Distinct signals conveyed by pheromone concentrations to the mouse vomeronasal organ

Journal of Neuroscience

Volumn 30, Issue 22, 2010, Pages 7473-7483

  He, Jie ^a   Ma, Limei ^a   Kim, Sangseong ^a   Schwartz, Joel ^a,c   Santilli, Michael ^a   Wood, Christopher ^a   Durnin, Michael H ^a   Yu, C Ron ^a,b  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHEROMONE;

ANIMAL EXPERIMENT; ARTICLE; CELL POPULATION; FEMALE; KIDNEY CONCENTRATING CAPACITY; MALE; MOUSE; MOUSE STRAIN; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; SEX DETERMINATION; URINALYSIS; URINE; UROGENITAL SYSTEM; VOMERONASAL ORGAN;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALMODULIN; CUES; DOSE-RESPONSE RELATIONSHIP, DRUG; EVOKED POTENTIALS; FEMALE; GREEN FLUORESCENT PROTEINS; LECTINS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; PATCH-CLAMP TECHNIQUES; PHEROMONES; RECOMBINANT FUSION PROTEINS; VOMERONASAL ORGAN;

EID: 77953220599     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0825-10.2010     Document Type: Article

References (77)

1. Beauchamp GK, Martin IG, Wysocki CJ, Wellington JL (1982) Chemoinvestigatory and sexual behavior of male guinea pigs following vomeronasal organ removal. Physiol Behav 29:329-336.
2. Belluscio L, Koentges G, Axel R, Dulac C (1999) A map of pheromone receptor activation in the mammalian brain. Cell 97:209-220. (Pubitemid 29194272)
3. Beynon RJ, Hurst JL (2003) Multiple roles of major urinary proteins in the house mouse, Mus domesticus. Biochem Soc Trans 31:142-146.
4. Birch MC (1974) Pheromones. New York: American Elsevier.
5. Blake R, Logothetis NK (2002) Visual competition. Nat Rev Neurosci 3:13-21.
6. Brennan PA, Kendrick KM (2006) Mammalian social odours: attraction and individual recognition. Philos Trans R Soc Lond B Biol Sci 361:2061-2078.
7. Bronson FH (1971) Rodent pheromones. Biol Reprod 4:344-357.
8. Bronson FH (1979) The reproductive ecology of the house mouse. Q Rev Biol 54:265-299.
9. Buck LB (2000) The molecular architecture of odor and pheromone sensing in mammals. Cell 100:611-618.
10. Clancy AN, Singer AG, Macrides F, Bronson FH, Agosta WC (1988) Experiential and endocrine dependence of gonadotropin responses in male mice to conspecific urine. Biol Reprod 38:183-191. (Pubitemid 18070301)
11. Del Punta K, Puche A, Adams NC, Rodriguez I, Mombaerts P (2002) A divergent pattern of sensory axonal projections is rendered convergent by second-order neurons in the accessory olfactory bulb. Neuron 35: 1057-1066. (Pubitemid 35279534)
12. Drickamer LC (1982) Delay and acceleration of puberty in female mice by urinary chemosignals from other females. Dev Psychobiol 15:433-445. (Pubitemid 12017975)
13. Drickamer LC (1986) Acceleration and delay of puberty in female mice via urinary chemosignals: age of the urine stimulus. Dev Psychobiol 19:155-161.
14. Drickamer LC, Assmann SM (1981) Acceleration and delay of puberty in female housemice: methods of delivery of the urinary stimulus. Dev Psychobiol 14:487-497.
15. Duchamp-Viret P, Duchamp A, Chaput MA (2003) Single olfactory sensory neurons simultaneously integrate the components of an odour mixture. Eur J Neurosci 18:2690-2696. (Pubitemid 37542121)
16. Dulac C, Axel R (1995) A novel family of genes encoding putative pheromone receptors in mammals. Cell 83:195-206.
17. He J, Ma L, Kim S, Nakai J, Yu CR (2008) Encoding gender and individual information in the mouse vomeronasal organ. Science 320:535-538. (Pubitemid 351590667)
18. Hendrickson RC, Krauthamer S, Essenberg JM, Holy TE (2008) Inhibition shapes sex selectivity in the mouse accessory olfactory bulb. J Neurosci 28:12523-12534.
19. Herrada G, Dulac C (1997) A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90:763-773. (Pubitemid 27357967)
20. Holy TE, Dulac C, Meister M (2000) Responses of vomeronasal neurons to natural stimuli. Science 289:1569-1572.
21. Humphries RE, Robertson DH, Beynon RJ, Hurst JL (1999) Unravelling the chemical basis of competitive scent marking in house mice. Anim Behav 58:1177-1190.
22. Hurst JL, Beynon RJ (2004) Scent wars: the chemobiology of competitive signalling in mice. Bioessays 26:1288-1298.
23. Jemiolo B, Harvey S, Novotny M (1986) Promotion of the Whitten effect in female mice by synthetic analogs of male urinary constituents. Proc Natl Acad Sci U S A 83:4576-4579. (Pubitemid 16057093)
24. Jemiolo B, Andreolini F, Xie TM, Wiesler D, Novotny M (1989) Puberty-affecting synthetic analogs of urinary chemosignals in the house mouse, Mus domesticus. Physiol Behav 46:293-298. (Pubitemid 19244093)
25. Johnston RE (1998) Pheromones, the vomeronasal system, and communication. From hormonal responses to individual recognition. Ann N Y Acad Sci 855:333-348.
26. Kaba H, Rosser A, Keverne B (1989) Neural basis of olfactory memory in the context of pregnancy block. Neuroscience 32:657-662. (Pubitemid 20008294)
27. Keverne EB (1998) Vomeronasal/accessory olfactory system and pheromonal recognition. Chem Senses 23:491-494.
28. Keverne EB (2002) Pheromones, vomeronasal function, and gender-specific behavior. Cell 108:735-738.
29. Kimoto H, Haga S, Sato K, Touhara K (2005) Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 437:898-901.
30. Kurahashi T, Lowe G, Gold GH (1994) Suppression of odorant responses by odorants in olfactory receptor cells. Science 265:118-120.
31. Leinders-Zufall T, Lane AP, Puche AC, Ma W, Novotny MV, Shipley MT, Zufall F (2000) Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405:792-796.
32. Leinders-Zufall T, Brennan P, Widmayer P, S PC, Maul-Pavicic A, Jäger M, Li XH, Breer H, Zufall F, Boehm T (2004) MHCclass I peptides as chemosensory signals in the vomeronasal organ. Science 306:1033-1037.
33. Leinders-Zufall T, Ishii T, Mombaerts P, Zufall F, Boehm T (2009) Structural requirements for the activation of vomeronasal sensory neurons by MHC peptides. Nat Neurosci 12:1551-1558.
34. Leypold BG, Yu CR, Leinders-Zufall T, Kim MM, Zufall F, Axel R (2002) Altered sexual and social behaviors in trp2 mutant mice. Proc Natl Acad Sci U S A 99:6376-6381.
35. Liman ER, Corey DP (1996) Electrophysiological characterization of chemosensory neurons from the mouse vomeronasal organ. J Neurosci 16:4625-4637.
36. Loconto J, Papes F, Chang E, Stowers L, Jones EP, Takada T, Kumánovics A, Fischer Lindahl K, Dulac C (2003) Functional expression of murine V2R pheromone receptors involves selective association with the M10 and M1 families of MHC class Ib molecules. Cell 112:607-618.
37. Logothetis NK (1998) Single units and conscious vision. Philos Trans R Soc Lond B Biol Sci 353:1801-1818.
38. Macknik SL (2006) Visual masking approaches to visual awareness. Prog Brain Res 155:177-215.
39. Macknik SL, Livingstone MS (1998) Neuronal correlates of visibility and invisibility in the primate visual system. Nat Neurosci 1:144-149.
40. Macknik SL, King M, Randi J, Robbins A, Teller, Thompson J, Martinez-Conde S (2008) Attention and awareness in stage magic: turning tricks into research. Nat Rev Neurosci 9:871-879.
41. Matsunami H, Buck LB (1997) A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90:775-784.
42. Meister M, Bonhoeffer T (2001) Tuning and topography in an odor map on the rat olfactory bulb. J Neurosci 21:1351-1360.
43. Meredith M, O'Connell RJ (1979) Efferent control of stimulus access to the hamster vomeronasal organ. J Physiol 286:301-316.
44. Meredith M, Marques DM, O'Connell RO, Stern FL (1980) Vomeronasal pump: significance for male hamster sexual behavior. Science 207: 1224-1226.
45. Mori K, Nagao H, Yoshihara Y (1999) The olfactory bulb: coding and processing of odor molecule information. Science 286:711-715.
46. Nevison CM, Armstrong S, Beynon RJ, Humphries RE, Hurst JL (2003) The ownership signature in mouse scent marks is involatile. Proc Biol Sci 270:1957-1963.
47. Nodari F, Hsu FF, Fu X, Holekamp TF, Kao LF, Turk J, Holy TE (2008) Sulfated steroids as natural ligands of mouse pheromone-sensing neurons. J Neurosci 28:6407-6418.
48. Novotny M, Schwende FJ, Wiesler D, Jorgenson JW, Carmack M (1984) 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. Experientia 40:217-219.
49. Novotny M, Harvey S, Jemiolo B, Alberts J (1985) Synthetic pheromones that promote inter-male aggression in mice. Proc Natl Acad Sci U S A 82:2059-2061. (Pubitemid 15060839)
50. Novotny M, Harvey S, Jemiolo B (1990) Chemistry of male dominance in the house mouse, Mus domesticus. Experientia 46:109-113.
51. Novotny MV, Ma W, Wiesler D, Zídek L (1999) Positive identification of the puberty-accelerating pheromone of the house mouse: the volatile ligands associating with the major urinary protein. Proc Biol Sci 266:2017-2022.
52. Novotny MV, Soini HA, Koyama S, Wiesler D, Bruce KE, Penn DJ (2007) Chemical identification of MHC-influenced volatile compounds in mouse urine. I. Quantitative proportions of major chemosignals. J Chem Ecol 33:417-434. (Pubitemid 46144086)
53. Pankevich D, Baum MJ, Cherry JA (2003) Removal of the superior cervical ganglia fails to block Fos induction in the accessory olfactory system of male mice after exposure to female odors. Neurosci Lett 345:13-16. (Pubitemid 36694838)
54. Pantages E, Dulac C (2000) A novel family of candidate pheromone receptors in mammals. Neuron 28:835-845. (Pubitemid 32038075)
55. Popper AN, Fay RR (1992) The mammalian auditory pathway: neurophysiology. New York: Springer.
56. Price MA, Vandenbergh JG (1992) Analysis of puberty-accelerating pheromones. J Exp Zool 264:42-45.
57. Ralls K (1971) Mammalian scent marking. Science 171:443-449.
58. Rich TJ, Hurst JL (1998) Scent marks as reliable signals of the competitive ability of mates. Anim Behav 56:727-735.
59. Rich TJ, Hurst JL (1999) The competing countermarks hypothesis: reliable assessment of competitive ability by potential mates. Anim Behav 58:1027-1037.
60. Rodriguez I, Feinstein P, Mombaerts P (1999) Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell 97:199-208. (Pubitemid 29194271)
61. Rospars JP, Lansky P, Chaput M, Duchamp-Viret P (2008) Competitive and noncompetitive odorant interactions in the early neural coding of odorant mixtures. J Neurosci 28:2659-2666. (Pubitemid 351348207)
62. Rubin BD, Katz LC (1999) Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron 23:499-511.
63. Ryba NJ, Tirindelli R (1997) Anew multigene family of putative pheromone receptors. Neuron 19:371-379.
64. Spehr M, Kelliher KR, Li XH, Boehm T, Leinders-Zufall T, Zufall F (2006) Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. J Neurosci 26:1961-1970. (Pubitemid 43295848)
65. Tan J, Savigner A, Ma M, Luo M (2010) Odor information processing by the olfactory bulb analyzed in gene-targeted mice. Neuron 65:912-926.
66. Tong F, Meng M, Blake R (2006) Neural bases of binocular rivalry. Trends Cogn Sci 10:502-511.
67. Tse PU, Martinez-Conde S, Schlegel AA, Macknik SL (2005) Visibility, visual awareness, and visual masking of simple unattended targets are confined to areas in the occipital cortex beyond human V1/V2. Proc Natl Acad Sci U S A 102:17178-17183.
68. Ukhanov K, Leinders-Zufall T, Zufall F (2007) Patch-clamp analysis of gene-targeted vomeronasal neurons expressing a defined V1r or V2r receptor: ionic mechanisms underlying persistent firing. J Neurophysiol 98:2357-2369.
69. Wagner S, Gresser AL, Torello AT, Dulac C (2006) A multireceptor genetic approach uncovers an ordered integration of VNO sensory inputs in the accessory olfactory bulb. Neuron 50:697-709.
70. Wyatt TD (2003) Pheromones and animal behaviour: communication by smell and taste. Cambridge, UK: Cambridge UP.
71. Wysocki CJ, Lepri JJ (1991) Consequences of removing the vomeronasal organ. J Steroid Biochem Mol Biol 39:661-669.
72. Wysocki CJ, Wellington JL, Beauchamp GK (1980) Access of urinary nonvolatiles to the mammalian vomeronasal organ. Science 207:781-783.
73. Yang H, Shi P, Zhang YP, Zhang J (2005) Composition and evolution of the V2r vomeronasal receptor gene repertoire in mice and rats. Genomics 86:306-315.
74. Yost WA, Popper AN, Fay RR (2008) Auditory perception of sound sources. New York: Springer.
75. Yu CR, Power J, Barnea G, O'Donnell S, Brown HE, Osborne J, Axel R, Gogos JA (2004) Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42:553-566.
76. Zeman A (2004) Theories of visual awareness. Prog Brain Res 144:321-329.
77. Zhang X, Rodriguez I, Mombaerts P, Firestein S (2004) Odorant and vomeronasal receptor genes in two mouse genome assemblies. Genomics 83: 802-811.