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Mitral cell dendrites: a comparative approach

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Abstract

Phylogenetically persistent structures such as the mitral cells of the vertebrate olfactory bulb undergo changes in their dendritic arbor in the course of evolution. The morphology of mitral cells and the main elements of the olfactory bulb circuit in all classes of vertebrates are reviewed in this paper. Most of the neuronal elements found in the mammalian olfactory bulb are present in anamniotes. However, in contrast to those of amniotes, the mitral cells of most anamniotes lack basal dendrites, and periglomerular cells are absent in fish. This suggests a different circuitry and therefore drastic changes in the processing of olfactory information within the olfactory bulb. Lateral inhibition, conferred by basal dendrites in amniotes, must then utilize other mechanisms in anamniotes. Moreover, the marked segregation of olfactory inputs onto mammalian mitral cells is less obvious in mitral cells of anamniotes that lack basal dendrites. The general role of dendrites, including those of mitral cells, is discussed in the light of increasing evidence for dendritic excitability. The evolutionary significance of mitral cell basal dendrites is also discussed.

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References

  • Andres KH (1965) Der Feinbau des Bulbus olfactorius der Ratte unter besonderer Berücksichtigung der Synaptischen Verbindungen. Z Zellforsch Mikrosk Anat 65:530–561

    Google Scholar 

  • Andres KH (1970) Anatomy and ultrastructure of the olfactory bulb in fish, amphibia, reptiles, birds, and mammals. In: Wolstenholme GEW, Knight J (eds) Ciba Foundation Symposium on Taste and Smell in Vertebrates. Churchill, London, pp 177–194

    Google Scholar 

  • Andres KH (1975) New morphological results for physiology and smell and taste. Arch Otolaryngol 210:1–41

    Google Scholar 

  • Ariens-Kappers CU (1920) Die Vergleichende Anatomie des Nervensystems der Wirbeltiere und des Menschen. II. Bohn. Haarlem

  • Ariens-Kappers CU, Huber GC, Crosby EC (1936) The comparative anatomy of the nervous system of vertebrates, including man. Macmillan, New York

    Google Scholar 

  • Baker H, Greer CA (1990) Region-specific consequences of PCD gene expression in the olfactory system. J Comp Neurol 293:125–133

    Google Scholar 

  • Bang BG, Cobb S (1968) The size of the olfactory bulb in 108 species of birds. Auk 85:55–61

    Google Scholar 

  • Barrett EF, Barrett JN (1976) Separation of two voltage-sensitive potassium currents and demonstration of a tetrodotoxin-resistant calcium current in frog motoneurons. J Physiol (Lond) 255:737–774

    Google Scholar 

  • Boycott BB, Wässle H (1974) The morphological types of ganglion cells of the domestic cat's retina. J Physiol (Lond) 240:397–419

    Google Scholar 

  • Breazile JE (1979) Systema nervosum centrale. In: Baumel JE (ed) Nomina anatomica avium. Academic Press, London, pp 417–472

    Google Scholar 

  • Buonviso N, Chaput MA, Scott JW (1991) Mitral cell-to-glomerulus connectivity: an HRP study of the orientation of mitral cell apical dendrites. J Comp Neurol 307:57–64

    Google Scholar 

  • Cajal S Ramon y (1911) Histologie du systéme nerveux de l'homme et des vertébrés. Maloine, Paris

    Google Scholar 

  • Carey JH (1982) The telencephalon of reptiles. In: Crosby EC, Schnitzlein HN (eds) Comparative correlative neuroanatomy of the vertebrate telencephalon. Macmillan, New York, pp 200–217

    Google Scholar 

  • Carroll RL (1987) Vertebrate paleontology and evolution. Freeman, New York

    Google Scholar 

  • Cleland BG, Lewick WR, Wässle H (1975) Physiological identification of a morphological class of cat retinal ganglion cells. J Physiol (Lond) 248:151–171

    Google Scholar 

  • Creuzfeldt OD (1975) Neurophysiological correlates of different functional states of the brain. In: Ingvar DH, Lassen NA (eds) Brain work. Alfred Benzon symposium VIII. Academic Press, New York, pp 21–46

    Google Scholar 

  • Crosby EG (1917) The forebrain of Alligator mississipiensis. J Comp Neurol 27:325–334

    Google Scholar 

  • Crosby EC, Humphrey T (1939) Studies of the vertebrate telencephalon. II. The nuclear configuration of the olfactory and accessory olfactory formations and of the nucleus olfactorius anterior of certain reptiles, birds, and mammals. J Comp Neurol 71:121–213

    Google Scholar 

  • Crosby EC, Schnitzlein HN (1982) Comparative correlative neuroanatomy of the vertebrate telencephalon. Macmillan, New York

    Google Scholar 

  • Dryer L, Graziadei PPC (1991) Heterogeneity and compartmentalization in the olfactory bulb of elasmobranch fishes. Soc Neurosci Abstr 17:1017

    Google Scholar 

  • Dryer L, Graziadei PPC (1992) Carbocyanine dyes as tracers in the elasmobranch olfactory system. Soc Neurosci Abstr 18:1199

    Google Scholar 

  • Dryer L, Graziadei PPC (1993) A pilot study on morphological compartmentalization and heterogeneity of the elasmobranch olfactory bulb. Anat Embryol 188:41–51

    Google Scholar 

  • Durward A (1932) Observations on the cell masses in the cerebral hemispheres of the New-Zealand kiwi (Apteryx australis). J Anat 66:437–477

    Google Scholar 

  • Ebbesson SOE, Bazer GT, Jane JA (1986) Some primary olfactory neurons project to the contralateral olfactory bulb in Xenopus laevis. Neurosci Lett 65:234–238

    Google Scholar 

  • Eccles JC, Fatt P, Koketsu K (1954) Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurons. J Physiol (Lond) 216:524–564

    Google Scholar 

  • Edinger L (1905) Die Deutung des Vorderhirns bei Petromyzon. Anat Anz 26:633–635

    Google Scholar 

  • Fifkova E, Morales M (1989) Calcium-regulated contractile and cytoskeletal proteins in dendritic spines may control synaptic plasticity. Ann NY Acad Sci 568:131–137

    Google Scholar 

  • Fujita I, Satou M, Ueda K (1988) Morphology of physiologically identified mitral cells in the carp olfactory bulb: a light microscopic study after intracellular staining with horseradish peroxidase. J Comp Neurol 267:253–268

    Google Scholar 

  • Fukuda Y, Hsiao CF, Watanabe M (1985) Morphological correlates of Y-, X-, and W-type ganglion cells in the cat's retina. Vision Res 25:319–327

    Google Scholar 

  • Garcia-Verdugo JM, LLahi S, Farinas J, Martin V (1986) Laminar organization of the main olfactory bulb of Podarcis hispanica: an EM and Golgi study. J Hirnforsch 27:87–100

    Google Scholar 

  • Gemne G, Døving KB (1969) Ultrastructural properties of primary olfactory neurons in fish (Lota lota L.). Am J Anat 126:457–476

    Google Scholar 

  • Getchell TV, Shepherd GM (1975) Synaptic actions on mitral and tufted cells elicited by olfactory nerve volleys in the rabbit. J Physiol (Lond) 251:497–522

    Google Scholar 

  • Gould RJ, Murphy KM, Snyder SH (1985) Autoradiographic localization of calcium channel antagonist receptors in rat brain with [3H] nitrendipine. Brain Res 330:217–223

    Google Scholar 

  • Graziadei PPC, Monti-Graziadei AG (1986) Principles of organization of the vertebrate olfactory glomerulus: an hypothesis. Neuroscience 19:1025–1035

    Google Scholar 

  • Green JD, Mancia M, Baumgarten R von (1962) Recurrent inhibition in the olfactory bulb. I. Effect of antidromic stimulation of the lateral olfactory tract. J Neurophysiol 25:467–488

    Google Scholar 

  • Greer CA (1987) Golgi analysis of dendritic organization among denervated olfactory bulb granule cells. J Comp Neurol 257:442–452

    Google Scholar 

  • Greer CA, Halasz N (1987) Plasticity of dendrodendritic microcircuits following mitral cell loss in the olfactory bulb of the murine mutant Purkinje Cell Degeneration. J Comp Neurol 256:284–298

    Google Scholar 

  • Greer CA, Shepherd GM (1982) Mitral cell degeneration and sensory function in the neurological mutant mouse Purkinje Cell Degeneration (PCD). Brain Res 235:156–161

    Google Scholar 

  • Greer CA, Stewart WB, Kauer JS, Shepherd GM (1981) Topographical and laminar localization of 2-deoxyglucose uptake in rat olfactory bulb induced by electrical stimulation of olfactory nerves. Brain Res 217:279–293

    Google Scholar 

  • Guthrie PB, Segal M, Kater SB (1991) Independent regulation of calcium revealed by imaging dendritic spines. Nature 354:76–79

    Google Scholar 

  • Haberly LB, Price JL (1977) The axonal projection patterns of the mitral and tufted cells of the olfactory bulb in the rat. Brain Res 129:152–157

    Google Scholar 

  • Henton WW, Smith JC, Tucker D (1966) Odor discrimination in pigeons. Science 153:1138–1139

    Google Scholar 

  • Herrick CJ (1921) The connections of the vomeronasal nerve, accessory bulb, and amygdala in amphibia. J Comp Neurol 33:213–280

    Google Scholar 

  • Herrick CJ (1924) The amphibian forebrain. II. The olfactory bulb in Amblystoma. J Comp Neurol 37:373–396

    Google Scholar 

  • Herrick CJ (1931) The amphibian forebrain. V. The olfactory bulb of Necturus. J Comp Neurol 53:55–69

    Google Scholar 

  • Herrick CJ (1948) The brain of the tiger salamander. University of Chicago Press, Chicago

    Google Scholar 

  • Holmer WR (1990) Is the function of dendritic spines to concentrate calcium? Brain Res 519:338–342

    Google Scholar 

  • Holmgren N (1922) Points of view concerning forebrain morphology in lower vertebrates. J Comp Neurol 34:391–459

    Google Scholar 

  • Hounsgaard J, Mitgaard J (1989) Dendrite processing in more ways than one. Trends Neurosci 12:313–315

    Google Scholar 

  • Huber GC, Crosby EC (1929) The nuclei and fiber paths of the avian diencephalon, with consideration of telencephalic and certain mesencephalic centers and connections. J Comp Neurol 48:1–186

    Google Scholar 

  • Hunter JL (1923) The forebrain of Apteryx australis. Kon Ned Akad Wet Proc Sect Sci 26:807–824

    Google Scholar 

  • Ichikawa M (1976) Fine structure of the olfactory bulb in the goldfish, Carassius auratus. Brain Res 115:43–56

    Google Scholar 

  • Iwahori N, Kiyota E, Nakamura K (1987) A Golgi study on the olfactory bulb in the lamprey, Lampetra japonica. Neurosci Res 5:126–139

    Google Scholar 

  • Iwahori N, Nakamura K, Mameya C (1989) A Golgi study on the main olfactory bulb in the snake Elaphe quadrivingata. Neurosci Res 6:411–425

    Google Scholar 

  • Iwahori N, Nakamura K, Kameda S (1992) A Golgi study on the olfactory bulb in the red stingray Dasyatis akajei. Okajimas Folia Anat Jpn 68:333–342

    Google Scholar 

  • Jahnsen H, Llinas R (1984) Ionis basis for the electro-responsiveness and oscillatory properties of guinea pig thalamic neurones in vitro. J Physiol (Lond) 349:227–247

    Google Scholar 

  • Jaslove SN (1992) The integrative properties of spiny distal dendrites. Neuroscience 47:495–519

    Google Scholar 

  • Jiang T, Holley A (1992) Morphological variations among output neurons of the olfactory bulb in the frog (Rana ridibunda). J Comp Neurol 320:86–96

    Google Scholar 

  • Johnston JB (1912) The telencephalon in cyclostomes. J Comp Neurol 22:341–404

    Google Scholar 

  • Johnston JB (1915) The cell masses in the forebrain of the turtle, Cistudo Carolina. J Comp Neurol 25:393–468

    Google Scholar 

  • Kemali M, Guglielmotti V (1987) A horseradish peroxidase study of the olfactory system of the frog, Rana esculenta. J Comp Neurol 263:400–417

    Google Scholar 

  • Kishi K, Mori K, Tazawa Y (1982) Three-dimensional analysis of dendritic trees in the rabbit olfactory bulb. Neurosci Lett 28:127–132

    Google Scholar 

  • Kishi K, Mori K, Ojima H (1984) Distribution of local axon collaterals of mitral, displaced mitral, and tufted cells in the rabbit olfactory bulb. J Comp Neurol 225:511–526

    Google Scholar 

  • Koch C, Zador A (1993) The function of dendritic spines: devices subserving biochemical rather than electrical compartmentalization. J Neurosci 13:413–422

    Google Scholar 

  • Kosaka T (1980) Ruffed cell: a new type of neuron with a distinctive initial unmyelinated portion of the axon in the olfactory bulb of the goldfish (Carassius auratus). II. Fine structure of the ruffed cell. J Comp Neurol 193:119–145

    Google Scholar 

  • Kosaka T, Hama K (1979) Ruffed cell: a new type of neuron with a distinctive initial unmyelinated portion of the axon in the olfactory bulb of the goldfish (Carassius auratus). I. Golgi impregnation and thin sectioning studies. J Comp Neurol 186:301–319

    Google Scholar 

  • Kosaka T, Hama K (1980) Presence of the ruffed cell in the olfactory bulb of the catfish, Parasilurus asotus, and the sea eel, Conger myriaster. J Comp Neurol 193:103–117

    Google Scholar 

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

    Google Scholar 

  • Kosaka T, Hama K (1982b) Structure of the mitral cell in the olfactory bulb of the goldfish (Carassius auratus). J Comp Neurol 212:365–384

    Google Scholar 

  • Lancet D, Greer CA, Kauer JS, Shepherd GM (1982) Mapping of odor-related neuronal activity in the olfactory bulb by high resolution 2-DG autoradiography. Proc Natl Acad Sci USA 79:670–674

    Google Scholar 

  • Leveteau J, Andriason I, Mac Leod P (1992) The bilateral bulbar projections of the primary olfactory neurons in the frog. Exp Brain Res 89:93–104

    Google Scholar 

  • Llinas R, Hess R (1976) Tetrodoxin-resistant dendritic spikes in avian Purkinje cells. Proc Natl Acad Sci USA 73:2520–2523

    Google Scholar 

  • Llinas R, Nicholson C (1971) Electrophysiological properties of dendrites and somata in Alligator Purkinje cells. J Neurophysiol 34:532–551

    Google Scholar 

  • Llinas R, Sugimori M (1980) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol (Lond) 305:197–213

    Google Scholar 

  • Loewenthal N (1894) Contribution á l'etude du lobe olfactif des reptiles. J Anat Physiol 30:249–261

    Google Scholar 

  • Lowenstein OE (1975) Comparative morphology and physiology of the vestibular system. In: Kornhuber HH (ed) Handbook of sensory physiology, vol 4. Springer, Berlin Heidelberg New York, pp 75–120

    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

    Google Scholar 

  • Madison DV, Malenka RC, Nicoll RA (1991) Mechanisms underlying long-term potentiation of synaptic transmission. Annu Rev Neurosci 14:379–397

    Google Scholar 

  • Maeda N, Wada K, Yukazi M, Mikoshiba K (1989) Autoradiographie visualization of a calcium channel antagonist, [125I]♦ GVIA, binding site in the brains of normal and cerebellar mutant mice (PCD and weaver). Brain Res 489:21–30

    Google Scholar 

  • Mjaatvedt AE, Wong-Riley MTT (1988) Relationship between synaptogenesis and cytochrome oxidase activity in Purkinje cells of the developing rat cerebellum. J Comp Neurol 277:155–182

    Google Scholar 

  • Monti-Graziadei AG, Graziadei PPC (1992) Sensory reinnervation after partial removal of the olfactory bulb. J Comp Neurol 316:32–44

    Google Scholar 

  • Mori K (1987) Membrane and synaptic properties of identified neurons in the olfactory bulb. Prog Neurobiol 29:275–320

    Google Scholar 

  • Mori K, Takagi SF (1975) Spike generation in the mitral cell dendrite of the rabbit olfactory bulb. Brain Res 100:685–689

    Google Scholar 

  • Mori K, Kishi K, Ojima H (1983) Distribution of dendrites of mitral, displaced mitral, tufted, and granule cells in the rabbit olfactory bulb. J Comp Neurol 219:339–355

    Google Scholar 

  • Mori K, Nowycky MC, Shephard GM (1982) Impulse activity in presynaptic dendrites: analysis of mitral cells in the isolated turtle olfactory bulb. J Neurosci 2:497–502

    Google Scholar 

  • Mori K, Nowycky MC, Shepherd GM (1984) Synaptic excitatory and inhibitory interactions at distal dendrites sites on mitral cells in the isolated turtle olfactory bulb. J Neurosci 4:2291–2296

    Google Scholar 

  • Mullen RJ, Eicher SM, Sidman RL (1976) Purkinje cell degeneration, a new neurological mutation in the mouse. Proc Natl Acad Sci USA 73:208–212

    Google Scholar 

  • Muller W, Connor JA (1991) Dendritic spines as individual neuronal compartments for synaptic Ca2+ responses. Nature 354:73–75

    Google Scholar 

  • Murase K, Randic M (1983) Electrophysiological properties of rat spinal dorsal neurones in vitro: calcium-dependent action potentials. J Physiol (Lond) 334:141–153

    Google Scholar 

  • Nickell WT, Behbehani MM, Shipley MT (1992) In vitro synaptic activation of adult rat olfactory bulb mitral cells recorded by conventional and whole cell patch techniques. Soc Neurosci Abstr 18:1200

    Google Scholar 

  • Nicoll RA (1971) Recurrent excitation of secondary olfactory neurons: a possible mechanism for signal amplification. Science 171:824–825

    Google Scholar 

  • Nicoll RA, Jahr CE (1982) Self excitation of olfactory bulb neurones. Nature 296:441–444

    Google Scholar 

  • Nieuwenhuys R (1967) Comparative anatomy of olfactory centers and tracts. Prog Brain Res 23:1–63

    Google Scholar 

  • O'Gorman S, Sidman R (1985) Degeneration of thalamic neurons in PCD mice. I. Distribution of neuronal loss. J Comp Neurol 234:298–316

    Google Scholar 

  • Oka Y (1983) Golgi, electron microscpic and combined Golgi-electron microscopic studies of the mitral cells in the goldfish olfactory bulb. Neuroscience 8:723–742

    Google Scholar 

  • Orona E, Rainer EC, Scott JW (1984) Dendritic and axonal organization of mitral and tufted cells in the rat olfactory bulb. J Comp Neurol 226:346–356

    Google Scholar 

  • Pearson R (1972) The avian brain. Academic Press, London, p 658

    Google Scholar 

  • Phillips CG, Powell TPS, Shepherd GM (1963) Responses of mitral cells to stimulation of the lateral olfactory tract in the rabbit. J Physiol (Lond) 168:65–88

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Pomeroy SL, Lamantia AS, Purves D (1990) Postnatal construction of neural circuitry in the mouse olfactory bulb. J Neurosci 10:1952–1966

    Google Scholar 

  • Pough FH, Heiser JB, McFarland WN (1989) Vertebrate life, 3rd edn. Macmillan, New York

    Google Scholar 

  • Price JL, Powell TPS (1970a) An electron-microscopic study of the termination of the afferent fibres to the olfactory bulb from the cerebral hemispheres. J Cell Sci 7:157–187

    Google Scholar 

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

    Google Scholar 

  • Rall W (1962) Theory of the physiological properties of dendrites. Ann NY Acad Sci 96:1071–3092

    Google Scholar 

  • Rall W, Segev I (1988) Synaptic integration and excitable dendritic spine clusters: structure and function. In: Lasek R, Black R (eds) Intrinsic determinants of neuronal form and function. Liss, New York, pp 263–282

    Google Scholar 

  • Reese TS (1970) Discussion. In: Wolstenholme GE, Knight J (eds) Ciba Foundation Symposium for Taste and Olfaction in Vertebrates. Churchill, London, pp 194–196

    Google Scholar 

  • Rose M (1914) Über die Cytoarchitektonische Gliederung des Vorderhirns der Vögel. J Psychol Neurol 21:278–352

    Google Scholar 

  • Royet JP, Souchier C, Jourdan F, Ploye H (1988) Morphometric study of the glomerular population in the mouse olfactory bulb: numerical density and size distribution along the rostrocaudal axis. J Comp Neurol 270:559–568

    Google Scholar 

  • Saito HA (1983) Morphology of physiologically identified X, Y, and W type retinal ganglion cells of the cat. J Comp Neurol 221:279–288

    Google Scholar 

  • Sanes DH, Goldstein NA, Ostad M, Millman DE (1990) Dendritic morphology of central auditory neurons correlates with their tonotopic position. J Comp Neurol 294:443–454

    Google Scholar 

  • Satou M (1990) Synaptic organization, local neuronal circuitry, and functional segregation of the teleost olfactory bulb. Prog Neurobiol 34:115–142

    Google Scholar 

  • Scalia F (1976) Structure of the olfactory and accessory olfactory systems. In: Llinas R, Precht W (eds) Frog neurobiology. Springer, Berlin Heidelberg New York, pp 213–233

    Google Scholar 

  • Scalia F, Gallousis G, Roca S (1991) A note on the organization of the amphibian olfactory bulb. J Comp Neurol 305:435–442

    Google Scholar 

  • Schild D, Riedel H (1991) Significance of glomerular compartmentalization for olfactory coding. Biophys J 61:704–715

    Google Scholar 

  • Scheibel ME, Scheibel AB (1975a) Dendrites as neuronal couplers: the dendrite bundle. In Santini M (ed) Golgi Centennial Symposium Proceedings. Raven Press, New York, pp 347–354

    Google Scholar 

  • Scheibel ME, Scheibel AB (1975b) Dendrite bundles, central programs and the olfactory bulb. Brain Res 95:407–421

    Google Scholar 

  • Schneider SP, Scott JW (1983) The orthodromic response properties of rat olfactory mitral and tufted cells correlate with their projection patterns. J Neurophysiol 50:358–378

    Google Scholar 

  • Schnitzlein HN (1982) The telencephalon of fishes. In: Crosby EC, Schnitzlein HN (eds) Comparative correlative neuroanatomy of the vertebrate telencephalon. MacMillan, New York, pp 3–160

    Google Scholar 

  • Scott JW (1981) Electrophysiological identification of mitral and tufted cells and distribution of their axons in the olfactory system of the rat. J Neurophysiol 46:918–931

    Google Scholar 

  • Scott JW, Mcbride RL, Schneider SP (1980) The organization of the projections from the olfactory bulb to the piriform cortex and olfactory tubercle in the rat. J Comp Neurol 194:519–534

    Google Scholar 

  • Segev I, Rall W (1991) Computer models of dendritic excitability. Soc Neurosci Abstr 17:1515

    Google Scholar 

  • Shepherd GM (1966) The orientation of mitral cell dendrites. Exp Neurol 14:390–395

    Google Scholar 

  • Shepherd GM (1972) Synaptic organization in the mammalian olfactory bulb. Physiol Rev 52:864–917

    Google Scholar 

  • Shepherd GM (1977) The olfactory bulb: a simple system in the mammalian brain. In: Brookhart JM, Mountcastle VB, Kandel ER (eds) Handbook of physiology, vol 1, part 2. American Physiological Society, Bethesda, pp 945–968

    Google Scholar 

  • Shepherd GM (1979) The synaptic organization of the brain. Oxford University Press, Oxford, pp 152–183

    Google Scholar 

  • Shepherd GM (1981) The olfactory glomerulus: its significance for sensory processing. In: Katsuki Y, Norgren R, Sato M (eds) Brain mechanisms of sensation. Wiley, New York, pp 209–223

    Google Scholar 

  • Sicard G, Royet JP, Jourdan F (1989) A comparative study of 2-deoxyglucose patterns of glomerular activation in the olfactory bulb of C57BL/6J and AKR/J mice. Brain Res 481:325–334

    Google Scholar 

  • Sieck MH, Wenzel BM (1969) Electrical activity of the olfactory bulb of the pigeon. Electroenceph Clin Neurophysiol 26:69–79

    Google Scholar 

  • Skatteble A, Triggle DJ (1987) Regional distribution of calcium channel ligand (1,4-dihydropyridine) binding sites and 45 Ca2+ uptake processes in rat brain. Biochem Pharmacol 36:4163–4166

    Google Scholar 

  • Skeen LC, Hall WC (1977) Efferent projections of the main and accessory bulb in the tree shrew (Tupaia glis). J Comp Neurol 172:1–36

    Google Scholar 

  • Stanford LR, Sherman SM (1984) Structure/function relationships of retinal ganglion cells in the cat. Brain Res 297:381–386

    Google Scholar 

  • Sterzi G (1909) Il systema nervoso centrale dei vertebrati, vol 2. Draghi, Padova

    Google Scholar 

  • Steward O (1983) Polyribosomes at the base of dendritic spines of central nervous system neurons — their possible role in synapse construction and modification. Cold Spring Harbor Symposia in Quantitative Biology 48:745–759

    Google Scholar 

  • Steward O (1987) Regulation of synaptogenesis through the local synthesis of protein at the postsynaptic site. Prog Brain Res 71:267–279

    Google Scholar 

  • Steward O, Reeves TM (1988) Protein-synthetic machinery beneath postsynaptic sites on CNS neurons: association between polyribosomes and other organelles at the synaptic site. J Neurosci 8:176–184

    Google Scholar 

  • Stewart W (1985) Labelling of olfactory bulb glomeruli following horseradish peroxidase lavege of nasal cavity. Brain Res 347:200–203

    Google Scholar 

  • Sugimori M, Llinas R (1992) Dual patch-clamping of mammalian Purkinje cells in cerebellar slices. Soc Neurosci Abstr 18:1358

    Google Scholar 

  • Takami S, Graziadei PPC (1991) Light microscopic Golgi study of mitral/tufted cells in the accessory olfactory bulb of the adult rat. J Comp Neurol 311:65–83

    Google Scholar 

  • Takeda T, Ishikawa A, Ohtomo K, Kobayashi Y, Matsuoka T (1992) Fractal dimension of dendritic tree of cerebellar Purkinje cell during onto- and phylogenetic development. Neurosci Res 13:19–31

    Google Scholar 

  • Tucker D (1965) Electrophysiological evidence for olfactory function in birds. Nature 207:34–36

    Google Scholar 

  • Tucker D, Smith JC (1976) Vertebrate olfaction. In: Masterson RB, Bitterman ME, Campbell CBG, Hotton N (eds) Evolution of brain and behavior in vertebrates. Wiley-Halsted Press, New York, pp 25–52

    Google Scholar 

  • Usowicz MM, Sugimori M, Cherksey B, Llinas R (1992) P-type Calcium channels in the somata and dendrites of adult cerebellar Purkinje cells. Neuron 9:1185–1199

    Google Scholar 

  • Wenzel BM (1967) Olfactory perception in birds. In: Hayashi T (ed) Olfaction and taste. Proc 2nd Int Symp. Pergamon Press, Oxford, pp 203–217

    Google Scholar 

  • Wenzel BM (1968) Olfactory prowess of the Kiwi. Nature 220:1133–1134

    Google Scholar 

  • Wenzel BM, Salzman A (1969) Olfactory bulb ablation or nerve section and behavior in pigeons in non-olfactory learning. Exp Neurol 22:472–479

    Google Scholar 

  • Wenzel BM, Sieck MH (1972) Olfactory perception and bulbar electrical activity in several avian species. Physiol Behav 9:287–293

    Google Scholar 

  • White EL (1972) Synaptic organization in the olfactory glomerulus of the mouse. Brain Res 37:69–80

    Google Scholar 

  • White EL (1973) Synaptic organization of the mammalian olfactory glomerulus: new findings including an intraspecific variation. Brain Res 60:299–313

    Google Scholar 

  • Wong RKS, Prince DA (1978) Participation of calcium spikes during intrinsic burst firing in hippocampal neurones. Brain Res 159:385–390

    Google Scholar 

  • Wong RKS, Prince DA, Basbaum AI (1979) Intradendritic recordings from hippocampal neurons. Proc Natl Acad Sci USA 76:986–990

    Google Scholar 

  • Wong-Riley MTT (1989) Cytochrome oxidase: an endogenous marker for neuronal activity. Trends Neurosci 12:94–101

    Google Scholar 

  • Woolf FT, Shepherd GM, Greer CA (1991) Local information processing in dendritic trees: subsets of spines on granule cells of the mammalian olfactory bulb. J Neurosci 11:1837–1854

    Google Scholar 

  • Wyss J, Stanfield B, Cowan W (1980) Structural abnormalities in the olfactory bulb of the Reeler mouse. Brain Res 188:566–571

    Google Scholar 

  • Yamamoto C, Yamamoto T, Iwama K (1963) The inhibitory system in the olfactory bulb studied by intracellular recording. J Neurophysiol 26:403–415

    Google Scholar 

  • Yang G, Masland R (1992) Direct visualization of the dendritic and receptive fields of directionally selective retinal ganglion cells. Science 258:1949–1952

    Google Scholar 

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Dryer, L., Graziadei, P.P.C. Mitral cell dendrites: a comparative approach. Anat Embryol 189, 91–106 (1994). https://doi.org/10.1007/BF00185769

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