Encoding social signals in the mouse main olfactory bulb

Mammalian urine releases complex mixtures of volatile compounds that are used in reproduction, territoriality and conspecific recognition. To understand how such complex mixtures are represented in the main olfactory bulb, we analysed the electrophysiological responses of individual mitral cells to volatile compounds in mouse urine. In both males and females, urine volatile compounds evoke robust responses in a small subset of mitral cells. Fractionation of the volatile compounds using gas chromatography showed that out of the hundreds of compounds present, mitral cells are activated by single compounds. One cohort of mitral cells responded exclusively to male urine; these neurons were activated by (methylthio)methanethiol, a potent, previously unknown semiochemical present only in male urine. When added to urine, synthetic (methylthio)methanethiol significantly enhances urine attractiveness to female mice. We conclude that mitral cells represent natural odorant stimuli by acting as selective feature detectors, and that their activation is largely independent of the presence of other components in the olfactory stimulus.

[1]  B. A. Baldwin,et al.  The effects of ablation of the olfactory bulbs on parturition and maternal behaviour in Soay sheep. , 1974, Animal behaviour.

[2]  M. Novotny,et al.  Thet complex of the mouse: Chemical characterization by urinary volatile profiles , 1991, Journal of Chemical Ecology.

[3]  Lawrence C. Katz,et al.  Odorant receptors instruct functional circuitry in the mouse olfactory bulb , 2002, Nature.

[4]  B. Slotnick,et al.  Odors Detected by Mice Deficient in Cyclic Nucleotide-Gated Channel Subunit A2 Stimulate the Main Olfactory System , 2004, The Journal of Neuroscience.

[5]  F. Zufall,et al.  Ultrasensitive pheromone detection by mammalian vomeronasal neurons , 2000, Nature.

[6]  W. Jöchle Dimethyl Disulfide: An attractant pheromone in hamster vaginal secretion , 1976 .

[7]  A. Chess,et al.  The family of genes encoding odorant receptors in the channel catfish , 1993, Cell.

[8]  H. Baek,et al.  Solid Phase Microextraction-Gas Chromatography-Olfactometry of Soy Sauce Based on Sample Dilution Analysis , 2004 .

[9]  J. Bautista,et al.  Identification of pheromones in mouse urine by head-space solid phase microextraction followed by gas chromatography-mass spectrometry. , 2003, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[10]  Carlos D. Brody,et al.  Simple Networks for Spike-Timing-Based Computation, with Application to Olfactory Processing , 2003, Neuron.

[11]  G. Preti,et al.  Carbon disulfide: A semiochemical mediating socially-induced diet choice in rats , 1988, Physiology & Behavior.

[12]  A. B. Robinson,et al.  Identification of compounds in mouse urine vapor by gas chromatography and mass spectrometry , 1980, Mechanisms of Ageing and Development.

[13]  G. Laurent,et al.  Multiplexing using synchrony in the zebrafish olfactory bulb , 2004, Nature Neuroscience.

[14]  Richard Axel,et al.  Coding of olfactory information: Topography of odorant receptor expression in the catfish olfactory epithelium , 1993, Cell.

[15]  G. Beauchamp,et al.  Distinctive urinary odors governed by the major histocompatibility locus of the mouse. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[16]  P. Wallace Individual discrimination of humans by odor , 1977, Physiology & Behavior.

[17]  T. Tanabe,et al.  Discrimination of odors in olfactory bulb, pyriform-amygdaloid areas, and orbitofrontal cortex of the monkey. , 1975, Journal of neurophysiology.

[18]  C. Dulac,et al.  Molecular detection of pheromone signals in mammals: from genes to behaviour , 2003, Nature Reviews Neuroscience.

[19]  J. Pawliszyn,et al.  Dynamics of organic compound extraction from water using liquid-coated fused silica fibers , 1992 .

[20]  Lawrence C Katz,et al.  Functional Topography of Connections Linking Mirror-Symmetric Maps in the Mouse Olfactory Bulb , 2003, Neuron.

[21]  John R. Carlson,et al.  A Novel Family of Divergent Seven-Transmembrane Proteins Candidate Odorant Receptors in Drosophila , 1999, Neuron.

[22]  G. Laurent,et al.  Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. , 2001, Science.

[23]  Gilles Laurent,et al.  Transformation of Olfactory Representations in the Drosophila Antennal Lobe , 2004, Science.

[24]  G. Galletti,et al.  Solid-phase microextraction gas chromatography/mass spectrometric analysis of volatile organic compounds in water , 1999, Rapid communications in mass spectrometry : RCM.

[25]  D. Restrepo,et al.  Olfactory Fingerprints for Major Histocompatibility Complex-Determined Body Odors II: Relationship among Odor Maps, Genetics, Odor Composition, and Behavior , 2002, The Journal of Neuroscience.

[26]  M. Novotny,et al.  Urinary volatile constituents of the house mouse,Mus musculus, and their endocrine dependency , 2005, Journal of Chemical Ecology.

[27]  M. Novotny,et al.  A unique urinary constituent, 6-hydroxy-6-methyl-3-heptanone, is a pheromone that accelerates puberty in female mice. , 1999, Chemistry & biology.

[28]  Fumiaki Motokizawa,et al.  Odor representation and discrimination in mitral/tufted cells of the rat olfactory bulb , 1996, Experimental Brain Research.

[29]  C. Barnard From Genes to Behaviour , 1983 .

[30]  Andrey Rzhetsky,et al.  A Spatial Map of Olfactory Receptor Expression in the Drosophila Antenna , 1999, Cell.

[31]  G. Contarini,et al.  Volatile fraction of milk: comparison between purge and trap and solid phase microextraction techniques. , 2002, Journal of agricultural and food chemistry.

[32]  D. Pfaff,et al.  Behavioral and electrophysiological responses of female mice to male urine odors. , 1970, Physiology & behavior.

[33]  R. Doty,et al.  Communication of gender from human breath odors: Relationship to perceived intensity and pleasantness , 1982, Hormones and Behavior.

[34]  J. G. Briñón,et al.  A sexually dimorphic group of atypical glomeruli in the mouse olfactory bulb. , 2001, Chemical senses.

[35]  Benoist Schaal,et al.  Chemical and behavioural characterization of the rabbit mammary pheromone , 2003, Nature.

[36]  M. Novotny,et al.  Identification of a testosterone-dependent unique volatile constituent of male mouse urine: 7-exo-ethyl-5-methyl-6,8-dioxabicyclo[3.2.1]-3-octene , 1984, Experientia.

[37]  M. Novotny,et al.  Dynamics of excretion of urinary chemosignals in the house mouse (Mus musclus) during the natural estrous cycle , 1987, Experientia.

[38]  篠田 晃 Necklace olfactory glomeruli form unique components of the rat primary olfactory system , 1990 .

[39]  M. Novotny,et al.  Chemistry of male dominance in the house mouse,Mus domesticus , 1990, Experientia.

[40]  Dong-Sun Lee,et al.  Comparative study of extraction techniques for determination of garlic flavor components by gas chromatography–mass spectrometry , 2003, Analytical and bioanalytical chemistry.

[41]  K. Mori,et al.  Relation of chemical structure to specificity of response in olfactory glomeruli , 1995, Current Opinion in Neurobiology.

[42]  A. Wong,et al.  Two-Photon Calcium Imaging Reveals an Odor-Evoked Map of Activity in the Fly Brain , 2003, Cell.

[43]  G. Shepherd,et al.  Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. , 1997, Annual review of neuroscience.

[44]  R. Bazemore,et al.  Aroma-active components in fermented bamboo shoots. , 2002, Journal of agricultural and food chemistry.

[45]  D. Restrepo,et al.  Olfactory Fingerprints for Major Histocompatibility Complex-Determined Body Odors , 2001, The Journal of Neuroscience.

[46]  S. Buxaderas,et al.  Volatile compounds of red and white wines by headspace--solid-phase microextraction using different fibers. , 2004, Journal of chromatographic science.

[47]  M. Novotny,et al.  Pattern of volatile compounds in dominant and subordinate male mouse urine , 1989, Journal of Chemical Ecology.

[48]  A. M. From genes to behaviour , 1974, Nature.

[49]  Gilles Laurent,et al.  Olfactory network dynamics and the coding of multidimensional signals , 2002, Nature Reviews Neuroscience.

[50]  Bill S Hansson,et al.  Novel natural ligands for Drosophila olfactory receptor neurones , 2003, Journal of Experimental Biology.

[51]  L. Wadhams Coupled Gas Chromatography — Single Cell Recording: a New Technique for Use in the Analysis of Insect Pheromones , 1982 .

[52]  Eric B. Keverne,et al.  Something in the Air? New Insights into Mammalian Pheromones , 2004, Current Biology.