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 289 (5484): 1569-1572

Copyright © 2000 by the American Association for the Advancement of Science

Responses of Vomeronasal Neurons to Natural Stimuli

Timothy E. Holy,1* Catherine Dulac,12 Markus Meister1

The vomeronasal organ (VNO) of mammals plays an essential role in the detection of pheromones. We obtained simultaneous recordings of action potentials from large subsets of VNO neurons. These cells responded to components of urine by increasing their firing rate. This chemosensory activation required phospholipase C function. Unlike most other sensory neurons, VNO neurons did not adapt under prolonged stimulus exposure. The full time course of the VNO spiking response is captured by a simple quantitative model of ligand binding. Many individual VNO neurons were strongly selective for either male or female mouse urine, with the effective concentrations differing as much as a thousandfold. These results establish a framework for understanding sensory coding in the vomeronasal system.

1 Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA.
2 Howard Hughes Medical Institute, Cambridge, MA 02138, USA.
*   To whom correspondence should be addressed. E-mail: timholy{at}mcb.harvard.edu


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Intermittency Coding in the Primary Olfactory System: A Neural Substrate for Olfactory Scene Analysis.
I. M. Park, Y. V. Bobkov, B. W. Ache, and J. C. Principe (2014)
J. Neurosci. 34, 941-952
   Abstract »    Full Text »    PDF »
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 »
Aggressive behaviour and physiological responses to pheromones are strongly impaired in mice deficient for the olfactory G-protein -subunit G8.
G. Montani, S. Tonelli, V. Sanghez, P. F. Ferrari, P. Palanza, A. Zimmer, and R. Tirindelli (2013)
J. Physiol. 591, 3949-3962
   Abstract »    Full Text »    PDF »
Robust Encoding of Stimulus Identity and Concentration in the Accessory Olfactory System.
H. A. Arnson and T. E. Holy (2013)
J. Neurosci. 33, 13388-13397
   Abstract »    Full Text »    PDF »
Responses to Sulfated Steroids of Female Mouse Vomeronasal Sensory Neurons.
F. Celsi, A. D'Errico, and A. Menini (2012)
Chem Senses 37, 849-858
   Abstract »    Full Text »    PDF »
Mapping a Complete Neural Population in the Retina.
O. Marre, D. Amodei, N. Deshmukh, K. Sadeghi, F. Soo, T. E. Holy, and M. J. Berry II (2012)
J. Neurosci. 32, 14859-14873
   Abstract »    Full Text »    PDF »
Calcium-activated chloride channels in the apical region of mouse vomeronasal sensory neurons.
M. Dibattista, A. Amjad, D. K. Maurya, C. Sagheddu, G. Montani, R. Tirindelli, and A. Menini (2012)
J. Gen. Physiol. 140, 3-15
   Abstract »    Full Text »    PDF »
Effect of Circadian Clock Gene Mutations on Nonvisual Photoreception in the Mouse.
L. Owens, E. Buhr, D. C. Tu, T. L. Lamprecht, J. Lee, and R. N. Van Gelder (2012)
Invest. Ophthalmol. Vis. Sci. 53, 454-460
   Abstract »    Full Text »    PDF »
G protein G{alpha}o is essential for vomeronasal function and aggressive behavior in mice.
P. Chamero, V. Katsoulidou, P. Hendrix, B. Bufe, R. Roberts, H. Matsunami, J. Abramowitz, L. Birnbaumer, F. Zufall, and T. Leinders-Zufall (2011)
PNAS 108, 12898-12903
   Abstract »    Full Text »    PDF »
Chemosensory burst coding by mouse vomeronasal sensory neurons.
H. A. Arnson and T. E. Holy (2011)
J Neurophysiol 106, 409-420
   Abstract »    Full Text »    PDF »
Distinct Signals Conveyed by Pheromone Concentrations to the Mouse Vomeronasal Organ.
J. He, L. Ma, S. Kim, J. Schwartz, M. Santilli, C. Wood, M. H. Durnin, and C. R. Yu (2010)
J. Neurosci. 30, 7473-7483
   Abstract »    Full Text »    PDF »
Odors activate dual pathways, a TRPC2 and a AA-dependent pathway, in mouse vomeronasal neurons.
P. Zhang, C. Yang, and R. J. Delay (2010)
Am J Physiol Cell Physiol 298, C1253-C1264
   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 »
From Pheromones to Behavior.
R. Tirindelli, M. Dibattista, S. Pifferi, and A. Menini (2009)
Physiol Rev 89, 921-956
   Abstract »    Full Text »    PDF »
Ca2+-Calmodulin Feedback Mediates Sensory Adaptation and Inhibits Pheromone-Sensitive Ion Channels in the Vomeronasal Organ.
J. Spehr, S. Hagendorf, J. Weiss, M. Spehr, T. Leinders-Zufall, and F. Zufall (2009)
J. Neurosci. 29, 2125-2135
   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 »
Absence of Long-Wavelength Photic Potentiation of Murine Intrinsically Photosensitive Retinal Ganglion Cell Firing In Vitro.
K. Mawad and R. N. Van Gelder (2008)
J Biol Rhythms 23, 387-391
   Abstract »    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 »
Encoding Gender and Individual Information in the Mouse Vomeronasal Organ.
J. He, L. Ma, S. Kim, J. Nakai, and C. R. Yu (2008)
Science 320, 535-538
   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 »
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 »
Melanopsin-Dependent Persistence and Photopotentiation of Murine Pupillary Light Responses.
Y. Zhu, D. C. Tu, D. Denner, T. Shane, C. M. Fitzgerald, and R. N. Van Gelder (2007)
Invest. Ophthalmol. Vis. Sci. 48, 1268-1275
   Abstract »    Full Text »    PDF »
Intrinsically Bursting Olfactory Receptor Neurons.
Y. V. Bobkov and B. W. Ache (2007)
J Neurophysiol 97, 1052-1057
   Abstract »    Full Text »    PDF »
Hypothalamic progesterone receptor-A mediates gonadotropin surges, self priming and receptivity in estrogen-primed female mice.
M. M White, I. Sheffer, J. Teeter, and E. M. Apostolakis (2007)
J. Mol. Endocrinol. 38, 35-50
   Abstract »    Full Text »    PDF »
Attenuation of the Production of Inositol 1,4,5-Trisphosphate in the Mouse Vomeronasal Organ by Antibodies Against the {alpha}q/11 Subfamily of G-Proteins.
R. N. Thompson, A. Napier, and K. S. Wekesa (2006)
Chem Senses 31, 613-619
   Abstract »    Full Text »    PDF »
Inner retinal photoreception independent of the visual retinoid cycle.
D. C. Tu, L. A. Owens, L. Anderson, M. Golczak, S. E. Doyle, M. McCall, M. Menaker, K. Palczewski, and R. N. Van Gelder (2006)
PNAS 103, 10426-10431
   Abstract »    Full Text »    PDF »
Female Snake Sex Pheromone Induces Membrane Responses in Vomeronasal Sensory Neurons of Male Snakes.
G.-Z. Huang, J.-J. Zhang, D. Wang, R. T. Mason, and M. Halpern (2006)
Chem Senses 31, 521-529
   Abstract »    Full Text »    PDF »
Electrophysiological Properties and Modeling of Murine Vomeronasal Sensory Neurons in Acute Slice Preparations.
R. Shimazaki, A. Boccaccio, A. Mazzatenta, G. Pinato, M. Migliore, and A. Menini (2006)
Chem Senses 31, 425-435
   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 »
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 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 »
Sex-specific Responses to Urinary Chemicals by the Mouse Vomeronasal Organ.
R. N. Thompson, B.K. Robertson, A. Napier, and K. S. Wekesa (2004)
Chem Senses 29, 749-754
   Abstract »    Full Text »    PDF »
Espins Are Multifunctional Actin Cytoskeletal Regulatory Proteins in the Microvilli of Chemosensory and Mechanosensory Cells.
G. Sekerkova, L. Zheng, P. A. Loomis, B. Changyaleket, D. S. Whitlon, E. Mugnaini, and J. R. Bartles (2004)
J. Neurosci. 24, 5445-5456
   Abstract »    Full Text »    PDF »
Apical and basal neurones isolated from the mouse vomeronasal organ differ for voltage-dependent currents.
F. Fieni, V. Ghiaroni, R. Tirindelli, P. Pietra, and A. Bigiani (2003)
J. Physiol. 552, 425-436
   Abstract »    Full Text »    PDF »
Functional Characterization of Olfactory Binding Proteins for Appeasing Compounds and Molecular Cloning in the Vomeronasal Organ of Pre-pubertal Pigs.
G. Guiraudie, P. Pageat, A.-H. Cain, I. Madec, and P. N.-L. Meillour (2003)
Chem Senses 28, 609-619
   Abstract »    Full Text »    PDF »
cAMP-independent olfactory transduction of amino acids in Xenopus laevis tadpoles.
I. Manzini and D. Schild (2003)
J. Physiol. 551, 115-123
   Abstract »    Full Text »    PDF »
Regulation by voltage and adenine nucleotides of a Ca2+-activated cation channel from hamster vomeronasal sensory neurons.
E. R Liman (2003)
J. Physiol. 548, 777-787
   Abstract »    Full Text »    PDF »
Involvement of Gq/11 in signal transduction in the mammalian vomeronasal organ.
K. S. Wekesa, S. Miller, and A. Napier (2003)
J. Exp. Biol. 206, 827-832
   Abstract »    Full Text »    PDF »
Encoding Pheromonal Signals in the Accessory Olfactory Bulb of Behaving Mice.
M. Luo, M. S. Fee, and L. C. Katz (2003)
Science 299, 1196-1201
   Abstract »    Full Text »    PDF »
Synthetic maternal pheromone stimulates feeding behavior and weight gain in weaned pigs.
J. J. McGlone and D. L. Anderson (2002)
J Anim Sci 80, 3179-3183
   Abstract »    Full Text »    PDF »
Arachidonic Acid Plays a Role in Rat Vomeronasal Signal Transduction.
M. Spehr, H. Hatt, and C. H. Wetzel (2002)
J. Neurosci. 22, 8429-8437
   Abstract »    Full Text »    PDF »
Identification of V1R-like Putative Pheromone Receptor Sequences in Non-human Primates. Characterization of V1R Pseudogenes in Marmoset, a Primate Species that Possesses an Intact Vomeronasal Organ.
D. Giorgi and S. Rouquier (2002)
Chem Senses 27, 529-537
   Abstract »    Full Text »    PDF »
Altered sexual and social behaviors in trp2 mutant mice.
B. G. Leypold, C. R. Yu, T. Leinders-Zufall, M. M. Kim, F. Zufall, and R. Axel (2002)
PNAS 99, 6376-6381
   Abstract »    Full Text »    PDF »
Patch-clamp analysis of voltage-activated and chemically activated currents in the vomeronasal organ of Sternotherus odoratus (stinkpot/musk turtle).
D. A. Fadool, M. Wachowiak, and J. H. Brann (2002)
J. Exp. Biol. 204, 4199-4212
   Abstract »    Full Text »    PDF »
Calcium Transients in the Garter Snake Vomeronasal Organ.
A. R. Cinelli, D. Wang, P. Chen, W. Liu, and M. Halpern (2002)
J Neurophysiol 87, 1449-1472
   Abstract »    Full Text »    PDF »
Loss of Sex Discrimination and Male-Male Aggression in Mice Deficient for TRP2.
L. Stowers, T. E. Holy, M. Meister, C. Dulac, and G. Koentges (2002)
Science 295, 1493-1500
   Abstract »    Full Text »    PDF »
Human Vomeronasal Organ Function: A Critical Review of Best and Worst Cases.
M. Meredith (2001)
Chem Senses 26, 433-445
   Abstract »    Full Text »    PDF »
Sex Difference and Steroid Modulation of Pheromone-Induced Immediate Early Genes in the Two Zones of the Mouse Accessory Olfactory System.
H. A. Halem, M. J. Baum, and J. A. Cherry (2001)
J. Neurosci. 21, 2474-2480
   Abstract »    Full Text »    PDF »
Co-Expression of Putative Pheromone Receptors in the Sensory Neurons of the Vomeronasal Organ.
S. Martini, L. Silvotti, A. Shirazi, N. J. P. Ryba, and R. Tirindelli (2001)
J. Neurosci. 21, 843-848
   Abstract »    Full Text »    PDF »
Sequence Diversity and Genomic Organization of Vomeronasal Receptor Genes in the Mouse.
K. Del Punta, A. Rothman, I. Rodriguez, and P. Mombaerts (2000)
Genome Res. 10, 1958-1967
   Abstract »    Full Text »
Loss of Sex Discrimination and Male-Male Aggression in Mice Deficient for TRP2.
L. Stowers, T. E. Holy, M. Meister, C. Dulac, and G. Koentges (2002)
Science 295, 1493-1500
   Abstract »    Full Text »    PDF »
Altered sexual and social behaviors in trp2 mutant mice.
B. G. Leypold, C. R. Yu, T. Leinders-Zufall, M. M. Kim, F. Zufall, and R. Axel (2002)
PNAS 99, 6376-6381
   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