Abstract
Long-term potentiation of synaptic transmission is considered to be an elementary process underlying the cellular mechanism of memory formation. In the present study we aimed to examine whether or not the dendrodendritic mitral-to-granule cell synapses in the carp olfactory bulb show plastic changes after their repeated activation. It was found that: (1) the dendrodendritic mitral-to-granule cell synapses showed three types of plasticity after tetanic electrical stimulation applied to the olfactory tract—long-term potentiation (potentiation lasting >1 h), short-term potentiation (potentiation lasting <1 h) and post-tetanic potentiation (potentiation lasting <10 min); (2) Long-term potentiation was generally induced when both the dendrodendritic mitral-to-granule cell synapses and centrifugal fiber-to-granule cell synapses were repeatedly and simultaneously activated; (3) long-term enhancement (>1 h) of the odor-evoked bulbar response accompanied the electrically-induced LTP, and; (4) repeated olfactory stimulation enhanced dendrodendritic mitral-to-granule cell transmission. Based on these results, it was proposed that long-term potentiation (as well as olfactory memory) occurs at the dendrodendritic mitral-to-granule cell synapses after strong and long-lasting depolarization of granule cells, which follows repeated and simultaneous synaptic activation of both the peripheral and deep dendrites (or somata).
Similar content being viewed by others
Abbreviations
- C2 :
-
Component 2 wave
- GC :
-
Granule cell
- lMOT :
-
Lateral MOT
- LOT :
-
Lateral olfactory tract
- MC :
-
Mitral cell
- MOT :
-
Medial olfactory tract
- ON :
-
Olfactory nerve
- OT :
-
Olfactory tract
References
Adrian ED (1950) The electrical activity of the mammalian olfactory bulb. Electroenceph clin Neurophysiol 2:377–388
Allison AC (1953) The morphology of the olfactory system in the vertebrates. Biol Rev 28:195–244
Alonso JR, Lara L, Miguel JJ, Aijón J (1987) Ruffed cells in the olfactory bulb of freshwater teleosts. I. Golgi impregnation. J Anat 155:101–107
Andres KH (1970) Anatomy and ultrastructure of the olfactory bulb in fish, amphibia, reptiles, birds and mammals. In: Wolstenholme GEW, Knight J (eds) Taste and Smell in Vertebrates. Ciba Foundation Symposium, Churchill, London, pp 177–196
Anzai S, Satou M (1996) Long-term and short-term plasticity in the dendro-dendritic mitral-to-granule cell synapse of the teleost olfactory bulb. Neurosci Res 20(Suppl):S223
Arévalo R, Alonso JR, Lara J, Brinon JG, Aijón J (1991) Ruffed cells in the olfactory bulb of freshwater teleosts. II. A Golgi/EM study of the ruff. J Hirnforsch 32:477–484
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
von Bartheld CS, Meyer DL, Fiebig E, Ebbesson SOE (1984) Central connections of the olfactory bulb in the goldfish, Carassius auratus. Cell Tissue Res 238:475–487
Bi G-Q, Poo M-M (2001) Synaptic modification by correlated activity: Hebb’s postulate revisited. Annu Rev Neurosci 24:139–166
Bliss TVP, Collingridge GL (1993) A synaptic model of memory : long-term potentiation in the hippocampus. Nature 361:31–39
Brennan PA, Keverne EB (1997) Neural mechanisms of mammalian olfactory learning. Prog Neurobiol 51:457–481
Brennan P, Kaba H, Keverne EB (1990) Olfactory recognition: a simple memory system. Science 250:1223–1226
Brown TH, Kairiss EW, Keenan CL (1990) Hebbian synapses: biophysical mechanisms and algorithms. Annu Rev Neurosci 13:475–511
Byrd CA, Brunjes PC (1995) Organization of the olfactory system in the adult zebrafish: histological, immunohistochemical, and quantitative analysis. J Comp Neurol 358:247–259
Chen WR, Xiong W, Shepherd GM (2000) Analysis of relations between NMDA receptors and GABA release at olfactory bulb reciprocal synapses. Neuron 25:625–633
Coopersmith R, Weihmuller FB, Kirstein CL, Marshall JF, Leon M (1991) Extracellular dopamine increases in neonatal olfactory bulb during odor preference training. Brain Res 564:149–153
Döving KB (1986) Functional properties of the fish olfactory system. In: Autrum H, Ottoson D, Perl ER, Schmidt RF, Shimazu H, Willis WD (eds) Progress in Sensory Physiology 6. Springer, Berlin Heidelberg, New York, Tokyo, pp 39–104
Durand M, Coronas V, Jourdan F, Quirion R (1998) Developmental and aging aspects of the cholinergic innervation of the olfactory bulb. Int J Devl Neurosci 16:777–785
Egger V, Svoboda K, Mainen ZF (2003) Mechanisms of lateral inhibition in the olfactory bulb: efficiency and modulation of spike-evoked calcium influx into granule cells. J Neurosci 23:7551–7558
Elaagouby A, Gervais R (1996) Induction of a calcium-dependent long-term enhancement of excitability in the rat olfactory bulb. Chem Senses 21:159–168
Ennis M, Linster C, Aroniadou-Anderjaska V, Ciombor K, Shipley M (1998) Glutamate and synaptic plasticity at mammalian primary olfactory synapses. Ann NY Acad Sci USA 855:457–466
Fujita I, Satou M, Ueda K (1984) A field-potential study of centripetal and centrifugal connections of the olfactory bulb in the carp, Cyprinus carpio (L.). Brain Res 321:33–44
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
Halabisky B, Friedman D, Radojicic M, Strawbridge BW (2000) Calcium influx through NMDA receptors directly evokes GABA release in olfactory bulb granule cells. J Neurosci 20:5124–5134
Halász N (1990) The Vertebrate Olfactory System: Chemical Anatomy, Function and Development. Akadémiai Kiadó, Budapest, pp 281
Hall BJ, Delaney KR (2002) Contribution of a calcium-activated non-specific conductance to NMDA receptor-mediated synaptic potentials in granule cells of the frog olfactory bulb. J Physiol 543:819–834
Hara TJ (1992) Fish Chemoreception. Chapman and Hall, London, pp 373
Hasegawa T, Satou M, Ueda K (1994) Intracellular study of generation mechanisms of induced wave in carp (Cyprinus carpio) olfactory bulb. Comp Biochem Physiol 108A:17–23
Hoshikawa R, Sato Y, Satou M (2000) An in vitro study of long-term potentiation in the carp olfactory bulb. In: Kato T (ed) Frontiers of the Mechanisms of Memory and Dementia. Elsevier, Amsterdam, pp 27–28
Huang G-Z, Kaba H (2001) Electrophysiological correlates of pheromonal memory. Neurosci Res Suppl 25:S74
Huang Y-Y, Nguyen PV, Abel T, Kandel ER (1996) Long-lasting forms of synaptic potentiation in the mammalian hippocampus. Learning Memory 3:74–85
Huruno M, Satou M (2000) Long-term potentiation and olfactory memory formation in the carp olfactory bulb. In: Kato T (ed) Frontiers of the Mechanisms of Memory and Dementia. Elsevier, Amsterdam, pp 25–26
Ichikawa M (1976) Fine structure of the olfactory bulb in the goldfish, Carassius auratus. Brain Res 115:43–56
Isaacson JS (2001) Mechanisms governing dendritic γ-aminobutyric acid (GABA) release in the rat olfactory bulb. Proc Natl Acad Sci USA 98:337–342
Isaacson JS, Strawbridge BW (1998) Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 20:749–761
Kaba H, Nakanishi S (1995) Synaptic mechanisms of olfactory recognition memory. Rev Neurosci 6:125–141
Kendrick KM, Levy F, Keverne EB (1992) Changes in the sensory processing of olfactory signals induced by birth in sheep. Science 256:833–836
Keverne EB (1983) Pheromonal influences on the endocrine regulation of reproduction. Trends Neurosci 6:381–384
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 ruffed cell. J Comp Neurol 193:119–145
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 serial thin sectioning studies. J Comp Neurol 186:301–319
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
Kosaka T, Hama K (1981) 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). III. Three-dimensional structure of the ruffed cell dendrite. J Comp Neurol 201:571–587
Laberge FL, Hara TJ (2001) Neurobiology of fish olfaction: a review. Brain Res Rev 36:46–59
Lévy F, Richard Ph, Meurisse M, Ravel N (1997) Scopolamine impairs the ability of parturient ewes to learn to recognise their lambs. Psychopharmacology 129:85–90
Lowe G (2003) Electrical signaling in the olfactory bulb. Current Opinion Neurobiol 13:476–481
Luo M, Katz LC (2001) Response correlation maps of neurons in the mammalian olfactory bulb. Neuron 32:1165–1179
Ma PM (1994) Catecholaminergic systems in the zebrafish. II. Projection pathways and pattern of termination of the locus coeruleus. J Comp Neurol 344:256–269
MacLeod NK (1976) Field potentials in the olfactory bulb of the codfish (Gadus morhua). Comp Biochem Physiol 55A:297–299
MacLeod NK, Lowe GA (1976) Field potentials in the olfactory bulb of the rainbow trout (Salmo gairdneri): evidence for a dendrodendritic inhibitory pathway. Expl Brain Res 25:255–266
Malenka RC, Nicoll RA (1999) Long-term potentiation—a decade of progress? Science 285:1870–1874
Malinow R, Mainen ZF, Hayashi Y (2000) LTP mechanisms: from silence to four-lane traffic. Curr Opin Neurobiol 10:352–357
Martin SJ, Grimwood PD, Morris RGM (2000) Synaptic plasticity and memory: An evaluation of the hypothesis. Annu Rev Neurosci 23:649–711
McLean JH, Darby-King A, Sullivan RM, King SR (1993) Serotonergic influence on olfactory learning in the neonate rat. Behav Neural Biol 60:152–162
McLean JH, Darby-King A, Hodge E (1996) 5-HT receptor involvement in conditioned olfactory learning in the neonate rat pup. Behav Neurosci 110:1426–1434
McNaughton BL (1982) Long-term synaptic enhancement and short-term potentiation in rat fascia dentata act through different mechanisms. J Physiol 324:249–262
Mori K (1987) Membrane and synaptic properties of identified neurons in the olfactory bulb. Prog Neurobiol 29:274–320
Mori K, Takagi SF (1977) Inhibition in the olfactory bulb: dendrodendritic interactions and their relation to the induced waves. In: Katsuki Y, Sato M, Takagi SF, Oomura Y (eds) Food Intakes and Chemical Senses. University of Tokyo Press, Tokyo, pp 33–43
Mori K, Nagao H, Yoshihara Y (1999) The olfactory bulb: coding and processing of odor molecule information. Science 286:711–715
Nieuwenhuys R (1967) Comparative anatomy of olfactory centres and tracts. Progr Brain Res 23:1–64
Rall W, Shepherd GM (1968) Theoretical reconstraction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. J Neurophysiol 31:884–915
Ravel N, Elaagouby A, Gervais R (1994) Scopolamine injection into the olfactory bulb impairs short-term olfactory memory in rats. Behav Neurosci 108:317–324
Satou M (1990) Synaptic organization, local neuronal circuitry, and functional segregation of the teleost olfactory bulb. Progr Neurobiol 34:115–142
Satou M (1992) Synaptic organization of the olfactory bulb and its central projection. In: Hara TJ (ed) Fish Chemoreception. Chapman and Hall, London, pp 40–59
Satou M, Ueda K (1978) Synchronized rhythmic discharges of the secondary olfactory neurons in carp. Brain Res 158:313–329
Satou M, Ichikawa M, Ueda K, Takagi SF (1979) Topographical relation between olfactory bulb and olfactory tracts in the carp. Brain Res 173:142–146
Satou M, Mori K, Tazawa Y, Takagi SF (1982) Two types of postsynaptic inhibition in pyriform cortex of the rabbit: fast and slow inhibitory postsynaptic potentials. J Neurophysiol 48:1142–1156
Satou M, Fujita I, Ichikawa M, Yamaguchi K, Ueda K (1983a) Field potential and intracellular potential studies of the olfactory bulb in the carp: evidence for a functional separation of the olfactory bulb into lateral and medial subdivisions. J Comp Physiol 152A:319–333
Satou M, Mori K, Tazawa Y, Takagi SF (1983b) Interneurons mediating fast postsynaptic inhibition in pyriform cortex of the rabbit. J Neurophysiol 50:89–101
Schoppa NE, Urban NN (2003) Dendritic processing within olfactory bulb circuits. Trends Neurosci 26:501–506
Schoppa NE, Kinzie JM, Sahara Y, Segerson TP, Westbrook GL (1998) Dendrodendritic inhibition in the olfactory bulb is driven by NMDA receptors. J Neurosci 18:6790–6802
Shepherd GM (1972) Synaptic organization of the mammalian olfactory bulb. Physiol Rev 52:864–917
Shepherd GM, Greer CA (1998) Olfactory bulb. In: The Synaptic Organization of the Brain. Shepherd GM (ed) Oxford University Press, New York, pp 159–203
Shipley MT, Ennis M (1996) Functional organization of olfactory system. J Neurobiol 30:123–176
Smeets WJAJ, González A (2000) Catecholamine systems in the brain of vertebrates: new perspectives through a comparative approach. Brain Res Rev 33:308–379
Stripling JS, Patneau DK (1999) Potentiation of late components in olfactory bulb and piriform cortex requires activation of cortical association fibers. Brain Res 841:27–42
Stripling JS, Patneau DK, Gramlich CA (1991) Characterization and anatomical distribution of selective long-term potentiation in the olfactory forebrain. Brain Res 542:107–122
Vetillard A, Benanni S, Saligaut C, Jego P, Bailhache T (2002) Localization of tyrosine hydroxylase and its messenger RNA in the brain of rainbow trout by immunocytochemistry and in situ hybridization. J Comp Neurol 449:374–389
Wilson DA, Sullivan RM (1994) Neurobiology of associative learning in the neonate, early olfactory learning. Behav Neural Biol 61:1–18
Yamaguchi K, Satou M, Ueda K (1988) Induced wave and its generation mechanism in the carp olfactory bulb. Comp Biochem Physiol 89A:605–608
Yokoi M, Mori K, Nakanishi S (1995) Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc Natl Acad Sci USA 92:3371–3375
Yuan Q, Harley CW, McLean JH (2003) Mitral cell β1 and 5-HT2A receptor colocalization and cAMP coregulation: a new model of norepinephrine-induced learning in the olfactory bulb. Learn Mem 10:5–15
Zippel H-P, Reschke CH, Korff V (1999) Simultaneous recordings from two physiologically different types of relay neurons, mitral cells and ruffed cells, in the olfactory bulb of goldfish. Cell Mol Biol 45:327–337
Zippel H-P, Gloger M, Lüthje L, Nasser S, Witcke S (2000) Pheromone discrimination ability of olfactory bulb mitral and ruffed cells in the goldfish (Carassius auratus). Chem Senses 25:339–349
Zucker RS (1999) Calcium- and activity-dependent synaptic plasticity. Curr Opin Neurobiol 9:305–313
Acknowledgements
This work was supported by grants from the Ministry of Education, Culture, Sports, Science and Technology of Japan and from the Ministry of Agriculture, Forestry and Fisheries of Japan. All experiments comply with the Animal Care and Use Committee guidelines of Yokohama City University and also with the regulations for the care and use of laboratory animals in Japan.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Satou, M., Anzai, S. & Huruno, M. Long-term potentiation and olfactory memory formation in the carp (Cyprinus carpio L.) olfactory bulb. J Comp Physiol A 191, 421–434 (2005). https://doi.org/10.1007/s00359-005-0600-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-005-0600-5