Skip to main content
Log in

Neuronal organization of the main olfactory bulb revisited

  • Review Article
  • Published:
Anatomical Science International Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • 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 6:1–6

    Article  CAS  PubMed  Google Scholar 

  • 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 432:389–407

    Article  CAS  PubMed  Google Scholar 

  • 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 137:433–458

    Article  CAS  PubMed  Google Scholar 

  • 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 727:337–390

    Article  Google Scholar 

  • Aungst JL, Heyward PM, Puche AC, Karnup SV, Hayar A, Szabo G, Shipley MT (2003) Centre-surround inhibition among olfactory bulb glomeruli. Nature 426:623–629

    Article  CAS  PubMed  Google Scholar 

  • Baker H, Kawano T, Margolis FL, Joh TH (1983) Transneuronal regulation of tyrosine hydroxylase expression in olfactory bulb of mouse and rat. J Neurosci 3:69–78

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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 215:601–610

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Borisovska M, Bensen AL, Chong G, Westbrook GL (2013) Distinct modes of dopamine and GABA release in a dual transmitter neuron. J Neurosci 33:1790–1796

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 407:404–414

    Article  PubMed  Google Scholar 

  • 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 429:554–570

    Article  PubMed  Google Scholar 

  • Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187

    Article  CAS  PubMed  Google Scholar 

  • 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 35:1573–1590

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 349:151–154

    Article  CAS  PubMed  Google Scholar 

  • Davis BJ, Macrides F (1983) Tyrosine hydroxylase immunoreactive neurons and fibers in the olfactory system of the hamster. J Comp Neurol 214:427–440

    Article  Google Scholar 

  • 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 27:657–664

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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 28:8217–8229

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 266:307–318

    Article  CAS  PubMed  Google Scholar 

  • Gire DH, Schoppa NE (2009) Control of on/off glomerular signaling by a local GABAergic microcircuit in the olfactory bulb. J Neurosci 29:13454–13464

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 489:467–479

    Article  PubMed  Google Scholar 

  • Halász N (1990) The vertebrate olfactory system: chemical neuroanatomy, function and development. Akadémiai Kiadó, Budapest

    Google Scholar 

  • 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 10:251–259

    Article  PubMed  Google Scholar 

  • Hinds JW (1968a) Autoradiographic study of histogenesis in the mouse olfactory bulb I. Time of origin of neurons and neuroglia. J Comp Neurol 134:287–304

    Article  CAS  PubMed  Google Scholar 

  • Hinds JW (1968b) Autoradiographic study of histogenesis in the mouse olfactory bulb II. Cell proliferation and migration. J Comp Neurol 134:305–322

    Article  CAS  PubMed  Google Scholar 

  • Imai T (2014) Construction of functional neuronal circuitry in the olfactory bulb. Semin Cell Dev Biol 35:180–188

    Article  PubMed  Google Scholar 

  • 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 30:1185–1196

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kosaka T, Hama K (1982–83) Synaptic organization in the teleost olfactory bulb. J Physiol 78:707–719

  • Kosaka K, Kosaka T (1999) Distinctive neuronal organization of the olfactory bulb of the laboratory shrew. NeuroReport 10:267–273

    Article  CAS  PubMed  Google Scholar 

  • 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 430:542–561

    Article  CAS  PubMed  Google Scholar 

  • Kosaka T, Kosaka K (2003) Neuronal gap junctions in the rat main olfactory bulb, with special reference to intraglomerular gap junctions. Neurosci Res 45:189–209

    Article  CAS  PubMed  Google Scholar 

  • 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 472:1–12

    Article  PubMed  Google Scholar 

  • Kosaka T, Kosaka K (2004b) Neuronal gap junctions between intraglomerular mitral/tufted cell dendrites in the mouse main olfactory bulb. Neurosci Res 49:373–378

    Article  PubMed  Google Scholar 

  • 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 80:80–90

    Article  PubMed  Google Scholar 

  • 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 131:611–625

    Article  CAS  PubMed  Google Scholar 

  • 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 1167:42–55

    Article  CAS  PubMed  Google Scholar 

  • Kosaka T, Kosaka K (2007b) Heterogeneity of nitric oxide synthase-containing neurons in the mouse olfactory bulb. Neurosci Res 57:165–178

    Article  CAS  PubMed  Google Scholar 

  • 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 60:56–72

    Article  CAS  PubMed  Google Scholar 

  • 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 60:349–354

    Article  CAS  PubMed  Google Scholar 

  • 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 64:436–441

    Article  CAS  PubMed  Google Scholar 

  • Kosaka T, Kosaka K (2009b) Olfactory bulb anatomy. In: Squire LR (ed) Encyclopedia of neuroscience, vol 7. Academic, Oxford, pp 59–69

    Chapter  Google Scholar 

  • Kosaka T, Kosaka K (2010) Heterogeneity of calbindin-containing neurons in the mouse olfactory bulb: I general description. Neurosci Res 67:275–292

    Article  CAS  PubMed  Google Scholar 

  • Kosaka T, Kosaka K (2011) “Interneurons” in the olfactory bulb revisited. Neurosci Res 69:93–99

    Article  CAS  PubMed  Google Scholar 

  • Kosaka T, Kosaka K (2013) Secretagogin-containing neurons in the mouse main olfactory bulb. Neurosci Res 77:16–32

    Article  CAS  PubMed  Google Scholar 

  • Kosaka T, Kosaka K (2014) Olfactory bulb anatomy. Reference Module in Biomedical Sciences. Elsevier. doi:10.1016/B978-0-12-801238-3.04705-X

  • 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 343:166–171

    Article  CAS  PubMed  Google Scholar 

  • 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 403:355–360

    Article  CAS  PubMed  Google Scholar 

  • 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 413:197–203

    Article  CAS  PubMed  Google Scholar 

  • 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 66:191–210

    Article  CAS  PubMed  Google Scholar 

  • 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 411:373–378

    Article  CAS  PubMed  Google Scholar 

  • 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 71:633–642

    Article  CAS  PubMed  Google Scholar 

  • 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 87:353–362

    Article  CAS  PubMed  Google Scholar 

  • 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 23:73–88

    Article  CAS  PubMed  Google Scholar 

  • 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 76:775–786

    Article  CAS  PubMed  Google Scholar 

  • 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 30:101–110

    Article  CAS  PubMed  Google Scholar 

  • 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 440:219–235

    Article  CAS  PubMed  Google Scholar 

  • Kosaka K, Künzle H, Kosaka T (2005a) Organization of the main olfactory bulb of lesser hedgehog tenrecs. Neurosci Res 53:353–362

    Article  PubMed  Google Scholar 

  • Kosaka T, Deans MR, Paul DL, Kosaka K (2005b) Neuronal gap junctions in the mouse main olfactory bulb: morphological analyses on transgenic mice. Neuroscience 134:757–769

    Article  CAS  PubMed  Google Scholar 

  • 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 62:176–186

    Article  CAS  PubMed  Google Scholar 

  • Lepousez G, Valley MT, Lledo PM (2013) The impact of adult neurogenesis on olfactory bulb circuits and computations. Annu Rev Physiol 75:339–363

    Article  CAS  PubMed  Google Scholar 

  • 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 33:2916–2926

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145–1148

    Article  CAS  PubMed  Google Scholar 

  • 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 301:243–261

    Article  PubMed  Google Scholar 

  • Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173–189

    Article  CAS  PubMed  Google Scholar 

  • Macrides F, Schneider SP (1982) Laminar organization of mitral and tufted cells in the main olfactory bulb of the adult hamster. J Comp Neurol 208:419–430

    Article  CAS  PubMed  Google Scholar 

  • Maher BJ, Westbrook GL (2008) Co-transmission of dopamine and GABA in periglomerular cells. J Neurophysiol 99:1559–1564

    Article  CAS  PubMed  Google Scholar 

  • Masland RH (2012) The neuronal organization of the retina. Neuron 76:266–280

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McQuiston AR, Katz LC (2001) Electrophysiology of interneurons in the glomerular layer of the rat olfactory bulb. J Neurophysiol 86:1899–1907

    CAS  PubMed  Google Scholar 

  • Merkle FT, Mirzadehe Z, Alvarez-Buylla A (2007) Mosaic organization of neural stem cells in the adult brain. Science 317:381–384

    Article  CAS  PubMed  Google Scholar 

  • 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 47:221–226

    Article  CAS  PubMed  Google Scholar 

  • 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 106:22492–22497

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nagayama S, Homma R, Imamura F (2014) Neuronal organization of olfactory bulb circuits. Front Neural Circuits 08–00098:1–19

    Google Scholar 

  • 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 502:990–1002

    Article  CAS  PubMed  Google Scholar 

  • 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 501:825–836

    Article  CAS  PubMed  Google Scholar 

  • Pignatelli A, Kobayashi K, Okano H, Belluzzi O (2005) Functional properties of dopaminergic neurons in the mouse olfactory bulb. J Physiol 564:501–514

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pinching AJ, Powell TPS (1971a) Ultrastructural features of transneuronal cell degeneration in the olfactory bulb. J Cell Sci 8:253–287

    CAS  PubMed  Google Scholar 

  • Pinching AJ, Powell TPS (1971b) The neuron types of the glomerular layer of the olfactory bulb. J Cell Sci 9:305–345

    CAS  PubMed  Google Scholar 

  • Pinching AJ, Powell TPS (1971c) The neuropil of the glomeruli of the olfactory bulb. J Cell Sci 9:347–377

    CAS  PubMed  Google Scholar 

  • Pinching AJ, Powell TPS (1971d) The neuropil of the periglomerular region of the olfactory bulb. J Cell Sci 9:379–409

    CAS  PubMed  Google Scholar 

  • Pinching AJ, Powell TPS (1972a) A study of termination of centrifugal fibres in the glomerular layer of the olfactory bulb. J Cell Sci 10:621–635

    CAS  PubMed  Google Scholar 

  • Pinching AJ, Powell TPS (1972b) The terminal degeneration in the olfactory bulb of the rat. J Cell Sci 10:585–619

    CAS  PubMed  Google Scholar 

  • Pinching AJ, Powell TPS (1972c) Experimental studies on the axons intrinsic to the glomerular layer of the olfactory bulb. J Cell Sci 10:637–655

    CAS  PubMed  Google Scholar 

  • Price JL, Powell TPS (1970a) The morphology of the granule cells of the olfactory bulb. J Cell Sci 7:91–123

    CAS  PubMed  Google Scholar 

  • 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 7:157–187

    CAS  PubMed  Google Scholar 

  • Price JL, Powell TPS (1970c) The mitral and short axon cells of the olfactory bulb. J Cell Sci 7:631–651

    CAS  PubMed  Google Scholar 

  • 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

  • Ribak CE, Vaughn JE, Saito K, Barber R, Roberts E (1977) Glutamate decarboxylase localization in neurons of the olfactory bulb. Brain Res 126:1–18

    Article  CAS  PubMed  Google Scholar 

  • Schneider SP, Macrides F (1978) Laminar distribution of interneurons in the main olfactory bulb of adult hamster. Brain Res Bull 3:73–82

    Article  CAS  PubMed  Google Scholar 

  • 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 255:503–518

    Article  Google Scholar 

  • Shepherd G (2004) The synaptic organization of the brain, 5th edn. Oxford University Press, New York

    Book  Google Scholar 

  • Valverde F (1965) Studies on the piriform lobe. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Whitman MC, Greer CA (2007) Adult-generated neurons exhibit diverse developmental fates. Dev Neurobiol 67:1079–1093

    Article  CAS  PubMed  Google Scholar 

  • 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 96:2354–2363

    Article  CAS  PubMed  Google Scholar 

  • Zhu P, Frank T, Friedrich RW (2013) Equalization of odor representations by a network of electrically coupled inhibitory interneurons. Nature Neurosci 16:1678–1686

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Ms. Chie Tanaka and Ms. Kazuyo Sawai for their technical and secretarial assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Toshio Kosaka.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Grant sponsor

JSPS KAKENHI Grants 23300124, 23500412, 26430039.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kosaka, T., Kosaka, K. Neuronal organization of the main olfactory bulb revisited. Anat Sci Int 91, 115–127 (2016). https://doi.org/10.1007/s12565-015-0309-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12565-015-0309-7

Keywords

Navigation