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Neural Computations with Mammalian Infochemicals

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Abstract

The mammalian olfactory system is the most sensitive and discriminating molecular recognition system known, able to detect a few dozen critical molecules in the face of strong and variable background odorants. The set of information-containing volatile molecules used to transmit information within and between mammalian species shows both great molecular and informational diversity. Chemosensory neuroscientists that apply traditional reductionist methods to the analysis of information processing and computational principles in the olfactory system find great value in understanding the ecological and ethological context in which mammalian olfactory communication occurs. This review highlights a subset of the molecular armamentarium and information transmissions relevant to understanding the uses of olfactory communication by mammals in an ecological context.

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Abbreviations

2DG:

2-deoxyglucose

AOB:

accessory olfactory bulb

CA1:

cornu ammonis field 1

CA3:

cornu ammonis field 3

c-FOS:

cellular-Finkel osteogenic sarcoma

Egr-1:

early growth response protein 1

fMRI:

functional magnetic resonance imaging

HLA:

human lymphocyte antigen

kDa:

kiloDalton

MHC:

major histocompatibility complex

MOB:

main olfactory bulb

MOE:

main olfactory epithelium

M/T:

mitral/tufted

MTMT:

(methylthio)methanethiol

ORN:

olfactory receptor neuron

VNO:

vomeronasal organ

References

  • Abaffy, T., Malhotra, A., and Luetje, C. W. 2007. The molecular basis for ligand specificity in a mouse olfactory receptor: a network of functionally important residues. J. Biol. Chem. 282:1216–1224.

    PubMed  CAS  Google Scholar 

  • Able, D. J. 1996. The contagion indicator hypothesis for parasite-mediated sexual selection. Proc. Natl. Acad. Sci. USA 93:2229–2233.

    PubMed  CAS  Google Scholar 

  • Abraham, N. M., Spors, H., Carleton, A., Margrie, T. W., Kuner, T., and Schaefer, A. T. 2004. Maintaining accuracy at the expense of speed: stimulus similarity defines odor discrimination time in mice. Neuron 44:865–876.

    PubMed  CAS  Google Scholar 

  • Aime, P., Duchamp-viret, P., Chaput, M. A., Savigner, A., Mahfouz, M., and Julliard, A. K. 2007. Fasting increases and satiation decreases olfactory detection for a neutral odor in rats. Behav. Brain Res. 179:258–264.

    PubMed  CAS  Google Scholar 

  • Alonso, M., Viollet, C., Gabellec, M. M., Meas-yedid, V., Olivo-marin, J. C., and Lledo, P. M. 2006. Olfactory discrimination learning increases the survival of adult-born neurons in the olfactory bulb. J. Neurosci. 26:10508–10513.

    PubMed  CAS  Google Scholar 

  • Apfelbach, R., Blanchard, C. D., Blanchard, R. J., Hayes, R. A., and Mcgregor, I. S. 2005. The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci. Biobehav. Rev. 29:1123–1144.

    PubMed  Google Scholar 

  • Araneda, R. C., Kini, A. D., and Firestein, S. 2000. The molecular receptive range of an odorant receptor. Nat. Neurosci. 3:1248–1255.

    PubMed  CAS  Google Scholar 

  • Arenkiel, B. R., Peca, J., Davison, I. G., Feliciano, C., Deisseroth, K., Augustine, G. J., Ehlers, M. D., and Feng, G. 2007. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54:205–218.

    PubMed  CAS  Google Scholar 

  • Axel, R. 2005. Scents and sensibility: a molecular logic of olfactory perception (Nobel lecture). Angew. Chem. Int. Ed. Engl. 44:6110–6127.

    PubMed  Google Scholar 

  • Balkovsky, E., and Shraiman, B. I. 2002. Olfactory search at high Reynolds number. Proc. Natl. Acad. Sci. USA 99:12583–12588.

    Google Scholar 

  • Baly, C., Aioun, J., Badonnel, K., Lacroix, M. C., Durieux, D., Schlegel, C., Salesse, R., and Caillol, M. 2007. Leptin and its receptors are present in the rat olfactory mucosa and modulated by the nutritional status. Brain Res. 1129:130–141.

    PubMed  CAS  Google Scholar 

  • Bargmann, C. I. 2006. Comparative chemosensation from receptors to ecology. Nature 444:295–301.

    PubMed  CAS  Google Scholar 

  • Barthelemy, M., Gabrion, C., and Petit, G. 2005. Does chronic malaria modify the odours of its male mouse host? Can. J. Zool. 83:1079–1086.

    Article  Google Scholar 

  • Bathellier, B., Lagier, S., Faure, P., and Lledo, P. M. 2006. Circuit properties generating gamma oscillations in a network model of the olfactory bulb. J Neurophysiol. 95:2678–2691.

    PubMed  Google Scholar 

  • Batterton, M. N., Robarts, D., Woodley, S. K., and Baum, M. J. 2006. Comparison of odor and mating-induced glomerular activation in the main olfactory bulb of estrous female ferrets. Neurosci. Lett. 400:224–229.

    PubMed  CAS  Google Scholar 

  • Baxi, K. N., Dorries, K. M., and Eisthen, H. L. 2006. Is the vomeronasal system really specialized for detecting pheromones? Trends Neurosci. 29:1–7.

    PubMed  CAS  Google Scholar 

  • Beauchamp, G. K., and Yamazaki, K. 2003. Chemical signaling in mice. Biochem. Soc. Trans. 31:147–151.

    PubMed  CAS  Google Scholar 

  • Beauchamp, G. K., Martin, I. G., Wysocki, C. J., and Wellington, J. L. 1982. Chemoinvestigatory and sexual behavior of male guinea pigs following vomeronasal organ removal. Physiol. Behav. 29:329–336.

    PubMed  CAS  Google Scholar 

  • Beshel, J., Kopell, N., and Kay, L. M. 2007. Olfactory bulb gamma oscillations are enhanced with task demands. J. Neurosci. 27:8358–8365.

    PubMed  CAS  Google Scholar 

  • Bhandawat, V., Reisert, J., and Yau, K. W. 2005. Elementary response of olfactory receptor neurons to odorants. Science 308:1931–1934.

    PubMed  CAS  Google Scholar 

  • Bisulco, S., and Slotnick, B. 2003. Olfactory discrimination of short chain fatty acids in rats with large bilateral lesions of the olfactory bulbs. Chem. Senses 28:361–370.

    PubMed  Google Scholar 

  • Boehm, U. 2006. The vomeronasal system in mice: from the nose to the hypothalamus—and back!. Semin. Cell Dev. Biol. 17:471–479.

    PubMed  Google Scholar 

  • Boehm, U., Zou, Z., and Buck, L. B. 2005. Feedback loops link odor and pheromone signaling with reproduction. Cell 123:683–695.

    PubMed  CAS  Google Scholar 

  • Boyse, E. A., Beauchamp, G., and Yamazaki, K. 1987. The genetics of body scent. Trends Genet. 3:97–102.

    Google Scholar 

  • Braun, T., Voland, P., Kunz, L., Prinz, C., and Gratzl, M. 2007. Enterochromaffin cells of the human gut: sensors for spices and odorants. Gastroenterology 132:1890–1901.

    PubMed  CAS  Google Scholar 

  • Breer, H., Fleischer, J., and Strotmann, J. 2006. The sense of smell: multiple olfactory subsystems. Cell Mol. Life Sci. 63:1465–1475.

    PubMed  CAS  Google Scholar 

  • Brennan, P. A., and Kendrick, K. M. 2006. Mammalian social odours: attraction and individual recognition. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 361:2061–2078.

    PubMed  CAS  Google Scholar 

  • Brody, C. D., and Hopfield, J. J. 2003. Simple networks for spike-timing-based computation, with application to olfactory processing. Neuron 37:843–852.

    PubMed  CAS  Google Scholar 

  • Bruce, H. M. 1959. An exteroceptive block to pregnancy in the mouse. Nature 184:105.

    PubMed  CAS  Google Scholar 

  • Buck, L. B. 2005. Unraveling the sense of smell (Nobel lecture). Angew. Chem. Int. Ed. Engl. 44:6128–6140.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Buonviso, N., Amat, C., and Litaudon, P. 2006. Respiratory modulation of olfactory neurons in the rodent brain. Chem. Senses 31:145–154.

    PubMed  Google Scholar 

  • Calu, D. J., Roesch, M. R., Stalnaker, T. A., and Schoenbaum, G. 2007. Associative encoding in posterior piriform cortex during odor discrimination and reversal learning. Cereb. Cortex 17:1342–1349.

    PubMed  Google Scholar 

  • Carleton, A., Petreanu, L. T., Lansford, R., Alvarez-buylla, A., and Lledo, P. M. 2003. Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci. 6:507–518.

    PubMed  CAS  Google Scholar 

  • Cecchi, G. A., Petreanu, L. T., Alvarez-buylla, A., and Magnasco, M. O. 2001. Unsupervised learning and adaptation in a model of adult neurogenesis. J Comput. Neurosci. 11:175–182.

    PubMed  CAS  Google Scholar 

  • Chabaud, P., Ravel, N., Wilson, D. A., Mouly, A. M., Vigouroux, M., Farget, V., and Gervais, R. 2000. Exposure to behaviourally relevant odour reveals differential characteristics in rat central olfactory pathways as studied through oscillatory activities. Chem. Senses 25:561–573.

    PubMed  CAS  Google Scholar 

  • Chalansonnet, M., and Chaput, M. A. 1998. Olfactory bulb output cell temporal response patterns to increasing odor concentrations in freely breathing rats. Chem. Senses 23:1–9.

    Article  PubMed  CAS  Google Scholar 

  • Chambers, R. A., and Conroy, S. K. 2007. Network modeling of adult neurogenesis: shifting rates of neuronal turnover optimally gears network learning according to novelty gradient. J. Cogn. Neurosci. 19:1–12.

    PubMed  Google Scholar 

  • Chen, W. R., and Shepherd, G. M. 2005. The olfactory glomerulus: a cortical module with specific functions. J. Neurocytol. 34:353–360.

    PubMed  Google Scholar 

  • Chu, S., and Downes, J. J. 2004. Proust reinterpreted: can Proust’s account of odour-cued autobiographical memory recall really be investigated? A reply to Jellinek. Chem. Senses 29:459–461.

    Google Scholar 

  • Cinelli, A. R., Hamilton, K. A., and Kauer, J. S. 1995. Salamander olfactory bulb neuronal activity observed by video rate, voltage-sensitive dye imaging. III. Spatial and temporal properties of responses evoked by odorant stimulation. J. Neurophysiol. 73:2053–2071.

    PubMed  CAS  Google Scholar 

  • Cleland, T. A., and Linster, C. 2005. Computation in the olfactory system. Chem. Senses 30:801–813.

    PubMed  Google Scholar 

  • Cleland, T. A., Johnson, B. A., Leon, M., and Linster, C. 2007. Relational representation in the olfactory system. Proc. Natl. Acad. Sci. USA 104:1953–1958.

    PubMed  CAS  Google Scholar 

  • Davila, N. G., Houpt, T. A., and Trombley, P. Q. 2007. Expression and function of kainate receptors in the rat olfactory bulb. Synapse 61:320–334.

    PubMed  CAS  Google Scholar 

  • Davison, I. G., and Katz, L. C. 2007. Sparse and selective odor coding by mitral/tufted neurons in the main olfactory bulb. J. Neurosci. 27:2091–2101.

    PubMed  CAS  Google Scholar 

  • Davison, A. P., Feng, J. F., and Brown, D. 2003. Dendrodendritic inhibition and simulated odor responses in a detailed olfactory bulb network model. J. Neurophysiol. 90:1921–1935.

    PubMed  CAS  Google Scholar 

  • De marchis, S., Bovetti, S., Carletti, B., Hsieh, Y. C., Garzotto, D., Peretto, P., Fasolo, A., Puche, A. C., and 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.

    PubMed  CAS  Google Scholar 

  • De souza, F. M. S., and Antunes, G. 2007. Biophysics of olfaction. Rep. Prog. Phys 70:451–491.

    Google Scholar 

  • Del punta, K., Leinders-zufall, T., Rodriguez, I., Jukam, D., Wysocki, C. J., Ogawa, S., Zufall, F., and Mombaerts, P. 2002. Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes. Nature 419:70–74.

    PubMed  CAS  Google Scholar 

  • Dielenberg, R. A., and Mcgregor, I. S. 2001. Defensive behavior in rats towards predatory odors: a review. Neurosci. Biobehav. Rev. 25:597–609.

    PubMed  CAS  Google Scholar 

  • Dolan, R. J. 2007. The human amygdala and orbital prefrontal cortex in behavioural regulation. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 362:787–799.

    PubMed  CAS  Google Scholar 

  • Dulac, C., and Wagner, S. 2006. Genetic analysis of brain circuits underlying pheromone signaling. Annu. Rev. Genet. 40:449–467.

    PubMed  CAS  Google Scholar 

  • Fendt, M., Endres, T., Lowry, C. A., Apfelbach, R., and Mcgregor, I. S. 2005. TMT-induced autonomic and behavioral changes and the neural basis of its processing. Neurosci. Biobehav. Rev. 29:1145–1156.

    PubMed  CAS  Google Scholar 

  • Ferkin, M. H., and Pierce, A. A. 2007. Perspectives on over-marking: is it good to be on top? J. Ethol. 25:107–116.

    Google Scholar 

  • Fletcher, M. L., and Wilson, D. A. 2003. Olfactory bulb mitral cell-tufted cell plasticity: odorant-specific tuning reflects previous odorant exposure. J. Neurosci. 23:6946–6955.

    PubMed  CAS  Google Scholar 

  • Fletcher, M. L., Smith, A. M., Best, A. R., and Wilson, D. A. 2005. High-frequency oscillations are not necessary for simple olfactory discriminations in young rats. J. Neurosci. 25:792–798.

    PubMed  CAS  Google Scholar 

  • Galef, B. G. JR, Mason, J. R., Preti, G., and Bean, N. J. 1988. Carbon disulfide: a semiochemical mediating socially-induced diet choice in rats. Physiol. Behav. 42:119–124.

    PubMed  CAS  Google Scholar 

  • Gelperin, A. 2006. Olfactory computations and network oscillations. J. Neurosci. 26:1663–1668.

    PubMed  CAS  Google Scholar 

  • Getchell, T. V., Margolis, F. L., and Getchell, M. L. 1984. Perireceptor and receptor events in vertebrate olfaction. Prog. Neurobiol. 23:317–345.

    PubMed  CAS  Google Scholar 

  • Getchell, T. V., Kwong, K., Saunders, C. P., Stromberg, A. J., and Getchell, M. L. 2006. Leptin regulates olfactory-mediated behavior in ob/ob mice. Physiol. Behav. 87:848–856.

    PubMed  CAS  Google Scholar 

  • Gheusi, G., and Lledo, P. M. 2007. Control of early events in olfactory processing by adult neurogenesis. Chem. Senses 32:397–409.

    PubMed  Google Scholar 

  • Gilad, Y., Bustamante, C. D., Lancet, D., and Paabo, S. 2003. Natural selection on the olfactory receptor gene family in humans and chimpanzees. Am. J. Hum. Genet. 73:489–501.

    PubMed  CAS  Google Scholar 

  • Gilad, Y., Wiebe, V., Przeworski, M., Lancet, D., and Paabo, S. 2004. Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. PLoS Biol. 2:E5.

    PubMed  Google Scholar 

  • Gilbert, A. N., Yamazaki, K., Beauchamp, G. K., and Thomas, L. 1986. Olfactory discrimination of mouse strains (Mus musculus) and major histocompatibility types by humans (Homo sapiens). J. Comp. Psych. 100:262–265.

    CAS  Google Scholar 

  • Gorojankina, T., Grebert, D., Salesse, R., Tanfin, Z., and Caillol, M. 2007. Study of orexins signal transduction pathways in rat olfactory mucosa and in olfactory sensory neurons-derived cell line Odora: multiple orexin signalling pathways. Regul. Pept. 141:73–85.

    PubMed  CAS  Google Scholar 

  • Gould, E. 2007. How widespread is adult neurogenesis in mammals? Nat. Rev. Neurosci. 8:481–488.

    PubMed  CAS  Google Scholar 

  • Goyert, H. F., Frank, M. E., Gent, J. F., and Hettinger, T. P. 2007. Characteristic component odors emerge from mixtures after selective adaptation. Brain Res. Bull. 72:1–9.

    PubMed  CAS  Google Scholar 

  • Graziadei, P. P. C., and Graziadei-monti, G. A. 1979. Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J. Neurocytol. 8:1–18.

    PubMed  CAS  Google Scholar 

  • Haga, S., Kimoto, H., and Touhara, K. 2007. Molecular characterization of vomeronasal sensory neurons responding to a male-specific peptide in tear fluid: sexual communication in mice. Pure Appl. Chem. 79:775–783.

    CAS  Google Scholar 

  • Halpern, M., and Martinez-marcos, A. 2003. Structure and function of the vomeronasal system: an update. Prog. Neurobiol. 70:245–318.

    PubMed  CAS  Google Scholar 

  • Hamilton, W. D., and Zuk, M. 1982. Heritable true fitness and bright birds: a role for parasites? Science 218:384–387.

    PubMed  CAS  Google Scholar 

  • Hardy, A. B., Aioun, J., Baly, C., Julliard, K. A., Caillol, M., Salesse, R., and Duchamp-viret, P. 2005. Orexin A modulates mitral cell activity in the rat olfactory bulb: patch-clamp study on slices and imunocytochemical localization of orexin receptors. Endocrinology 146:4042–4053.

    PubMed  CAS  Google Scholar 

  • Heale, V. R., and Vanderwolf, C. H. 1994. Toluene and weasel (2-propylthierane) odors suppress feeding in the rat. J. Chem. Ecol. 20:2953–2958.

    CAS  Google Scholar 

  • Heale, V. R., Vanderwolf, C. H., and Kavaliers, M. 1994. Components of weasel and fox odors elicit fast wave bursts in the dentate gyrus of rats. Behav. Brain Res. 63:159–165.

    PubMed  CAS  Google Scholar 

  • Hirota, J., Omura, M., and Mombaerts, P. 2007. Differential impact of Lhx2 deficiency on expression of class I and class II odorant receptor genes in mouse. Mol. Cell Neurosci. 34:679–688.

    PubMed  CAS  Google Scholar 

  • Holy, T. E., Dulac, C., and Meister, M. 2000. Responses of vomeronasal neurons to natural stimuli. Science 289:1569–1572.

    PubMed  CAS  Google Scholar 

  • Hopfield, J. J. 1999. Odor space and olfactory processing: collective algorithms and neural implementation. Proc. Natl. Acad. Sci. USA 96:12506–12511.

    PubMed  CAS  Google Scholar 

  • Hopfield, J. F., and Gelperin, A. 1989. Differential conditioning to a compound stimulus and its components in the terrestrial mollusc Limax maximus. Behav. Neurosci. 103:274–293.

    Google Scholar 

  • Hoppe, R., Lambert, T. D., Samollow, P. B., Breer, H., and Strotmann, J. 2006. Evolution of the “OR37” subfamily of olfactory receptors: a cross-species comparison. J. Mol. Evol. 62:460–472.

    PubMed  CAS  Google Scholar 

  • Hurst, J. L., Robertson, D. H. L., Tolladay, U., and Beynon, R. J. 1998. Proteins in urine scent marks of male house mice extend the longevity of olfactory signals. Anim. Behav. 55:1289–1297.

    PubMed  Google Scholar 

  • Ishikawa, T., Sato, T., Shimizu, A., Tsutsui, K., De curtis, M., and Iijima, T. 2007. Odor-driven activity in the olfactory cortex of an in vitro isolated guinea pig whole brain with olfactory epithelium. J. Neurophysiol. 97:670–679.

    PubMed  Google Scholar 

  • Jellinek, J. S. 2004. Proust remembered: has Proust’s account of odor-cued autobiographical memory recall really been investigated? Chem. Senses 29:455–458 (author reply 459–461).

    PubMed  Google Scholar 

  • Johnson, B. A., and Leon, M. 2007. Chemotopic odorant coding in a mammalian olfactory system. J. Comp. Neurol. 503:1–34.

    PubMed  CAS  Google Scholar 

  • Johnston, R. E., Sorokin, E. S., and Ferkin, M. H. 1997. Female voles discriminate males’ over-marks and prefer top-scent males. Anim. Behav. 54:679–690.

    PubMed  Google Scholar 

  • Johnson, B. A., Arguello, S., and Leon, M. 2007a. Odorants with multiple oxygen-containing functional groups and other odorants with high water solubility preferentially activate posterior olfactory bulb glomeruli. J. Comp. Neurol. 502:468–482.

    PubMed  CAS  Google Scholar 

  • Johnson, B. A., Ong, J., Lee, K., Ho, S. L., Arguello, S., and Leon, M. 2007b. Effects of double and triple bonds on the spatial representations of odorants in the rat olfactory bulb. J. Comp. Neurol. 500:720–733.

    PubMed  CAS  Google Scholar 

  • Jortner, R. A., Farivar, S. S., and Laurent, G. 2007. A simple connectivity scheme for sparse coding in an olfactory system. J. Neurosci. 27:1659–1669.

    PubMed  CAS  Google Scholar 

  • Julliard, A. K., Chaput, M. A., Apelbaum, A., Aime, P., Mahfouz, M., and Duchamp-viret, P. 2007. Changes in rat olfactory detection performance induced by orexin and leptin mimicking fasting and satiation. Behav. Brain Res. 183:123–129.

    PubMed  CAS  Google Scholar 

  • Kadohisa, M., and Wilson, D. A. 2006. Olfactory cortical adaptation facilitates detection of odors against background. J. Neurophysiol. 95:1888–1896.

    PubMed  Google Scholar 

  • Kajiya, K., Inaki, K., Tanaka, M., Haga, T., Kataoka, H., and Touhara, K. 2001. Molecular bases of odor discrimination: reconstitution of olfactory receptors that recognize overlapping sets of odorants. J. Neurosci. 21:6018–6025.

    PubMed  CAS  Google Scholar 

  • Kats, L. B., and Dill, L. M. 1998. The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394.

    Google Scholar 

  • Kavaliers, M., Choleris, E., and Pfaff, D. W. 2005a. Genes, odours and the recognition of parasitized individuals by rodents. Trends Parasitol. 21:423–429.

    PubMed  CAS  Google Scholar 

  • Kavaliers, M., Choleris, E., and Pfaff, D. W. 2005b. Recognition and avoidance of the odors of parasitized conspecifics and predators: differential genomic correlates. Neurosci. Biobehav. Rev. 29:1347–1359.

    PubMed  Google Scholar 

  • Kay, L. M. 2003. Two species of gamma oscillations in the olfactory bulb: dependence on behavioral state and synaptic interactions. J. Integr. Neurosci. 2:31–44.

    PubMed  Google Scholar 

  • Kay, L. M., and Laurent, G. 1999. Odor- and context-dependent modulation of mitral cell activity in behaving rats. Nature Neurosci. 2:1003–1009.

    PubMed  CAS  Google Scholar 

  • Kay, L. M., and Sherman, S. M. 2007. An argument for an olfactory thalamus. Trends Neurosci. 30:47–53.

    PubMed  CAS  Google Scholar 

  • Kay, L. M., Lowry, C. A., and Jacobs, H. A. 2003. Receptor contributions to configural and elemental odor mixture perception. Behav. Neurosci. 117:1108–1114.

    PubMed  Google Scholar 

  • Kay, L. M., Crk, T., and Thorngate, J. 2005. A redefinition of odor mixture quality. Behav. Neurosci. 119:726–733.

    PubMed  CAS  Google Scholar 

  • Keller, A., and Vosshall, L. B. 2007. Influence of odorant receptor repertoire on odor perception in humans and fruit flies. Proc. Natl. Acad. Sci. USA 104:5614–5619.

    PubMed  CAS  Google Scholar 

  • Kelliher, K. R., Spehr, M., Li, X. H., Zufall, F., and Leinders-zufall, T. 2006. Pheromonal recognition memory induced by TRPC2-independent vomeronasal sensing. Eur. J. Neurosci. 23:3385–3390.

    PubMed  Google Scholar 

  • Kelliher, K. R., Ziesmann, J., Munger, S. D., Reed, R. R., and Zufall, F. 2003. Importance of the CNGA4 channel gene for odor discrimination and adaptation in behaving mice. Proc. Natl. Acad. Aci. USA 100:4299–4304.

  • Kent, P. F., Mozell, M. M., Murphy, S. J., and Hornung, D. E. 1996. The interaction of imposed and inherent olfactory mucosal activity patterns and their composite representation in a mammalian species using voltage-sensitive dyes. J. Neurosci. 16:345–353.

    PubMed  CAS  Google Scholar 

  • Kent, P. F., Mozell, M. M., Youngentob, S. L., and Yurco, P. 2003. Mucosal activity patterns as a basis for olfactory discrimination: comparing behavior and optical recordings. Brain Res. 981:1–11.

    PubMed  CAS  Google Scholar 

  • Kepecs, A., Uchida, N., and Mainen, Z. F. 2006. The sniff as a unit of olfactory processing. Chem. Senses 31:167–179.

    PubMed  Google Scholar 

  • Keverne, E. B. 1999. The vomeronasal organ. Science 286:716–720.

    PubMed  CAS  Google Scholar 

  • Kimoto, H., Haga, S., Sato, K., and Touhara, K. 2005. Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 437:898–901.

    PubMed  CAS  Google Scholar 

  • Kini, A. D., and Firestein, S. 2001. The molecular basis of olfaction. Chimia 55:453–459.

    CAS  Google Scholar 

  • Knapp, L. A. 2005. The ABCs of MHC. Evol. Anthropol. 14:28–37.

    Google Scholar 

  • Knapp, L. A., Robson, J., and Waterhouse, J. S. 2006. Olfactory signals and the MHC: a review and a case study in Lemur catta. Am. J. Primatol. 68:568–584.

    PubMed  CAS  Google Scholar 

  • Kobayakawa, K., Kobayakawa, R., Matsumoto, H., Oka, Y., Imai, T., Ikawa, M., Okabe, M., Ikeda, T., Itohara, S., Kikusui, T. et al. 2007. Innate versus learned odour processing in the mouse olfactory bulb. Nature 450:503–508.

    PubMed  CAS  Google Scholar 

  • Koulakov, A., Rinberg, D., and Gelperin, A. 2007. Olfactory coding with all-or-nothing glomeruli. J. Neurophysiol. 98:3134–3142.

    PubMed  Google Scholar 

  • Kurtz, D. B., Zhao, K., Hornung, D. E., and Scherer, P. 2004. Experimental and numerical determination of odorant solubility in nasal and olfactory mucosa. Chem. Senses 29:763–773.

    PubMed  Google Scholar 

  • Lai, W. S., Ramiro, L. L., Yu, H. A., and Johnston, R. E. 2005. Recognition of familiar individuals in golden hamsters: a new method and functional neuroanatomy. J. Neurosci. 25:11239–11247.

    PubMed  CAS  Google Scholar 

  • Laing, D. G. 1986. Identification of single dissimilar odors is achieved by humans with a single sniff. Physiol. Behav. 37:163–170.

    PubMed  CAS  Google Scholar 

  • Laurent, G., Stopfer, M., Friedrich, R. W., Rabinovich, M. I., Volkovskii, A., and Abarbanel, H. D. 2001. Odor encoding as an active, dynamical process: experiments, computation, and theory. Annu. Rev. Neurosci. 24:263–297.

    PubMed  CAS  Google Scholar 

  • Lehmkuhle, M. J., Normann, R. A., and Maynard, E. M. 2006. Trial-by-trial discrimination of three enantiomer pairs by neural ensembles in mammalian olfactory bulb. J. Neurophysiol. 95:1369–1379.

    PubMed  CAS  Google Scholar 

  • Leinders-zufall, T., Lane, A. P., Puche, A. C., Ma, W., Novotny, M. V., Shipley, M. T., and Zufall, F. 2000. Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405:792–796.

    PubMed  CAS  Google Scholar 

  • Leinders-zufall, T., Brennan, P., Widmayer, P., Chandramani, P. S., Maul-pavicic, A., Jager, M., Li, X. H., Breer, H., Zufall, F., and Boehm, T. 2004. MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 306:1033–1037.

    PubMed  CAS  Google Scholar 

  • Lepri, J. J., and Wysocki, C. J. 1987. Removal of the vomeronasal organ disrupts the activation of reproduction in female voles. Physiol. Behav. 40:349–355.

    PubMed  CAS  Google Scholar 

  • Leung, C. T., Coulombe, P. A., and Reed, R. R. 2007. Contribution of olfactory neural stem cells to tissue maintenance and regeneration. Nat. Neurosci. 10:720–726.

    PubMed  CAS  Google Scholar 

  • Levai, O., Feistel, T., Breer, H., and Strotmann, J. 2006. Cells in the vomeronasal organ express odorant receptors but project to the accessory olfactory bulb. J. Comp. Neurol. 498:476–490.

    PubMed  CAS  Google Scholar 

  • Leypold, B. G., Yu, C. R., Leinders-zufall, T., Kim, M. M., Zufall, F., and Axel, R. 2002. Altered sexual and social behaviors in trp2 mutant mice. Proc. Natl. Acad. Sci. USA 99:6376–6381.

    PubMed  CAS  Google Scholar 

  • Lin, W., Arellano, J., Slotnick, B., and Restrepo, D. 2004. Odors detected by mice deficient in cyclic nucleotide-gated channel subunit A2 stimulate the main olfactory system. J. Neurosci. 24:3703–3710.

    PubMed  CAS  Google Scholar 

  • Lin, D. Y., Zhang, S. Z., Block, E., and Katz, L. C. 2005. Encoding social signals in the mouse main olfactory bulb. Nature 434:470–477.

    PubMed  CAS  Google Scholar 

  • Lin, D. Y., Shea, S. D., and Katz, L. C. 2006. Representation of natural stimuli in the rodent main olfactory bulb. Neuron 50:937–949.

    CAS  Google Scholar 

  • Lin, W., Margolskee, R., Donnert, G., Hell, S. W., and Restrepo, D. 2007. Olfactory neurons expressing transient receptor potential channel M5 (TRPM5) are involved in sensing semiochemicals. Proc. Natl. Acad. Sci. USA 104:2471–2476.

    PubMed  CAS  Google Scholar 

  • Linster, C., Henry, L., Kadohisa, M., and Wilson, D. A. 2007. Synaptic adaptation and odor-background segmentation. Neurobiol. Learn. Mem. 87:352–360.

    PubMed  Google Scholar 

  • Lledo, P. M., Alonso, M., and Grubb, M. S. 2006. Adult neurogenesis and functional plasticity in neuronal circuits. Nat. Rev. Neurosci. 7:179–193.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Lorig, T. S. 2000. The application of electroencephalographic techniques to the study of human olfaction: a review and tutorial. Int. J. Psychophysiol. 36:91–104.

    PubMed  CAS  Google Scholar 

  • Lowe, G. 2003. Flash photolysis reveals a diversity of ionotropic glutamate receptors on the mitral cell somatodendritic membrane. J. Neurophysiol. 90:1737–1746.

    PubMed  CAS  Google Scholar 

  • Lowry, C. A., and Kay, L. M. 2007. Chemical factors determine olfactory system Beta oscillations in waking rats. J. Neurophysiol. 98:394–404.

    PubMed  CAS  Google Scholar 

  • Lu, X. C. M., and Slotnick, B. M. 1998. Olfaction in rats with extensive lesions of the olfactory bulbs: implications for odor coding. Neuroscience 84:849–866.

    PubMed  CAS  Google Scholar 

  • Luo, M., Fee, M. S., and Katz, L. C. 2003. Encoding pheromonal signals in the accessory olfactory bulb of behaving mice. Science 299:1196–1201.

    PubMed  CAS  Google Scholar 

  • Ma, J., and Lowe, G. 2007. Calcium permeable AMPA receptors and autoreceptors in external tufted cells of rat olfactory bulb. Neuroscience 144:1094–1108.

    PubMed  CAS  Google Scholar 

  • Magavi, S. S. P., Mitchell, B. D., Szentirmai, O., Carter, B. S., and Macklis, J. D. 2005. Adult-born and preexisting olfactory granule neurons undergo distinct experience-dependent modifications of their olfactory responses in vivo. J. Neurosci. 25:10729–10739.

    PubMed  CAS  Google Scholar 

  • Maico, L. M., Burrows, A. M., Mooney, M. P., Siegel, M. I., Bhatnagar, K. P., and Smith, T. D. 2003. Size of the vomeronasal organ in wild Microtus with different mating strategies. Acta Biol. Hung. 54:263–273.

    PubMed  Google Scholar 

  • Mainen, Z. F. 2006. Behavioral analysis of olfactory coding and computation in rodents. Curr. Opin. Neurobiol. 16:429–434.

    Google Scholar 

  • Mainland, J., and Sobel, N. 2006. The sniff is part of the olfactory percept. Chem. Senses 31:181–196.

    PubMed  Google Scholar 

  • Mak, G. K., Enwere, E. K., Gregg, C., Pakarainen, T., Poutanen, M., Huhtaniemi, I., and Weiss, S. 2007. Male pheromone-stimulated neurogenesis in the adult female brain: possible role in mating behavior. Nat. Neurosci. 10:1003–1011.

    PubMed  CAS  Google Scholar 

  • Malnic, B., Hirono, J., Sato, T., and Buck, L. 1999. Combinatorial receptor codes for odors. Cell 96:713–723.

    PubMed  CAS  Google Scholar 

  • Man, O., Gilad, Y., and Lancet, D. 2004. Prediction of the odorant binding site of olfactory receptor proteins by human-mouse comparisons. Protein Sci. 13:240–254.

    PubMed  CAS  Google Scholar 

  • Mandairon, N., Sacquet, J., Garcia, S., Ravel, N., Jourdan, F., and Didier, A. 2006a. Neurogenic correlates of an olfactory discrimination task in the adult olfactory bulb. Eur. J. Neurosci. 24:3578–3588.

    PubMed  Google Scholar 

  • Mandairon, N., Sacquet, J., Jourdan, F., and Didier, A. 2006b. Long-term fate and distribution of newborn cells in the adult mouse olfactory bulb: influences of olfactory deprivation. Neuroscience 141:443–451.

    PubMed  CAS  Google Scholar 

  • Mandairon, N., Stack, C., and Linster, C. 2006c. Olfactory enrichment improves the recognition of individual components in mixtures. Physiol. Behav. 89:379–384.

    PubMed  CAS  Google Scholar 

  • Martin, C., Gervais, R., Chabaud, P., Messaoudi, B., and Ravel, N. 2004. Learning-induced modulation of oscillatory activities in the mammalian olfactory system: the role of the centrifugal fibres. J. Physiol. Paris 98:467–478.

    PubMed  Google Scholar 

  • Martin, C., Gervais, R., Messaoudi, B., and Ravel, N. 2006. Learning-induced oscillatory activities correlated to odour recognition: a network activity. Eur. J. Neurosci. 23:1801–1810.

    PubMed  Google Scholar 

  • Martinez-marcos, A., Jia, C., Quan, W., and Halpern, M. 2005. Neurogenesis, migration, and apoptosis in the vomeronasal epithelium of adult mice. J. Neurobiol. 63:173–187.

    PubMed  CAS  Google Scholar 

  • Mcbride, K., and Slotnick, B. 2006. Discrimination between the enantiomers of carvone and of terpinen-4-ol odorants in normal rats and those with lesions of the olfactory bulbs. J. Neurosci. 26:9892–9901.

    PubMed  CAS  Google Scholar 

  • Menini, A., Picco, C., and Firestein, S. 1995. Quantal-like current fluctuations induced by odorants in olfactory receptor cells. Nature 373:435–437.

    PubMed  CAS  Google Scholar 

  • Meredith, M. 1992. Neural circuit computation—complex patterns in the olfactory bulb. Brain Res. Bull. 29:111–117.

    PubMed  CAS  Google Scholar 

  • Meredith, M. 1994. Chronic recording of vomeronasal pump activation in awake behaving hamsters. Physiol. Behav. 56:345–354.

    PubMed  CAS  Google Scholar 

  • Miller, G. L., Loudon, C., and Freed, S. 2007. Position around a tree: consequences for pheromone detection. J. Chem. Ecol. 33:541–554.

    PubMed  CAS  Google Scholar 

  • Mizrahi, A. 2007. Dendritic development and plasticity of adult-born neurons in the mouse olfactory bulb. Nat. Neurosci. 10:444–452.

    PubMed  CAS  Google Scholar 

  • Mizrahi, A., Lu, J., Irving, R., Feng, G., and Katz, L. C. 2006. In vivo imaging of juxtaglomerular neuron turnover in the mouse olfactory bulb. Proc. Natl. Acad. Sci. USA 103:1912–1917.

    PubMed  CAS  Google Scholar 

  • More, L. 2006. Mouse major urinary proteins trigger ovulation via the vomeronasal organ. Chem. Senses 31:393–401.

    PubMed  CAS  Google Scholar 

  • Mori, I., Nishiyama, Y., Yokochi, T., and Kimura, Y. 2005. Olfactory transmission of neurotropic viruses. J. Neurovirol. 11:129–137.

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Mozell, M. M., and Jagodowicz, M. 1973. Chromatographic separation of odorants by the nose: retention times measured across in vivo olfactory mucosa. Science 181:1247–1249.

    PubMed  CAS  Google Scholar 

  • Mozell, M. M., and Jagodowicz, M. 1974. Mechanisms underlying the analysis of odorant quality at the level of the olfactory mucosa. I. Spatiotemporal sorption patterns. Ann. NY Acad. Sci. 237:76–90.

    PubMed  CAS  Google Scholar 

  • Murlis, J., Elkinton, J. S., and Carde, R. T. 1992. Odor plumes and how insects use them. Ann. Rev. Entomol. 37:505–532.

    Google Scholar 

  • Murlis, J., Willis, M. A., and Carde, R. T. 2000. Spatial and temporal structures of pheromone plumes in fields and forests. Physiol. Entomol. 25:211–222.

    CAS  Google Scholar 

  • Murray, E. A., O’doherty, J. P., and Schoenbaum, G. 2007. What we know and do not know about the functions of the orbitofrontal cortex after 20 years of cross-species studies. J. Neurosci. 27:8166–8169.

    PubMed  CAS  Google Scholar 

  • Novotny, M. V., Soini, H. A., Koyama, S., Wiesler, D., Bruce, K. E., and Penn, D. J. 2007. Chemical identification of MHC-influenced volatile compounds in mouse urine. I. Quantitative proportions of major chemosignals. J. Chem. Ecol. 33:417–434.

    PubMed  CAS  Google Scholar 

  • Ogawa, S., Lee, T. M., Nayak, A. S., and Glynn, P. 1990. Oxygenation-sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields. Magn. Reson. Med. 14:68–78.

    PubMed  CAS  Google Scholar 

  • Olariu, A., Cleaver, K. M., Shore, L. E., Brewer, M. D., and Cameron, H. A. 2005. A natural form of learning can increase and decrease the survival of new neurons in the dentate gyrus. Hippocampus 15:750–762.

    PubMed  Google Scholar 

  • Olshausen, B. A., and Field, D. J. 2004. Sparse coding of sensory inputs. Curr. Opin. Neurobiol. 14:481–487.

    PubMed  CAS  Google Scholar 

  • Pause, B. M., Krauel, K., Sojka, B., and Ferstl, R. 1998. Body odor evoked potentials: a new method to study the chemosensory perception of self and non-self in humans. Genetica 104:285–294.

    PubMed  Google Scholar 

  • Pause, B. M., Krauel, K., Schrader, C., Sojka, B., Westphal, E., Muller-ruchholtz, W., and Ferstl, R. 2006. The human brain is a detector of chemosensorily transmitted HLA-class I-similarity in same- and opposite-sex relations. Proc. Biol. Sci. 273:471–478.

    PubMed  CAS  Google Scholar 

  • Penn, D. J. 2002. The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108:1–21.

    Google Scholar 

  • Penn, D. J., Oberzaucher, E., Grammer, K., Fischer, G., Soini, H. A., Wiesler, D., Novotny, M. V., Dixon, S. J., Xu, Y., and Brereton, R. G. 2007. Individual and gender fingerprints in human body odour. J. R. Soc. Interface 4:331–340.

    PubMed  Google Scholar 

  • Peters, A. 2007. Testosterone and carotenoids: an integrated view of trade-offs between immunity and sexual signalling. Bioessays 29:427–430.

    PubMed  CAS  Google Scholar 

  • Petreanu, L., and Alvarez-buylla, A. 2002. Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J. Neurosci. 22:6106–6113.

    PubMed  CAS  Google Scholar 

  • Pierce, A. A., Vaughn, A. A., and Ferkin, M. H. 2007. Food deprivation suppresses a preference for the top-scent mark of an over-mark in meadow voles (Microtus pennsylvanicus). Ethology 113:480–486.

    Google Scholar 

  • Ramus, S. J., and Eichenbaum, H. 2000. Neural correlates of olfactory recognition memory in the rat orbitofrontal cortex. J. Neurosci. 20:8199–8208.

    PubMed  CAS  Google Scholar 

  • Rawson, N. E., and Gomez, G. 2002. Cell and molecular biology of human olfaction. Microsc. Res. Tech. 58:142–151.

    PubMed  CAS  Google Scholar 

  • Reisert, J. 2005. Signal transduction in vertebrate olfactory receptor cells. Lect. Notes Math. 1867:155–171.

    CAS  Google Scholar 

  • Rennaker, R. L., Chen, C. F., Ruyle, A. M., Sloan, A. M., and Wilson, D. A. 2007. Spatial and temporal distribution of odorant-evoked activity in the piriform cortex. J. Neurosci. 27:1534–1542.

    PubMed  CAS  Google Scholar 

  • Restrepo, D., Teeter, J. H., and Schild, D. 1996. Second messenger signaling in olfactory transduction. J. Neurobiol. 30:37–48.

    PubMed  CAS  Google Scholar 

  • Restrepo, D., Arellano, J., Oliva, A. M., Schafer, M. L., and Lin, W. 2004. Emerging views on the distinct but related roles of the main and accessory olfactory systems in responsiveness to chemosensory signals in mice. Horm. Behav. 46:247–256.

    PubMed  CAS  Google Scholar 

  • Restrepo, D., Lin, W., Salcedo, E., Yamazaki, K., and Beauchamp, G. 2006. Odortypes and MHC peptides: complementary chemosignals of MHC haplotype? Trends Neurosci. 29:604–609.

    PubMed  CAS  Google Scholar 

  • Rinberg, D., and Gelperin, A. 2006. Olfactory neuronal dynamics in behaving animals. Semin. Cell Dev. Biol. 17:454–461.

    PubMed  Google Scholar 

  • Rinberg, D., Koulakov, A., and Gelperin, A. 2006. Sparse odor coding in the behaving mouse. J. Neurosci. 26:8857–8865.

    PubMed  CAS  Google Scholar 

  • Robertson, D. H., Hurst, J. L., Searle, J. B., Gunduz, I., and Beynon, R. J. 2007. Characterization and comparison of major urinary proteins from the house mouse, Mus musculus domesticus, and the aboriginal mouse, Mus macedonicus. J. Chem. Ecol. 33:613–630.

    PubMed  CAS  Google Scholar 

  • Rosen, J. B., West, E. A., and Donley, M. P. 2006. Not all rat strains are equal: differential unconditioned fear responses to the synthetic fox odor 2,4,5-trimethylthiazoline in three outbred rat strains. Behav. Neurosci. 120:290–297.

    PubMed  CAS  Google Scholar 

  • Roux, S. G., Garcia, S., Bertrand, B., Cenier, T., Vigouroux, M., Buonviso, N., and Litaudon, P. 2006. Respiratory cycle as time basis: an improved method for averaging olfactory neural events. J. Neurosci. Methods 152:173–178.

    PubMed  Google Scholar 

  • Sakurai, T., Amemiya, A., Ishii, M., Matsuzaki, I., Chemelli, R. M., Tanaka, H., Williams, S. C., Richardson, J. A., Kozlowski, G. P., Wilson, S. et al. 1998. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92:573–585.

    PubMed  CAS  Google Scholar 

  • Sbarbati, A., and Osculati, F. 2006. Allelochemical communication in vertebrates: kairomones, allomones and synomones. Cells Tissues Organs 183:206–219.

    PubMed  CAS  Google Scholar 

  • Schaefer, A. T., and Margrie, T. W. 2007. Spatiotemporal representations in the olfactory system. Trends Neurosci. 30:92–100.

    PubMed  CAS  Google Scholar 

  • Schafer, J. R., Kida, I., Xu, F., Rothman, D. L., and Hyder, F. 2006. Reproducibility of odor maps by fMRI in rodents. Neuroimage 31:1238–1246.

    PubMed  Google Scholar 

  • Schildknecht, H., Wilz, I., Enzmann, F., Grund, N., and Ziegler, M. 1976. Mustelan, the malodorous substance from the anal gland of the mink (Mustela vison) and the polecat (Mustela putorius). Angew. Chem. Int. Ed. Engl. 15:242–243.

    PubMed  CAS  Google Scholar 

  • Schlief, M. L., and Wilson, R. I. 2007. Olfactory processing and behavior downstream from highly selective receptor neurons. Nat. Neurosci. 10:623–630.

    PubMed  CAS  Google Scholar 

  • Scordato, E. S., Dubay, G., and Drea, C. M. 2007. Chemical composition of scent marks in the ringtailed lemur (Lemur catta): glandular differences, seasonal variation, and individual signatures. Chem. Senses 32:493–504.

    PubMed  CAS  Google Scholar 

  • Scott, J. W. 2006. Sniffing and spatiotemporal coding in olfaction. Chem. Senses 31:119–130.

    PubMed  Google Scholar 

  • Scott, J. W., Acevedo, H. P., and Sherrill, L. 2006. Effects of concentration and sniff flow rate on the rat electroolfactogram. Chem. Senses 31:581–593.

    PubMed  Google Scholar 

  • Settles, G. S. 2005. Sniffers: fluid-dynamic sampling for olfactory trace detection in nature and homeland security—the 2004 Freeman scholar lecture. J. Fluids Eng. 127:189–218.

    Google Scholar 

  • Shepherd, G. M. 2004. The human sense of smell: are we better than we think? PLoS Biol. 2:572–575.

    CAS  Google Scholar 

  • Shepherd, G. M., Chen, W. R., and Greer, C. A. 2004. Olfactory bulb, pp. 133–169, in G. M. Shepherd (ed.). The Synaptic Organization of the Brain, 5th edn. Oxford University Press, New York.

    Google Scholar 

  • Shipley, M. T., and Ennis, M. 1995. Functional organization of olfactory system. J. Neurobiol. 30:123–176.

    Google Scholar 

  • Singer, B. H., Kim, S., and Zochowski, M. 2007. Binaral interaction and centrifugal input enhances spatial contrast in olfactory bulb activation. Eur. J. Neurosci. 25:576–586.

    PubMed  Google Scholar 

  • Slotnick, B. 2007a. Olfactory performance of rats after selective deafferentation of the olfactory bulb by 3-methyl indole. Chem. Senses 32:173–181.

    PubMed  CAS  Google Scholar 

  • Slotnick, B. 2007b. Response accuracy and odor sampling time in mice trained to discriminate between enantiomers of carvone and those of terpinen-4-ol. Chem. Senses 32:721–725.

    PubMed  Google Scholar 

  • Slotnick, B., and Bisulco, S. 2003. Detection and discrimination of carvone entantiomers in rats with olfactory bulb lesions. Neuroscience 121:451–457.

    PubMed  CAS  Google Scholar 

  • Slotnick, B., Cockerham, R., and Pickett, E. 2004. Olfaction in olfactory bulbectomized rats. J. Neurosci. 24:9195–9200.

    PubMed  CAS  Google Scholar 

  • Slotnick, B., Sanguino, A., Husband, S., Marquino, G., and Silberberg, A. 2007. Olfaction and olfactory epithelium in mice treated with zinc gluconate. Laryngoscope 117:743–749.

    PubMed  CAS  Google Scholar 

  • Smith, T. D., Bhatnagar, K. P., Dennis, J. C., Morrison, E. E., and Park, T. J. 2007. Growth-deficient vomeronasal organs in the naked mole-rat (Heterocephalus glaber). Brain Res. 1132:78–83.

    PubMed  CAS  Google Scholar 

  • Soucy, E. R., Albeanu, D. F., Murthy, V. N., and Meister, M. 2007. Comparing glomerular maps in the olfactory bulbs of mice and rats, in Cosyne 2007 Abstracts, p. 55, Salt Lake City, UT.

  • Spehr, M., Gisselmann, G., Poplawski, A., Riffell, J. A., Wetzel, C. H., Zimmer, R. K., and Hatt, H. 2003. Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 299:2054–2058.

    PubMed  CAS  Google Scholar 

  • Spehr, M., Schwane, K., Riffell, J. A., Zimmer, R. K., and Hatt, H. 2006. Odorant receptors and olfactory-like signaling mechanisms in mammalian sperm. Mol. Cell Endocrinol. 250:128–136.

    PubMed  CAS  Google Scholar 

  • Staples, L. G., and Mcgregor, I. S. 2006. Defensive responses of Wistar and Sprague–Dawley rats to cat odour and TMT. Behav. Brain Res. 172:351–354.

    PubMed  CAS  Google Scholar 

  • Stopfer, M. 2007. Olfactory processing: massive convergence onto sparse codes. Curr. Biol. 17:R363–R364.

    PubMed  CAS  Google Scholar 

  • Stopkova, R., Stopka, P., Janotova, K., and Jedelsky, P. L. 2007. Species-specific expression of major urinary proteins in the house mice (Mus musculus musculus and Mus musculus domesticus). J. Chem. Ecol. 33:861–869.

    PubMed  CAS  Google Scholar 

  • Storan, M. J., and Key, B. 2006. Septal organ of Gruneberg is part of the olfactory system. J. Comp. Neurol. 494:834–844.

    PubMed  Google Scholar 

  • Stowers, L., Holy, T. E., Meister, M., Dulac, C., and Koentges, G. 2002. Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 295:1493–1500.

    PubMed  CAS  Google Scholar 

  • Szobota, S., Gorostiza, P., Del bene, F., Wyart, C., Fortin, D. L., Kolstad, K. D., Tulyathan, O., Volgraf, M., Numano, R., Aaron, H. L. et al. 2007. Remote control of neuronal activity with a light-gated glutamate receptor. Neuron 54:535–545.

    PubMed  CAS  Google Scholar 

  • Thesen, T., and Murphy, C. 2002. Reliability analysis of event-related brain potentials to olfactory stimuli. Psychophysiology 39:733–738.

    PubMed  Google Scholar 

  • Thom, M. D., and Hurst, J. L. 2004. Individual recognition by scent. Ann. Zool. Fenn. 41:765–787.

    Google Scholar 

  • Thompson, R. N., Mcmillon, R., Napier, A., and Wekesa, K. S. 2007. Pregnancy block by MHC class I peptides is mediated via the production of inositol 1,4,5-trisphosphate in the mouse vomeronasal organ. J. Exp. Biol. 210:1406–1412.

    PubMed  CAS  Google Scholar 

  • Uchida, N., and Mainen, Z. F. 2003. Speed and accuracy of olfactory discrimination in the rat. Nat. Neurosci. 6:1224–1229.

    PubMed  CAS  Google Scholar 

  • Uchida, N., Kepecs, A., and Mainen, Z. F. 2006. Seeing at a glance, smelling in a whiff: rapid forms of perceptual decision making. Nat. Rev. Neurosci. 7:485–491.

    PubMed  CAS  Google Scholar 

  • Vanderhaeghen, P., Schurmans, S., Vassart, G., and Parmentier, M. 1993. Olfactory receptors are displayed on dog mature sperm cells. J. Cell Biol. 123:1441–1452.

    PubMed  CAS  Google Scholar 

  • Vendruscolo, L. F., Vendruscolo, J. C., Terenina-rigaldie, E., Raba, F., Ramos, A., Takahashi, R. N., and Mormede, P. 2006. Genetic influences on behavioral and neuroendocrine responses to predator-odor stress in rats. Neurosci. Lett. 409:89–94.

    PubMed  CAS  Google Scholar 

  • Vergassola, M., Villermaux, E., and Shraiman, B. I. 2007. ‘Infotaxis’ as a strategy for searching without gradients. Nature 445:406–409.

    PubMed  CAS  Google Scholar 

  • Verhagen, J. V., Wesson, D. W., Netoff, T. I., White, J. A., and Wachowiak, M. 2007. Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat. Neurosci. 10:631–639.

    PubMed  CAS  Google Scholar 

  • Vickers, N. J. 2000. Mechanisms of animal navigation in odor plumes. Biol. Bull. 198:203–212.

    PubMed  CAS  Google Scholar 

  • Vos, M., Vet, L. E. M., Wackers, F. L., Middelburg, J. J., Van der putten, W. H., Mooij, W. M., Heip, C. H. R., and Van donk, E. 2006. Infochemicals structure marine, terrestrial and freshwater food webs: implications for ecological informatics. Ecol. Inform. 1:23–32.

    Google Scholar 

  • Vyas, A., Kim, S. K., Giacomini, N., Boothroyd, J. C., and Sapolsky, R. M. 2007a. Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc. Natl. Acad. Sci. USA 104:6442–6447.

    PubMed  CAS  Google Scholar 

  • Vyas, A., Kim, S. K., and Sapolsky, R. M. 2007b. The effects of toxoplasma infection on rodent behavior are dependent on dose of the stimulus. Neuroscience 148:342–348.

    PubMed  CAS  Google Scholar 

  • Wachowiak, M., and Shipley, M. T. 2006. Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Semin. Cell Dev. Biol. 17:411–423.

    PubMed  Google Scholar 

  • Wagner, S., Gresser, A. L., Torello, A. T., and Dulac, C. 2006. A multireceptor genetic approach uncovers an ordered integration of VNO sensory inputs in the accessory olfactory bulb. Neuron 50:697–709.

    PubMed  CAS  Google Scholar 

  • Weiler, E., Mcculloch, M. A., and Farbman, A. I. 1999. Proliferation in the vomeronasal organ of the rat during postnatal development. Eur. J. Neurosci. 11:700–711.

    PubMed  CAS  Google Scholar 

  • Whittle, C. L., Fakharzadeh, S., Eades, J., and Preti, G. 2007. Human breath odors and their use in diagnosis. Ann. NY Acad. Sci. 1098:252–266.

    PubMed  CAS  Google Scholar 

  • Willhite, D. C., Nguyen, K. T., Masurkar, A. V., Greer, C. A., Shepherd, G. M., and Chen, W. R. 2006. Viral tracing identifies distributed columnar organization in the olfactory bulb. Proc. Natl. Acad. Sci. USA 103:12592–12597.

    PubMed  CAS  Google Scholar 

  • Willmore, B., and Tolhurst, D. J. 2001. Characterizing the sparseness of neural codes. Network 12:255–270.

    PubMed  CAS  Google Scholar 

  • Willse, A., Belcher, A. M., Preti, G., Wahl, J. H., Thresher, M., Yang, P., Yamazaki, K., and Beauchamp, G. K. 2005. Identification of major histocompatibility complex-regulated body odorants by statistical analysis of a comparative gas chromatography/mass spectrometry experiment. Anal. Chem. 77:2348–2361.

    PubMed  CAS  Google Scholar 

  • Willse, A., Kwak, J., Yamazaki, K., Preti, G., Wahl, J. H., and Beauchamp, G. K. 2006. Individual odortypes: interaction of MHC and background genes. Immunogenetics 58:967–982.

    PubMed  CAS  Google Scholar 

  • Wilson, R. I., and Mainen, Z. F. 2006. Early events in olfactory processing. Annu. Rev. Neurosci. 29:163–201.

    PubMed  CAS  Google Scholar 

  • Wilson, D. A., and Stevenson, R. J. 2006. Learning to Smell. p. 309. Johns Hopkins University Press, Baltimore, MD.

    Google Scholar 

  • Wilson, D. A., Kadohisa, M., and Fletcher, M. L. 2006. Cortical contributions to olfaction: plasticity and perception. Semin. Cell Dev. Biol. 17:462–470.

    PubMed  Google Scholar 

  • Winston, J. S., Gottfried, J. A., Kilner, J. M., and Dolan, R. J. 2005. Integrated neural representations of odor intensity and affective valence in human amygdala. J. Neurosci. 25:8903–8907.

    PubMed  CAS  Google Scholar 

  • Woodley, S. K., and Baum, M. J. 2004. Differential activation of glomeruli in the ferret’s main olfactory bulb by anal scent gland odours from males and females: an early step in mate identification. Eur. J. Neurosci. 20:1025–1032.

    PubMed  Google Scholar 

  • Wyart, C., Webster, W. W., Chen, J. H., Wilson, S. R., Mcclary, A., Khan, R. M., and Sobel, N. 2007. Smelling a single component of male sweat alters levels of cortisol in women. J. Neurosci. 27:1261–1265.

    PubMed  CAS  Google Scholar 

  • Wysocki, C. J. 1979. Neurobehavioral evidence for the involvement of the vomeronasal system in mammalian reproduction. Neurosci. Biobehav. Rev. 3:301–341.

    PubMed  CAS  Google Scholar 

  • Wysocki, C. J., and Preti, G. 2004. Facts, fallacies, fears, and frustrations with human pheromones. Anat. Rec. 281A:1201–1211.

    CAS  Google Scholar 

  • Wysocki, C. J., and Preti, G. 2008. Pheromones: mammalian pheromones, in Encyclopedia of Neuroscience.

  • Wysocki, C. J., Wellington, J. L., and Beauchamp, G. K. 1980. Access of urinary nonvolatiles to the mammalian vomeronasal organ. Science 207:781–783.

    PubMed  CAS  Google Scholar 

  • Wysocki, C. J., Yamazaki, K., Curran, M., Wysocki, L. M., and Beauchamp, G. K. 2004. Mice (Mus musculus) lacking a vomeronasal organ can discriminate MHC-determined odortypes. Horm. Behav. 46:241–246.

    PubMed  CAS  Google Scholar 

  • Xu, F., Greer, C. A., and Shepherd, G. M. 2000. Odor maps in the olfactory bulb. J. Comp. Neurol. 422:489–495.

    PubMed  CAS  Google Scholar 

  • Xu, F. Q., Schaefer, M., Kida, I., Schafer, J., Liu, N., Rothman, D. L., Hyder, F., Restrepo, D., and Shepherd, G. M. 2005. Simultaneous activation of mouse main and accessory olfactory bulbs by odors or pheromones. J. Comp. Neurol. 489:491–500.

    PubMed  Google Scholar 

  • Yadon, C. A., and Wilson, D. A. 2005. The role of metabotropic glutamate receptors and cortical adaptation in habituation of odor-guided behavior. Learn. Mem. 12:601–605.

    PubMed  Google Scholar 

  • Yamazaki, K., Boyse, E. A., Bard, J., Curran, M., Kim, D., Ross, S. R., and Beauchamp, G. K. 2002. Presence of mouse mammary tumor virus specifically alters the body odor of mice. Proc. Natl. Acad. Sci. USA 99:5612–5615.

    PubMed  CAS  Google Scholar 

  • Young, J. M., and Trask, B. J. 2002. The sense of smell: genomics of vertebrate odorant receptors. Hum. Mol. Genet. 11:1153–1160.

    PubMed  CAS  Google Scholar 

  • Young, J. M., Friedman, C., Williams, E. M., Ross, J. A., Tonnes-priddy, L., and Trask, B. J. 2002. Different evolutionary processes shaped the mouse and human olfactory receptor gene families. Hum. Mol. Genet. 11:535–546.

    PubMed  CAS  Google Scholar 

  • Young, K. M., Fogarty, M., Kessaris, N., and Richardson, W. D. 2007. Subventricular zone stem cells are heterogeneous with respect to their embryonic origins and neurogenic fates in the adult olfactory bulb. J. Neurosci. 27:8286–8296.

    PubMed  CAS  Google Scholar 

  • Youngentob, S. L., Johnson, B. A., Leon, M., Sheehe, P. R., and Kent, P. F. 2006. Predicting odorant quality perceptions from multidimensional scaling of olfactory bulb glomerular activity patterns. Behav. Neurosci. 120:1337–1345.

    PubMed  Google Scholar 

  • Zelano, C., and Sobel, N. 2005. Humans as an animal model for systems-level organization of olfaction. Neuron 48:431–454.

    PubMed  CAS  Google Scholar 

  • Zhang, X., and Firestein, S. 2002. The olfactory gene superfamily in the mouse. Nature Neurosci. 5:124–133.

    PubMed  CAS  Google Scholar 

  • Zhang, J. X., Soini, H. A., Bruce, K. E., Wiesler, D., Woodley, S. K., Baum, M. J., and Novotny, M. V. 2005. Putative chemosignals of the ferret (Mustela furo) associated with individual and gender recognition. Chem. Senses 30:727–737.

    PubMed  CAS  Google Scholar 

  • Zhao, K., and Dalton, P. 2007. The way the wind blows: implications of modeling nasal airflow. Curr. Allergy Asthma Rep. 7:117–125.

    PubMed  Google Scholar 

  • Zhao, K., Dalton, P., Yang, G. C., and Scherer, P. W. 2006. Numerical modeling of turbulent and laminar airflow and odorant transport during sniffing in the human and rat nose. Chem. Senses 31:107–118.

    PubMed  Google Scholar 

  • Zou, Z., and Buck, L. B. 2006. Combinatorial effects of odorant mixes in olfactory cortex. Science 311:1477–1481.

    PubMed  CAS  Google Scholar 

  • Zou, Z., Li, F., and Buck, L. B. 2005. Odor maps in the olfactory cortex. Proc. Natl Acad. Sci. USA 102:7724–7729.

    PubMed  CAS  Google Scholar 

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Acknowledgments

I thank Gary Beauchamp and Charles Wysocki for insightful comments on the manuscript. I thank Lex Kravitz for drawing my attention to the work on Toxoplasma infection and altered odor processing. Work from the author’s laboratory was supported by funds from the Whitehall Foundation.

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Correspondence to A. Gelperin.

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Dedicated to Tom Eisner, for his inspiring example of how to do science well and joyfully.

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Gelperin, A. Neural Computations with Mammalian Infochemicals. J Chem Ecol 34, 928–942 (2008). https://doi.org/10.1007/s10886-008-9483-6

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