Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Subscribe

Logo for

Science 299 (5610): 1196-1201

Copyright © 2003 by the American Association for the Advancement of Science

Encoding Pheromonal Signals in the Accessory Olfactory Bulb of Behaving Mice

Minmin Luo,1* Michale S. Fee,2 Lawrence C. Katz1

Many mammalian species rely on pheromones--semiochemicals produced by other members of the same species--to communicate social status and reproductive readiness. To assess how the central nervous system integrates the complex repertoire of pheromones, we recorded from single neurons in the accessory olfactory bulb, a nucleus that processes pheromonal signals, of male mice engaged in natural behaviors. Neuronal firing was robustly modulated by physical contact with male and female conspecifics, with individual neurons activated selectively by specific combinations of the sex and strain of conspecifics. We infer that mammals encode social and reproductive information by integrating vomeronasal sensory activity specific to sex and genetic makeup.

1 Howard Hughes Medical Institute and Department of Neurobiology, Duke University Medical Center, Durham, NC 27710, USA.
2 Biological Computation Research Department, Bell Laboratories, Lucent Technologies, Murray Hill, NJ 07974, USA.
*   To whom correspondence should be addressed. E-mail: luo{at}neuro.duke.edu



THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Reliable Sex and Strain Discrimination in the Mouse Vomeronasal Organ and Accessory Olfactory Bulb.
I. I. Tolokh, X. Fu, and T. E. Holy (2013)
J. Neurosci. 33, 13903-13913
   Abstract »    Full Text »    PDF »
Contrasted Evolution of the Vomeronasal Receptor Repertoires in Mammals and Squamate Reptiles.
U. Brykczynska, A. C. Tzika, I. Rodriguez, and M. C. Milinkovitch (2013)
Genome Biol Evol 5, 389-401
   Abstract »    Full Text »    PDF »
Activity Regulates Functional Connectivity from the Vomeronasal Organ to the Accessory Olfactory Bulb.
K. R. Hovis, R. Ramnath, J. E. Dahlen, A. L. Romanova, G. LaRocca, M. E. Bier, and N. N. Urban (2012)
J. Neurosci. 32, 7907-7916
   Abstract »    Full Text »    PDF »
Calcium-Activated Sustained Firing Responses Distinguish Accessory from Main Olfactory Bulb Mitral Cells.
G. Shpak, A. Zylbertal, Y. Yarom, and S. Wagner (2012)
J. Neurosci. 32, 6251-6262
   Abstract »    Full Text »    PDF »
Organization of Vomeronasal Sensory Coding Revealed by Fast Volumetric Calcium Imaging.
D. Turaga and T. E. Holy (2012)
J. Neurosci. 32, 1612-1621
   Abstract »    Full Text »    PDF »
Human Tears Contain a Chemosignal.
S. Gelstein, Y. Yeshurun, L. Rozenkrantz, S. Shushan, I. Frumin, Y. Roth, and N. Sobel (2011)
Science 331, 226-230
   Abstract »    Full Text »    PDF »
In vivo vomeronasal stimulation reveals sensory encoding of conspecific and allospecific cues by the mouse accessory olfactory bulb.
Y. Ben-Shaul, L. C. Katz, R. Mooney, and C. Dulac (2010)
PNAS 107, 5172-5177
   Abstract »    Full Text »    PDF »
Neural correlates of behavior in the moth Manduca sexta in response to complex odors.
J. A. Riffell, H. Lei, and J. G. Hildebrand (2009)
PNAS 106, 19219-19226
   Abstract »    Full Text »    PDF »
From Pheromones to Behavior.
R. Tirindelli, M. Dibattista, S. Pifferi, and A. Menini (2009)
Physiol Rev 89, 921-956
   Abstract »    Full Text »    PDF »
Subthreshold Glutamate Release from Mitral Cell Dendrites.
J. B. Castro and N. N. Urban (2009)
J. Neurosci. 29, 7023-7030
   Abstract »    Full Text »    PDF »
Female behaviour plays a critical role in controlling murine pregnancy block.
S. D Becker and J. L Hurst (2009)
Proc R Soc B 276, 1723-1729
   Abstract »    Full Text »    PDF »
Modulation in Reproductive Tissue Redox Profile in Sexually Receptive Female Rats after Short-Term Exposure to Male Chemical Cues.
G. A. Behr, L. L. da Motta, M. R. de Oliveira, M. W. S. Oliveira, D. P. Gelain, and J. C. F. Moreira (2009)
Chem Senses 34, 317-323
   Abstract »    Full Text »    PDF »
Inhibition Shapes Sex Selectivity in the Mouse Accessory Olfactory Bulb.
R. C. Hendrickson, S. Krauthamer, J. M. Essenberg, and T. E. Holy (2008)
J. Neurosci. 28, 12523-12534
   Abstract »    Full Text »    PDF »
Large-Scale Chronically Implantable Precision Motorized Microdrive Array for Freely Behaving Animals.
J. Yamamoto and M. A. Wilson (2008)
J Neurophysiol 100, 2430-2440
   Abstract »    Full Text »    PDF »
Encoding choosiness: female attraction requires prior physical contact with individual male scents in mice.
S. A Ramm, S. A Cheetham, and J. L Hurst (2008)
Proc R Soc B 275, 1727-1735
   Abstract »    Full Text »    PDF »
Sulfated Steroids as Natural Ligands of Mouse Pheromone-Sensing Neurons.
F. Nodari, F.-F. Hsu, X. Fu, T. F. Holekamp, L.-F. Kao, J. Turk, and T. E. Holy (2008)
J. Neurosci. 28, 6407-6418
   Abstract »    Full Text »    PDF »
The human vomeronasal type-1 receptor family-- detection of volatiles and cAMP signaling in HeLa/Olf cells.
E. Shirokova, J. D. Raguse, W. Meyerhof, and D. Krautwurst (2008)
FASEB J 22, 1416-1425
   Abstract »    Full Text »    PDF »
Patch-Clamp Analysis of Gene-Targeted Vomeronasal Neurons Expressing a Defined V1r or V2r Receptor: Ionic Mechanisms Underlying Persistent Firing.
K. Ukhanov, T. Leinders-Zufall, and F. Zufall (2007)
J Neurophysiol 98, 2357-2369
   Abstract »    Full Text »    PDF »
Sex Selectivity of Mouse Ultrasonic Songs.
Z. Guo and T. E. Holy (2007)
Chem Senses 32, 463-473
   Abstract »    Full Text »    PDF »
Recurrent Dendrodendritic Inhibition of Accessory Olfactory Bulb Mitral Cells Requires Activation of Group I Metabotropic Glutamate Receptors.
J. B. Castro, K. R. Hovis, and N. N. Urban (2007)
J. Neurosci. 27, 5664-5671
   Abstract »    Full Text »    PDF »
Firing Properties of Accessory Olfactory Bulb Mitral/Tufted Cells in Response to Urine Delivered to the Vomeronasal Organ of Gray Short-Tailed Opossums.
J.-J. Zhang, G.-Z. Huang, and M. Halpern (2007)
Chem Senses 32, 355-360
   Abstract »    Full Text »    PDF »
Sparse and Selective Odor Coding by Mitral/Tufted Neurons in the Main Olfactory Bulb.
I. G. Davison and L. C. Katz (2007)
J. Neurosci. 27, 2091-2101
   Abstract »    Full Text »    PDF »
Intraspecific Communication Through Chemical Signals in Female Mice: Reinforcing Properties of Involatile Male Sexual Pheromones.
J. Martinez-Ricos, C. Agustin-Pavon, E. Lanuza, and F. Martinez-Garcia (2007)
Chem Senses 32, 139-148
   Abstract »    Full Text »    PDF »
Mammalian social odours: attraction and individual recognition.
P. A Brennan and K. M Kendrick (2006)
Phil Trans R Soc B 361, 2061-2078
   Abstract »    Full Text »    PDF »
Temporary basolateral amygdala lesions disrupt acquisition of socially transmitted food preferences in rats.
Y. Wang, A. Fontanini, and D. B. Katz (2006)
Learn. Mem. 13, 794-800
   Abstract »    Full Text »    PDF »
Destruction of the Main Olfactory Epithelium Reduces Female Sexual Behavior and Olfactory Investigation in Female Mice.
M. Keller, Q. Douhard, M. J. Baum, and J. Bakker (2006)
Chem Senses 31, 315-323
   Abstract »    Full Text »    PDF »
Sexually Dimorphic Synaptic Organization of the Medial Amygdala.
B. M. Cooke and C. S. Woolley (2005)
J. Neurosci. 25, 10759-10767
   Abstract »    Full Text »    PDF »
Heterogeneity of Voltage- and Chemosignal-Activated Response Profiles in Vomeronasal Sensory Neurons.
A. Labra, J. H. Brann, and D. A. Fadool (2005)
J Neurophysiol 94, 2535-2548
   Abstract »    Full Text »    PDF »
Alarm Pheromone that Aggravates Stress-induced Hyperthermia is Soluble in Water.
Y. Kiyokawa, T. Kikusui, Y. Takeuchi, and Y. Mori (2005)
Chem Senses 30, 513-519
   Abstract »    Full Text »    PDF »
Tuft Calcium Spikes in Accessory Olfactory Bulb Mitral Cells.
N. N. Urban and J. B. Castro (2005)
J. Neurosci. 25, 5024-5028
   Abstract »    Full Text »    PDF »
MHC odours are not required or sufficient for recognition of individual scent owners.
J. L Hurst, M. D Thom, C. M Nevison, R. E Humphries, and R. J Beynon (2005)
Proc R Soc B 272, 715-724
   Abstract »    Full Text »    PDF »
Information Processing in the Mammalian Olfactory System.
P.-M. Lledo, G. Gheusi, and J.-D. Vincent (2005)
Physiol Rev 85, 281-317
   Abstract »    Full Text »    PDF »
Induction of c-Fos Expression in Mouse Vomeronasal Neurons by Sex-specific Non-volatile Pheromone(s).
H. Kimoto and K. Touhara (2005)
Chem Senses 30, i146-i147
   Full Text »    PDF »
Vomeronasal Mechanisms of Mate Recognition in Mice.
P. A. Brennan and E. K. Binns (2005)
Chem Senses 30, i148-i149
   Full Text »    PDF »
MHC Class I Peptides as Chemosensory Signals in the Vomeronasal Organ.
T. Leinders-Zufall, P. Brennan, P. Widmayer, P. C. S., A. Maul-Pavicic, M. Jager, X.-H. Li, H. Breer, F. Zufall, and T. Boehm (2004)
Science 306, 1033-1037
   Abstract »    Full Text »    PDF »
Action Potential Backpropagation and Multiglomerular Signaling in the Rat Vomeronasal System.
J. Ma and G. Lowe (2004)
J. Neurosci. 24, 9341-9352
   Abstract »    Full Text »    PDF »
Olfactory Sex Discrimination Persists, Whereas the Preference for Urinary Odorants from Estrous Females Disappears in Male Mice after Vomeronasal Organ Removal.
D. E. Pankevich, M. J. Baum, and J. A. Cherry (2004)
J. Neurosci. 24, 9451-9457
   Abstract »    Full Text »    PDF »
Effects of Vomeronasal Organ Removal on Olfactory Sex Discrimination and Odor Preferences of Female Ferrets.
S.K. Woodley, A.L. Cloe, P. Waters, and M.J. Baum (2004)
Chem Senses 29, 659-669
   Abstract »    Full Text »    PDF »
Distinctive Responses in the Medial Amygdala to Same-Species and Different-Species Pheromones.
M. Meredith and J. M. Westberry (2004)
J. Neurosci. 24, 5719-5725
   Abstract »    Full Text »    PDF »
Genetic Evidence for the Coexistence of Pheromone Perception and Full Trichromatic Vision in Howler Monkeys.
D. M. Webb, L. Cortes-Ortiz, and J. Zhang (2004)
Mol. Biol. Evol. 21, 697-704
   Abstract »    Full Text »    PDF »
Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates.
J. Zhang and D. M. Webb (2003)
PNAS 100, 8337-8341
   Abstract »    Full Text »    PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882