Skip to main content
Top
Published in: Brain Structure and Function 9/2016

01-12-2016 | Original Article

Differential morphology of the superior olivary complex of Meriones unguiculatus and Monodelphis domestica revealed by calcium-binding proteins

Authors: I. Bazwinsky-Wutschke, W. Härtig, R. Kretzschmar, R. Rübsamen

Published in: Brain Structure and Function | Issue 9/2016

Login to get access

Abstract

In mammals, the superior olivary complex (SOC) of the brainstem is composed of nuclei that integrate afferent auditory originating from both ears. Here, the expression of different calcium-binding proteins in subnuclei of the SOC was studied in distantly related mammals, the Mongolian gerbil (Meriones unguiculatus) and the gray short-tailed opossum (Monodelphis domestica) to get a better understanding of the basal nuclear organization of the SOC. Combined immunofluorescence labeling of the calcium-binding proteins (CaBPs) parvalbumin, calbindin-D28k, and calretinin as well as pan-neuronal markers displayed characteristic distribution patterns highlighting details of neuronal architecture of SOC nuclei. Parvalbumin was found in almost all neurons of SOC nuclei in both species, while calbindin and calretinin were restricted to specific cell types and axonal terminal fields. In both species, calbindin displayed a ubiquitous and mostly selective distribution in neurons of the medial nucleus of trapezoid body (MNTB) including their terminal axonal fields in different SOC targets. In Meriones, calretinin and calbindin showed non-overlapping expression patterns in neuron somata and terminal fields throughout the SOC. In Monodelphis, co-expression of calbindin and calretinin was observed in the MNTB, and hence both CaBPs were also co-localized in terminal fields within the adjacent SOC nuclei. The distribution patterns of CaBPs in both species are discussed with respect to the intrinsic neuronal SOC circuits as part of the auditory brainstem system that underlie the binaural integrative processing of acoustic signals as the basis for localization and discrimination of auditory objects.
Literature
go back to reference Adams JC, Mugnaini E (1990) Immunocytochemical evidence for inhibitory and disinhibitory circuits in the superior olive. Hear Res 49:281–298PubMedCrossRef Adams JC, Mugnaini E (1990) Immunocytochemical evidence for inhibitory and disinhibitory circuits in the superior olive. Hear Res 49:281–298PubMedCrossRef
go back to reference Ahlfeld J, Mustari M, Horn AK (2011) Sources of calretinin inputs to motoneurons of extraocular muscles involved in upgaze. Ann N Y Acad Sci 1233:91–99PubMedPubMedCentralCrossRef Ahlfeld J, Mustari M, Horn AK (2011) Sources of calretinin inputs to motoneurons of extraocular muscles involved in upgaze. Ann N Y Acad Sci 1233:91–99PubMedPubMedCentralCrossRef
go back to reference Aitkin L (1996) The anatomy of the cochlear nuclei and superior olivary complex of arboreal australian marsupials. Brain Behav Evol 48:103–114PubMedCrossRef Aitkin L (1996) The anatomy of the cochlear nuclei and superior olivary complex of arboreal australian marsupials. Brain Behav Evol 48:103–114PubMedCrossRef
go back to reference Aitkin LM, Byers M, Nelson JE (1986) Brain stem auditory nuclei and their connections in a carnivorous marsupial, the northern native cat (Dasyurus hallucatus). Brain Behav Evol 29:1–16PubMedCrossRef Aitkin LM, Byers M, Nelson JE (1986) Brain stem auditory nuclei and their connections in a carnivorous marsupial, the northern native cat (Dasyurus hallucatus). Brain Behav Evol 29:1–16PubMedCrossRef
go back to reference Aitkin L, Cochran S, Frost S, Martsi-McClintock A, Masterton B (1997) Features of the auditory development of the short-tailed Brazilian opossum, Monodelphis domestica: evoked responses, neonatal vocalizations and synapses in the inferior colliculus. Hear Res 113:69–75PubMedCrossRef Aitkin L, Cochran S, Frost S, Martsi-McClintock A, Masterton B (1997) Features of the auditory development of the short-tailed Brazilian opossum, Monodelphis domestica: evoked responses, neonatal vocalizations and synapses in the inferior colliculus. Hear Res 113:69–75PubMedCrossRef
go back to reference Andressen C, Blümcke I, Celio MR (1993) Calcium-binding proteins: selective markers of nerve cells. Cell Tissue Res 271:181–208PubMedCrossRef Andressen C, Blümcke I, Celio MR (1993) Calcium-binding proteins: selective markers of nerve cells. Cell Tissue Res 271:181–208PubMedCrossRef
go back to reference Baimbridge KG, Celio MR, Rogers JH (1992) Calcium-binding proteins in the nervous system. Trends Neurosci 15:303–308PubMedCrossRef Baimbridge KG, Celio MR, Rogers JH (1992) Calcium-binding proteins in the nervous system. Trends Neurosci 15:303–308PubMedCrossRef
go back to reference Banks MI, Smith PH (1992) Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body. J Neurosci 12:2819–2837PubMed Banks MI, Smith PH (1992) Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body. J Neurosci 12:2819–2837PubMed
go back to reference Barnes-Davies M, Barker MC, Osmani F, Forsythe ID (2004) Kv1 currents mediate a gradient of principal neuron excitability across the tonotopic axis in the rat lateral superior olive. Eur J Neurosci 19:325–333PubMedCrossRef Barnes-Davies M, Barker MC, Osmani F, Forsythe ID (2004) Kv1 currents mediate a gradient of principal neuron excitability across the tonotopic axis in the rat lateral superior olive. Eur J Neurosci 19:325–333PubMedCrossRef
go back to reference Bazwinsky I, Hilbig H, Bidmon H-J, 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 H-J, 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 Bazwinsky I, Bidmon H-J, Zilles K, Hilbig H (2005) Characterization of the rhesus monkey superior olivary complex by calcium binding proteins and synaptophysin. J Anat 207:745–761PubMedPubMedCentralCrossRef Bazwinsky I, Bidmon H-J, Zilles K, Hilbig H (2005) Characterization of the rhesus monkey superior olivary complex by calcium binding proteins and synaptophysin. J Anat 207:745–761PubMedPubMedCentralCrossRef
go back to reference Bazwinsky I, Härtig W, Rübsamen R (2008) Characterization of cochlear nucleus principal cells of Meriones unguiculatus and Monodelphis domestica by use of calcium-binding protein immunolabeling. J Chem Neuroanat 35:158–174PubMedCrossRef Bazwinsky I, Härtig W, Rübsamen R (2008) Characterization of cochlear nucleus principal cells of Meriones unguiculatus and Monodelphis domestica by use of calcium-binding protein immunolabeling. J Chem Neuroanat 35:158–174PubMedCrossRef
go back to reference Caicedo A, d’Aldin C, Puel JL, Eybalin M (1996) Distribution of calcium binding protein immunoreactivities in the guinea pig auditory brainstem. Anat Embryol 194:465–478PubMedCrossRef Caicedo A, d’Aldin C, Puel JL, Eybalin M (1996) Distribution of calcium binding protein immunoreactivities in the guinea pig auditory brainstem. Anat Embryol 194:465–478PubMedCrossRef
go back to reference Cant NB (1984) The fine structure of the lateral superior olivary nucleus of the cat. J Comp Neurol 227:63–77PubMedCrossRef Cant NB (1984) The fine structure of the lateral superior olivary nucleus of the cat. J Comp Neurol 227:63–77PubMedCrossRef
go back to reference Cant NB (1991) Projections to the lateral and medial superior olivary nuclei from the spherical and globular bushy cells of the anteroventral cochlear nucleus. In: Altschuler RA, Bobbin RP, Clopton BM, Hoffmann DW (eds) Neurobiology of hearing: the central auditory system. Raven Press, New York, pp 99–119 Cant NB (1991) Projections to the lateral and medial superior olivary nuclei from the spherical and globular bushy cells of the anteroventral cochlear nucleus. In: Altschuler RA, Bobbin RP, Clopton BM, Hoffmann DW (eds) Neurobiology of hearing: the central auditory system. Raven Press, New York, pp 99–119
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 Cant NB, Casseday JH (1986) Projections from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei. J Comp Neurol 247:457–476PubMedCrossRef Cant NB, Casseday JH (1986) Projections from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei. J Comp Neurol 247:457–476PubMedCrossRef
go back to reference Cant NB, Hyson RL (1992) Projections from the lateral nucleus of the trapezoid body to the medial superior olivary nucleus in the gerbil. Hear Res 58:26–34PubMedCrossRef Cant NB, Hyson RL (1992) Projections from the lateral nucleus of the trapezoid body to the medial superior olivary nucleus in the gerbil. Hear Res 58:26–34PubMedCrossRef
go back to reference Celio MR, Baier W, Schärer L, de Viragh PA, Gerday CH (1988) Monoclonal antibodies directed against the calcium binding protein parvalbumin. Cell Calcium 9:81–86PubMedCrossRef Celio MR, Baier W, Schärer L, de Viragh PA, Gerday CH (1988) Monoclonal antibodies directed against the calcium binding protein parvalbumin. Cell Calcium 9:81–86PubMedCrossRef
go back to reference Celio MR, Baier W, Schärer L, Gregersen HJ, de Viragh PA, Norman AW (1990) Monoclonal antibodies directed against the calcium binding protein calbindin D-28k. Cell Calcium 11:599–602PubMedCrossRef Celio MR, Baier W, Schärer L, Gregersen HJ, de Viragh PA, Norman AW (1990) Monoclonal antibodies directed against the calcium binding protein calbindin D-28k. Cell Calcium 11:599–602PubMedCrossRef
go back to reference Couchman K, Grothe B, Felmy F (2012) Functional localization of neurotransmitter receptors and synaptic inputs to mature neurons of the medial superior olive. J Neurophysiol 107:1186–1198PubMedCrossRef Couchman K, Grothe B, Felmy F (2012) Functional localization of neurotransmitter receptors and synaptic inputs to mature neurons of the medial superior olive. J Neurophysiol 107:1186–1198PubMedCrossRef
go back to reference Englitz B, Tolnai S, Typlt M, Kopp-Scheinpflug C, Jost J, Rübsamen R (2009) Reliability of Signal transmission at the giant synapses of Held in vivo. PLoS One 4:e7014PubMedPubMedCentralCrossRef Englitz B, Tolnai S, Typlt M, Kopp-Scheinpflug C, Jost J, Rübsamen R (2009) Reliability of Signal transmission at the giant synapses of Held in vivo. PLoS One 4:e7014PubMedPubMedCentralCrossRef
go back to reference Felmy F, Schneggenburger R (2004) Developmental expression of the Ca2+-binding proteins calretinin and parvalbumin at the calyx of held of rats and mice. Eur J Neurosci 20:1473–1482PubMedCrossRef Felmy F, Schneggenburger R (2004) Developmental expression of the Ca2+-binding proteins calretinin and parvalbumin at the calyx of held of rats and mice. Eur J Neurosci 20:1473–1482PubMedCrossRef
go back to reference Finlayson PG, Caspary DM (1991) Low-frequency neurons in the lateral superior olive exhibit phase-sensitive binaural inhibition. J Neurophysiol 65:598–605PubMed Finlayson PG, Caspary DM (1991) Low-frequency neurons in the lateral superior olive exhibit phase-sensitive binaural inhibition. J Neurophysiol 65:598–605PubMed
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 (1993) Transient Appearance of Calbindin-D28k-positive neurons in the superior olivary complex of developing rats. J Comp Neurol 334:59–74PubMedCrossRef Friauf E (1993) Transient Appearance of Calbindin-D28k-positive neurons in the superior olivary complex of developing rats. J Comp Neurol 334:59–74PubMedCrossRef
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 Frisina RD, Zettel ML, Kelley PE, Walton JP (1995) Distribution of calbindin D-28k immunoreactivity in the cochlear nucleus of the young adult chinchilla. Hear Res 85:53–68PubMedCrossRef Frisina RD, Zettel ML, Kelley PE, Walton JP (1995) Distribution of calbindin D-28k immunoreactivity in the cochlear nucleus of the young adult chinchilla. Hear Res 85:53–68PubMedCrossRef
go back to reference Frost SB, Masterton RB (1994) Hearing in primitive mammals: Monodelphis domestica and Marmosa elegans. Hear Res 76:67–72PubMedCrossRef Frost SB, Masterton RB (1994) Hearing in primitive mammals: Monodelphis domestica and Marmosa elegans. Hear Res 76:67–72PubMedCrossRef
go back to reference Gallyas F, Wolff JR, Böttcher H, Záborszky L (1980) A reliable method for demonstrating axonal degeneration shortly after axotomy. Stain Technol 55:291–297PubMedCrossRef Gallyas F, Wolff JR, Böttcher H, Záborszky L (1980) A reliable method for demonstrating axonal degeneration shortly after axotomy. Stain Technol 55:291–297PubMedCrossRef
go back to reference Gibb R, Kolb B (1998) A method for vibratome sectioning of Golgi–Cox stained whole rat brain. J Neurosci Methods 79:1–4PubMedCrossRef Gibb R, Kolb B (1998) A method for vibratome sectioning of Golgi–Cox stained whole rat brain. J Neurosci Methods 79:1–4PubMedCrossRef
go back to reference Glaser EM, Van der Loos H (1981) Analysis of thick brain sections by obverse-reverse computer microscopy: application of a new, high clarity Golgi–Nissl stain. J Neurosci Methods 4:117–125PubMedCrossRef Glaser EM, Van der Loos H (1981) Analysis of thick brain sections by obverse-reverse computer microscopy: application of a new, high clarity Golgi–Nissl stain. J Neurosci Methods 4:117–125PubMedCrossRef
go back to reference Glendenning KK, Masterton RB (1998) Comparative morphometry of mammalian central auditory systems: variation in nuclei and form of the ascending system. Brain Behav Evol 51:59–89PubMedCrossRef Glendenning KK, Masterton RB (1998) Comparative morphometry of mammalian central auditory systems: variation in nuclei and form of the ascending system. Brain Behav Evol 51:59–89PubMedCrossRef
go back to reference Glendenning KK, Brunso-Bechtold JK, Thompson GC, Masterton RB (1981) Ascending auditory afferents to the nuclei of the lateral lemniscus. J Comp Neurol 197:673–703PubMedCrossRef Glendenning KK, Brunso-Bechtold JK, Thompson GC, Masterton RB (1981) Ascending auditory afferents to the nuclei of the lateral lemniscus. J Comp Neurol 197:673–703PubMedCrossRef
go back to reference Glendenning KK, Hutson KA, Nudo RJ, Masterton RB (1985) Acoustic chiasm II: Anatomical basis of binaurality in lateral superior olive of cat. J Comp Neurol 232:261–285PubMedCrossRef Glendenning KK, Hutson KA, Nudo RJ, Masterton RB (1985) Acoustic chiasm II: Anatomical basis of binaurality in lateral superior olive of cat. J Comp Neurol 232:261–285PubMedCrossRef
go back to reference Glendenning KK, Masterton RB, Baker BN, Wenthold RJ (1991) Acoustic chiasm III: nature, distribution, and sources of afferents to the lateral superior olive in the cat. J Comp Neurol 310:377–400PubMedCrossRef Glendenning KK, Masterton RB, Baker BN, Wenthold RJ (1991) Acoustic chiasm III: nature, distribution, and sources of afferents to the lateral superior olive in the cat. J Comp Neurol 310:377–400PubMedCrossRef
go back to reference Grothe B (2000) The evolution of temporal processing in the medial superior olive, an auditory brainstem structure. Prog Neurobiol 61:581–610PubMedCrossRef Grothe B (2000) The evolution of temporal processing in the medial superior olive, an auditory brainstem structure. Prog Neurobiol 61:581–610PubMedCrossRef
go back to reference Grothe B (2003) New roles for synaptic inhibition in sound localization. Nat Rev Neurosci 4:540–550PubMedCrossRef Grothe B (2003) New roles for synaptic inhibition in sound localization. Nat Rev Neurosci 4:540–550PubMedCrossRef
go back to reference Grothe B, Pecka M, McAlpine D (2010) Mechanisms of sound localization in mammals. Physiol Rev 90:983–1012PubMedCrossRef Grothe B, Pecka M, McAlpine D (2010) Mechanisms of sound localization in mammals. Physiol Rev 90:983–1012PubMedCrossRef
go back to reference Guinan JJ Jr, Guinan SS, Norris BE (1972a) Single auditory units in the olivary complex I. Responses to sounds and classifications based on physiological properties. Int J Neurosci 4:101–120CrossRef Guinan JJ Jr, Guinan SS, Norris BE (1972a) Single auditory units in the olivary complex I. Responses to sounds and classifications based on physiological properties. Int J Neurosci 4:101–120CrossRef
go back to reference Guinan JJ Jr, Norris BE, Guinan SS (1972b) Single auditory units in the olivary complex II. Superior olivary complex II: location of unit categories and tonotopic organization. Int J Neurosci 4:147–166CrossRef Guinan JJ Jr, Norris BE, Guinan SS (1972b) Single auditory units in the olivary complex II. Superior olivary complex II: location of unit categories and tonotopic organization. Int J Neurosci 4:147–166CrossRef
go back to reference Heizmann CW, Braun K (1995) Calcium regulation by calcium-binding proteins in neurodegenerative disorders. Springer, HeidelbergCrossRef Heizmann CW, Braun K (1995) Calcium regulation by calcium-binding proteins in neurodegenerative disorders. Springer, HeidelbergCrossRef
go back to reference Helfert RH, Schwartz IR (1987) Morphological features of five neuronal classes in the gerbil lateral superior olive. Am J Anat 179:55–69PubMedCrossRef Helfert RH, Schwartz IR (1987) Morphological features of five neuronal classes in the gerbil lateral superior olive. Am J Anat 179:55–69PubMedCrossRef
go back to reference Johnston J, Forsythe ID, Kopp-Scheinpflug C (2010) Going native: voltage-gated potassium channels controlling neuronal excitability. J Physiol 588:3187–3200PubMedPubMedCentralCrossRef Johnston J, Forsythe ID, Kopp-Scheinpflug C (2010) Going native: voltage-gated potassium channels controlling neuronal excitability. J Physiol 588:3187–3200PubMedPubMedCentralCrossRef
go back to reference Kägi U, Berchtold MW, Heizmann CW (1987) Ca2+-binding parvalbumin in rat testis. J Biol Chem 262:7314–7320PubMed Kägi U, Berchtold MW, Heizmann CW (1987) Ca2+-binding parvalbumin in rat testis. J Biol Chem 262:7314–7320PubMed
go back to reference Kandler K, Friauf E (1995) Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats. J Neurosci 15:6890–6904PubMed Kandler K, Friauf E (1995) Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats. J Neurosci 15:6890–6904PubMed
go back to reference Keast A (1977) Historical biogeography of the marsupials. In: Stonehouse G, Gilmore D (eds) The biology of marsupials. Mac-Millan, London, pp 69–95CrossRef Keast A (1977) Historical biogeography of the marsupials. In: Stonehouse G, Gilmore D (eds) The biology of marsupials. Mac-Millan, London, pp 69–95CrossRef
go back to reference Kelley PE, Frisina RD, Zettel ML, Walton JP (1992) Differential calbindin-like immunoreactivity in the brain stem auditory system of the chinchilla. J Comp Neurol 319:196–212CrossRef Kelley PE, Frisina RD, Zettel ML, Walton JP (1992) Differential calbindin-like immunoreactivity in the brain stem auditory system of the chinchilla. J Comp Neurol 319:196–212CrossRef
go back to reference Kevetter GA, Leonard RB (1997) Use of calcium-binding proteins to map inputs in vestibular nuclei of the gerbil. J Comp Neurol 386:317–327PubMedCrossRef Kevetter GA, Leonard RB (1997) Use of calcium-binding proteins to map inputs in vestibular nuclei of the gerbil. J Comp Neurol 386:317–327PubMedCrossRef
go back to reference Kil J, Kageyama GH, Semple MN, Kitzes LM (1995) Development of ventral cochlear nucleus projections to the superior olivary complex in gerbil. J Comp Neurol 353:317–340PubMedCrossRef Kil J, Kageyama GH, Semple MN, Kitzes LM (1995) Development of ventral cochlear nucleus projections to the superior olivary complex in gerbil. J Comp Neurol 353:317–340PubMedCrossRef
go back to reference Korada S, Schwartz IR (2000) Calcium binding proteins and the AMPA glutamate receptor subunits in gerbil cochlear nucleus. Hear Res 140:23–37PubMedCrossRef Korada S, Schwartz IR (2000) Calcium binding proteins and the AMPA glutamate receptor subunits in gerbil cochlear nucleus. Hear Res 140:23–37PubMedCrossRef
go back to reference Kulesza RJ Jr (2014) Characterization of human auditory brainstem circuits by calcium-binding protein immunohistochemistry. Neuroscience 258:318–331PubMedCrossRef Kulesza RJ Jr (2014) Characterization of human auditory brainstem circuits by calcium-binding protein immunohistochemistry. Neuroscience 258:318–331PubMedCrossRef
go back to reference Kulesza RJ Jr, Kadner A, Berrebi AS (2007) Distinct roles for glycine and GABA in shaping the response properties of neurons in the superior paraolivary nucleus of the rat. J Neurophysiol 97:1610–1620PubMedCrossRef Kulesza RJ Jr, Kadner A, Berrebi AS (2007) Distinct roles for glycine and GABA in shaping the response properties of neurons in the superior paraolivary nucleus of the rat. J Neurophysiol 97:1610–1620PubMedCrossRef
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 Lohmann C, Friauf E (1996) Distribution of the calcium-binding proteins parvalbumin and calretinin in the auditory brainstem of adult and developing rats. J Comp Neurol 367:90–109PubMedCrossRef Lohmann C, Friauf E (1996) Distribution of the calcium-binding proteins parvalbumin and calretinin in the auditory brainstem of adult and developing rats. J Comp Neurol 367:90–109PubMedCrossRef
go back to reference Marangos PJ, Schmechel DE (1987) Neuron specific enolase, a clinically useful marker for neurons and neuroendocrine cells. Annu Rev Neurosci 10:269–295PubMedCrossRef Marangos PJ, Schmechel DE (1987) Neuron specific enolase, a clinically useful marker for neurons and neuroendocrine cells. Annu Rev Neurosci 10:269–295PubMedCrossRef
go back to reference Matsubara JA (1990) Calbindin D-28k immunoreactivity in the cat’s superior olivary complex. Brain Res 508:353–357PubMedCrossRef Matsubara JA (1990) Calbindin D-28k immunoreactivity in the cat’s superior olivary complex. Brain Res 508:353–357PubMedCrossRef
go back to reference McAlpine D, Grothe B (2003) Sound localization and delay lines-do mammals fit the model? Trends Neurosci 26:347–350PubMedCrossRef McAlpine D, Grothe B (2003) Sound localization and delay lines-do mammals fit the model? Trends Neurosci 26:347–350PubMedCrossRef
go back to reference Morest DK (1968a) The collateral system of the medial nucleus of the trapezoid body of the cat, its neuronal architecture and relation to the olivo-cochlear bundle. Brain Res 9:288–311PubMedCrossRef Morest DK (1968a) The collateral system of the medial nucleus of the trapezoid body of the cat, its neuronal architecture and relation to the olivo-cochlear bundle. Brain Res 9:288–311PubMedCrossRef
go back to reference Morest DK (1968b) The growth of synaptic endings in the mammalian brain: a study of the calyces of the trapezoid body. Brain Res 127:201–220 Morest DK (1968b) The growth of synaptic endings in the mammalian brain: a study of the calyces of the trapezoid body. Brain Res 127:201–220
go back to reference Morest DK, Winer JA (1986) The comparative anatomy of neurons: homologous neurons in the medial geniculate body of the opossum and the cat. Adv Anat Embryol Cell Biol 97:1–96PubMedCrossRef Morest DK, Winer JA (1986) The comparative anatomy of neurons: homologous neurons in the medial geniculate body of the opossum and the cat. Adv Anat Embryol Cell Biol 97:1–96PubMedCrossRef
go back to reference Myoga MH, Lehnert S, Leibold C, Felmy F, Grothe B (2014) Glycinergic inhibition tunes coincidence detection in the auditory brainstem. Nat Commun 5:3790PubMedPubMedCentralCrossRef Myoga MH, Lehnert S, Leibold C, Felmy F, Grothe B (2014) Glycinergic inhibition tunes coincidence detection in the auditory brainstem. Nat Commun 5:3790PubMedPubMedCentralCrossRef
go back to reference Oertel D (1999) The role of timing in the brain stem auditory of developing auditory brainstem circuits. Nat Neurosci 12:711–717 Oertel D (1999) The role of timing in the brain stem auditory of developing auditory brainstem circuits. Nat Neurosci 12:711–717
go back to reference Reimer K (1995) Hearing in the marsupial Monodelphis domestica as determined by auditory-evoked brainstem responses. Audiology 34:334–342PubMedCrossRef Reimer K (1995) Hearing in the marsupial Monodelphis domestica as determined by auditory-evoked brainstem responses. Audiology 34:334–342PubMedCrossRef
go back to reference Rogers JH (1987) Calretinin: a gene for a novel calcium-binding protein expressed principally in neurons. J Cell Biol 105:1343–1353PubMedCrossRef Rogers JH (1987) Calretinin: a gene for a novel calcium-binding protein expressed principally in neurons. J Cell Biol 105:1343–1353PubMedCrossRef
go back to reference Rothman JS, Manis PB (2003) The roles potassium currents play in regulating the electrical activity of ventral cochlear nucleus neurons. J Neurophysiol 89:3097–3113PubMedCrossRef Rothman JS, Manis PB (2003) The roles potassium currents play in regulating the electrical activity of ventral cochlear nucleus neurons. J Neurophysiol 89:3097–3113PubMedCrossRef
go back to reference Rowe M (1990) Organization of the cerebral cortex in monotremes and marsupials. In: Jones EG, Peters A (eds) cerebral cortex, vol 8B., Comparative structure and evolution of cerebral cortexPlenum Press, New York, pp 263–334CrossRef Rowe M (1990) Organization of the cerebral cortex in monotremes and marsupials. In: Jones EG, Peters A (eds) cerebral cortex, vol 8B., Comparative structure and evolution of cerebral cortexPlenum Press, New York, pp 263–334CrossRef
go back to reference Sanes DH, Merickel M, Rubel EW (1989) Evidence for an alteration of the tonotopic map in the gerbil cochlea during development. J Comp Neurol 279:436–444PubMedCrossRef Sanes DH, Merickel M, Rubel EW (1989) Evidence for an alteration of the tonotopic map in the gerbil cochlea during development. J Comp Neurol 279:436–444PubMedCrossRef
go back to reference Sanes DH, Goldstein NA, Ostad M, Hillman DE (1990) Dendritic morphology of central auditory neurons correlates with their tonotopic position. J Comp Neurol 294(443–444):5 Sanes DH, Goldstein NA, Ostad M, Hillman DE (1990) Dendritic morphology of central auditory neurons correlates with their tonotopic position. J Comp Neurol 294(443–444):5
go back to reference Schofield BR (1994) Projections to the cochlear nuclei from principal cells in the medial nucleus of the trapezoid body in guinea pigs. J Comp Neurol 344:83–100PubMedCrossRef Schofield BR (1994) Projections to the cochlear nuclei from principal cells in the medial nucleus of the trapezoid body in guinea pigs. J Comp Neurol 344:83–100PubMedCrossRef
go back to reference Schwaller B (2012) The use of transgenic mouse models to reveal the functions of Ca(2+) buffer proteins in excitable cells. Biochim Biophys Acta 1820:1294–1303PubMedCrossRef Schwaller B (2012) The use of transgenic mouse models to reveal the functions of Ca(2+) buffer proteins in excitable cells. Biochim Biophys Acta 1820:1294–1303PubMedCrossRef
go back to reference Schwaller B, Buchwald P, Blümcke I, Celio MR, Hunziker W (1993) Characterization of a polyclonal antiserum against the purified human recombinant calcium binding protein calretinin. Cell Calcium 14:639–648PubMedCrossRef Schwaller B, Buchwald P, Blümcke I, Celio MR, Hunziker W (1993) Characterization of a polyclonal antiserum against the purified human recombinant calcium binding protein calretinin. Cell Calcium 14:639–648PubMedCrossRef
go back to reference Schwaller B, Brückner G, Celio MR, Härtig W (1999) A polyclonal goat antiserum against the calcium-binding protein calretinin is a versatile tool for various immunochemical techniques. J Neurosci Methods 92:137–144PubMedCrossRef Schwaller B, Brückner G, Celio MR, Härtig W (1999) A polyclonal goat antiserum against the calcium-binding protein calretinin is a versatile tool for various immunochemical techniques. J Neurosci Methods 92:137–144PubMedCrossRef
go back to reference Schwartz IR (1992) The superior olivary complex and lateral lemniscal nuclei. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway: neuroanatomy. Springer, New York, pp 66–116 Schwartz IR (1992) The superior olivary complex and lateral lemniscal nuclei. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway: neuroanatomy. Springer, New York, pp 66–116
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 Sonntag M, Englitz B, Typlt M, Rübsamen R (2011) The calyx of Held develops adult-like dynamics and reliability by hearing onset in the mouse in vivo. J Neurosci 31:6699–6709PubMedCrossRef Sonntag M, Englitz B, Typlt M, Rübsamen R (2011) The calyx of Held develops adult-like dynamics and reliability by hearing onset in the mouse in vivo. J Neurosci 31:6699–6709PubMedCrossRef
go back to reference Spangler KM, Warr WB, Henkel CK (1985) The projections of the principal cells of the medial nucleus of the trapezoid body in the cat. J Comp Neurol 238:249–262PubMedCrossRef Spangler KM, Warr WB, Henkel CK (1985) The projections of the principal cells of the medial nucleus of the trapezoid body in the cat. J Comp Neurol 238:249–262PubMedCrossRef
go back to reference Svirskis G, Kotak V, Sanes DH, Rinzel J (2002) Enhancement of signal-to-noise ratio and phase locking for small inputs by a low-threshold outward current in auditory neurons. J Neurosci 22:11019–11025PubMedPubMedCentral Svirskis G, Kotak V, Sanes DH, Rinzel J (2002) Enhancement of signal-to-noise ratio and phase locking for small inputs by a low-threshold outward current in auditory neurons. J Neurosci 22:11019–11025PubMedPubMedCentral
go back to reference Takahashi TT, Carr CE, Brecha N, Konishi M (1987) Calcium binding protein-like immunoreactivity labels the terminal field of nucleus laminaris of the barn owl. J Neurosci 7:1843–1856PubMed Takahashi TT, Carr CE, Brecha N, Konishi M (1987) Calcium binding protein-like immunoreactivity labels the terminal field of nucleus laminaris of the barn owl. J Neurosci 7:1843–1856PubMed
go back to reference Thompson AM, Schofield BR (2000) Afferent projections of the superior olivary complex. Microsc Res Tech 51:330–354PubMedCrossRef Thompson AM, Schofield BR (2000) Afferent projections of the superior olivary complex. Microsc Res Tech 51:330–354PubMedCrossRef
go back to reference Thompson RJ, Doran JF, Jackson P, Dhillon AP, Rhode J (1983) PGP 9.5—a new marker for vertebrate neurons and neuroendocrine cells. Brain Res 278:224–228PubMedCrossRef Thompson RJ, Doran JF, Jackson P, Dhillon AP, Rhode J (1983) PGP 9.5—a new marker for vertebrate neurons and neuroendocrine cells. Brain Res 278:224–228PubMedCrossRef
go back to reference Tinner R, Oertle M, Heizmann CW, Bosshard HR (1990) Ca2+-binding site of carp parvalbumin recognized by monoclonal antibody. Cell Calcium 11:19–23PubMedCrossRef Tinner R, Oertle M, Heizmann CW, Bosshard HR (1990) Ca2+-binding site of carp parvalbumin recognized by monoclonal antibody. Cell Calcium 11:19–23PubMedCrossRef
go back to reference Tollin DJ (2003) The lateral superior olive: a functional role in sound source localization. Neuroscientist 9:127–143PubMedCrossRef Tollin DJ (2003) The lateral superior olive: a functional role in sound source localization. Neuroscientist 9:127–143PubMedCrossRef
go back to reference Tollin DJ, Yin TC (2005) Interaural phase and level difference sensitivity in low-frequency neurons in the lateral superior olive. J Neurosci 25:10648–10657PubMedPubMedCentralCrossRef Tollin DJ, Yin TC (2005) Interaural phase and level difference sensitivity in low-frequency neurons in the lateral superior olive. J Neurosci 25:10648–10657PubMedPubMedCentralCrossRef
go back to reference Tsuchitani C (1997) Input from the medial nucleus of trapezoid body to an interaural level detector. Hear Res 105:211–224PubMedCrossRef Tsuchitani C (1997) Input from the medial nucleus of trapezoid body to an interaural level detector. Hear Res 105:211–224PubMedCrossRef
go back to reference Vater M, Braun K (1994) Parvalbumin, calbindin D-28k, and calretinin immunoreactivity in the ascending auditory pathway of horseshoe bats. J Comp Neurol 341:534–558PubMedCrossRef Vater M, Braun K (1994) Parvalbumin, calbindin D-28k, and calretinin immunoreactivity in the ascending auditory pathway of horseshoe bats. J Comp Neurol 341:534–558PubMedCrossRef
go back to reference Warr WB (1966) Fiber degeneration following lesions in the anterior ventral cochlear nucleus of the cat. Exp Neurol 14:453–474PubMedCrossRef Warr WB (1966) Fiber degeneration following lesions in the anterior ventral cochlear nucleus of the cat. Exp Neurol 14:453–474PubMedCrossRef
go back to reference Webster WR, Batini C, Buisseret-Delmas C, Compoint C, Guegan M, Thomasset M (1990) Colocalization of calbindin and GABA in medial nucleus of the trapezoid body of the rat. Neurosci Lett 111:252–257PubMedCrossRef Webster WR, Batini C, Buisseret-Delmas C, Compoint C, Guegan M, Thomasset M (1990) Colocalization of calbindin and GABA in medial nucleus of the trapezoid body of the rat. Neurosci Lett 111:252–257PubMedCrossRef
go back to reference Willard FH, Martin GF (1983) The auditory brainstem nuclei and some of their projections to the inferior colliculus in the North American opossum. Neuroscience 10:1203–1232PubMedCrossRef Willard FH, Martin GF (1983) The auditory brainstem nuclei and some of their projections to the inferior colliculus in the North American opossum. Neuroscience 10:1203–1232PubMedCrossRef
go back to reference Willard FH, Martin GF (1984) Collateral innervation of the inferior colliculus in the North American opossum: a study using fluorescent markers in a double-labeling paradigm. Brain Res 303:171–182PubMedCrossRef Willard FH, Martin GF (1984) Collateral innervation of the inferior colliculus in the North American opossum: a study using fluorescent markers in a double-labeling paradigm. Brain Res 303:171–182PubMedCrossRef
go back to reference Winsky L, Nakata H, Martin BM, Jacobowitz DM (1989) Isolation, partial amino acid sequence, and immunohistochemical localization of a brain-specific calcium-binding protein. Proc Natl Acad Sci USA 86:10139–10143PubMedPubMedCentralCrossRef Winsky L, Nakata H, Martin BM, Jacobowitz DM (1989) Isolation, partial amino acid sequence, and immunohistochemical localization of a brain-specific calcium-binding protein. Proc Natl Acad Sci USA 86:10139–10143PubMedPubMedCentralCrossRef
go back to reference Yavuzoglu A, Schofield BR, Wenstrup JJ (2010) Substrates of auditory frequency integration in a nucleus of the lateral lemniscus. Neuroscience 169:906–919PubMedPubMedCentralCrossRef Yavuzoglu A, Schofield BR, Wenstrup JJ (2010) Substrates of auditory frequency integration in a nucleus of the lateral lemniscus. Neuroscience 169:906–919PubMedPubMedCentralCrossRef
go back to reference Zettel ML, Carr CE, O’Neill WE (1991) Calbindin-like immunoreactivity in the central auditory system of the mustached bat, Pteronotus parnelli. J Comp Neurol 313:1–16PubMedCrossRef Zettel ML, Carr CE, O’Neill WE (1991) Calbindin-like immunoreactivity in the central auditory system of the mustached bat, Pteronotus parnelli. J Comp Neurol 313:1–16PubMedCrossRef
go back to reference Zook JM, DiCaprio RA (1988) Intracellular labeling of afferents to the lateral superior olive in the bat, Eptesicus fuscus. Hear Res 34:141–147PubMedCrossRef Zook JM, DiCaprio RA (1988) Intracellular labeling of afferents to the lateral superior olive in the bat, Eptesicus fuscus. Hear Res 34:141–147PubMedCrossRef
Metadata
Title
Differential morphology of the superior olivary complex of Meriones unguiculatus and Monodelphis domestica revealed by calcium-binding proteins
Authors
I. Bazwinsky-Wutschke
W. Härtig
R. Kretzschmar
R. Rübsamen
Publication date
01-12-2016
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 9/2016
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-015-1181-x

Other articles of this Issue 9/2016

Brain Structure and Function 9/2016 Go to the issue