349–371, 1993a.
go back to reference Smith PH, Joris PX, Yin TCT. Projections of physiologically characterized spherical bushy cell axons from the cochlear nucleus of the cat: Evidence for delay lines to the medial superior olive. J. Comp. Neurol 331:245–260, 1993b.PubMedCrossRef Smith PH, Joris PX, Yin TCT. Projections of physiologically characterized spherical bushy cell axons from the cochlear nucleus of the cat: Evidence for delay lines to the medial superior olive. J. Comp. Neurol 331:245–260, 1993b.PubMedCrossRef
go back to reference Sorra KE, Mishra A, Kirov SA, Harris KM. Dense core vesicles resemble active-zone transport vesicles and are diminished following synaptogenesis in mature hippocampal slices. Neuroscience 141:2097–2106, 2006.PubMedCrossRef Sorra KE, Mishra A, Kirov SA, Harris KM. Dense core vesicles resemble active-zone transport vesicles and are diminished following synaptogenesis in mature hippocampal slices. Neuroscience 141:2097–2106, 2006.PubMedCrossRef
go back to reference Spangler KM, Cant NB, Henkel CK, Farley GR, Warr WB. Descending projections from the superior olivary complex to the cochlear nucleus of the cat. J. Comp. Neurol 259:452–465, 1987.PubMedCrossRef Spangler KM, Cant NB, Henkel CK, Farley GR, Warr WB. Descending projections from the superior olivary complex to the cochlear nucleus of the cat. J. Comp. Neurol 259:452–465, 1987.PubMedCrossRef
go back to reference Sridhar TS, Brown MC, Sewell WF. Unique post-synaptic signaling at the hair cell efferent synapse permits calcium to evoke changes on two time scales. J. Neurosci 17:428–437, 1997.PubMed Sridhar TS, Brown MC, Sewell WF. Unique post-synaptic signaling at the hair cell efferent synapse permits calcium to evoke changes on two time scales. J. Neurosci 17:428–437, 1997.PubMed
go back to reference Stach BA, Jerger JF, Jenkins HA. The human acoustic tensor tympani reflex. A case report. Scand. Audiol 13:93–99, 1984.PubMed Stach BA, Jerger JF, Jenkins HA. The human acoustic tensor tympani reflex. A case report. Scand. Audiol 13:93–99, 1984.PubMed
go back to reference Stevens SS, Davis H. Hearing: Its Psychology and Physiology. New York, Wiley, 1938. Stevens SS, Davis H. Hearing: Its Psychology and Physiology. New York, Wiley, 1938.
go back to reference Strutz J, Munker G, Zollner C. The motor innervation of the tympanic muscles in the guinea pig. Arch. Oto-rhino-laryngol 245:108–111, 1988.CrossRef Strutz J, Munker G, Zollner C. The motor innervation of the tympanic muscles in the guinea pig. Arch. Oto-rhino-laryngol 245:108–111, 1988.CrossRef
go back to reference Thompson GC, Igarashi M, Stach BA. Identification of stapedius muscle motoneurons in squirrel monkey and bush baby. J. Comp. Neurol 231:270–279, 1985.PubMedCrossRef Thompson GC, Igarashi M, Stach BA. Identification of stapedius muscle motoneurons in squirrel monkey and bush baby. J. Comp. Neurol 231:270–279, 1985.PubMedCrossRef
go back to reference Thompson AM, Thompson GC, Britton BH. Serotoninergic innervation of stapedial and tensor tympani motoneurons. Brain Res 787:175–178, 1998.PubMedCrossRef Thompson AM, Thompson GC, Britton BH. Serotoninergic innervation of stapedial and tensor tympani motoneurons. Brain Res 787:175–178, 1998.PubMedCrossRef
go back to reference Tredici G, Pizzini G, Milanesi S. The ultrastructure of the nucleus of the oculomotor nerve (somatic efferent portion) of the cat. Anat. Embryol. (Berl) 149:323–346, 1976.CrossRef Tredici G, Pizzini G, Milanesi S. The ultrastructure of the nucleus of the oculomotor nerve (somatic efferent portion) of the cat. Anat. Embryol. (Berl) 149:323–346, 1976.CrossRef
go back to reference Treeck HH, Pirsig W. Differentiation of nerve endings in the cochlear nucleus on morphological and experimental basis. Acta Oto-laryngol 87:47–60, 1979.CrossRef Treeck HH, Pirsig W. Differentiation of nerve endings in the cochlear nucleus on morphological and experimental basis. Acta Oto-laryngol 87:47–60, 1979.CrossRef
go back to reference Uchizono K. Characteristics of exitatory and inhibitory synapses in the central nervous systems of the cat. Nature 207:642–643, 1965.PubMedCrossRef Uchizono K. Characteristics of exitatory and inhibitory synapses in the central nervous systems of the cat. Nature 207:642–643, 1965.PubMedCrossRef
go back to reference Vacher SR, Guinan JJ, Jr., Kobler JB. Intracellularly labeled stapedius-motoneuron cell bodies in the cat are spatially organized according to their physiologic responses. J. Comp. Neurol 289:401–415, 1989.PubMedCrossRef Vacher SR, Guinan JJ, Jr., Kobler JB. Intracellularly labeled stapedius-motoneuron cell bodies in the cat are spatially organized according to their physiologic responses. J. Comp. Neurol 289:401–415, 1989.PubMedCrossRef
go back to reference Valdivia O. Methods of fixation and the morphology of synaptic vesicles. J. Comp. Neurol 142:257–273, 1971.PubMedCrossRef Valdivia O. Methods of fixation and the morphology of synaptic vesicles. J. Comp. Neurol 142:257–273, 1971.PubMedCrossRef
go back to reference van den Berge H, van der Wal JC. The innervation of the middle ear muscles of the rat. J. Anat 170:99–109, 1990.PubMed van den Berge H, van der Wal JC. The innervation of the middle ear muscles of the rat. J. Anat 170:99–109, 1990.PubMed
go back to reference Warr WB. Fiber degeneration following lesions in the multipolar and globular cell areas in the ventral cochlear nucleus of the cat. Brain Res 40:247–270, 1972.PubMedCrossRef Warr WB. Fiber degeneration following lesions in the multipolar and globular cell areas in the ventral cochlear nucleus of the cat. Brain Res 40:247–270, 1972.PubMedCrossRef
go back to reference Wiener-Vacher SR, Guinan JJ, Jr., Kobler JB, Norris BE. Motoneuron axon distribution in the cat stapedius muscle. Hear. Res 133:139–148, 1999.PubMedCrossRef Wiener-Vacher SR, Guinan JJ, Jr., Kobler JB, Norris BE. Motoneuron axon distribution in the cat stapedius muscle. Hear. Res 133:139–148, 1999.PubMedCrossRef
go back to reference Windsor A, Roska B, Brown MC, Lee DJ. Transneuronal analysis of the middle ear muscle reflex pathways using pseudorabies virus. Abstr. Assoc. Res. Otolaryngol. 30, 2007. Windsor A, Roska B, Brown MC, Lee DJ. Transneuronal analysis of the middle ear muscle reflex pathways using pseudorabies virus. Abstr. Assoc. Res. Otolaryngol. 30, 2007.
Metadata
Title
Diverse Synaptic Terminals on Rat Stapedius Motoneurons
Authors
Daniel J. Lee
Thane E. Benson
M. Christian Brown
Publication date
01-09-2008
Publisher
Springer-Verlag
Published in
Journal of the Association for Research in Otolaryngology / Issue 3/2008
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI
https://doi.org/10.1007/s10162-008-0125-z

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