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Erschienen in: Anatomical Science International 2/2016

01.03.2016 | Review Article

Neuronal organization of the main olfactory bulb revisited

verfasst von: Toshio Kosaka, Katsuko Kosaka

Erschienen in: Anatomical Science International | Ausgabe 2/2016

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Abstract

The main olfactory bulb is now one of the most interesting parts of the brain; firstly as an excellent model for understanding the neural mechanisms of sensory information processing, and secondly as one of the most prominent sites whose interneurons are generated continuously in the postnatal and adult periods. The neuronal organization of the main olfactory bulb is fundamentally important as the basis of ongoing and future studies. In this review we focus on four issues, some of which appear not to have been recognized previously: (1) axons of periglomerular cells, (2) the heterogeneity and peculiarity of dopamine-GABAergic juxtaglomerular cells, (3) neurons participating in the interglomerular connections, and (4) newly found transglomerular cells.
Literatur
Zurück zum Zitat Alonso JR, Arévalo R, Porteros Á, Briñón JG, Lara J, Aijón J (1993) Calbindin D-28 K and NADPH-diaphorase activity are localized in different populations of periglomerular cells in the rat olfactory bulb. J Chem Neuroanat 6:1–6CrossRefPubMed Alonso JR, Arévalo R, Porteros Á, Briñón JG, Lara J, Aijón J (1993) Calbindin D-28 K and NADPH-diaphorase activity are localized in different populations of periglomerular cells in the rat olfactory bulb. J Chem Neuroanat 6:1–6CrossRefPubMed
Zurück zum Zitat Alonso JR, Briñón JG, Crespo C, Bravo IG, Arévalo R, Aijón J (2001) Chemical organization of the macaque monkey olfactory bulb: II. Calretinin, calbindin D-28 k, parvalbumin, and neurocalcin immunoreactivity. J Comp Neurol 432:389–407CrossRefPubMed Alonso JR, Briñón JG, Crespo C, Bravo IG, Arévalo R, Aijón J (2001) Chemical organization of the macaque monkey olfactory bulb: II. Calretinin, calbindin D-28 k, parvalbumin, and neurocalcin immunoreactivity. J Comp Neurol 432:389–407CrossRefPubMed
Zurück zum Zitat Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 137:433–458CrossRefPubMed Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 137:433–458CrossRefPubMed
Zurück zum Zitat Altman J, Das GD (1966) Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis is some brain regions. J Comp Neurol 727:337–390CrossRef Altman J, Das GD (1966) Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis is some brain regions. J Comp Neurol 727:337–390CrossRef
Zurück zum Zitat Aungst JL, Heyward PM, Puche AC, Karnup SV, Hayar A, Szabo G, Shipley MT (2003) Centre-surround inhibition among olfactory bulb glomeruli. Nature 426:623–629CrossRefPubMed Aungst JL, Heyward PM, Puche AC, Karnup SV, Hayar A, Szabo G, Shipley MT (2003) Centre-surround inhibition among olfactory bulb glomeruli. Nature 426:623–629CrossRefPubMed
Zurück zum Zitat Baker H, Kawano T, Margolis FL, Joh TH (1983) Transneuronal regulation of tyrosine hydroxylase expression in olfactory bulb of mouse and rat. J Neurosci 3:69–78PubMed Baker H, Kawano T, Margolis FL, Joh TH (1983) Transneuronal regulation of tyrosine hydroxylase expression in olfactory bulb of mouse and rat. J Neurosci 3:69–78PubMed
Zurück zum Zitat Baker H, Kawano T, Albert V, Joh TH, Reis DL, Margolis FL (1984) Olfactory bulb dopamine neurons survive deafferentation-induced loss of tyrosine hydroxylase. Neurosci 4:638–653 Baker H, Kawano T, Albert V, Joh TH, Reis DL, Margolis FL (1984) Olfactory bulb dopamine neurons survive deafferentation-induced loss of tyrosine hydroxylase. Neurosci 4:638–653
Zurück zum Zitat Barreiro-Iglesias A, Villar-Cerviño V, Anadón R, Rodicio MC (2009) Dopamine and gamma-aminobutyric acid are colocalized in restricted groups of neurons in the sea lamprey brain: insights into the early evolution of neurotransmitter colocalization in vertebrates. J Anat 215:601–610PubMedCentralCrossRefPubMed Barreiro-Iglesias A, Villar-Cerviño V, Anadón R, Rodicio MC (2009) Dopamine and gamma-aminobutyric acid are colocalized in restricted groups of neurons in the sea lamprey brain: insights into the early evolution of neurotransmitter colocalization in vertebrates. J Anat 215:601–610PubMedCentralCrossRefPubMed
Zurück zum Zitat Borisovska M, Bensen AL, Chong G, Westbrook GL (2013) Distinct modes of dopamine and GABA release in a dual transmitter neuron. J Neurosci 33:1790–1796PubMedCentralCrossRefPubMed Borisovska M, Bensen AL, Chong G, Westbrook GL (2013) Distinct modes of dopamine and GABA release in a dual transmitter neuron. J Neurosci 33:1790–1796PubMedCentralCrossRefPubMed
Zurück zum Zitat Briñón JG, Martínez-Guijarro FJ, Bravo IG, Arévalo R, Crespo C, Okazaki K, Hidaka H, Aijón J, Alonso JR (1999) Coexpression of neurocalcin with other calcium-binding proteins in the rat main olfactory bulb. J Comp Neurol 407:404–414CrossRefPubMed Briñón JG, Martínez-Guijarro FJ, Bravo IG, Arévalo R, Crespo C, Okazaki K, Hidaka H, Aijón J, Alonso JR (1999) Coexpression of neurocalcin with other calcium-binding proteins in the rat main olfactory bulb. J Comp Neurol 407:404–414CrossRefPubMed
Zurück zum Zitat Briñón JG, Weruaga E, Crespo C, Porteros A, Arévalo R, Aijón J, Alonso JR (2001) Calretinin-, neurocalcin-, and parvalbumin- immunoreactive elements in the olfactory bulb of the hedgehog (Erinaceus europaeus). J Comp Neurol 429:554–570CrossRefPubMed Briñón JG, Weruaga E, Crespo C, Porteros A, Arévalo R, Aijón J, Alonso JR (2001) Calretinin-, neurocalcin-, and parvalbumin- immunoreactive elements in the olfactory bulb of the hedgehog (Erinaceus europaeus). J Comp Neurol 429:554–570CrossRefPubMed
Zurück zum Zitat Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187CrossRefPubMed Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187CrossRefPubMed
Zurück zum Zitat Chand AN, Galliano E, Chesters RA, Grubb MS (2015) A distinct subtype of dopaminergic interneuron displays inverted structural plasticity at the axon initial segment. J Neurosci 35:1573–1590PubMedCentralCrossRefPubMed Chand AN, Galliano E, Chesters RA, Grubb MS (2015) A distinct subtype of dopaminergic interneuron displays inverted structural plasticity at the axon initial segment. J Neurosci 35:1573–1590PubMedCentralCrossRefPubMed
Zurück zum Zitat Crespo C, Gracia-Llanes FJ, Blasco-Ibáñez JM, Gutièrrez-Mecinas M, Marqués-Mari AI, Martínez-Guijarro FJ (2003) Nitric oxide synthase containing periglomerular cells are GABAergic in the rat olfactory bulb. Neurosci Lett 349:151–154CrossRefPubMed Crespo C, Gracia-Llanes FJ, Blasco-Ibáñez JM, Gutièrrez-Mecinas M, Marqués-Mari AI, Martínez-Guijarro FJ (2003) Nitric oxide synthase containing periglomerular cells are GABAergic in the rat olfactory bulb. Neurosci Lett 349:151–154CrossRefPubMed
Zurück zum Zitat Davis BJ, Macrides F (1983) Tyrosine hydroxylase immunoreactive neurons and fibers in the olfactory system of the hamster. J Comp Neurol 214:427–440CrossRef Davis BJ, Macrides F (1983) Tyrosine hydroxylase immunoreactive neurons and fibers in the olfactory system of the hamster. J Comp Neurol 214:427–440CrossRef
Zurück zum Zitat De Marchis S, Bovetti S, Carletti B, Hsieh YC, Garzotto D, Peretto P, Fasolo A, Puche AC, Rossi F (2007) Generation of distinct types of periglomerular olfactory bulb interneurons during development and in adult mice: implication for intrinsic properties of the subventricular zone progenitor population. J Neurosci 27:657–664CrossRefPubMed De Marchis S, Bovetti S, Carletti B, Hsieh YC, Garzotto D, Peretto P, Fasolo A, Puche AC, Rossi F (2007) Generation of distinct types of periglomerular olfactory bulb interneurons during development and in adult mice: implication for intrinsic properties of the subventricular zone progenitor population. J Neurosci 27:657–664CrossRefPubMed
Zurück zum Zitat Ennis M, Puche AC, Holy T, Shipley MT (2015) The olfactory system. In: Paxinos G (ed) The rat nervous system, 4th edn, Chap. 27. Academic, London, pp 761–803 Ennis M, Puche AC, Holy T, Shipley MT (2015) The olfactory system. In: Paxinos G (ed) The rat nervous system, 4th edn, Chap. 27. Academic, London, pp 761–803
Zurück zum Zitat Eyre MD, Antal M, Nusser Z (2008) Distinct deep short-axon cell subtypes of the main olfactory bulb provide novel intrabulbar and extrabulbar GABAergic connections. J Neurosci 28:8217–8229PubMedCentralCrossRefPubMed Eyre MD, Antal M, Nusser Z (2008) Distinct deep short-axon cell subtypes of the main olfactory bulb provide novel intrabulbar and extrabulbar GABAergic connections. J Neurosci 28:8217–8229PubMedCentralCrossRefPubMed
Zurück zum Zitat Gall CM, Hendry SHC, Seroogy KB, Jones EG, Haycock JW (1987) Evidence for coexistence of GABA and dopamine in neurons of the rat olfactory bulb. J Comp Neurol 266:307–318CrossRefPubMed Gall CM, Hendry SHC, Seroogy KB, Jones EG, Haycock JW (1987) Evidence for coexistence of GABA and dopamine in neurons of the rat olfactory bulb. J Comp Neurol 266:307–318CrossRefPubMed
Zurück zum Zitat Gire DH, Schoppa NE (2009) Control of on/off glomerular signaling by a local GABAergic microcircuit in the olfactory bulb. J Neurosci 29:13454–13464PubMedCentralCrossRefPubMed Gire DH, Schoppa NE (2009) Control of on/off glomerular signaling by a local GABAergic microcircuit in the olfactory bulb. J Neurosci 29:13454–13464PubMedCentralCrossRefPubMed
Zurück zum Zitat Gutièrrez-Mecinas M, Crespo C, Blasco-Ibáñez JM, Gracia-Llanes FJ, Marqués-Mari AI, Martínez-Guijarro FJ (2005) Characterization of somatostatin- and cholecystokinin-immunoreactive periglomerular cells in the rat olfactory bulb. J Comp Neurol 489:467–479CrossRefPubMed Gutièrrez-Mecinas M, Crespo C, Blasco-Ibáñez JM, Gracia-Llanes FJ, Marqués-Mari AI, Martínez-Guijarro FJ (2005) Characterization of somatostatin- and cholecystokinin-immunoreactive periglomerular cells in the rat olfactory bulb. J Comp Neurol 489:467–479CrossRefPubMed
Zurück zum Zitat Halász N (1990) The vertebrate olfactory system: chemical neuroanatomy, function and development. Akadémiai Kiadó, Budapest Halász N (1990) The vertebrate olfactory system: chemical neuroanatomy, function and development. Akadémiai Kiadó, Budapest
Zurück zum Zitat Halász N, Johansson O, Hökfelt T, Ljungdahl Å, Goldstein M (1981) Immunohistochemical identification of two types of dopamine neuron in the rat olfactory bulbs as seen by serial sectioning. J Neurocytol 10:251–259CrossRefPubMed Halász N, Johansson O, Hökfelt T, Ljungdahl Å, Goldstein M (1981) Immunohistochemical identification of two types of dopamine neuron in the rat olfactory bulbs as seen by serial sectioning. J Neurocytol 10:251–259CrossRefPubMed
Zurück zum Zitat Hinds JW (1968a) Autoradiographic study of histogenesis in the mouse olfactory bulb I. Time of origin of neurons and neuroglia. J Comp Neurol 134:287–304CrossRefPubMed Hinds JW (1968a) Autoradiographic study of histogenesis in the mouse olfactory bulb I. Time of origin of neurons and neuroglia. J Comp Neurol 134:287–304CrossRefPubMed
Zurück zum Zitat Hinds JW (1968b) Autoradiographic study of histogenesis in the mouse olfactory bulb II. Cell proliferation and migration. J Comp Neurol 134:305–322CrossRefPubMed Hinds JW (1968b) Autoradiographic study of histogenesis in the mouse olfactory bulb II. Cell proliferation and migration. J Comp Neurol 134:305–322CrossRefPubMed
Zurück zum Zitat Imai T (2014) Construction of functional neuronal circuitry in the olfactory bulb. Semin Cell Dev Biol 35:180–188CrossRefPubMed Imai T (2014) Construction of functional neuronal circuitry in the olfactory bulb. Semin Cell Dev Biol 35:180–188CrossRefPubMed
Zurück zum Zitat Kiyokage E, Pan YZ, Shao Z, Kobayashi K, Szabo G, Yanagawa Y, Obata K, Okano H, Toida K, Puche A, Shipley MT (2010) Molecular identity of periglomerular and short axon cells. J Neurosci 30:1185–1196PubMedCentralCrossRefPubMed Kiyokage E, Pan YZ, Shao Z, Kobayashi K, Szabo G, Yanagawa Y, Obata K, Okano H, Toida K, Puche A, Shipley MT (2010) Molecular identity of periglomerular and short axon cells. J Neurosci 30:1185–1196PubMedCentralCrossRefPubMed
Zurück zum Zitat Kosaka T, Hama K (1982–83) Synaptic organization in the teleost olfactory bulb. J Physiol 78:707–719 Kosaka T, Hama K (1982–83) Synaptic organization in the teleost olfactory bulb. J Physiol 78:707–719
Zurück zum Zitat Kosaka K, Kosaka T (1999) Distinctive neuronal organization of the olfactory bulb of the laboratory shrew. NeuroReport 10:267–273CrossRefPubMed Kosaka K, Kosaka T (1999) Distinctive neuronal organization of the olfactory bulb of the laboratory shrew. NeuroReport 10:267–273CrossRefPubMed
Zurück zum Zitat Kosaka K, Kosaka T (2001) Nidus and tasseled cell: distinctive neuronal organization of the main olfactory bulb of the laboratory musk shrew (Suncus murinus). J Comp Neurol 430:542–561CrossRefPubMed Kosaka K, Kosaka T (2001) Nidus and tasseled cell: distinctive neuronal organization of the main olfactory bulb of the laboratory musk shrew (Suncus murinus). J Comp Neurol 430:542–561CrossRefPubMed
Zurück zum Zitat Kosaka T, Kosaka K (2003) Neuronal gap junctions in the rat main olfactory bulb, with special reference to intraglomerular gap junctions. Neurosci Res 45:189–209CrossRefPubMed Kosaka T, Kosaka K (2003) Neuronal gap junctions in the rat main olfactory bulb, with special reference to intraglomerular gap junctions. Neurosci Res 45:189–209CrossRefPubMed
Zurück zum Zitat Kosaka K, Kosaka T (2004a) Organization of the main olfactory bulbs of some mammals: musk shrews, moles, hedgehogs, tree shrews, bats, mice, and rats. J Comp Neurol 472:1–12CrossRefPubMed Kosaka K, Kosaka T (2004a) Organization of the main olfactory bulbs of some mammals: musk shrews, moles, hedgehogs, tree shrews, bats, mice, and rats. J Comp Neurol 472:1–12CrossRefPubMed
Zurück zum Zitat Kosaka T, Kosaka K (2004b) Neuronal gap junctions between intraglomerular mitral/tufted cell dendrites in the mouse main olfactory bulb. Neurosci Res 49:373–378CrossRefPubMed Kosaka T, Kosaka K (2004b) Neuronal gap junctions between intraglomerular mitral/tufted cell dendrites in the mouse main olfactory bulb. Neurosci Res 49:373–378CrossRefPubMed
Zurück zum Zitat Kosaka K, Kosaka T (2005) Synaptic organization of the glomerulus in the main olfactory bulb: the compartments of the glomerulus and the heterogeneity of the periglomerular cells. Anat Sci Int 80:80–90CrossRefPubMed Kosaka K, Kosaka T (2005) Synaptic organization of the glomerulus in the main olfactory bulb: the compartments of the glomerulus and the heterogeneity of the periglomerular cells. Anat Sci Int 80:80–90CrossRefPubMed
Zurück zum Zitat Kosaka T, Kosaka K (2005) Intraglomerular dendritic link connected by gap junctions and chemical synapses in the mouse main olfactory bulb: electron microscopic serial section analyses. Neuroscience 131:611–625CrossRefPubMed Kosaka T, Kosaka K (2005) Intraglomerular dendritic link connected by gap junctions and chemical synapses in the mouse main olfactory bulb: electron microscopic serial section analyses. Neuroscience 131:611–625CrossRefPubMed
Zurück zum Zitat Kosaka K, Kosaka T (2007a) Chemical properties of type 1 and type 2 periglomerular cells in the mouse olfactory bulb are different from those in the rat olfactory bulb. Brain Res 1167:42–55CrossRefPubMed Kosaka K, Kosaka T (2007a) Chemical properties of type 1 and type 2 periglomerular cells in the mouse olfactory bulb are different from those in the rat olfactory bulb. Brain Res 1167:42–55CrossRefPubMed
Zurück zum Zitat Kosaka T, Kosaka K (2007b) Heterogeneity of nitric oxide synthase-containing neurons in the mouse olfactory bulb. Neurosci Res 57:165–178CrossRefPubMed Kosaka T, Kosaka K (2007b) Heterogeneity of nitric oxide synthase-containing neurons in the mouse olfactory bulb. Neurosci Res 57:165–178CrossRefPubMed
Zurück zum Zitat Kosaka T, Kosaka K (2008a) Heterogeneity of parvalbumin-containing neurons in the mouse olfactory bulb, with special reference to short-axon cells and βIV-spectrin positive dendritic segments. Neurosci Res 60:56–72CrossRefPubMed Kosaka T, Kosaka K (2008a) Heterogeneity of parvalbumin-containing neurons in the mouse olfactory bulb, with special reference to short-axon cells and βIV-spectrin positive dendritic segments. Neurosci Res 60:56–72CrossRefPubMed
Zurück zum Zitat Kosaka T, Kosaka K (2008b) Tyrosine hydroxylase-positive GABAergic juxtaglomerular neurons are the main source of the interglomerular connections in the mouse main olfactory bulb. Neurosci Res 60:349–354CrossRefPubMed Kosaka T, Kosaka K (2008b) Tyrosine hydroxylase-positive GABAergic juxtaglomerular neurons are the main source of the interglomerular connections in the mouse main olfactory bulb. Neurosci Res 60:349–354CrossRefPubMed
Zurück zum Zitat Kosaka T, Kosaka K (2009a) Two types of tyrosine hydroxylase positive GABAergic juxtaglomerular neurons in the mouse main olfactory bulb are different in their time of origin. Neurosci Res 64:436–441CrossRefPubMed Kosaka T, Kosaka K (2009a) Two types of tyrosine hydroxylase positive GABAergic juxtaglomerular neurons in the mouse main olfactory bulb are different in their time of origin. Neurosci Res 64:436–441CrossRefPubMed
Zurück zum Zitat Kosaka T, Kosaka K (2009b) Olfactory bulb anatomy. In: Squire LR (ed) Encyclopedia of neuroscience, vol 7. Academic, Oxford, pp 59–69CrossRef Kosaka T, Kosaka K (2009b) Olfactory bulb anatomy. In: Squire LR (ed) Encyclopedia of neuroscience, vol 7. Academic, Oxford, pp 59–69CrossRef
Zurück zum Zitat Kosaka T, Kosaka K (2010) Heterogeneity of calbindin-containing neurons in the mouse olfactory bulb: I general description. Neurosci Res 67:275–292CrossRefPubMed Kosaka T, Kosaka K (2010) Heterogeneity of calbindin-containing neurons in the mouse olfactory bulb: I general description. Neurosci Res 67:275–292CrossRefPubMed
Zurück zum Zitat Kosaka T, Kosaka K (2011) “Interneurons” in the olfactory bulb revisited. Neurosci Res 69:93–99CrossRefPubMed Kosaka T, Kosaka K (2011) “Interneurons” in the olfactory bulb revisited. Neurosci Res 69:93–99CrossRefPubMed
Zurück zum Zitat Kosaka T, Kosaka K (2013) Secretagogin-containing neurons in the mouse main olfactory bulb. Neurosci Res 77:16–32CrossRefPubMed Kosaka T, Kosaka K (2013) Secretagogin-containing neurons in the mouse main olfactory bulb. Neurosci Res 77:16–32CrossRefPubMed
Zurück zum Zitat Kosaka T, Hataguchi Y, Hama K, Nagatsu I, Wu JY (1985) Coexistence of immunoreactivities for glutamate decarboxylase and tyrosine hydroxylase in some neurons in the periglomerular region of the rat main olfactory bulb: possible coexistence of gamma-aminobutyric acid (GABA) and dopamine. Brain Res 343:166–171CrossRefPubMed Kosaka T, Hataguchi Y, Hama K, Nagatsu I, Wu JY (1985) Coexistence of immunoreactivities for glutamate decarboxylase and tyrosine hydroxylase in some neurons in the periglomerular region of the rat main olfactory bulb: possible coexistence of gamma-aminobutyric acid (GABA) and dopamine. Brain Res 343:166–171CrossRefPubMed
Zurück zum Zitat Kosaka K, Hama K, Nagatsu I, Wu JY, Ottersen OP, Storm-Mathisen J, Kosaka T (1987a) Postnatal development of neurons containing both catecholaminergic and GABAergic traits in the rat main olfactory bulb. Brain Res 403:355–360CrossRefPubMed Kosaka K, Hama K, Nagatsu I, Wu JY, Ottersen OP, Storm-Mathisen J, Kosaka T (1987a) Postnatal development of neurons containing both catecholaminergic and GABAergic traits in the rat main olfactory bulb. Brain Res 403:355–360CrossRefPubMed
Zurück zum Zitat Kosaka T, Kosaka K, Hama K, Wu J-Y, Nagatsu I (1987b) Differential effect of functional olfactory deprivation on the GABAergic and catecholaminergic traits in the rat main olfactory bulb. Brain Res 413:197–203CrossRefPubMed Kosaka T, Kosaka K, Hama K, Wu J-Y, Nagatsu I (1987b) Differential effect of functional olfactory deprivation on the GABAergic and catecholaminergic traits in the rat main olfactory bulb. Brain Res 413:197–203CrossRefPubMed
Zurück zum Zitat Kosaka T, Kosaka K, Hataguchi Y, Nagatsu I, Wu JY, Ottersen OP, Storm-Mathisen J, Hama K (1987c) Catecholaminergic neurons containing GABA-like and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat. Exp Brain Res 66:191–210CrossRefPubMed Kosaka T, Kosaka K, Hataguchi Y, Nagatsu I, Wu JY, Ottersen OP, Storm-Mathisen J, Hama K (1987c) Catecholaminergic neurons containing GABA-like and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat. Exp Brain Res 66:191–210CrossRefPubMed
Zurück zum Zitat Kosaka T, Kosaka K, Heizmann CW, Nagatsu I, Wu JY, Yanaihara N, Hama K (1987d) An aspect of the organization of the GABAergic system in the rat main olfactory bulb: laminar distribution of immunohistochemically defined subpopulations of GABAergic neurons. Brain Res 411:373–378CrossRefPubMed Kosaka T, Kosaka K, Heizmann CW, Nagatsu I, Wu JY, Yanaihara N, Hama K (1987d) An aspect of the organization of the GABAergic system in the rat main olfactory bulb: laminar distribution of immunohistochemically defined subpopulations of GABAergic neurons. Brain Res 411:373–378CrossRefPubMed
Zurück zum Zitat Kosaka K, Hama K, Nagatsu I, Wu JY, Kosaka T (1988) Possible coexistence of amino acid (γ-aminobutyric acid), amine (dopamine) and peptide (substance P); neurons containing immunoreactivities for glutamic acid decarboxylase, tyrosine hydroxylase and substance P in the hamster main olfactory bulb. Exp Brain Res 71:633–642CrossRefPubMed Kosaka K, Hama K, Nagatsu I, Wu JY, Kosaka T (1988) Possible coexistence of amino acid (γ-aminobutyric acid), amine (dopamine) and peptide (substance P); neurons containing immunoreactivities for glutamic acid decarboxylase, tyrosine hydroxylase and substance P in the hamster main olfactory bulb. Exp Brain Res 71:633–642CrossRefPubMed
Zurück zum Zitat Kosaka T, Kosaka K, Nagatsu I (1991) Tyrosine hydroxylase-like immunoreactive neurons in the olfactory bulb of the snake, Elaphe quadrivirgata, with special reference to colocalization of tyrosine hydroxylase- and GABA-like immunoreactivities. Exp Brain Res 87:353–362CrossRefPubMed Kosaka T, Kosaka K, Nagatsu I (1991) Tyrosine hydroxylase-like immunoreactive neurons in the olfactory bulb of the snake, Elaphe quadrivirgata, with special reference to colocalization of tyrosine hydroxylase- and GABA-like immunoreactivities. Exp Brain Res 87:353–362CrossRefPubMed
Zurück zum Zitat Kosaka K, Aika Y, Toida K, Heizmann CW, Hunziker W, Jacobowitz DM, Nagatsu I, Streit P, Visser TJ, Kosaka T (1995) Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb. Neurosci Res 23:73–88CrossRefPubMed Kosaka K, Aika Y, Toida K, Heizmann CW, Hunziker W, Jacobowitz DM, Nagatsu I, Streit P, Visser TJ, Kosaka T (1995) Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb. Neurosci Res 23:73–88CrossRefPubMed
Zurück zum Zitat Kosaka K, Toida K, Margolis FL, Kosaka T (1997) Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb, II. Prominent differences in the intraglomerular dendritic arborization and their relationship to olfactory nerve terminals. Neuroscience 76:775–786CrossRefPubMed Kosaka K, Toida K, Margolis FL, Kosaka T (1997) Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb, II. Prominent differences in the intraglomerular dendritic arborization and their relationship to olfactory nerve terminals. Neuroscience 76:775–786CrossRefPubMed
Zurück zum Zitat Kosaka K, Toida K, Aika Y, Kosaka T (1998) How simple is the organization of the olfactory glomerulus? The heterogeneity of so-called periglomerular cells. Neurosci Res 30:101–110CrossRefPubMed Kosaka K, Toida K, Aika Y, Kosaka T (1998) How simple is the organization of the olfactory glomerulus? The heterogeneity of so-called periglomerular cells. Neurosci Res 30:101–110CrossRefPubMed
Zurück zum Zitat Kosaka K, Aika Y, Toida K, Kosaka T (2001) Structure of intraglomerular dendritic tufts of mitral cells and their contacts with olfactory nerve terminals and calbindin-immunoreactive type 2 periglomerular neurons. J Comp Neurol 440:219–235CrossRefPubMed Kosaka K, Aika Y, Toida K, Kosaka T (2001) Structure of intraglomerular dendritic tufts of mitral cells and their contacts with olfactory nerve terminals and calbindin-immunoreactive type 2 periglomerular neurons. J Comp Neurol 440:219–235CrossRefPubMed
Zurück zum Zitat Kosaka K, Künzle H, Kosaka T (2005a) Organization of the main olfactory bulb of lesser hedgehog tenrecs. Neurosci Res 53:353–362CrossRefPubMed Kosaka K, Künzle H, Kosaka T (2005a) Organization of the main olfactory bulb of lesser hedgehog tenrecs. Neurosci Res 53:353–362CrossRefPubMed
Zurück zum Zitat Kosaka T, Deans MR, Paul DL, Kosaka K (2005b) Neuronal gap junctions in the mouse main olfactory bulb: morphological analyses on transgenic mice. Neuroscience 134:757–769CrossRefPubMed Kosaka T, Deans MR, Paul DL, Kosaka K (2005b) Neuronal gap junctions in the mouse main olfactory bulb: morphological analyses on transgenic mice. Neuroscience 134:757–769CrossRefPubMed
Zurück zum Zitat Kosaka T, Komada M, Kosaka K (2008) Sodium channel cluster, βIV-spectrin and ankyrinG positive “hot spots” on dendritic segments of parvalbumin-containing neurons and some other neurons in the mouse and rat olfactory bulbs. Neurosci Res 62:176–186CrossRefPubMed Kosaka T, Komada M, Kosaka K (2008) Sodium channel cluster, βIV-spectrin and ankyrinG positive “hot spots” on dendritic segments of parvalbumin-containing neurons and some other neurons in the mouse and rat olfactory bulbs. Neurosci Res 62:176–186CrossRefPubMed
Zurück zum Zitat Lepousez G, Valley MT, Lledo PM (2013) The impact of adult neurogenesis on olfactory bulb circuits and computations. Annu Rev Physiol 75:339–363CrossRefPubMed Lepousez G, Valley MT, Lledo PM (2013) The impact of adult neurogenesis on olfactory bulb circuits and computations. Annu Rev Physiol 75:339–363CrossRefPubMed
Zurück zum Zitat Liu S, Plachez C, Shao Z, Puche A, Shipley MT (2013) Olfactory bulb short axon cell release of GABA and dopamine produces a temporally biphasic inhibition-excitation response in external tufted cells. J Neurosci 33:2916–2926PubMedCentralCrossRefPubMed Liu S, Plachez C, Shao Z, Puche A, Shipley MT (2013) Olfactory bulb short axon cell release of GABA and dopamine produces a temporally biphasic inhibition-excitation response in external tufted cells. J Neurosci 33:2916–2926PubMedCentralCrossRefPubMed
Zurück zum Zitat Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145–1148CrossRefPubMed Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145–1148CrossRefPubMed
Zurück zum Zitat López-Mascaraque L, De Carlos JA, Valverde F (1990) Structure of the olfactory bulb of the hedgehog (Erinaceus europaeus): a Golgi study of the intrinsic organization of the superficial layers. J Comp Neurol 301:243–261CrossRefPubMed López-Mascaraque L, De Carlos JA, Valverde F (1990) Structure of the olfactory bulb of the hedgehog (Erinaceus europaeus): a Golgi study of the intrinsic organization of the superficial layers. J Comp Neurol 301:243–261CrossRefPubMed
Zurück zum Zitat Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173–189CrossRefPubMed Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173–189CrossRefPubMed
Zurück zum Zitat Macrides F, Schneider SP (1982) Laminar organization of mitral and tufted cells in the main olfactory bulb of the adult hamster. J Comp Neurol 208:419–430CrossRefPubMed Macrides F, Schneider SP (1982) Laminar organization of mitral and tufted cells in the main olfactory bulb of the adult hamster. J Comp Neurol 208:419–430CrossRefPubMed
Zurück zum Zitat Maher BJ, Westbrook GL (2008) Co-transmission of dopamine and GABA in periglomerular cells. J Neurophysiol 99:1559–1564CrossRefPubMed Maher BJ, Westbrook GL (2008) Co-transmission of dopamine and GABA in periglomerular cells. J Neurophysiol 99:1559–1564CrossRefPubMed
Zurück zum Zitat McQuiston AR, Katz LC (2001) Electrophysiology of interneurons in the glomerular layer of the rat olfactory bulb. J Neurophysiol 86:1899–1907PubMed McQuiston AR, Katz LC (2001) Electrophysiology of interneurons in the glomerular layer of the rat olfactory bulb. J Neurophysiol 86:1899–1907PubMed
Zurück zum Zitat Merkle FT, Mirzadehe Z, Alvarez-Buylla A (2007) Mosaic organization of neural stem cells in the adult brain. Science 317:381–384CrossRefPubMed Merkle FT, Mirzadehe Z, Alvarez-Buylla A (2007) Mosaic organization of neural stem cells in the adult brain. Science 317:381–384CrossRefPubMed
Zurück zum Zitat Mugnaini E, Oertel WH, Wouterlood FG (1984) Immunocytochemical localization of GABAergic neurons and dopaminergic neurons in the rat main and accessory olfactory bulbs. Neurosci Lett 47:221–226CrossRefPubMed Mugnaini E, Oertel WH, Wouterlood FG (1984) Immunocytochemical localization of GABAergic neurons and dopaminergic neurons in the rat main and accessory olfactory bulbs. Neurosci Lett 47:221–226CrossRefPubMed
Zurück zum Zitat Mulder J, Zilberter M, Spence L, Tortoriello G, Uhlén M, Yanagawa Y, Aujard F, Hökfelt T, Harkany T (2009) Secretagogin is a Ca2+-binding protein specifying subpopulations of telencephalic neurons. Proc Natl Acad Sci USA 106:22492–22497PubMedCentralCrossRefPubMed Mulder J, Zilberter M, Spence L, Tortoriello G, Uhlén M, Yanagawa Y, Aujard F, Hökfelt T, Harkany T (2009) Secretagogin is a Ca2+-binding protein specifying subpopulations of telencephalic neurons. Proc Natl Acad Sci USA 106:22492–22497PubMedCentralCrossRefPubMed
Zurück zum Zitat Nagayama S, Homma R, Imamura F (2014) Neuronal organization of olfactory bulb circuits. Front Neural Circuits 08–00098:1–19 Nagayama S, Homma R, Imamura F (2014) Neuronal organization of olfactory bulb circuits. Front Neural Circuits 08–00098:1–19
Zurück zum Zitat Panzanelli P, Fritsch JM, Yanagawa Y, Obata K, Sassoè-Pognetto M (2007) GABAergic phenotype of periglomerular cells in the rodent olfactory bulb. J Comp Neurol 502:990–1002CrossRefPubMed Panzanelli P, Fritsch JM, Yanagawa Y, Obata K, Sassoè-Pognetto M (2007) GABAergic phenotype of periglomerular cells in the rodent olfactory bulb. J Comp Neurol 502:990–1002CrossRefPubMed
Zurück zum Zitat Parrish-Aungst S, Shipley MT, Erdelyi F, Szabo G, Puche AC (2007) Quantitative analysis of neuronal diversity in the mouse olfactory bulb. J Comp Neurol 501:825–836CrossRefPubMed Parrish-Aungst S, Shipley MT, Erdelyi F, Szabo G, Puche AC (2007) Quantitative analysis of neuronal diversity in the mouse olfactory bulb. J Comp Neurol 501:825–836CrossRefPubMed
Zurück zum Zitat Pignatelli A, Kobayashi K, Okano H, Belluzzi O (2005) Functional properties of dopaminergic neurons in the mouse olfactory bulb. J Physiol 564:501–514PubMedCentralCrossRefPubMed Pignatelli A, Kobayashi K, Okano H, Belluzzi O (2005) Functional properties of dopaminergic neurons in the mouse olfactory bulb. J Physiol 564:501–514PubMedCentralCrossRefPubMed
Zurück zum Zitat Pinching AJ, Powell TPS (1971a) Ultrastructural features of transneuronal cell degeneration in the olfactory bulb. J Cell Sci 8:253–287PubMed Pinching AJ, Powell TPS (1971a) Ultrastructural features of transneuronal cell degeneration in the olfactory bulb. J Cell Sci 8:253–287PubMed
Zurück zum Zitat Pinching AJ, Powell TPS (1971b) The neuron types of the glomerular layer of the olfactory bulb. J Cell Sci 9:305–345PubMed Pinching AJ, Powell TPS (1971b) The neuron types of the glomerular layer of the olfactory bulb. J Cell Sci 9:305–345PubMed
Zurück zum Zitat Pinching AJ, Powell TPS (1971c) The neuropil of the glomeruli of the olfactory bulb. J Cell Sci 9:347–377PubMed Pinching AJ, Powell TPS (1971c) The neuropil of the glomeruli of the olfactory bulb. J Cell Sci 9:347–377PubMed
Zurück zum Zitat Pinching AJ, Powell TPS (1971d) The neuropil of the periglomerular region of the olfactory bulb. J Cell Sci 9:379–409PubMed Pinching AJ, Powell TPS (1971d) The neuropil of the periglomerular region of the olfactory bulb. J Cell Sci 9:379–409PubMed
Zurück zum Zitat Pinching AJ, Powell TPS (1972a) A study of termination of centrifugal fibres in the glomerular layer of the olfactory bulb. J Cell Sci 10:621–635PubMed Pinching AJ, Powell TPS (1972a) A study of termination of centrifugal fibres in the glomerular layer of the olfactory bulb. J Cell Sci 10:621–635PubMed
Zurück zum Zitat Pinching AJ, Powell TPS (1972b) The terminal degeneration in the olfactory bulb of the rat. J Cell Sci 10:585–619PubMed Pinching AJ, Powell TPS (1972b) The terminal degeneration in the olfactory bulb of the rat. J Cell Sci 10:585–619PubMed
Zurück zum Zitat Pinching AJ, Powell TPS (1972c) Experimental studies on the axons intrinsic to the glomerular layer of the olfactory bulb. J Cell Sci 10:637–655PubMed Pinching AJ, Powell TPS (1972c) Experimental studies on the axons intrinsic to the glomerular layer of the olfactory bulb. J Cell Sci 10:637–655PubMed
Zurück zum Zitat Price JL, Powell TPS (1970a) The morphology of the granule cells of the olfactory bulb. J Cell Sci 7:91–123PubMed Price JL, Powell TPS (1970a) The morphology of the granule cells of the olfactory bulb. J Cell Sci 7:91–123PubMed
Zurück zum Zitat Price JL, Powell TPS (1970b) An electron-microscopic study of the termination of the afferent fibres to the olfactory bulb from the cerebral hemisphere. J Cell Sci 7:157–187PubMed Price JL, Powell TPS (1970b) An electron-microscopic study of the termination of the afferent fibres to the olfactory bulb from the cerebral hemisphere. J Cell Sci 7:157–187PubMed
Zurück zum Zitat Price JL, Powell TPS (1970c) The mitral and short axon cells of the olfactory bulb. J Cell Sci 7:631–651PubMed Price JL, Powell TPS (1970c) The mitral and short axon cells of the olfactory bulb. J Cell Sci 7:631–651PubMed
Zurück zum Zitat Ramón y Cajal S (1995) Histology of the nervous system of man and vertebrates (Translated by N. Swanson and L. W. Swanson from the French; French edition, Histologie du Système Nerveux de l’homme et des Vertébrés, reviewed and updated by the author, translated from the Spanish by Dr. L. Azoulay, published in 1911). Oxford University Press, New York Ramón y Cajal S (1995) Histology of the nervous system of man and vertebrates (Translated by N. Swanson and L. W. Swanson from the French; French edition, Histologie du Système Nerveux de l’homme et des Vertébrés, reviewed and updated by the author, translated from the Spanish by Dr. L. Azoulay, published in 1911). Oxford University Press, New York
Zurück zum Zitat Ribak CE, Vaughn JE, Saito K, Barber R, Roberts E (1977) Glutamate decarboxylase localization in neurons of the olfactory bulb. Brain Res 126:1–18CrossRefPubMed Ribak CE, Vaughn JE, Saito K, Barber R, Roberts E (1977) Glutamate decarboxylase localization in neurons of the olfactory bulb. Brain Res 126:1–18CrossRefPubMed
Zurück zum Zitat Schneider SP, Macrides F (1978) Laminar distribution of interneurons in the main olfactory bulb of adult hamster. Brain Res Bull 3:73–82CrossRefPubMed Schneider SP, Macrides F (1978) Laminar distribution of interneurons in the main olfactory bulb of adult hamster. Brain Res Bull 3:73–82CrossRefPubMed
Zurück zum Zitat Schoenfeld TA, Marchand JE, Macrides F (1985) Topographic organization of tufted cell axonal projections in the hamster main olfactory bulb: an intrabulbar associational system. J Comp Neurol 255:503–518CrossRef Schoenfeld TA, Marchand JE, Macrides F (1985) Topographic organization of tufted cell axonal projections in the hamster main olfactory bulb: an intrabulbar associational system. J Comp Neurol 255:503–518CrossRef
Zurück zum Zitat Shepherd G (2004) The synaptic organization of the brain, 5th edn. Oxford University Press, New YorkCrossRef Shepherd G (2004) The synaptic organization of the brain, 5th edn. Oxford University Press, New YorkCrossRef
Zurück zum Zitat Valverde F (1965) Studies on the piriform lobe. Harvard University Press, CambridgeCrossRef Valverde F (1965) Studies on the piriform lobe. Harvard University Press, CambridgeCrossRef
Zurück zum Zitat Whitman MC, Greer CA (2007) Adult-generated neurons exhibit diverse developmental fates. Dev Neurobiol 67:1079–1093CrossRefPubMed Whitman MC, Greer CA (2007) Adult-generated neurons exhibit diverse developmental fates. Dev Neurobiol 67:1079–1093CrossRefPubMed
Zurück zum Zitat Zhou Z, Xiong W, Masurkar AV, Chen WR, Shepherd GM (2006) Dendritic calcium plateau potentials modulate input-output properties of juxtaglomerular cells in the rat olfactory bulb. J Neurophysiol 96:2354–2363CrossRefPubMed Zhou Z, Xiong W, Masurkar AV, Chen WR, Shepherd GM (2006) Dendritic calcium plateau potentials modulate input-output properties of juxtaglomerular cells in the rat olfactory bulb. J Neurophysiol 96:2354–2363CrossRefPubMed
Zurück zum Zitat Zhu P, Frank T, Friedrich RW (2013) Equalization of odor representations by a network of electrically coupled inhibitory interneurons. Nature Neurosci 16:1678–1686CrossRefPubMed Zhu P, Frank T, Friedrich RW (2013) Equalization of odor representations by a network of electrically coupled inhibitory interneurons. Nature Neurosci 16:1678–1686CrossRefPubMed
Metadaten
Titel
Neuronal organization of the main olfactory bulb revisited
verfasst von
Toshio Kosaka
Katsuko Kosaka
Publikationsdatum
01.03.2016
Verlag
Springer Japan
Erschienen in
Anatomical Science International / Ausgabe 2/2016
Print ISSN: 1447-6959
Elektronische ISSN: 1447-073X
DOI
https://doi.org/10.1007/s12565-015-0309-7

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