Molecular organization of vomeronasal chemoreception
Open accessAbstract
The vomeronasal organ (VNO) has a key role in mediating the social and defensive responses of many terrestrial vertebrates to species- and sex-specific chemosignals. More than 250 putative pheromone receptors have been identified in the mouse VNO, but the nature of the signals detected by individual VNO receptors has not yet been elucidated. To gain insight into the molecular logic of VNO detection leading to mating, aggression or defensive responses, we sought to uncover the response profiles of individual vomeronasal receptors to a wide range of animal cues. Here we describe the repertoire of behaviourally and physiologically relevant stimuli detected by a large number of individual vomeronasal receptors in mice, and define a global map of vomeronasal signal detection. We demonstrate that the two classes (V1R and V2R) of vomeronasal receptors use fundamentally different strategies to encode chemosensory information, and that distinct receptor subfamilies have evolved towards the specific recognition of certain animal groups or chemical structures. The association of large subsets of vomeronasal receptors with cognate, ethologically and physiologically relevant stimuli establishes the molecular foundation of vomeronasal information coding, and opens new avenues for further investigating the neural mechanisms underlying behaviour specificity.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Vomeronasal receptors detect pheromonal cues emitted during social encounters, leading to activation of distinct neural ensembles in the vomeronasal organ.
“Vomeronasal receptors (VRs) detect pheromonal cues emitted during social encounters, leading to the activation of distinct neural ensembles in the vomeronasal organ (VNO) (Dulac and Torello, 2003; Holy et al., 2000; Isogai et al., 2011).”
From Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice (2017) · cites this paper as Isogai et al., 2011
There is significant signal integration at this level of the VNO pathway compared to the initial narrow tuning demonstrated in most VRs.
“In virgin mice, 58% ± 6% (mean ± SD) of the recorded MeApd neurons responded to more than one social stimulus, suggesting the existence of significant signal integration at this level of the VNO pathway compared to the initial narrow tuning demonstrated in most VRs (Isogai et al., 2011) (Figure 4C).”
From Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice (2017) · cites this paper as Isogai et al., 2011
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
A novel multigene family may encode odorant receptors: A molecular basis for odor recognition
Buck, L., & Axel, R. (1991) · Cell · doi:10.1016/0092-8674(91)90418-x · Cited by 4,987 · see citing works
Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators
Tian, L., Hires, S. A., Mao, T., Huber, D., Chiappe, M. E., Chalasani, S. H., Petreanu, L., Akerboom, J., McKinney, S. A., Schreiter, E. R., et al. (2009) · Nature Methods · doi:10.1038/nmeth.1398 · Cited by 1,967 · see citing works
Schaeren‐Wiemers, N., & Gerfin-Moser, A. (1993) · Histochemistry and Cell Biology · doi:10.1007/bf00267823 · Cited by 1,162 · see citing works
A novel family of genes encoding putative pheromone receptors in mammals
Dulac, C., & Axel, R. (1995) · Cell · doi:10.1016/0092-8674(95)90161-2 · Cited by 1,001 · see citing works
Self-citationLoss of Sex Discrimination and Male-Male Aggression in Mice Deficient for TRP2
Stowers, L., Holy, T. E., Meister, M., Dulac, C. G., & Koentges, G. (2002) · Science · doi:10.1126/science.1069259 · Cited by 880 · see citing works
Self-citationMolecular detection of pheromone signals in mammals: from genes to behaviour
Dulac, C. G., & Torello, A. T. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1140 · Cited by 662 · see citing works
Self-citationUltrasensitive pheromone detection by mammalian vomeronasal neurons
Leinders-Zufall, T., Lane, A. P., Puche, A. C., Ma, W., Novotny, M. V., Shipley, M. T., & Zufall, F. (2000) · Nature · doi:10.1038/35015572 · Cited by 576 · see citing works
Formyl peptide receptor-like proteins are a novel family of vomeronasal chemosensors
Rivière, S., Challet, L., Fluegge, D., Spehr, M., & Rodríguez, I. (2009) · Nature · doi:10.1038/nature08029 · Cited by 383 · see citing works
The effects of owl predation on the foraging behavior of heteromyid rodents
Brown, J. S., Kotler, B. P., Smith, R. J., & Wirtz, W. O. (1988) · Oecologia · doi:10.1007/bf00377036 · Cited by 381 · see citing works
Haga‐Yamanaka, S., Hattori, T., Sato, T., Sato, K., Matsuda, S., Kobayakawa, R., Sakano, H., Yoshihara, Y., Kikusui, T., & Touhara, K. (2010) · Nature · doi:10.1038/nature09142 · Cited by 376 · see citing works
Papes, F., Logan, D. W., & Stowers, L. (2010) · Cell · doi:10.1016/j.cell.2010.03.037 · Cited by 360 · see citing works
Holekamp, T. F., Turaga, D., & Holy, T. E. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.011 · Cited by 337 · see citing works
Wild mice: an ever-increasing contribution to a popular mammalian model
Guénet, J.-L., & Bonhomme, F. (2002) · Trends in Genetics · doi:10.1016/s0168-9525(02)00007-0 · Cited by 324 · see citing works
Berghard, A., & Buck, L. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-03-00909.1996 · Cited by 298 · see citing works
Responses of vomeronasal neurons to natural stimuli
Holy, T. E., Dulac, C., & Meister, M. (2000) · Science · doi:10.1126/science.289.5484.1569 · Cited by 275 · see citing works
Self-citationJia, C., & Halpern, M. (1996) · Brain Research · doi:10.1016/0006-8993(96)00110-2 · Cited by 267 · see citing works
Formyl peptide receptors are candidate chemosensory receptors in the vomeronasal organ
Liberles, S. D., Horowitz, L. F., Kuang, D., Contos, J. J. A., Wilson, K. L., Siltberg-Liberles, J., Liberles, D. A., & Buck, L. B. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904464106 · Cited by 246 · see citing works
Pheromone detection mediated by a V1r vomeronasal receptor
Boschat, C., Pélofi, C., Randin, O., Roppolo, D., Lüscher, C., Broillet, M.-C., & Rodríguez, I. (2002) · Nature Neuroscience · doi:10.1038/nn978 · Cited by 242 · see citing works
Genetic Analysis of Brain Circuits Underlying Pheromone Signaling
Dulac, C. G., & Wagner, S. (2006) · Annual Review of Genetics · doi:10.1146/annurev.genet.39.073003.093937 · Cited by 227 · see citing works
Self-citationSulfated Steroids as Natural Ligands of Mouse Pheromone-Sensing Neurons
Nodari, F., Hsu, F., Fu, X., Holekamp, T. F., Kao, L.-F., TURK, J. W., & Holy, T. E. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1425-08.2008 · Cited by 213 · see citing works
Co-Expression of Putative Pheromone Receptors in the Sensory Neurons of the Vomeronasal Organ
Martini, S., Silvotti, L., Shirazi, A., Ryba, N. J. P., & Tirindelli, R. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-03-00843.2001 · Cited by 191 · see citing works
Ben-Shaul, Y., Katz, L. C., Mooney, R., & Dulac, C. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0915147107 · Cited by 173 · see citing works
Self-citationEncoding Gender and Individual Information in the Mouse Vomeronasal Organ
He, J., Ma, L., Kim, S. S., Nakai, J., & Yu, C. (2008) · Science · doi:10.1126/science.1154476 · Cited by 167 · see citing works
DANCIGER, E., Mettling, C., Vidal, M., Morris, R. J., & Margolis, F. L. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.21.8565 · Cited by 151 · see citing works
Wagner, S., Gresser, A. L., Torello, A. T., & Dulac, C. (2006) · Neuron · doi:10.1016/j.neuron.2006.04.033 · Cited by 144 · see citing works
Self-citationStructural requirements for the activation of vomeronasal sensory neurons by MHC peptides
Leinders‐Zufall, T., Ishii, T., Mombaerts, P., Zufall, F., & Boehm, T. L. J. (2009) · Nature Neuroscience · doi:10.1038/nn.2452 · Cited by 135 · see citing works
Molecular phylogeny of the genus Mus (Rodentia: Murinae) based on mitochondrial and nuclear data
Chevret, P., Veyrunes, F., & Britton‐Davidian, J. (2005) · Biological Journal of the Linnean Society · doi:10.1111/j.1095-8312.2005.00444.x · Cited by 108 · see citing works
Sundell, J., Dudek, D., Klemme, I., Koivisto, E., Pusenius, J., & Yl�nen, H. (2004) · Oecologia · doi:10.1007/s00442-004-1490-x · Cited by 60 · see citing works
Samuelsen, C. L., & Meredith, M. J. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.09.030 · Cited by 55 · see citing works
Miller, R. A., Dysko, R. C., Chrisp, C. E., Seguin, R., Linsalata, L., Buehner, G., Harper, J. M., & Austad, S. N. (2000) · Journal of Zoology · doi:10.1111/j.1469-7998.2000.tb00580.x · Cited by 53 · see citing works
High-Throughput Microarray Detection of Vomeronasal Receptor Gene Expression in Rodents
Zhang, X., Marcucci, F., & Firestein, S. (2010) · Frontiers in Neuroscience · doi:10.3389/fnins.2010.00164 · Cited by 27 · see citing works
Taha, M., McMillon, R., Napier, A., & Wekesa, K. S. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.05.006 · Cited by 11 · see citing works
V1R promoters are well conserved and exhibit common putative regulatory motifs
Stewart, R., & Lane, R. P. (2007) · BMC Genomics · doi:10.1186/1471-2164-8-253 · Cited by 8 · see citing works
Barnard, C. J. (1983) · Animal Behaviour · doi:10.1007/978-1-4615-9781-0_3 · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Galanin neurons in the medial preoptic area govern parental behaviour
Wu, Z., Autry, A. E., Bergan, J. F., Watabe‐Uchida, M., & Dulac, C. G. (2014) · Nature · doi:10.1038/nature13307 · Cited by 592 · see citing works
Self-citationGenomic analyses identify distinct patterns of selection in domesticated pigs and Tibetan wild boars
Li, M., Tian, S., Jin, L. G., Zhou, G., Li, Y., Zhang, Y., Wang, T., Yeung, C. K. L., Chen, L., Ma, J., et al. (2013) · Nature Genetics · doi:10.1038/ng.2811 · Cited by 553 · see citing works
Functional circuit architecture underlying parental behaviour
Kohl, J., Babayan, B. M., Rubinstein, N. D., Autry, A. E., Marin-Rodriguez, B., Kapoor, V., Miyamichi, K., Zweifel, L. S., Luo, L., Uchida, N., et al. (2018) · Nature · doi:10.1038/s41586-018-0027-0 · Cited by 459 · see citing works
Self-citationDetecting Activated Cell Populations Using Single-Cell RNA-Seq
Wu, Y. E., Pan, L., Zuo, Y., Li, X., & Hong, W. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.026 · Cited by 438 · see citing works
Molecular Profiling of Activated Neurons by Phosphorylated Ribosome Capture
Knight, Z. A., Tan, K., Birsoy, K., Schmidt, S. F., Garrison, J. L., Wysocki, R. W., Emiliano, A. B., Ekstrand, M. I., & Friedman, J. M. (2012) · Cell · doi:10.1016/j.cell.2012.10.039 · Cited by 312 · see citing works
Liberles, S. D. (2013) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021113-170334 · Cited by 292 · see citing works
Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice
Li, Y., Mathis, A., Grewe, B. F., Osterhout, J. A., Ahanonu, B., Schnitzer, M. J., Murthy, V. N., & Dulac, C. (2017) · Cell · doi:10.1016/j.cell.2017.10.015 · Cited by 291 · see citing works
Self-citationCorticoamygdala Transfer of Socially Derived Information Gates Observational Learning
Allsop, S. A., Wichmann, R., Mills, F., Burgos-Robles, A., Chang, C.-J., Felix-Ortiz, A. C., Vienne, A., Beyeler, A., Izadmehr, E. M., Glober, G., et al. (2018) · Cell · doi:10.1016/j.cell.2018.04.004 · Cited by 288 · see citing works
Sex-specific processing of social cues in the medial amygdala
Bergan, J. F., Ben-Shaul, Y., & Dulac, C. (2014) · eLife · doi:10.7554/elife.02743 · Cited by 237 · see citing works
Self-citationCyclic regulation of sensory perception by a female hormone alters behavior
Dey, S., Chamero, P., Pru, J. K., Chien, M.-S., Ibarra-Soria, X., Spencer, K. R., Logan, D. W., Matsunami, H., Peluso, J. J., & Stowers, L. (2015) · Cell · doi:10.1016/j.cell.2015.04.052 · Cited by 204 · see citing works
Kaur, A. W., Ackels, T., Kuo, T.-H., Cichy, A., Dey, S., Hays, C. K., Kateri, M., Logan, D. W., Marton, T. F., Spehr, M., et al. (2014) · Cell · doi:10.1016/j.cell.2014.02.025 · Cited by 207 · see citing works
Representing Sex in the Brain, One Module at a Time
Yang, C. F., & Shah, N. M. (2014) · Neuron · doi:10.1016/j.neuron.2014.03.029 · Cited by 197 · see citing works
Synchronous Evolution of an Odor Biosynthesis Pathway and Behavioral Response
Li, Q., Korzan, W. J., Ferrero, D. M., Chang, R. B., Roy, D. S., Buchi, M., Lemon, J. K., Kaur, A. W., Stowers, L., Fendt, M., et al. (2012) · Current Biology · doi:10.1016/j.cub.2012.10.047 · Cited by 190 · see citing works
The neural circuits of innate fear: detection, integration, action, and memorization
Silva, B. A., Gross, C. T., & Gräff, J. (2016) · Learning & Memory · doi:10.1101/lm.042812.116 · Cited by 186 · see citing works
A labeled-line neural circuit for pheromone-mediated sexual behaviors in mice
Ishii, K. K., Osakada, T., Mori, H., Miyasaka, N., Yoshihara, Y., Miyamichi, K., & Touhara, K. (2017) · Neuron · doi:10.1016/j.neuron.2017.05.038 · Cited by 185 · see citing works
Mouse alarm pheromone shares structural similarity with predator scents
Brechbühl, J., Moine, F., Klaey‐Tassone, M., Nenniger-Tosato, M., Hurni, N., Sporkert, F., Giroud, C., & Broillet, M.-C. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1214249110 · Cited by 176 · see citing works
Wired for behaviors: from development to function of innate limbic system circuitry
Sokolowski, K., & Corbin, J. G. (2012) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2012.00055 · Cited by 174 · see citing works
Genetic and Neural Mechanisms that Inhibit Drosophila from Mating with Other Species
Fan, P., Manoli, D. S., Ahmed, O. M., Chen, Y., Agarwal, N., Kwong, S., Cai, A. G., Neitz, J., Renslo, A., Baker, B. S., et al. (2013) · Cell · doi:10.1016/j.cell.2013.06.008 · Cited by 164 · see citing works
The Olfactory Transcriptomes of Mice
Ibarra-Soria, X., Levitin, M. O., Saraiva, L. R., & Logan, D. W. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004593 · Cited by 156 · see citing works
Pardo‐Bellver, C., Cádiz‐Moretti, B., Novejarque, A., Martínez‐Garciá, F., & Lanuza, E. (2012) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2012.00033 · Cited by 157 · see citing works
Social Control of Hypothalamus-Mediated Male Aggression
Yang, T., Yang, C. F., Chizari, M., Maheswaranathan, N., Burke, K. J., Borius, M., Inoue, S., Chiang, M. C., Bender, K. J., Ganguli, S., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.046 · Cited by 158 · see citing works
Olfactory systems and neural circuits that modulate predator odor fear
Takahashi, L. K. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00072 · Cited by 162 · see citing works
From genes to social communication: molecular sensing by the vomeronasal organ.
Chamero, P., Leinders-Zufall, T., & Zufall, F. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.04.011 · Cited by 149 · see citing works
Oxytocin signaling in the medial amygdala is required for sex discrimination of social cues
Yao, S., Bergan, J., Lanjuin, A., & Dulac, C. (2017) · eLife · doi:10.7554/elife.31373 · Cited by 151 · see citing works
Self-citationA family of non-GPCR chemosensors defines an alternative logic for mammalian olfaction
Greer, P. L., Bear, D. M., Lassance, J.-M., Bloom, M. L., Tsukahara, T., Pashkovski, S. L., Masuda, F. K., Nowlan, A. C., Kirchner, R., Hoekstra, H. E., et al. (2016) · Cell · doi:10.1016/j.cell.2016.05.001 · Cited by 148 · see citing works
Gur, R., Tendler, A., & Wagner, S. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.03.022 · Cited by 144 · see citing works
An olfactory cocktail party: figure-ground segregation of odorants in rodents
Rokni, D., Hemmelder, V., Kapoor, V., & Murthy, V. N. (2014) · Nature Neuroscience · doi:10.1038/nn.3775 · Cited by 143 · see citing works
Self-citationTaste and smell processing in the brain
Rolls, E. T. (2019) · Handbook of clinical neurology · doi:10.1016/b978-0-444-63855-7.00007-1 · Cited by 141 · see citing works
The Evolving Neural and Genetic Architecture of Vertebrate Olfaction
Bear, D. M., Lassance, J., Hoekstra, H. E., & Datta, S. R. (2016) · Current Biology · doi:10.1016/j.cub.2016.09.011 · Cited by 133 · see citing works
Molecular profiling of activated olfactory neurons identifies odorant receptors for odors in vivo
Jiang, Y., Gong, N. N., Hu, X. S., Ni, M. J., Pasi, R., & Matsunami, H. (2015) · Nature Neuroscience · doi:10.1038/nn.4104 · Cited by 133 · see citing works
Anholt, R. R. H., & Mackay, T. F. C. (2012) · Annual Review of Genetics · doi:10.1146/annurev-genet-110711-155514 · Cited by 135 · see citing works
Limbic Neurons Shape Sex Recognition and Social Behavior in Sexually Naive Males
Bayless, D. W., Yang, T., Mason, M. M., Susanto, A. A. T., Lobdell, A., & Shah, N. M. (2019) · Cell · doi:10.1016/j.cell.2018.12.041 · Cited by 131 · see citing works
<scp>O</scp>xytocin modulation of neural circuits for social behavior
Marlin, B. J., & Froemke, R. C. (2017) · Developmental Neurobiology · doi:10.1002/dneu.22452 · Cited by 130 · see citing works
Multisensory Logic of Infant-Directed Aggression by Males
Isogai, Y., Wu, Z., Love, M. I., Ahn, M. H., Bambah-Mukku, D., Hua, V. J., Farrell, K., & Dulac, C. G. (2018) · Cell · doi:10.1016/j.cell.2018.11.032 · Cited by 130 · see citing works
Self-citationOxytocin mediates entrainment of sensory stimuli to social cues of opposing valence
Choe, H. K., Reed, M. D., Benavidez, N., Montgomery, D., Soares, N., Yim, Y. S., & Choi, G. B. (2015) · Neuron · doi:10.1016/j.neuron.2015.06.022 · Cited by 124 · see citing works
Signal Detection and Coding in the Accessory Olfactory System
Mohrhardt, J., Nagel, M., Fleck, D., Ben‐Shaul, Y., & Spehr, M. (2018) · Chemical Senses · doi:10.1093/chemse/bjy061 · Cited by 114 · see citing works
Simultaneous multiplane imaging with reverberation two-photon microscopy
Beaulieu, D. R., Davison, I. G., Kılıç, K., Bifano, T. G., & Mertz, J. C. (2020) · Nature Methods · doi:10.1038/s41592-019-0728-9 · Cited by 107 · see citing works
From molecules to mating: Rapid evolution and biochemical studies of reproductive proteins
Wilburn, D. B., & Swanson, W. J. (2015) · Journal of Proteomics · doi:10.1016/j.jprot.2015.06.007 · Cited by 110 · see citing works
Integrated action of pheromone signals in promoting courtship behavior in male mice
Haga‐Yamanaka, S., Ma, L., He, J., Qiu, Q., Lavis, L. D., Looger, L. L., & Yu, C. R. (2014) · eLife · doi:10.7554/elife.03025 · Cited by 110 · see citing works
Xiong, Z., Zhu, X., Geng, J., Xu, Y., Wu, R., Li, C., Fan, D., Qin, X. S., Du, Y., Tian, Y., et al. (2022) · Immunity · doi:10.1016/j.immuni.2022.03.001 · Cited by 109 · see citing works
Of Pheromones and Kairomones: What Receptors Mediate Innate Emotional Responses?
Fortes-Marco, L., Lanuza, E., & Martínez‐Garciá, F. (2013) · The Anatomical Record · doi:10.1002/ar.22745 · Cited by 101 · see citing works
Mammalian pheromones; emerging properties and mechanisms of detection
Stowers, L., & Kuo, T.-H. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.02.005 · Cited by 85 · see citing works
Johnson, M. A., Korsak, L. I. T., Roy, D. S., Valenzuela, D. H., Mosley, C., Magklara, A., Lomvardas, S., Liberles, S. D., & Barnea, G. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1206724109 · Cited by 100 · see citing works
Chemical signals in terrestrial vertebrates: search for design features.
Apps, P., Weldon, P., & Kramer, M. (2015) · Natural product reports (Print) · doi:10.1039/c5np00029g · Cited by 80 · see citing works
Antagonism in olfactory receptor neurons and its implications for the perception of odor mixtures
Reddy, G., Zak, J. D., Vergassola, M., & Murthy, V. N. (2018) · eLife · doi:10.7554/elife.34958 · Cited by 94 · see citing works
Self-citationAntagonistic odor interactions in olfactory sensory neurons are widespread in freely breathing mice
Zak, J. D., Reddy, G., Vergassola, M., & Murthy, V. N. (2020) · Nature Communications · doi:10.1038/s41467-020-17124-5 · Cited by 87 · see citing works
Self-citationCádiz‐Moretti, B., Otero‐García, M., Martínez‐Garciá, F., & Lanuza, E. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0954-y · Cited by 88 · see citing works
The genomic basis of vomeronasal-mediated behaviour
Ibarra-Soria, X., Levitin, M. O., & Logan, D. W. (2013) · Mammalian Genome · doi:10.1007/s00335-013-9463-1 · Cited by 85 · see citing works
Sensory Ecology of Predator-Induced Phenotypic Plasticity
Weiss, L. C. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00330 · Cited by 83 · see citing works
First evidence for functional vomeronasal 2 receptor genes in primates
Hohenbrink, P., Mundy, N. I., Zimmermann, E., & Radespiel, U. (2012) · Biology Letters · doi:10.1098/rsbl.2012.1006 · Cited by 83 · see citing works
Principles of odor coding in vertebrates and artificial chemosensory systems
Manzini, I., Schild, D., & Natale, C. D. (2021) · Physiological Reviews · doi:10.1152/physrev.00036.2020 · Cited by 84 · see citing works
Nucleus Accumbens Dopamine Signaling Regulates Sexual Preference for Females in Male Mice
Beny, Y., Zilkha, N., Lavi‐Avnon, Y., Bezalel, N., Rogachev, I., Brandis, A. S., Dayan, M., & Kimchi, T. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.11.062 · Cited by 82 · see citing works
Distribution of oxytocin and co-localization with arginine vasopressin in the brain of mice
Otero‐García, M., Agustín‐Pavón, C., Lanuza, E., & Martínez‐Garciá, F. (2015) · Brain Structure and Function · doi:10.1007/s00429-015-1111-y · Cited by 76 · see citing works
Guimarães, A. T. B., Freitas, Í. N., Mubarak, N. M., Rahman, M. M., Rodrigues, F. P., Rodrigues, A. S. D. L., Barceló, ., Islam, A. R. M. T., & Malafaia, G. (2022) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2022.130004 · Cited by 77 · see citing works
Neural control of sexually dimorphic behaviors
Manoli, D. S., Fan, P., Fraser, E. J., & Shah, N. M. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.04.005 · Cited by 76 · see citing works
Neural coding of sex-specific social information in the mouse brain
Li, Y., & Dulac, C. G. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.07.005 · Cited by 76 · see citing works
Self-citationState-dependent responses to sex pheromones in mouse
Stowers, L., & Liberles, S. D. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.04.001 · Cited by 75 · see citing works
Trouillet, A., Keller, M., Weiss, J., Leinders‐Zufall, T., Birnbaumer, L., Zufall, F., & Chamero, P. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1821492116 · Cited by 74 · see citing works
Processing by the main olfactory system of chemosignals that facilitate mammalian reproduction
Baum, M. J., & Cherry, J. A. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.06.003 · Cited by 73 · see citing works
Molecular Evolutionary Characterization of a V1R Subfamily Unique to Strepsirrhine Primates
Yoder, A. D., Chan, L. M., dos Reis, M., Larsen, P. A., Campbell, C. R., Rasoloarison, R. M., Barrett, M., Roos, C., Kappeler, P. M., Bielawski, J. P., et al. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu006 · Cited by 72 · see citing works
Sexual rejection via a vomeronasal receptor-triggered limbic circuit
Osakada, T., Ishii, K. K., Mori, H., Eguchi, R., Ferrero, D. M., Yoshihara, Y., Liberles, S. D., Miyamichi, K., & Touhara, K. (2018) · Nature Communications · doi:10.1038/s41467-018-07003-5 · Cited by 78 · see citing works
Urocortin-3 neurons in the mouse perifornical area promote infant-directed neglect and aggression
Autry, A. E., Wu, Z., Kapoor, V., Kohl, J., Bambah-Mukku, D., Rubinstein, N. D., Marin-Rodriguez, B., Carta, I., Sedwick, V. M., Tang, M., et al. (2021) · eLife · doi:10.7554/elife.64680 · Cited by 72 · see citing works
Self-citationChemosensory signals and their receptors in the olfactory neural system
Ihara, S., Yoshikawa, K., & Touhara, K. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.08.063 · Cited by 70 · see citing works
Chen, A.-X., Yan, J., Zhang, W., Wang, L. A., Yu, Z., Ding, X., Wang, D., Zhang, M., Zhang, Y., Song, N., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.08.025 · Cited by 66 · see citing works
Organization of Vomeronasal Sensory Coding Revealed by Fast Volumetric Calcium Imaging
Turaga, D., & Holy, T. E. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5339-11.2012 · Cited by 66 · see citing works
Experience-Dependent Plasticity Drives Individual Differences in Pheromone-Sensing Neurons
Xu, P. S., Lee, D., & Holy, T. E. (2016) · Neuron · doi:10.1016/j.neuron.2016.07.034 · Cited by 64 · see citing works
Mutual influences between the main olfactory and vomeronasal systems in development and evolution
Suárez, R., García‐González, D., & de Castro, F. (2012) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2012.00050 · Cited by 63 · see citing works
Olfactory marker protein (OMP) regulates formation and refinement of the olfactory glomerular map
Albeanu, D. F., Provost, A. C., Agarwal, P., Soucy, E. R., Zak, J. D., & Murthy, V. N. (2018) · Nature Communications · doi:10.1038/s41467-018-07544-9 · Cited by 62 · see citing works
Self-citationMolecular and neural control of sexually dimorphic social behaviors
Yang, T., & Shah, N. M. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.04.015 · Cited by 61 · see citing works
The evolution of red color vision is linked to coordinated rhodopsin tuning in lycaenid butterflies
Liénard, M. A., Bernard, G. D., Allen, A. A., Lassance, J., Song, S., Childers, R. R., Yu, N., Ye, D., Stephenson, A., Valencia‐Montoya, W. A., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2008986118 · Cited by 57 · see citing works
Gutiérrez‐Castellanos, N., Pardo‐Bellver, C., Martínez‐Garciá, F., & Lanuza, E. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12393 · Cited by 59 · see citing works
Functional organization of glomerular maps in the mouse accessory olfactory bulb
Hammen, G. F., Turaga, D., Holy, T. E., & Meeks, J. P. (2014) · Nature Neuroscience · doi:10.1038/nn.3738 · Cited by 58 · see citing works
Roles of sex and gonadal steroids in mammalian pheromonal communication
Baum, M. J., & Bakker, J. (2013) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.07.004 · Cited by 58 · see citing works
Xie, Z., Gu, H., Huang, M., Cheng, X., Shang, C., Tao, T., Li, D., Xie, Y., Zhao, J., Lü, W., et al. (2022) · Nature Neuroscience · doi:10.1038/s41593-021-00985-4 · Cited by 57 · see citing works
Ominous odors: olfactory control of instinctive fear and aggression in mice
Stowers, L., Cameron, P. A., & Keller, J. A. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.01.007 · Cited by 57 · see citing works
Visualization of odor-induced neuronal activity by immediate early gene expression
Bepari, A. K., Watanabe, K., Yamaguchi, M., Tamamaki, N., & Takebayashi, H. (2012) · BMC Neuroscience · doi:10.1186/1471-2202-13-140 · Cited by 56 · see citing works
van der Linden, C., Jakob, S., Gupta, P., Dulac, C. G., & Santoro, S. W. (2018) · Nature Communications · doi:10.1038/s41467-018-07120-1 · Cited by 56 · see citing works
Self-citationBaum, M. J. (2012) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2012.00020 · Cited by 55 · see citing works
Zilkha, N., Sofer, Y., Beny, Y., & Kimchi, T. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.04.014 · Cited by 51 · see citing works
Coding of pheromones by vomeronasal receptors
Tirindelli, R. (2021) · Cell and Tissue Research · doi:10.1007/s00441-020-03376-6 · Cited by 53 · see citing works
Behrens, M., Frank, O., Rawel, H. M., Ahuja, G., Potting, C., Hofmann, T. F., Meyerhof, W., & Korsching, S. I. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.573162 · Cited by 52 · see citing works
Faecal bile acids are natural ligands of the mouse accessory olfactory system
Doyle, W. I., Dinser, J. A., Cansler, H. L., Zhang, X., Dinh, D. D., Browder, N. S., Riddington, I. M., & Meeks, J. P. (2016) · Nature Communications · doi:10.1038/ncomms11936 · Cited by 52 · see citing works
Sensory coding mechanisms revealed by optical tagging of physiologically defined neuronal types
Lee, D., Kume, M., & Holy, T. E. (2019) · Science · doi:10.1126/science.aax8055 · Cited by 50 · see citing works
Larsen, P. A., Heilman, A. M., & Yoder, A. D. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-720 · Cited by 50 · see citing works
Innate and learned aspects of pheromone-mediated social behaviours
Beny, Y., & Kimchi, T. (2014) · Animal Behaviour · doi:10.1016/j.anbehav.2014.09.014 · Cited by 49 · see citing works
Oboti, L., Ibarra-Soria, X., Pérez‐Gómez, A., Schmid, A., Pyrski, M. M., Paschek, N., Kircher, S., Logan, D. W., Leinders‐Zufall, T., Zufall, F., et al. (2015) · BMC Biology · doi:10.1186/s12915-015-0211-8 · Cited by 46 · see citing works
Reading Out Olfactory Receptors: Feedforward Circuits Detect Odors in Mixtures without Demixing
Mathis, A., Rokni, D., Kapoor, V., Bethge, M., & Murthy, V. N. (2016) · Neuron · doi:10.1016/j.neuron.2016.08.007 · Cited by 48 · see citing works
Self-citationMorphological and Immunohistochemical Features of the Vomeronasal System in Dogs
Salazar, I., Cifuentes, J. M., & Sánchez‐Quinteiro, P. (2012) · The Anatomical Record · doi:10.1002/ar.22617 · Cited by 46 · see citing works
Arakawa, H., Kelliher, K. R., Zufall, F., & Munger, S. D. (2013) · Chemical Senses · doi:10.1093/chemse/bjt015 · Cited by 46 · see citing works
A Nose for Death: Integrating Trophic and Informational Networks for Conservation and Management
Jones, M. E., Apfelbach, R., Banks, P. B., Cameron, E. Z., Dickman, C. R., Frank, A. S. K., McLean, S., McGregor, I. S., Müller‐Schwarze, D., Parsons, M. H., et al. (2016) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2016.00124 · Cited by 46 · see citing works
Excreted Steroids in Vertebrate Social Communication
Doyle, W. I., & Meeks, J. P. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2488-17.2018 · Cited by 45 · see citing works
Functional evolution of vertebrate sensory receptors
Baldwin, M. W., & Ko, M. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104771 · Cited by 43 · see citing works
Zebrafish olfactory receptors ORAs differentially detect bile acids and bile salts
Cong, X., Zheng, Q., Ren, W., Chéron, J.-B., Fiorucci, S., Wen, T., Zhang, C., Yu, H., Golebiowski, J., & Yu, Y. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.006483 · Cited by 42 · see citing works
Genomic variation in the vomeronasal receptor gene repertoires of inbred mice
Wynn, E. H., Sánchez-Andrade, G., Carss, K., & Logan, D. W. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-415 · Cited by 41 · see citing works
Bufe, B., Teuchert, Y., Schmid, A., Pyrski, M. M., Pérez‐Gómez, A., Eisenbeis, J., Timm, T., Ishii, T., Lochnit, G., Bischoff, M., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12842-x · Cited by 44 · see citing works
deCarvalho, T., Akitake, C. M., Thisse, C., Thisse, B., & Halpern, M. E. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00098 · Cited by 41 · see citing works
Sparse and stereotyped encoding implicates a core glomerulus for ant alarm behavior
Hart, T., Frank, D. D., Lopes, L. E., Olivos-Cisneros, L., Lacy, K. D., Trible, W., Ritger, A. L., Valdés-Rodríguez, S., & Kronauer, D. J. C. (2023) · Cell · doi:10.1016/j.cell.2023.05.025 · Cited by 39 · see citing works
Smadja, C. M., Loire, É., Caminade, P., Thoma, M., Latour, Y., Roux, C., Thoß, M., Penn, D. J., Ganem, G., & Boursot, P. (2015) · Molecular Ecology · doi:10.1111/mec.13301 · Cited by 39 · see citing works
Identification of an Intra- and Inter-specific Tear Protein Signal in Rodents
Tsunoda, M., Miyamichi, K., Eguchi, R., Sakuma, Y., Yoshihara, Y., Kikusui, T., Kuwahara, M., & Touhara, K. (2018) · Current Biology · doi:10.1016/j.cub.2018.02.060 · Cited by 38 · see citing works
Neural circuit control of innate behaviors
Wei, X., Jiao, Z., Senol, E., Yao, J., Zhao, M., Zhao, Z., Chen, X., Cao, P., Fu, Y., Gao, Z., et al. (2021) · Science China Life Sciences · doi:10.1007/s11427-021-2043-2 · Cited by 38 · see citing works
- Authors
- Isogai, Y., Si, S., Pont-Lezica, L., Tan, T., Kapoor, V., Murthy, V. N., & Dulac, C.
- Affiliations
- Harvard University (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Dulac, Catherine
- Venue
- Nature
- Published
- 2011-09-21
- Volume
- 478
- Issue
- 7368
- Pages
- 241-245
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3192931
- OpenAlex
- W2152243497
- Cited by
- 317
- References
- 34
- Citations by year
- 2026: 10 · 2025: 8 · 2024: 22 · 2023: 21 · 2022: 15 · 2021: 25 · 2020: 24 · 2019: 19 · 2018: 27 · 2017: 16 · 2016: 27 · 2015: 21 · 2014: 31 · 2013: 25 · 2012: 21
- FWCI
- 13.80
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute on Deafness and Other Communication Disorders (R01DC003903, R01DC009019)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Health Sciences › Nursing › Nutrition and Dietetics › Biochemical Analysis and Sensing Techniques
- Keywords
- vomeronasal organ, vomeronasal receptors, pheromone receptors, V1R, V2 receptor, kairomones, pheromones, innate behavior, social behavior, aggression, mating behavior, mice
- MeSH terms
- Animals, Birds, Chemoreceptor Cells, Cues, Female, Gene Expression Regulation, Male, Mammals, Pheromones, Predatory Behavior, Sex Characteristics, Species Specificity, Receptors, Odorant, Vomeronasal Organ, Mice, Early Growth Response Protein 1
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review