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Zebrafish Olfactory System

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The Olfactory System

Abstract

Similar to other animal species, fishes efficiently use the sense of smell for locating food, detecting danger, communicating social information, and memorizing beneficial and detrimental conditions. This review summarizes recent advances in our knowledge of the olfactory system in the zebrafish (Danio rerio), which has become one of the most useful and important model organisms in neurobiology. Olfactory receptors belonging to the OR, V1R, V2R, and TAAR families are differentially expressed in three types of the olfactory sensory neurons (ciliated, microvillus, and crypt) in the olfactory epithelium. In the olfactory bulb, nine glomerular clusters are clearly delineated by anatomical features and molecular markers, serving as functional units important for odor information categorization, coding, and processing. Individual output neurons of the olfactory bulb project axons to a combination of four major target regions in the forebrain: the posterior zone of dorsal telencephalon, the ventral nucleus of ventral telencephalon, the posterior tuberculum, and the right habenula. Distinct modes of odor information decoding are employed by the individual olfactory centers: either nonselective or biased as well as either diffuse or convergent, which contribute to eliciting different physiological and behavioral responses. By taking advantage of its small brain, transparency of larvae, and amenability to various genetic and imaging techniques, zebrafish will pave the way toward understanding the functional organization of the olfactory system as a whole.

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References

  • Agetsuma M, Aizawa H, Aoki T, Nakayama R, Takahoko M, Goto M, Sassa T, Amo R, Shiraki T, Kawakami K, Hosoya T, Higashijima S, Okamoto H (2010) The habenula is crucial for experience-dependent modification of fear responses in zebrafish. Nat Neurosci 13:1354–1356

    CAS  PubMed  Google Scholar 

  • Ahrens MB, Orger MB, Robson DN, Li JM, Keller PJ (2013) Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat Methods 10:413–420

    CAS  PubMed  Google Scholar 

  • Aizawa H, Bianco IH, Hamaoka T, Miyashita T, Uemura O, Concha ML, Russell C, Wilson SW, Okamoto H (2005) Laterotopic representation of left-right information onto the dorso-ventral axis of a zebrafish midbrain target nucleus. Curr Biol 15:238–243

    CAS  PubMed Central  PubMed  Google Scholar 

  • Alioto TS, Ngai J (2005) The odorant receptor repertoire of teleost fish. BMC Genomics 6:173. doi:10.1186/1471-2164-6-173

    PubMed Central  PubMed  Google Scholar 

  • Alioto TS, Ngai J (2006) The repertoire of olfactory C family G protein-coupled receptors in zebrafish: candidate chemosensory receptors for amino acids. BMC Genomics 7:309. doi:10.1186/1471-2164-7-309

    PubMed Central  PubMed  Google Scholar 

  • Amo R, Aizawa H, Takahoko M, Kobayashi M, Takahashi R, Aoki T, Okamoto H (2010) Identification of the zebrafish ventral habenula as a homolog of the mammalian lateral habenula. J Neurosci 30:1566–1574

    CAS  PubMed  Google Scholar 

  • Asakawa K, Suster ML, Mizusawa K, Nagayoshi S, Kotani T, Urasaki A, Kishimoto Y, Hibi M, Kawakami K (2008) Genetic dissection of neural circuits by Tol2 transposon-mediated Gal4 gene and enhancer trapping in zebrafish. Proc Natl Acad Sci USA 105:1255–1260

    CAS  PubMed Central  PubMed  Google Scholar 

  • Baier H, Korsching S (1994) Olfactory glomeruli in the zebrafish form an invariant pattern and are identifiable across animals. J Neurosci 14:219–230

    CAS  PubMed  Google Scholar 

  • Bargmann CI, Hartwieg E, Horvitz HR (1993) Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74:515–527

    CAS  PubMed  Google Scholar 

  • Barth AL, Nicholas JJ, Ngai J (1996) Asynchronous onset of odorant receptor expression in the developing zebrafish olfactory system. Neuron 16:23–34

    CAS  PubMed  Google Scholar 

  • Barth AL, Dugas JC, Ngai J (1997) Noncoordinate expression of odorant receptor genes tightly linked in the zebrafish genome. Neuron 19:359–369

    CAS  PubMed  Google Scholar 

  • Bedell VM, Wang W, Campbell JM, Poshusta TL, Starker CG, Krug RG 2nd, Tan W, Penheiter SG, Ma AC, Leung AY, Fahrenkrug SC, Carlson DF, Voytas DF, Clark KJ, Essner JJ, Ekker SC (2012) In vivo genome editing using a high-efficiency TALEN system. Nature (Lond) 491:114–118

    CAS  Google Scholar 

  • Bianco IH, Wilson SW (2009) The habenular nuclei: a conserved asymmetric relay station in the vertebrate brain. Philos Trans R Soc Lond B Biol Sci 364:1005–1020

    PubMed Central  PubMed  Google Scholar 

  • Blumhagen F, Zhu P, Shum J, Scharer YP, Yaksi E, Deisseroth K, Friedrich RW (2011) Neuronal filtering of multiplexed odour representations. Nature (Lond) 479:493–498

    CAS  Google Scholar 

  • Braubach OR, Wood HD, Gadbois S, Fine A, Croll RP (2009) Olfactory conditioning in the zebrafish (Danio rerio). Behav Brain Res 198:190–198

    PubMed  Google Scholar 

  • Braubach OR, Fine A, Croll RP (2012) Distribution and functional organization of glomeruli in the olfactory bulbs of zebrafish (Danio rerio). J Comp Neurol 520:2317–2339

    PubMed  Google Scholar 

  • Braubach OR, Miyasaka N, Koide T, Yoshihara Y, Croll RP, Fine A (2013) Experience-dependent versus experience-independent postembryonic development of distinct groups of zebrafish olfactory glomeruli. J Neurosci 33:6905–6916

    CAS  PubMed  Google Scholar 

  • Buck LB (2000) The molecular architecture of odor and pheromone sensing in mammals. Cell 100:611–618

    CAS  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

    CAS  PubMed  Google Scholar 

  • Cao Y, Oh BC, Stryer L (1998) Cloning and localization of two multigene receptor families in goldfish olfactory epithelium. Proc Natl Acad Sci USA 95:11987–11992

    CAS  PubMed Central  PubMed  Google Scholar 

  • Caron SJ, Ruta V, Abbott LF, Axel R (2013) Random convergence of olfactory inputs in the Drosophila mushroom body. Nature (Lond) 497:113–117

    CAS  Google Scholar 

  • Carr WES (1988) The molecular nature of chemical stimuli in the aquatic environment. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, New York, pp 3–27

    Google Scholar 

  • Chess A, Simon I, Cedar H, Axel R (1994) Allelic inactivation regulates olfactory receptor gene expression. Cell 78:823–834

    CAS  PubMed  Google Scholar 

  • DeFraipont M, Sorensen PW (1993) Exposure to the pheromone 17α,20β-dihydroxy-4-pregnen-3-one enhances behavioral spawning success, sperm production, and sperm motility of male goldfish. Anim Behav 46:245–256

    Google Scholar 

  • Derjean D, Moussaddy A, Atallah E, St.-Pierre M, Auclair F, Chang S, Ren X, Zielinski B, Dubac R (2010) A novel neural substrate for the transformation of olfactory inputs into motor output. PLoS Biol 8:e1000567

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dewan A, Pacifico R, Zhan R, Rinberg D, Bozza T (2013) Non-redundant coding of aversive odours in the main olfactory pathway. Nature (Lond) 497:486–489

    CAS  Google Scholar 

  • Dittman A, Quinn T (1996) Homing in Pacific salmon: mechanisms and ecological basis. J Exp Biol 199:83–91

    PubMed  Google Scholar 

  • Ellingsen S, Laplante MA, Konig M, Kikuta H, Furmanek T, Hoivik EA, Becker TS (2005) Large-scale enhancer detection in the zebrafish genome. Development (Camb) 132:3799–3811

    CAS  Google Scholar 

  • Ferrero DM, Lemon JK, Fluegge D, Pashkovski SL, Korzan WJ, Datta SR, Spehr M, Fendt M, Liberles SD (2011) Detection and avoidance of a carnivore odor by prey. Proc Natl Acad Sci USA 108:11235–11240

    CAS  PubMed Central  PubMed  Google Scholar 

  • Friedrich RW (2006) Mechanisms of odor discrimination: neurophysiological and behavioral approaches. Trends Neurosci 29:40–47

    CAS  PubMed  Google Scholar 

  • Friedrich RW, Korsching SI (1997) Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron 18:737–752

    CAS  PubMed  Google Scholar 

  • Friedrich RW, Korsching SI (1998) Chemotopic, combinatorial, and noncombinatorial odorant representations in the olfactory bulb revealed using a voltage-sensitive axon tracer. J Neurosci 18:9977–9988

    CAS  PubMed  Google Scholar 

  • Friedrich RW, Laurent G (2001) Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. Science 291:889–894

    CAS  PubMed  Google Scholar 

  • Friedrich RW, Habermann CJ, Laurent G (2004) Multiplexing using synchrony in the zebrafish olfactory bulb. Nat Neurosci 7:862–871

    CAS  PubMed  Google Scholar 

  • Friedrich RW, Yaksi E, Judkewitz B, Wiechert MT (2009) Processing of odor representations by neuronal circuits in the olfactory bulb. Ann N Y Acad Sci 1170:293–297

    PubMed  Google Scholar 

  • Fuss SH, Korsching SI (2001) Odorant feature detection: activity mapping of structure response relationships in the zebrafish olfactory bulb. J Neurosci 21:8396–8407

    CAS  PubMed  Google Scholar 

  • Ganz J, Kaslin J, Freudenreich D, Machate A, Geffarth M, Brand M (2012) Subdivisions of the adult zebrafish subpallium by molecular marker analysis. J Comp Neurol 520:633–655

    CAS  PubMed  Google Scholar 

  • Germana A, Montalbano G, Laura R, Ciriaco E, dell Calle ME, Vega JA (2004) S100 protein-like immunoreactivity in the crypt olfactory neurons of the adult zebrafish. Neurosci Lett 371:196–198

    CAS  PubMed  Google Scholar 

  • Germana A, Paruta S, Germana GP, Ochoa-Erena FJ, Montalbano G, Cobo J, Vega JA (2007) Differential distribution of S100 protetin and calretinin in mechanosensory and chemosensory cells of adult zebrafish (Danio rerio). Brain Res 1162:48–55

    CAS  PubMed  Google Scholar 

  • Ghosh S, Larson SD, Hefzi H, Marnoy Z, Cutforth T, Dokka K, Baldwin KK (2011) Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons. Nature (Lond) 472:217–220

    CAS  Google Scholar 

  • Gloriam DEI, Bjarnadottir TK, Yan YL, Postlethwait JH, Schioth HB, Fredriksson R (2005) The repertoire of trace amine G-protein-coupled receptors: large expansion in zebrafish. Mol Phylogenet Evol 35:470–482

    CAS  PubMed  Google Scholar 

  • Goldman AL, Van der Goes van Naters W, Lessing D, Warr CG, Carlson JR (2005) Coexpression of two functional odor receptors in one neuron. Neuron 45:661–666

    CAS  PubMed  Google Scholar 

  • Hagey LR, Moller PR, Hofmann AF, Krasowski MD (2010) Diversity of bile salts and amphibians: evolution of a complex biochemical pathway. Physiol Biochem Zool 83:308–321

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hamdani EH, Doving KB (2002) The alarm reaction in crucian carp is mediated by olfactory neurons with long dendrites. Chem Senses 27:395–398

    Google Scholar 

  • Hamdani EH, Doving KB (2006) Specific projection of the sensory crypt cells in the olfactory system in crucian carp, Carassius carassius. Chem Senses 31:63–67

    Google Scholar 

  • Hamdani EH, Alexander G, Doving KB (2001) Projection of sensory neurons with microvilli to the lateral olfactory tract indicates their participation in feeding behaviour in crucian carp. Chem Senses 26:1139–1144

    CAS  PubMed  Google Scholar 

  • Hansen A, Zeiske E (1998) The peripheral olfactory organ of the zebrafish, Danio rerio: an ultrastructural study. Chem Senses 23:39–48

    CAS  PubMed  Google Scholar 

  • Hansen A, Rolen SH, Anderson K, Morita Y, Caprio J, Finger TE (2003) Correlation between olfactory receptor cell type and function in the channel catfish. J Neurosci 23:347–359

    Google Scholar 

  • Hansen A, Anderson KT, Finger TE (2004) Differential distribution of olfactory receptor neurons in goldfish: structural and molecular correlates. J Comp Neurol 477:347–359

    CAS  PubMed  Google Scholar 

  • Harden MV, Newton LA, Lloyd RC, Whitlock KE (2006) Olfactory imprinting is correlated with changes in gene expression in the olfactory epithelia of the zebrafish. J Neurobiol 66:1452–1466

    CAS  PubMed  Google Scholar 

  • Hashiguchi Y, Nishida M (2006) Evolution and origin of vomeronasal-type odorant receptor gene repertoire in fishes. BMC Evol Biol 6:76

    PubMed Central  PubMed  Google Scholar 

  • Hashiguchi Y, Nishida M (2007) Evolution of trace amine-associated receptor (TAAR) gene family in vertebrates: lineage-specific expansions and degradations of a second class of vertebrate chemosensory receptors expressed in the olfactory epithelium. Mol Biol Evol 24:2099–2107

    CAS  PubMed  Google Scholar 

  • Herbert P, Atema J (1977) Olfactory discrimination of male and female conspecifics in bullhead catfish, Ictalurus nebulosus. Biol Bull 153:429–430

    Google Scholar 

  • Howe K, Clark MD et al (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature (Lond) 496:498–503

    CAS  Google Scholar 

  • Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JR, Joung JK (2013) Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 31:227–229

    CAS  PubMed Central  PubMed  Google Scholar 

  • Igarashi KM, Ieki N, An M, Yamaguchi Y, Nagayama S, Kobayakawa K, Kobayakawa R, Tanifuji M, Sakano H, Chen WR, Mori K (2012) Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. J Neurosci 32:7970–7985

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jefferis GS, Potter CJ, Chan AM, Marin EC, Rohlfing T, Maurer CR Jr, Luo L (2007) Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128:1187–1203

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kang J, Caprio J (1995) Electrophysiological response of single olfactory bulb neurons to amino acids in the channel catfish, Ictalurus punctatus. J Neurophysiol 74:1421–1434

    CAS  PubMed  Google Scholar 

  • Kasumyan AO, Lebedeva NY (1975) New data on the nature of the alarm pheromone in cyprinids. J Ichthyol 19:109–114

    Google Scholar 

  • Kettleborough RN, Busch-Nentwich EM, Harvey SA, Dooley CM, de Bruijn E, van Eeden F, Sealy I, White RJ, Herd C, Nijman IJ, Fenyes F, Mehroke S, Scahill C, Gibbons R, Wali N, Carruthers S, Hall A, Yen J, Cuppen E, Stemple DL (2013) A systematic genome-wide analysis of zebrafish protein-coding gene function. Nature (Lond) 496:494–497

    CAS  Google Scholar 

  • Koide T, Miyasaka N, Morimoto K, Asakawa K, Urasaki A, Kawakami K, Yoshihara Y (2009) Olfactory neural circuitry for attraction to amino acids revealed by transposon-mediated gene trap approach in zebrafish. Proc Natl Acad Sci USA 106:9884–9889

    CAS  PubMed Central  PubMed  Google Scholar 

  • Korsching S (2009) The molecular evolution of teleost olfactory receptor gene families. Results Probl Cell Differ 47:37–55

    CAS  PubMed  Google Scholar 

  • Laberge F, Hara TJ (2001) Neurobiology of fish olfaction: a review. Brain Res Rev 36:41–59

    Google Scholar 

  • Larsson MC, Domingos AI, Jones WD, Chiappe E, Amrein H, Vosshall LB (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43:703–714

    CAS  PubMed  Google Scholar 

  • Lebedeva NY, Malyukina GA, Kasumyan AO (1975) The natural repellent in the skin of cyprinids. J Ichthyol 15:472–480

    Google Scholar 

  • Lee A, Mathuru AS, Teh C, Kibat C, Korzh V, Penney TB, Jesuthasan S (2010) The habenula prevents helpless behavior in larval zebrafish. Curr Biol 20:2211–2216

    CAS  PubMed  Google Scholar 

  • Li W, Scott AP, Siefkes MJ, Yan H, Liu Q, Yun SS, Gage DA (2002) Bile acid secreted by male sea lamprey that acts as a sex pheromone. Science 296:138–141

    CAS  PubMed  Google Scholar 

  • Li J, Mack JA, Souren M, Yaksi E, Higashijima S, Mione M, Fetcho JR, Friedrich RW (2005) Early development of functional spatial maps in the zebrafish olfactory bulb. J Neurosci 25:5784–5795

    CAS  PubMed  Google Scholar 

  • Li Q, Korzan WJ, Ferrero DM, Chang RB, Roy DS, Buchi M, Lemon JK, Kaur AW, Stowers L, Fendt M, Liberles SD (2013) Synchronous evolution of an odor biosynthesis pathway and behavioral response. Curr Biol 23:11–20

    PubMed Central  PubMed  Google Scholar 

  • Liberles SD, Buck LB (2006) A second class of chemosensory receptors in the olfactory epithelium. Nature (Lond) 442:645–650

    CAS  Google Scholar 

  • Lin HH, Lai JS, Chin AL, Chen YC, Chiang AS (2007) A map of olfactory representation in the Drosophila mushroom body. Cell 128:1205–1217

    CAS  PubMed  Google Scholar 

  • Lipschitz DL, Michel WC (2002) Amino acid odorants stimulate microvillar sensory neurons. Chem Senses 27:277–286

    PubMed  Google Scholar 

  • Little EE (1977) Conditioned cardiac response to the olfactory stimuli of amino acids in the channel catfish, Ictalurus punctatus. Physiol Behav 27:691–697

    Google Scholar 

  • Luu P, Acher F, Bertrand HO, Fan J, Ngai J (2004) Molecular determinants of ligand selectivity in a vertebrate odorant receptor. J Neurosci 24:10128–10137

    CAS  PubMed  Google Scholar 

  • Manteifel YB, Karelina MA (1996) Conditioned food aversion in the goldfish, Carassius auratus. Comp Biochem Phys A 115:31–35

    Google Scholar 

  • Martini S, Silvotti L, Shirazi A, Ryba NJP, Tirindelli R (2001) Co-expression of putative pheromone receptors in the sensory neurons of the vomeronasal organ. J Neurosci 21:843–848

    CAS  PubMed  Google Scholar 

  • Mathuru AS, Kibat C, Cheong WF, Shui G, Wenk MR, Friedrich RW, Jesuthasan S (2012) Chondroitin fragments are odorants that trigger fear behavior in fish. Curr Biol 22:538–544

    CAS  PubMed  Google Scholar 

  • Michel WC (1999) Cyclic nucleotide-gated channel activation is not required for activity-dependent labeling of zebrafish olfactory receptor neurons by amino acids. Biol Signals Recept 8:338–347

    CAS  PubMed  Google Scholar 

  • Michel WC, Derbidge DS (1997) Evidence of distinct amino acid and bile salt receptors in the olfactory system of the zebrafish, Danio rerio. Brain Res 764:179–187

    CAS  PubMed  Google Scholar 

  • Michel WC, Lubomudrov LM (1995) Specificity and sensitivity of the olfactory organ of the zebrafish, Danio rerio. J Comp Physiol A 177:191–199

    CAS  PubMed  Google Scholar 

  • Michel WC, Sanderson MJ, Olson JK, Lipschitz DL (2003) Evidence of a novel transduction pathway mediating detection of polyamines by the zebrafish olfactory system. J Exp Biol 206:1697–1706

    CAS  PubMed  Google Scholar 

  • Miklavc P, Valentincic T (2012) Chemotopy of amino acids on the olfactory bulb predicts olfactory discrimination capabilities of zebrafish Danio rerio. Chem Senses 37:65–75

    CAS  PubMed  Google Scholar 

  • Miyamichi K, Amat F, Moussavi F, Wang C, Wickersham I, Wall NR, Taniguchi H, Tasic B, Huang ZJ, He Z, Callaway EM, Horowitz MA, Luo L (2011) Cortical representations of olfactory input by trans-synaptic tracing. Nature (Lond) 472:191–196

    CAS  Google Scholar 

  • Miyasaka N, Sato Y, Yeo SY, Hutson LD, Chien CB, Okamoto H, Yoshihara Y (2005) Robo2 is required for establishment of a precise glomerular map in the zebrafish olfactory system. Development (Camb) 132:1283–1293

    CAS  Google Scholar 

  • Miyasaka N, Knaut H, Yoshihara Y (2007) Cxcl12/Cxcr4 chemokine signaling is required for placode assembly and sensory axon pathfinding in the zebrafish olfactory system. Development (Camb) 134:2459–2468

    CAS  Google Scholar 

  • Miyasaka N, Morimoto K, Tsubokawa T, Higashijima S, Okamoto H, Yoshihara Y (2009) From the olfactory bulb to higher brain centers: genetic visualization of secondary olfactory pathways in zebrafish. J Neurosci 29:4756–4767

    CAS  PubMed  Google Scholar 

  • Miyasaka N, Arganda-Carreras I, Wakisaka N, Masuda M, Seung HS, Yoshihar Y (2014) Olfactory projectomes in the zebrafish forebrain revealed by genetic single-neuron labeling. Nat Commun 5:3639. doi: 10.1038/ncomms4639

    PubMed  Google Scholar 

  • Mombaerts P (2004) Genes and ligands for odorant, vomeronasal and taste receptors. Nat Rev Neurosci 5:263–278

    CAS  PubMed  Google Scholar 

  • Mori K, Sakano H (2011) How is the olfactory map formed and interpreted in the mammalian brain? Annu Rev Neurosci 34:467–499

    CAS  PubMed  Google Scholar 

  • Mori K, Mataga N, Imamura K (1992) Differential specificities of single mitral cells in rabbit olfactory bulb for a homologous series of fatty acid odor molecules. J Neurophysiol 67:786–789

    CAS  PubMed  Google Scholar 

  • Mori K, Nagao H, Yoshihara Y (1999) The olfactory bulb: coding and processing of odor molecule information. Science 286:711–715

    CAS  PubMed  Google Scholar 

  • Mori K, Takahashi YK, Igarashi KM, Yamaguchi M (2006) Maps of odorant molecular features in the mammalian olfactory bulb. Physiol Rev 86:409–433

    CAS  PubMed  Google Scholar 

  • Morita Y, Finger TE (1998) Differential projections of ciliated and microvillous olfactory receptor cells in the catfish, Ictalurus punctatus. J Comp Neurol 398:539–550

    CAS  PubMed  Google Scholar 

  • Muto A, Ohkura M, Abe G, Nakai J, Kawakami K (2013) Real-time visualization of neuronal activity during perception. Curr Biol 23:307–311

    CAS  PubMed  Google Scholar 

  • Ngai J, Alioto TS (2007) Genomics of odor receptors in zebrafish. In: Firestein S, Beauchamp GK (eds) The senses: a comprehensive reference, vol 4, Olfaction and taste. Academic Press, Oxford/San Diego, pp 553–560

    Google Scholar 

  • Niessing J, Friedrich RW (2010) Olfactory pattern classification by discrete neuronal network states. Nature (Lond) 465:47–52

    CAS  Google Scholar 

  • Nikonov AA, Caprio J (2001) Electrophysiological evidence for a chemotopy of biological relevant odors in the olfactory bulb of the channel catfish. J Neurophysiol 86:1869–1876

    CAS  PubMed  Google Scholar 

  • Nikonov AA, Caprio J (2007) Highly specific olfactory receptor neurons for types of amino acids in the channel catfish. J Neurophysiol 98:1909–1918

    CAS  PubMed  Google Scholar 

  • Nikonov AA, Finger TE, Caprio J (2005) Beyond the olfactory bulb: an odotopic map in the forebrain. Proc Natl Acad Sci USA 102:18688–18693

    CAS  PubMed Central  PubMed  Google Scholar 

  • Oka Y, Saraiva LR, Korsching SI (2012) Crypt neurons express a single V1R-related ora gene. Chem Senses 37:219–227

    CAS  PubMed  Google Scholar 

  • Okamoto H, Agetsuma M, Aizawa H (2012) Genetic dissection of the zebrafish habenula, a possible switching board for selection of behavioral strategy to cope with fear and anxiety. Dev Neurobiol 72:386–394

    PubMed  Google Scholar 

  • Pfeiffer W (1977) The distribution of fright reaction and alarm substance cells in fishes. Copeia 4:653–665

    Google Scholar 

  • Pfeiffer W, Riegelbauer G, Meier G, Sheibler B (1985) Effect of hypoxanthine-3(N)-oxide and hypoxanthine-1(N)-oxide on central nervous excitation of the black tetra Gymnocorymbus ternetzi (Characidae, Ostariophysi, Pisces) indicated by dorsal light response. J Chem Ecol 11:507–523

    CAS  PubMed  Google Scholar 

  • Ren X, Chang S, Laframboise A, Green W, Dubac R, Zielinski B (2009) Projections from the accessory olfactory organ into the medial region of the olfactory bulb in the sea lamprey (Petromyzon marinus): a novel vertebrate sensory structure? J Comp Neurol 516:105–116

    PubMed  Google Scholar 

  • Rink E, Wullimann MF (2004) Connections of the ventral telencephalon (subpallium) in the zebrafish (Danio rerio). Brain Res 1011:206–220

    CAS  PubMed  Google Scholar 

  • Rubin BD, Katz LC (1999) Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron 23:499–511

    CAS  PubMed  Google Scholar 

  • Saraiva LR, Korsching SI (2007) A novel olfactory receptor gene family in teleost fish. Genome Res 17:1448–1457

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sato Y, Miyasaka N, Yoshihara Y (2005) Mutually exclusive glomerular innervation by two distinct types of olfactory sensory neurons revealed in transgenic zebrafish. J Neurosci 25:4889–4897

    CAS  PubMed  Google Scholar 

  • Sato T, Hamaoka T, Aizawa H, Hosoya T, Okamoto H (2007a) Genetic single-cell mosaic analysis implicates ephrinB2 reverse signaling in projections from the posterior tectum to the hindbrain in zebrafish. J Neurosci 27:5271–5279

    CAS  PubMed  Google Scholar 

  • Sato Y, Miyasaka N, Yoshihara Y (2007b) Hierarchical regulation of odorant receptor gene choice and subsequent axonal projection of olfactory sensory neurons in zebrafish. J Neurosci 27:1606–1615

    CAS  PubMed  Google Scholar 

  • Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature (Lond) 452:1002–1006

    CAS  Google Scholar 

  • Scholz AT, Horrall RM, Cooper JC, Hasler AD (1976) Imprinting to chemical cues: the basis for home stream selection in salmon. Science 192:1247–1249

    CAS  PubMed  Google Scholar 

  • Schweitzer J, Lohr H, Filippi A, Driever W (2012) Dopaminergic and noradrenergic circuit development in zebrafish. Dev Neurobiol 72:256–268

    CAS  PubMed  Google Scholar 

  • Serizawa S, Miyamichi K, Nakatani H, Suzuki M, Saito M, Yoshihara Y, Sakano H (2003) Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse. Science 302:2088–2094

    CAS  PubMed  Google Scholar 

  • Shi P, Zhang J (2009) Extraordinary diversity of chemosensory receptor gene repertoires among vertebrates. Results Probl Cell Differ 47:1–23

    CAS  PubMed  Google Scholar 

  • Sorensen PW, Caprio J (1998) Chemoreception. In: Evans DH (ed) The physiology of fishes, 2nd edn. CRC Press, Boca Raton, pp 375–405

    Google Scholar 

  • Sorensen PW, Hara TJ, Stacey NE, Goetz FW (1988) F prostaglandins function as potent olfactory stimulants comprising the post-ovulatory sex pheromone in the goldfish. Biol Reprod 39:1039–1050

    CAS  PubMed  Google Scholar 

  • Sorensen PW, Christensen TA, Stacey NE (1998) Discrimination of pheromonal cues in fish: emerging parallels with insects. Curr Opin Neurobiol 8:458–467

    CAS  PubMed  Google Scholar 

  • Sorensen PW, Fine JM, Dvornikovs V, Jeffrey CS, Shao F, Wang J, Vrieze LA, Anderson KR, Hoye TR (2005) Mixture of new sulfated steroids functions as a migratory pheromone in the sea lamprey. Nat Chem Biol 1:324–328

    CAS  PubMed  Google Scholar 

  • Sosulski DL, Bloom ML, Cutforth T, Axel R, Datta SR (2011) Distinct representations of olfactory information in different cortical centres. Nature (Lond) 472:213–216

    CAS  Google Scholar 

  • Speca DJ, Lin DM, Sorensen PW, Isacoff EY, Ngai J, Dittman AH (1999) Functional identification of a goldfish odorant receptor. Neuron 23:497–498

    Google Scholar 

  • Speedie N, Gerlai R (2008) Alarm substance induced behavioral responses in zebrafish (Danio rerio). Behav Brain Res 188:168–177

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stacey NE, Sorensen PW, Van der Kraak GJ, Dulka JG (1989) Direct evidence that 17α,20β-dihydroxy-4-pregnen-3-one functions as a goldfish primer pheromone: preovulatory release is closely associated with male endocrine system. Gen Comp Endocrinol 75:62–70

    CAS  PubMed  Google Scholar 

  • Steele CW, Owens DW, Scarfe AD (1990) Attraction of zebrafish Brachydanio rerio to alanine and its suppression by copper. J Fish Biol 36:341–352

    CAS  Google Scholar 

  • Steele CW, Scarfe AD, Owens DW (1991) Effects of group size on the responsiveness of zebrafish Brachydanio rerio to alanine, a chemical attractant. J Fish Biol 38:553–564

    CAS  Google Scholar 

  • Suboski MD, Bain S, Carty AE, McQuoid LM, Seelen MI, Seifert M (1990) Alarm reaction in acquisition and social transmission of simulated-predator recognition by zebra danio fish (Brachydanio rerio). J Comp Psychol 104:101–112

    Google Scholar 

  • Tay TL, Ronneberger O, Ryu S, Nitschke R, Driever W (2011) Comprehensive catecholaminergic projectome analysis reveals single-neuron integration of zebrafish ascending and descending dopaminergic systems. Nat Commun 2:171

    PubMed Central  PubMed  Google Scholar 

  • Troemel ER, Chou JH, Dwyer ND, Colbert HA, Bargmann CI (1995) Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83:207–218

    CAS  PubMed  Google Scholar 

  • Uchida N, Takahashi YK, Tanifuji M, Mori K (2000) Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features. Nat Neurosci 3:1035–1043

    CAS  PubMed  Google Scholar 

  • Valentincic T, Metelko J, Ota D, Pirc V, Blejec A (2000) Olfactory discrimination of amino acids in brown bulhead catfish. Chem Senses 25:21–29

    CAS  PubMed  Google Scholar 

  • von Frisch K (1938) Zur psychologie des Fische-Schwarmes. Naturwissenschaften 26:601–606

    Google Scholar 

  • Vosshall LB, Stocker RF (2007) Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30:505–533

    CAS  PubMed  Google Scholar 

  • Wang JW, Wong AM, Flores J, Vosshall LB, Axel R (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112:271–282

    CAS  PubMed  Google Scholar 

  • Westerfield M (1995) The zebrafish book, 3rd edn. University of Oregon Press, Eugene

    Google Scholar 

  • Wicher D, Schafer R, Bauernfeind R, Stensmyr MC, Heller R, Heinemann SH, Hansson BS (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature (Lond) 452:1007–1011

    CAS  Google Scholar 

  • Wiechert MT, Judkewitz B, Riecke H, Friedrich RW (2010) Mechanisms of pattern decorrelation by recurrent neuronal circuits. Nat Neurosci 13:1003–1010

    CAS  PubMed  Google Scholar 

  • Wullimann MF, Mueller T (2004) Teleostean and mammalian forebrains contrasted: evidence from genes to behavior. J Comp Neurol 475:143–162

    CAS  PubMed  Google Scholar 

  • Yaksi E, von Saint Paul F, Niessing J, Bundschuh ST, Friedrich RW (2009) Transformation of odor representations in target areas of the olfactory bulb. Nat Neurosci 12:474–482

    CAS  PubMed  Google Scholar 

  • Yamamoto Y, Hino H, Ueda H (2010) Olfactory imprinting of amino acids in lacustrine sockeye salmon. PLoS One 5:e8633

    PubMed Central  PubMed  Google Scholar 

  • Yoshihara Y (2009) Molecular genetic dissection of the zebrafish olfactory system. Results Probl Cell Differ 47:97–120

    CAS  PubMed  Google Scholar 

  • Zielinski BS, Hara TJ (2007) Olfaction. In: Hara T, Zielinski B (eds) Fish physiology, vol 25, Sensory systems neuroscience. Academic Press, San Diego/London, pp 1–43

    Google Scholar 

  • Zu Y, Tong X, Wang Z, Liu D, Pan R, Li Z, Hu Y, Luo Z, Huang P, Wu Q, Zhu Z, Zhang B, Lin S (2013) TALEN-mediated precise genome modification by homologous recombination in zebrafish. Nat Methods 10:329–331

    CAS  PubMed  Google Scholar 

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Acknowledgments

The author thanks Nobuhiko Miyasaka, Tetsuya Koide, Noriko Wakisaka, Miwa Masuda, and Yoichi Yabuki for help in preparation of the figures and critical reading of the manuscript, and Takumi Akagi and Tsutomu Hashikawa in the Support Unit for Animal Resources Development, RIKEN BSI Research Resources Center for help in electron microscopy. This work was supported in part by a Grant-in-Aid for Scientific Research (B) and a Grant-in-Aid for Scientific Research on Innovative Areas (Systems Molecular Ethology) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan, and a Grant from the Human Frontier Science Program (HFSP).

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  1. RIKEN Brain Science Institute, 2-1 Hirosawa, Wako, Saitama, 351-0198, Japan

    Yoshihiro Yoshihara

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Correspondence to Yoshihiro Yoshihara .

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  1. Department of Physiology, The University of Tokyo, Tokyo, Japan

    Kensaku Mori

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Yoshihara, Y. (2014). Zebrafish Olfactory System. In: Mori, K. (eds) The Olfactory System. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54376-3_5

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