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Published in: Brain Structure and Function 1/2012

01-01-2012 | Original Article

Distribution of SMI-32-immunoreactive neurons in the central auditory system of the rat

Authors: Ladislav Ouda, Rastislav Druga, Josef Syka

Published in: Brain Structure and Function | Issue 1/2012

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Abstract

SMI-32 antibody recognizes a non-phosphorylated epitope of neurofilament proteins, which are thought to be necessary for the maintenance of large neurons with highly myelinated processes. We investigated the distribution and quantity of SMI-32-immunoreactive(-ir) neurons in individual parts of the rat auditory system. SMI-32-ir neurons were present in all auditory structures; however, in most regions they constituted only a minority of all neurons (10–30%). In the cochlear nuclei, a higher occurrence of SMI-32-ir neurons was found in the ventral cochlear nucleus. Within the superior olivary complex, SMI-32-ir cells were particularly abundant in the medial nucleus of the trapezoid body (MNTB), the only auditory region where SMI-32-ir neurons constituted an absolute majority of all neurons. In the inferior colliculus, a region with the highest total number of neurons among the rat auditory subcortical structures, the percentage of SMI-32-ir cells was, in contrast to the MNTB, very low. In the medial geniculate body, SMI-32-ir neurons were prevalent in the ventral division. At the cortical level, SMI-32-ir neurons were found mainly in layers III, V and VI. Within the auditory cortex, it was possible to distinguish the Te1, Te2 and Te3 areas on the basis of the variable numerical density and volumes of SMI-32-ir neurons, especially when the pyramidal cells of layer V were taken into account. SMI-32-ir neurons apparently form a representative subpopulation of neurons in all parts of the rat central auditory system and may belong to both the inhibitory and excitatory systems, depending on the particular brain region.
Literature
go back to reference Alibardi L (1998) Ultrastructural and immunocytochemical characterization of neurons in the rat ventral cochlear nucleus projecting to the inferior colliculus. Ann Anat 180:415–426PubMedCrossRef Alibardi L (1998) Ultrastructural and immunocytochemical characterization of neurons in the rat ventral cochlear nucleus projecting to the inferior colliculus. Ann Anat 180:415–426PubMedCrossRef
go back to reference Alibardi L (2003) Ultrastructural distribution of glycinergic and GABAergic neurons and axon terminals in the rat dorsal cochlear nucleus, with emphasis on granule cell areas. J Anat 203:31–56PubMedCrossRef Alibardi L (2003) Ultrastructural distribution of glycinergic and GABAergic neurons and axon terminals in the rat dorsal cochlear nucleus, with emphasis on granule cell areas. J Anat 203:31–56PubMedCrossRef
go back to reference Altschuler RA, Hoffman DW, Wenthold RJ (1986) Neurotransmitters of the cochlea and cochlear nucleus: immunocytochemical evidence. Am J Otolaryngol 7:100–106PubMedCrossRef Altschuler RA, Hoffman DW, Wenthold RJ (1986) Neurotransmitters of the cochlea and cochlear nucleus: immunocytochemical evidence. Am J Otolaryngol 7:100–106PubMedCrossRef
go back to reference Andersen BB, Gundersen HJG (1999) Pronounced loss of cell nuclei and anisotropic deformation of thick sections. J Microsc 196:69–73PubMedCrossRef Andersen BB, Gundersen HJG (1999) Pronounced loss of cell nuclei and anisotropic deformation of thick sections. J Microsc 196:69–73PubMedCrossRef
go back to reference Andjelic S, Gallopin T, Cauli B, Hill EL, Roux L, Badr S, Hu E, Tamás G, Lambolez B (2009) Glutamatergic nonpyramidal neurons from neocortical layer VI and their comparison with pyramidal and spiny stellate neurons. J Neurophysiol 101:641–654PubMedCrossRef Andjelic S, Gallopin T, Cauli B, Hill EL, Roux L, Badr S, Hu E, Tamás G, Lambolez B (2009) Glutamatergic nonpyramidal neurons from neocortical layer VI and their comparison with pyramidal and spiny stellate neurons. J Neurophysiol 101:641–654PubMedCrossRef
go back to reference Ashwell KW (2008) Topography and chemoarchitecture of the striatum and pallidum in a monotreme, the short-beaked echidna (Tachyglossus aculeatus). Somatosens Mot Res 25:171–187PubMedCrossRef Ashwell KW (2008) Topography and chemoarchitecture of the striatum and pallidum in a monotreme, the short-beaked echidna (Tachyglossus aculeatus). Somatosens Mot Res 25:171–187PubMedCrossRef
go back to reference Awatramani GB, Turecek R, Trussell LO (2004) Inhibitory control at a synaptic relay. J Neurosci 24:2643–2647PubMedCrossRef Awatramani GB, Turecek R, Trussell LO (2004) Inhibitory control at a synaptic relay. J Neurosci 24:2643–2647PubMedCrossRef
go back to reference Bajo VM, Moore DR (2005) Descending projections from the auditory cortex to the inferior colliculus in the gerbil, Meriones unguiculatus. J Comp Neurol 486:101–116PubMedCrossRef Bajo VM, Moore DR (2005) Descending projections from the auditory cortex to the inferior colliculus in the gerbil, Meriones unguiculatus. J Comp Neurol 486:101–116PubMedCrossRef
go back to reference Bajo VM, Merchán MA, López DE, Rouiller EM (1993) Neuronal morphology and efferent projections of the dorsal nucleus of the lateral lemniscus in the rat. J Comp Neurol 334:241–262PubMedCrossRef Bajo VM, Merchán MA, López DE, Rouiller EM (1993) Neuronal morphology and efferent projections of the dorsal nucleus of the lateral lemniscus in the rat. J Comp Neurol 334:241–262PubMedCrossRef
go back to reference Baldauf ZB (2005) SMI-32 parcellates the visual cortical areas of the marmoset. Neurosci Lett 383:109–114PubMedCrossRef Baldauf ZB (2005) SMI-32 parcellates the visual cortical areas of the marmoset. Neurosci Lett 383:109–114PubMedCrossRef
go back to reference Bazwinsky I, Hilbig H, Bidmon HJ, Rübsamen R (2003) Characterization of the human superior olivary complex by calcium binding proteins and neurofilament H (SMI-32). J Comp Neurol 456:292–303PubMedCrossRef Bazwinsky I, Hilbig H, Bidmon HJ, Rübsamen R (2003) Characterization of the human superior olivary complex by calcium binding proteins and neurofilament H (SMI-32). J Comp Neurol 456:292–303PubMedCrossRef
go back to reference Bickford ME, Guido W, Godwin DW (1998) Neurofilament proteins in Y-cells of the cat lateral geniculate nucleus: normal expression and alteration with visual deprivation. J Neurosci 18:6549–6557PubMed Bickford ME, Guido W, Godwin DW (1998) Neurofilament proteins in Y-cells of the cat lateral geniculate nucleus: normal expression and alteration with visual deprivation. J Neurosci 18:6549–6557PubMed
go back to reference Boire D, Desgent S, Matteau I, Ptito M (2005) Regional analysis of neurofilament protein immunoreactivity in the hamster’s cortex. J Chem Neuroanat 29:193–208PubMedCrossRef Boire D, Desgent S, Matteau I, Ptito M (2005) Regional analysis of neurofilament protein immunoreactivity in the hamster’s cortex. J Chem Neuroanat 29:193–208PubMedCrossRef
go back to reference Bourne JA, Rosa MG (2003) Laminar expression of neurofilament protein in the superior colliculus of the marmoset monkey (Callithrix jacchus). Brain Res 973:142–145PubMedCrossRef Bourne JA, Rosa MG (2003) Laminar expression of neurofilament protein in the superior colliculus of the marmoset monkey (Callithrix jacchus). Brain Res 973:142–145PubMedCrossRef
go back to reference Budinger E, Heil P, Scheich H (2000) Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus) III. Anatomical subdivisions and corticocortical connections. Eur J Neurosci 12:2425–2451PubMedCrossRef Budinger E, Heil P, Scheich H (2000) Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus) III. Anatomical subdivisions and corticocortical connections. Eur J Neurosci 12:2425–2451PubMedCrossRef
go back to reference Burianova J, Ouda L, Profant O, Syka J (2009) Age-related changes in GAD levels in the central auditory system of the rat. Exp Gerontol 44:161–169PubMedCrossRef Burianova J, Ouda L, Profant O, Syka J (2009) Age-related changes in GAD levels in the central auditory system of the rat. Exp Gerontol 44:161–169PubMedCrossRef
go back to reference Campbell MJ, Morrison JH (1989) Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex. J Comp Neurol 282:191–205PubMedCrossRef Campbell MJ, Morrison JH (1989) Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex. J Comp Neurol 282:191–205PubMedCrossRef
go back to reference Cant NB, Benson CG (2003) Parallel auditory pathways: projection patterns of the different neuronal populations in the dorsal and ventral cochlear nuclei. Brain Res Bull 60:457–474PubMedCrossRef Cant NB, Benson CG (2003) Parallel auditory pathways: projection patterns of the different neuronal populations in the dorsal and ventral cochlear nuclei. Brain Res Bull 60:457–474PubMedCrossRef
go back to reference Chaudhuri A, Zangenehpour S, Matsubara JA, Cynader MS (1996) Differential expression of neurofilament protein in the visual system of the vervet monkey. Brain Res 709:17–26PubMedCrossRef Chaudhuri A, Zangenehpour S, Matsubara JA, Cynader MS (1996) Differential expression of neurofilament protein in the visual system of the vervet monkey. Brain Res 709:17–26PubMedCrossRef
go back to reference Chernock ML, Larue DT, Winer JA (2004) A periodic network of neurochemical modules in the inferior colliculus. Hear Res 188:12–20PubMedCrossRef Chernock ML, Larue DT, Winer JA (2004) A periodic network of neurochemical modules in the inferior colliculus. Hear Res 188:12–20PubMedCrossRef
go back to reference Cudkowicz M, Kowall NW (1990) Degeneration of pyramidal projection neurons in Huntington’s disease cortex. Ann Neurol 27:200–204PubMedCrossRef Cudkowicz M, Kowall NW (1990) Degeneration of pyramidal projection neurons in Huntington’s disease cortex. Ann Neurol 27:200–204PubMedCrossRef
go back to reference Duffy KR, Slusar JE (2009) Monocular deprivation provokes alteration of the neuronal cytoskeleton in developing cat lateral geniculate nucleus. Vis Neurosci 26:319–328PubMedCrossRef Duffy KR, Slusar JE (2009) Monocular deprivation provokes alteration of the neuronal cytoskeleton in developing cat lateral geniculate nucleus. Vis Neurosci 26:319–328PubMedCrossRef
go back to reference Fredrich M, Reisch A, Illing RB (2009) Neuronal subtype identity in the rat auditory brainstem as defined by molecular profile and axonal projection. Exp Brain Res 195:241–260PubMedCrossRef Fredrich M, Reisch A, Illing RB (2009) Neuronal subtype identity in the rat auditory brainstem as defined by molecular profile and axonal projection. Exp Brain Res 195:241–260PubMedCrossRef
go back to reference Friauf E (1994) Distribution of calcium-binding protein calbindin-D28k in the auditory system of adult and developing rats. J Comp Neurol 349:193–211PubMedCrossRef Friauf E (1994) Distribution of calcium-binding protein calbindin-D28k in the auditory system of adult and developing rats. J Comp Neurol 349:193–211PubMedCrossRef
go back to reference Goldstein ME, Sternberger LA, Sternberger NH (1987) Varying degrees of phosphorylation determine microheterogeneity of the heavy neurofilament polypeptide (Nf-H). J Neuroimmunol 14:135–148PubMedCrossRef Goldstein ME, Sternberger LA, Sternberger NH (1987) Varying degrees of phosphorylation determine microheterogeneity of the heavy neurofilament polypeptide (Nf-H). J Neuroimmunol 14:135–148PubMedCrossRef
go back to reference Gundersen HJG, Jensen EBV, Kieu K, Nielsen J (1999) The efficiency of systematic sampling in stereology-reconsidered. J Microsc 193:199–211PubMedCrossRef Gundersen HJG, Jensen EBV, Kieu K, Nielsen J (1999) The efficiency of systematic sampling in stereology-reconsidered. J Microsc 193:199–211PubMedCrossRef
go back to reference Hassiotis M, Paxinos G, Ashwell KW (2004) Cyto- and chemoarchitecture of the cerebral cortex of the Australian echidna (Tachyglossus aculeatus) I. Areal organization. J Comp Neurol 475:493–517PubMedCrossRef Hassiotis M, Paxinos G, Ashwell KW (2004) Cyto- and chemoarchitecture of the cerebral cortex of the Australian echidna (Tachyglossus aculeatus) I. Areal organization. J Comp Neurol 475:493–517PubMedCrossRef
go back to reference Hazama M, Kimura A, Donishi T, Sakoda T, Tamai Y (2004) Topography of corticothalamic projections from the auditory cortex of the rat. Neuroscience 124:655–667PubMedCrossRef Hazama M, Kimura A, Donishi T, Sakoda T, Tamai Y (2004) Topography of corticothalamic projections from the auditory cortex of the rat. Neuroscience 124:655–667PubMedCrossRef
go back to reference Herbert H, Aschoff A, Ostwald J (1991) Topography of projections from the auditory cortex to the inferior colliculus in the rat. J Comp Neurol 304:103–122PubMedCrossRef Herbert H, Aschoff A, Ostwald J (1991) Topography of projections from the auditory cortex to the inferior colliculus in the rat. J Comp Neurol 304:103–122PubMedCrossRef
go back to reference Hof PR, Morrison JH (1990) Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer’s disease: II. Primary and secondary visual cortex. J Comp Neurol 301:55–64PubMedCrossRef Hof PR, Morrison JH (1990) Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer’s disease: II. Primary and secondary visual cortex. J Comp Neurol 301:55–64PubMedCrossRef
go back to reference Hoffman PN, Cleveland DW, Griffin JW, Landes PW, Cowan NJ, Price DL (1987) Neurofilament gene expression: a major determinant of axonal caliber. Proc Natl Acad Sci USA 84:3472–3476PubMedCrossRef Hoffman PN, Cleveland DW, Griffin JW, Landes PW, Cowan NJ, Price DL (1987) Neurofilament gene expression: a major determinant of axonal caliber. Proc Natl Acad Sci USA 84:3472–3476PubMedCrossRef
go back to reference Idrizbegovic E, Canlon B, Bross LS, Willott JF, Bogdanovic N (2001) The total number of neurons and calcium binding protein positive neurons during aging in the cochlear nucleus of CBA/CaJ mice: a quantitative study. Hear Res 158:102–115PubMedCrossRef Idrizbegovic E, Canlon B, Bross LS, Willott JF, Bogdanovic N (2001) The total number of neurons and calcium binding protein positive neurons during aging in the cochlear nucleus of CBA/CaJ mice: a quantitative study. Hear Res 158:102–115PubMedCrossRef
go back to reference Idrizbegovic E, Bogdanovic N, Willott JF, Canlon B (2004) Age-related increases in calcium-binding protein immunoreactivity in the cochlear nucleus of hearing impaired C57BL/6J mice. Neurobiol Aging 25:1085–1093PubMedCrossRef Idrizbegovic E, Bogdanovic N, Willott JF, Canlon B (2004) Age-related increases in calcium-binding protein immunoreactivity in the cochlear nucleus of hearing impaired C57BL/6J mice. Neurobiol Aging 25:1085–1093PubMedCrossRef
go back to reference Irvine KA, Blakemore WF (2006) Age increases axon loss associated with primary demyelination in cuprizone-induced demyelination in C57BL/6 mice. J Neuroimmunol 175:69–76PubMedCrossRef Irvine KA, Blakemore WF (2006) Age increases axon loss associated with primary demyelination in cuprizone-induced demyelination in C57BL/6 mice. J Neuroimmunol 175:69–76PubMedCrossRef
go back to reference Kirkcaldie MT, Dickson TC, King CE, Grasby D, Riederer BM, Vickers JC (2002) Neurofilament triplet proteins are restricted to a subset of neurons in the rat neocortex. J Chem Neuroanat 24:163–171PubMedCrossRef Kirkcaldie MT, Dickson TC, King CE, Grasby D, Riederer BM, Vickers JC (2002) Neurofilament triplet proteins are restricted to a subset of neurons in the rat neocortex. J Chem Neuroanat 24:163–171PubMedCrossRef
go back to reference Kopp-Scheinpflug C, Tolnai S, Malmierca MS, Rübsamen R (2008) The medial nucleus of the trapezoid body: comparative physiology. Neuroscience 154:160–170PubMedCrossRef Kopp-Scheinpflug C, Tolnai S, Malmierca MS, Rübsamen R (2008) The medial nucleus of the trapezoid body: comparative physiology. Neuroscience 154:160–170PubMedCrossRef
go back to reference Kulesza RJ Jr (2007) Cytoarchitecture of the human superior olivary complex: medial and lateral superior olive. Hear Res 225:80–90PubMedCrossRef Kulesza RJ Jr (2007) Cytoarchitecture of the human superior olivary complex: medial and lateral superior olive. Hear Res 225:80–90PubMedCrossRef
go back to reference Kulesza RJ Jr, Berrebi AS (2000) Superior paraolivary nucleus of the rat is a GABAergic nucleus. J Assoc Res Otolaryngol 1:255–269PubMedCrossRef Kulesza RJ Jr, Berrebi AS (2000) Superior paraolivary nucleus of the rat is a GABAergic nucleus. J Assoc Res Otolaryngol 1:255–269PubMedCrossRef
go back to reference Kulesza RJ, Viñuela A, Saldaña E, Berrebi AS (2002) Unbiased stereological estimates of neuron number in subcortical auditory nuclei of the rat. Hear Res 168:12–24PubMedCrossRef Kulesza RJ, Viñuela A, Saldaña E, Berrebi AS (2002) Unbiased stereological estimates of neuron number in subcortical auditory nuclei of the rat. Hear Res 168:12–24PubMedCrossRef
go back to reference Kuwabara N, Zook JM (1991) Classification of the principal cells of the medial nucleus of the trapezoid body. J Comp Neurol 314:707–720PubMedCrossRef Kuwabara N, Zook JM (1991) Classification of the principal cells of the medial nucleus of the trapezoid body. J Comp Neurol 314:707–720PubMedCrossRef
go back to reference Kuwabara N, DiCaprio RA, Zook JM (1991) Afferents to the medial nucleus of the trapezoid body and their collateral projections. J Comp Neurol 314:684–706PubMedCrossRef Kuwabara N, DiCaprio RA, Zook JM (1991) Afferents to the medial nucleus of the trapezoid body and their collateral projections. J Comp Neurol 314:684–706PubMedCrossRef
go back to reference Lasek RJ (1988) Studying the intrinsic determinants of neuronal form and function. In: Lasek RJ, Black MM (eds) Intrinsic determinants of neuronal form and fiction. Alan R. Liss, New York, pp 1–60 Lasek RJ (1988) Studying the intrinsic determinants of neuronal form and function. In: Lasek RJ, Black MM (eds) Intrinsic determinants of neuronal form and fiction. Alan R. Liss, New York, pp 1–60
go back to reference Lawson SN, Waddell PJ (1991) Soma neurofilament immunoreactivity is related to cell size and fibre conduction velocity in rat primary sensory neurons. J Physiol 435:41–63PubMed Lawson SN, Waddell PJ (1991) Soma neurofilament immunoreactivity is related to cell size and fibre conduction velocity in rat primary sensory neurons. J Physiol 435:41–63PubMed
go back to reference Lee MK, Cleveland DW (1994) Neurofilament function and dysfunction: involvement in axonal growth and neuronal disease. Curr Opin Cell Biol 6:34–40PubMedCrossRef Lee MK, Cleveland DW (1994) Neurofilament function and dysfunction: involvement in axonal growth and neuronal disease. Curr Opin Cell Biol 6:34–40PubMedCrossRef
go back to reference Lee CC, Winer JA (2008a) Connections of cat auditory cortex: I. Thalamocortical system. J Comp Neurol 507:1879–1900PubMedCrossRef Lee CC, Winer JA (2008a) Connections of cat auditory cortex: I. Thalamocortical system. J Comp Neurol 507:1879–1900PubMedCrossRef
go back to reference Lee CC, Winer JA (2008b) Connections of cat auditory cortex: II. Commissural system. J Comp Neurol 507:1901–1919PubMedCrossRef Lee CC, Winer JA (2008b) Connections of cat auditory cortex: II. Commissural system. J Comp Neurol 507:1901–1919PubMedCrossRef
go back to reference Lee CC, Winer JA (2008c) Connections of cat auditory cortex: III. Corticocortical system. J Comp Neurol 507:1920–1943PubMedCrossRef Lee CC, Winer JA (2008c) Connections of cat auditory cortex: III. Corticocortical system. J Comp Neurol 507:1920–1943PubMedCrossRef
go back to reference Luján R, Shigemoto R, Kulik A, Juiz JM (2004) Localization of the GABAB receptor 1a/b subunit relative to glutamatergic synapses in the dorsal cochlear nucleus of the rat. J Comp Neurol 475:36–46PubMedCrossRef Luján R, Shigemoto R, Kulik A, Juiz JM (2004) Localization of the GABAB receptor 1a/b subunit relative to glutamatergic synapses in the dorsal cochlear nucleus of the rat. J Comp Neurol 475:36–46PubMedCrossRef
go back to reference Luppino G, Hamed SB, Gamberini M, Matelli M, Galletti C (2005) Occipital (V6) and parietal (V6A) areas in the anterior wall of the parieto-occipital sulcus of the macaque: a cytoarchitectonic study. Eur J Neurosci 21:3056–3076PubMedCrossRef Luppino G, Hamed SB, Gamberini M, Matelli M, Galletti C (2005) Occipital (V6) and parietal (V6A) areas in the anterior wall of the parieto-occipital sulcus of the macaque: a cytoarchitectonic study. Eur J Neurosci 21:3056–3076PubMedCrossRef
go back to reference Malmierca MS (2003) The structure and physiology of the rat auditory system: an overview. Int Rev Neurobiol 56:147–211PubMedCrossRef Malmierca MS (2003) The structure and physiology of the rat auditory system: an overview. Int Rev Neurobiol 56:147–211PubMedCrossRef
go back to reference Mancardi G, Hart B, Roccatagliata L, Brok H, Giunti D, Bontrop R, Massacesi L, Capello E, Uccelli A (2001) Demyelination and axonal damage in a non-human primate model of multiple sclerosis. J Neurol Sci 184:41–49PubMedCrossRef Mancardi G, Hart B, Roccatagliata L, Brok H, Giunti D, Bontrop R, Massacesi L, Capello E, Uccelli A (2001) Demyelination and axonal damage in a non-human primate model of multiple sclerosis. J Neurol Sci 184:41–49PubMedCrossRef
go back to reference Mayhew TM, Gunderesen HJG (1996) ‘If you assume, you can make an ass out of u and me’: a decade of the dissector for stereological counting of particles in 3D space. J Anat 188:1–15PubMed Mayhew TM, Gunderesen HJG (1996) ‘If you assume, you can make an ass out of u and me’: a decade of the dissector for stereological counting of particles in 3D space. J Anat 188:1–15PubMed
go back to reference Mellott JG, Van der Gucht E, Lee CC, Carrasco A, Winer JA, Lomber SG (2010) Areas of cat auditory cortex as defined by neurofilament proteins expressing SMI-32. Hear Res 267:119–136PubMedCrossRef Mellott JG, Van der Gucht E, Lee CC, Carrasco A, Winer JA, Lomber SG (2010) Areas of cat auditory cortex as defined by neurofilament proteins expressing SMI-32. Hear Res 267:119–136PubMedCrossRef
go back to reference Merchán M, Aguilar LA, Lopez-Poveda EA, Malmierca MS (2005) The inferior colliculus of the rat: quantitative immunocytochemical study of GABA and glycine. Neuroscience 136:907–925PubMedCrossRef Merchán M, Aguilar LA, Lopez-Poveda EA, Malmierca MS (2005) The inferior colliculus of the rat: quantitative immunocytochemical study of GABA and glycine. Neuroscience 136:907–925PubMedCrossRef
go back to reference Molnár Z, Cheung AF (2006) Towards the classification of subpopulations of layer V pyramidal projection neurons. Neurosci Res 55:105–115PubMedCrossRef Molnár Z, Cheung AF (2006) Towards the classification of subpopulations of layer V pyramidal projection neurons. Neurosci Res 55:105–115PubMedCrossRef
go back to reference Moore MJ, Caspary DM (1983) Strychnine blocks binaural inhibition in lateral superior olivary neurons. J Neurosci 3:237–242PubMed Moore MJ, Caspary DM (1983) Strychnine blocks binaural inhibition in lateral superior olivary neurons. J Neurosci 3:237–242PubMed
go back to reference Moore JK, Moore RY (1971) A comparative study of the superior olivary complex in the primate brain. Folia Primatol (Basel) 16:35–51CrossRef Moore JK, Moore RY (1971) A comparative study of the superior olivary complex in the primate brain. Folia Primatol (Basel) 16:35–51CrossRef
go back to reference Morel A, Loup F, Magnin M, Jeanmonod D (2002) Neurochemical organization of the human basal ganglia: anatomofunctional territories defined by the distributions of calcium-binding proteins and SMI-32. J Comp Neurol 443:86–103PubMedCrossRef Morel A, Loup F, Magnin M, Jeanmonod D (2002) Neurochemical organization of the human basal ganglia: anatomofunctional territories defined by the distributions of calcium-binding proteins and SMI-32. J Comp Neurol 443:86–103PubMedCrossRef
go back to reference Oliver DL, Kuwada S, Yin TC, Haberly LB, Henkel CK (1991) Dendritic and axonal morphology of HRP-injected neurons in the inferior colliculus of the cat. J Comp Neurol 303:75–100PubMedCrossRef Oliver DL, Kuwada S, Yin TC, Haberly LB, Henkel CK (1991) Dendritic and axonal morphology of HRP-injected neurons in the inferior colliculus of the cat. J Comp Neurol 303:75–100PubMedCrossRef
go back to reference Paxinos G, Watson C (1998) The rat brain, 4th edn. Academic Press, New York Paxinos G, Watson C (1998) The rat brain, 4th edn. Academic Press, New York
go back to reference Paxinos G, Kus L, Ashwell KWS, Watson C (1998a) Chemoarchitectonic atlas of the rat brainstem. Academic Press, New York Paxinos G, Kus L, Ashwell KWS, Watson C (1998a) Chemoarchitectonic atlas of the rat brainstem. Academic Press, New York
go back to reference Paxinos G, Kus L, Ashwell KWS, Watson C (1998b) Chemoarchitectonic atlas of the rat forebrain. Academic Press, New York Paxinos G, Kus L, Ashwell KWS, Watson C (1998b) Chemoarchitectonic atlas of the rat forebrain. Academic Press, New York
go back to reference Polley DB, Read HL, Storace DA, Merzenich MM (2007) Multiparametric auditory receptive field organization across five cortical fields in the albino rat. J Neurophysiol 97:3621–3638PubMedCrossRef Polley DB, Read HL, Storace DA, Merzenich MM (2007) Multiparametric auditory receptive field organization across five cortical fields in the albino rat. J Neurophysiol 97:3621–3638PubMedCrossRef
go back to reference Prieto JJ, Winer JA (1999) Layer VI in cat primary auditory cortex: Golgi study and sublaminar origins of projection neurons. J Comp Neurol 404:332–358PubMedCrossRef Prieto JJ, Winer JA (1999) Layer VI in cat primary auditory cortex: Golgi study and sublaminar origins of projection neurons. J Comp Neurol 404:332–358PubMedCrossRef
go back to reference Rietzel HJ, Friauf E (1998) Neuron types in the rat lateral superior olive and developmental changes in the complexity of their dendritic arbors. J Comp Neurol 390:20–40PubMedCrossRef Rietzel HJ, Friauf E (1998) Neuron types in the rat lateral superior olive and developmental changes in the complexity of their dendritic arbors. J Comp Neurol 390:20–40PubMedCrossRef
go back to reference Riquelme R, Saldana E, Osen KK, Ottersen OP, Merchan MA (2001) Colocalization of GABA and glycine in the ventral nucleus of the lateral lemniscus in rat: an in situ hybridization and semiquantitative immunocytochemical study. J Comp Neurol 432:409–424PubMedCrossRef Riquelme R, Saldana E, Osen KK, Ottersen OP, Merchan MA (2001) Colocalization of GABA and glycine in the ventral nucleus of the lateral lemniscus in rat: an in situ hybridization and semiquantitative immunocytochemical study. J Comp Neurol 432:409–424PubMedCrossRef
go back to reference Saldaña E, Aparicio MA, Fuentes-Santamaría V, Berrebi AS (2009) Connections of the superior paraolivary nucleus of the rat: projections to the inferior colliculus. Neuroscience 163:372–387PubMedCrossRef Saldaña E, Aparicio MA, Fuentes-Santamaría V, Berrebi AS (2009) Connections of the superior paraolivary nucleus of the rat: projections to the inferior colliculus. Neuroscience 163:372–387PubMedCrossRef
go back to reference Sanes DH, Friauf E (2000) Development and influence of inhibition in the lateral superior olivary nucleus. Hear Res 147:46–58PubMedCrossRef Sanes DH, Friauf E (2000) Development and influence of inhibition in the lateral superior olivary nucleus. Hear Res 147:46–58PubMedCrossRef
go back to reference Smith PH, Joris PX, Yin TC (1998) Anatomy and physiology of principal cells of the medial nucleus of the trapezoid body (MNTB) of the cat. J Neurophysiol 79:3127–3142PubMed Smith PH, Joris PX, Yin TC (1998) Anatomy and physiology of principal cells of the medial nucleus of the trapezoid body (MNTB) of the cat. J Neurophysiol 79:3127–3142PubMed
go back to reference Soares JG, Rosado De Castro PH, Fiorani M, Nascimento-Silva S, Gattass R (2008) Distribution of neurofilament proteins in the lateral geniculate nucleus, primary visual cortex, and area MT of adult Cebus monkeys. J Comp Neurol 508:605–614PubMedCrossRef Soares JG, Rosado De Castro PH, Fiorani M, Nascimento-Silva S, Gattass R (2008) Distribution of neurofilament proteins in the lateral geniculate nucleus, primary visual cortex, and area MT of adult Cebus monkeys. J Comp Neurol 508:605–614PubMedCrossRef
go back to reference Sommer I, Lingenhöhl K, Friauf E (1993) Principal cells of the rat medial nucleus of the trapezoid body: an intracellular in vivo study of their physiology and morphology. Exp Brain Res 95:223–239PubMedCrossRef Sommer I, Lingenhöhl K, Friauf E (1993) Principal cells of the rat medial nucleus of the trapezoid body: an intracellular in vivo study of their physiology and morphology. Exp Brain Res 95:223–239PubMedCrossRef
go back to reference Sternberger LA, Sternberger NH (1983) Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ. Proc Natl Acad Sci USA 80:6126–6130PubMedCrossRef Sternberger LA, Sternberger NH (1983) Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ. Proc Natl Acad Sci USA 80:6126–6130PubMedCrossRef
go back to reference Taschenberger H, von Gersdorff H (2000) Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci 20:9162–9173PubMed Taschenberger H, von Gersdorff H (2000) Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci 20:9162–9173PubMed
go back to reference Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mörk S, Bö L (1998) Axonal transection in the lesions of multiple sclerosis. New Engl J Med 338:278–285PubMedCrossRef Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mörk S, Bö L (1998) Axonal transection in the lesions of multiple sclerosis. New Engl J Med 338:278–285PubMedCrossRef
go back to reference Tsang YM, Chiong F, Kuznetsov D, Kasarskis E, Geula C (2000) Motor neurons are rich in non-phosphorylated neurofilaments: crossspecies comparison and alterations in ALS. Brain Res 861:45–58PubMedCrossRef Tsang YM, Chiong F, Kuznetsov D, Kasarskis E, Geula C (2000) Motor neurons are rich in non-phosphorylated neurofilaments: crossspecies comparison and alterations in ALS. Brain Res 861:45–58PubMedCrossRef
go back to reference Ueyama T, Sato K, Kakimoto S, Houtani T, Sakuma S, Ohishi H, Kase M, Sugimoto T (1999) Comparative distribution of GABAergic and peptide-containing neurons in the lateral lemniscal nuclei of the rat. Brain Res 849:220–225PubMedCrossRef Ueyama T, Sato K, Kakimoto S, Houtani T, Sakuma S, Ohishi H, Kase M, Sugimoto T (1999) Comparative distribution of GABAergic and peptide-containing neurons in the lateral lemniscal nuclei of the rat. Brain Res 849:220–225PubMedCrossRef
go back to reference Van De Werd HJ, Uylings HB (2008) The rat orbital and agranular insular prefrontal cortical areas: a cytoarchitectonic and chemoarchitectonic study. Brain Struct Funct 212:387–401CrossRef Van De Werd HJ, Uylings HB (2008) The rat orbital and agranular insular prefrontal cortical areas: a cytoarchitectonic and chemoarchitectonic study. Brain Struct Funct 212:387–401CrossRef
go back to reference Van der Gucht E, Vandesande F, Arckens L (2001) Neurofilament protein: a selective marker for the architectonic parcellation of the visual cortex in adult cat brain. J Comp Neurol 441:345–368PubMedCrossRef Van der Gucht E, Vandesande F, Arckens L (2001) Neurofilament protein: a selective marker for the architectonic parcellation of the visual cortex in adult cat brain. J Comp Neurol 441:345–368PubMedCrossRef
go back to reference Vickers JC, Costa M (1992) The neurofilament triplet is present in distinct subpopulations of neurons in the central nervous system of the guinea-pig. Neuroscience 49:73–100PubMedCrossRef Vickers JC, Costa M (1992) The neurofilament triplet is present in distinct subpopulations of neurons in the central nervous system of the guinea-pig. Neuroscience 49:73–100PubMedCrossRef
go back to reference Vickers JC, Delacourte A, Morrison JH (1992) Progressive transformation of the cytoskeleton associated with normal aging and Alzheimer’s disease. Brain Res 594:273–278PubMedCrossRef Vickers JC, Delacourte A, Morrison JH (1992) Progressive transformation of the cytoskeleton associated with normal aging and Alzheimer’s disease. Brain Res 594:273–278PubMedCrossRef
go back to reference Voelker CC, Garin N, Taylor JS, Gähwiler BH, Hornung JP, Molnár Z (2004) Selective neurofilament (SMI-32, FNP-7 and N200) expression in subpopulations of layer V pyramidal neurons in vivo and in vitro. Cereb Cortex 14:1276–1286PubMedCrossRef Voelker CC, Garin N, Taylor JS, Gähwiler BH, Hornung JP, Molnár Z (2004) Selective neurofilament (SMI-32, FNP-7 and N200) expression in subpopulations of layer V pyramidal neurons in vivo and in vitro. Cereb Cortex 14:1276–1286PubMedCrossRef
go back to reference Von Gersdorff H, Borst JG (2002) Short-term plasticity at the calyx of held. Nat Rev Neurosci 3:53–64CrossRef Von Gersdorff H, Borst JG (2002) Short-term plasticity at the calyx of held. Nat Rev Neurosci 3:53–64CrossRef
go back to reference West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482–497PubMedCrossRef West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482–497PubMedCrossRef
go back to reference Winer JA, Larue DT (1996) Evolution of GABAergic circuitry in the mammalian medial geniculate body. Proc Natl Acad Sci USA 93:3083–3087PubMedCrossRef Winer JA, Larue DT (1996) Evolution of GABAergic circuitry in the mammalian medial geniculate body. Proc Natl Acad Sci USA 93:3083–3087PubMedCrossRef
go back to reference Winer JA, Prieto JJ (2001) Layer V in cat primary auditory cortex (AI): cellular architecture and identification of projection neurons. J Comp Neurol 434:379–412PubMedCrossRef Winer JA, Prieto JJ (2001) Layer V in cat primary auditory cortex (AI): cellular architecture and identification of projection neurons. J Comp Neurol 434:379–412PubMedCrossRef
go back to reference Winer JA, Kelly JB, Larue DT (1999) Neural architecture of the rat medial geniculate body. Hear Res 130:19–41PubMedCrossRef Winer JA, Kelly JB, Larue DT (1999) Neural architecture of the rat medial geniculate body. Hear Res 130:19–41PubMedCrossRef
go back to reference Wong P, Kaas JH (2008) Architectonic subdivisions of neocortex in the gray squirrel (Sciurus carolinensis). Anat Rec (Hoboken) 291:1301–1333CrossRef Wong P, Kaas JH (2008) Architectonic subdivisions of neocortex in the gray squirrel (Sciurus carolinensis). Anat Rec (Hoboken) 291:1301–1333CrossRef
go back to reference Wong P, Kaas JH (2009) Architectonic subdivisions of neocortex in the tree shrew (Tupaia belangeri). Anat Rec (Hoboken) 292:994–1027 Wong P, Kaas JH (2009) Architectonic subdivisions of neocortex in the tree shrew (Tupaia belangeri). Anat Rec (Hoboken) 292:994–1027
go back to reference Wu SH, Kelly JB (1991) Physiological properties of neurons in the mouse superior olive: membrane characteristics and postsynaptic responses studied in vitro. J Neurophysiol 65:230–246PubMed Wu SH, Kelly JB (1991) Physiological properties of neurons in the mouse superior olive: membrane characteristics and postsynaptic responses studied in vitro. J Neurophysiol 65:230–246PubMed
go back to reference Wu SH, Kelly JB (1993) Response of neurons in the lateral superior olive and medial nucleus of the trapezoid body to repetitive stimulation: intracellular and extracellular recordings from mouse brain slice. Hear Res 68:189–201PubMedCrossRef Wu SH, Kelly JB (1993) Response of neurons in the lateral superior olive and medial nucleus of the trapezoid body to repetitive stimulation: intracellular and extracellular recordings from mouse brain slice. Hear Res 68:189–201PubMedCrossRef
go back to reference Wu SH, Kelly JB (1995) Inhibition in the superior olivary complex: pharmacological evidence from mouse brain slice. J Neurophysiol 73:256–269PubMed Wu SH, Kelly JB (1995) Inhibition in the superior olivary complex: pharmacological evidence from mouse brain slice. J Neurophysiol 73:256–269PubMed
go back to reference Zhang DX, Li L, Kelly JB, Wu SH (1998) GABAergic projections from the lateral lemniscus to the inferior colliculus of the rat. Hear Res 117:1–12PubMedCrossRef Zhang DX, Li L, Kelly JB, Wu SH (1998) GABAergic projections from the lateral lemniscus to the inferior colliculus of the rat. Hear Res 117:1–12PubMedCrossRef
go back to reference Zilles K (1985) The cortex of the rat. A stereotaxic atlas. Springer, Berlin Zilles K (1985) The cortex of the rat. A stereotaxic atlas. Springer, Berlin
Metadata
Title
Distribution of SMI-32-immunoreactive neurons in the central auditory system of the rat
Authors
Ladislav Ouda
Rastislav Druga
Josef Syka
Publication date
01-01-2012
Publisher
Springer-Verlag
Published in
Brain Structure and Function / Issue 1/2012
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-011-0329-6

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