Something in the Air? New Insights into Mammalian Pheromones

Brennan, Peter A.; Keverne, Eric B.

doi:10.1016/j.cub.2003.12.052

Cited by 236Olfactory and Sensory Function StudiesIon Channels and ReceptorsBiochemical Analysis and Sensing Techniques

Something in the Air? New Insights into Mammalian Pheromones

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Brennan, Peter A., Keverne, Eric B.·2004·Current Biology

DOI 10.1016/j.cub.2003.12.052

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Abstract

Olfaction is the dominant sensory modality for most animals and chemosensory communication is particularly well developed in many mammals. Our understanding of this form of communication has grown rapidly over the last ten years since the identification of the first olfactory receptor genes. The subsequent cloning of genes for rodent vomeronasal receptors, which are important in pheromone detection, has revealed an unexpected diversity of around 250 receptors belonging to two structurally different classes. This review will focus on the chemical nature of mammalian pheromones and the complementary roles of the main olfactory system and vomeronasal system in mediating pheromonal responses. Recent studies using genetically modified mice and electrophysiological recordings have highlighted the complexities of chemosensory communication via the vomeronasal system and the role of this system in handling information about sex and genetic identity. Although the vomeronasal organ is often regarded as only a pheromone detector, evidence is emerging that suggests it might respond to a much broader variety of chemosignals.

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The MeA is the first site where signals from the olfactory bulb and vomeronasal system converge.
“It is the first site where signals from the olfactory bulb and vomeronasal system converge, thus positioning the MeA to recognize, analyze, and categorize incoming chemosensory information 11 .”
From Ucn3 and CRF-R2 in the medial amygdala regulate complex social dynamics (2016) · cites this paper as [11]

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Background
Mother–infant bonding and the evolution of mammalian social relationships
Broad, K. D., Curley, J. P., & Keverne, E. B. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1940 · Cited by 283 · see citing works
“Through this chemosensory system, pheromone signals are able to change endocrine states (e.g. advance the onset of oestrus) and regulate parental and sexual behaviour (Brennan & Keverne 2004).”
BackgroundSelf-citation
Info-disruption: pollution and the transfer of chemical information between organisms
Lürling, M., & Scheffer, M. (2007) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2007.04.002 · Cited by 279 · 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
Evolutionary dynamics of olfactory and other chemosensory receptor genes in vertebrates
Niimura, Y., & Nei, M. (2006) · Journal of Human Genetics · doi:10.1007/s10038-006-0391-8 · Cited by 238 · see citing works
“However, it appears that Ciona intestinalis, a basal chordate, does not have any genes that are orthologous to vertebrate ORs (Satoh 2005), though its whole genome draft sequence is known (Dehal et al. 2002).”
BackgroundInfluential
Scent marking behavior as an odorant communication in mice
Arakawa, H., Blanchard, D. C., Arakawa, K., Dunlap, C., & Blanchard, R. J. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.05.012 · Cited by 229 · see citing works
“, 2001) are largely expressed in the liver under stimulation by androgens and their products are released in the urine by filtration from blood serum, providing long-lasting nonvolatile odor (Bacchini et al., 1992; Brennan and Keverne, 2004).”
Background
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
“Similarly, the few mammalian compounds known to activate the VNO and to trigger behavioral responses act mostly as groups of structurally related molecules (8, 19).”
Background
Genes, brains and mammalian social bonds
Curley, J. P., & Keverne, E. B. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.05.018 · Cited by 214 · see citing works
“These receptors are the first processing stage of the vomeronasal (or ‘accessory’) olfactory system, which is the major pheromone chemosensory system in small-brained mammals [ 32 ,33].”
BackgroundSelf-citation
Neurogenetics of Aggressive Behavior: Studies in Rodents
Takahashi, A., & Miczek, K. A. (2013) · Current topics in behavioral neurosciences · doi:10.1007/7854_2013_263 · Cited by 212 · see citing works
“For rodents, olfaction is the major sensory input regulating social behaviors (Brennan and Keverne 2004).”
Background
Sexually Dimorphic Synaptic Organization of the Medial Amygdala
Cooke, B. M., & Woolley, C. S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2919-05.2005 · Cited by 194 · see citing works
“Rodents use their main and accessory olfactory systems for social recognition and territoriality and to initiate neuroendocrine reflexes (Brennan and Keverne, 2004).”
Background
MHC peptides and the sensory evaluation of genotype.
Boehm, T., & Zufall, F. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2005.11.006 · Cited by 175 · see citing works
“It has also become clear that innate behavioral responses are not the only ones regulated by the VNO: in the pregnancy-block phenomenon, the behavioral outcome depends on prior olfactory memory formation (i.e. olfactory learning) [ 31 ,36,38].”
BackgroundInfluential
The main and the accessory olfactory systems interact in the control of mate recognition and sexual behavior
Keller, M., Baum, M. J., Brock, O., Brennan, P., & Bakker, J. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.01.020 · Cited by 172 · see citing works
“In addition, both types of receptors are expressed in different regions of the VNO: V1Rs are expressed in the apical part of the VNO, near the lumen, while V2Rs are expressed in the more basal region [14,38].”
Self-citation
The main olfactory system and social learning in mammals
Sánchez-Andrade, G., & Kendrick, K. M. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.12.021 · Cited by 166 · see citing works
Paternal care in rodents: Weakening support for hormonal regulation of the transition to behavioral fatherhood in rodent animal models of biparental care
Wynne‐Edwards, K. E., & Timonin, M. E. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.03.018 · Cited by 163 · see citing works
Central Control Circuit for Context-Dependent Micturition
Hou, X. H., Hyun, M., Taranda, J., Huang, K. W., Emmalee, T., Feng, D. D., Atwater, E., Croney, D. M., Zeidel, M. L., Osten, P., et al. (2016) · Cell · doi:10.1016/j.cell.2016.08.073 · Cited by 158 · see citing works
“Micturition is also critical for social communication in many animal species; volatile and non-volatile components in urine convey information about the individual, including its sex, species, and identity (Bacchini et al., 1992; Beynon et al., 2002; Brennan and Keverne, 2004; Hurst and Beynon, 2004; Hurst et al., 199…”
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 150 · see citing works
Olfactory-mediated parasite recognition and avoidance: linking genes to behavior.
Kavaliers, M., Choleris, E., Ågmo, A., & Pfaff, D. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.03.005 · Cited by 128 · see citing works
Rodent tests of depression and anxiety: Construct validity and translational relevance
Gencturk, S., & Unal, G. (2024) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-024-01171-2 · Cited by 138 · see citing works
“As the dominant sensory modality of rodents (Brennan & Keverne, 2004), utilizing olfaction in behavioral testing enhances its ecological relevance.”
Background
Sex- and Strain-Specific Expression and Vomeronasal Activity of Mouse ESP Family Peptides
Kimoto, H., Sato, K., Nodari, F., Haga‐Yamanaka, S., Holy, T. E., & Touhara, K. (2007) · Current Biology · doi:10.1016/j.cub.2007.09.042 · Cited by 144 · see citing works
Signaling in the Chemosensory Systems
Spehr, M., Spehr, J., Ukhanov, K., Kelliher, K. R., Leinders‐Zufall, T., & Zufall, F. (2006) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-006-6109-4 · Cited by 144 · see citing works
Sex recognition by odour and variation in the uropygial gland secretion in starlings
Amo, L., Avilés, J. M., Parejo, D., Peña, A., Rodríguez, J., & Tomás, G. (2012) · Journal of Animal Ecology · doi:10.1111/j.1365-2656.2011.01940.x · Cited by 139 · see citing works
“For example, at an intraspecific level, mammal scents have been shown to vary between individuals and to reveal body condition, parasite load, health state and even genetic compatibility (e.g. major histocompatibility complex, Brennan & Keverne 2004).”
Background
What is it like to be a rat? Rat sensory perception and its implications for experimental design and rat welfare
Burn, C. C. (2008) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2008.02.007 · Cited by 133 · see citing works
“However, since the vomeronasal organ requires direct physical contact to detect some pheromones (Brennan & Keverne, 2004), the problem might only exist if the scent is volatile.”
BackgroundInfluential
From models to mechanisms: Odorant communication as a key determinant of social behavior in rodents during illness-associated states
Arakawa, H., Cruz, S., & Deak, T. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.03.007 · Cited by 131 · see citing works
“This investigation–recognition strategy heavily relies on the physical distance toward conspecific-relevant stimuli (e.g., Blanchard et al., 2001, 2003; Brennan and Keverne, 2004; Broad and Keverne, 2008).”
Background
Pheromonal recognition memory induced by TRPC2‐independent vomeronasal sensing
Kelliher, K. R., Spehr, M., Li, X., Zufall, F., & Leinders‐Zufall, T. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04866.x · Cited by 115 · see citing works
“…et al., 2002; Leypold et al., 2002; Lucas et al., 2003) and TRPC2– ⁄ – mice constitute an important genetic model for investigating the role of the vomeronasal organ (VNO) in mammalian pheromonal sensing (Leypold et al., 2002; McCarthy & Auger, 2002; Stowers et al., 2002; Brennan & Keverne, 2004).”
Background
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
“2001; Brennan 2004).”
Oxytocin and vasopressin in the medial amygdala differentially modulate approach and avoidance behavior toward illness-related social odor
Arakawa, H., Arakawa, K., & Terrence Deak, B. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.10.013 · Cited by 114 · see citing works
Recognition and avoidance of the odors of parasitized conspecifics and predators: Differential genomic correlates
Kavaliers, M., Choleris, E., & Pfaff, D. W. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.011 · Cited by 112 · see citing works
MHC odours are not required or sufficient for recognition of individual scent owners
Hurst, J. L., Thom, M. D. F., Nevison, C. M., Humphries, R. E., & Beynon, R. J. (2005) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2004.3004 · Cited by 107 · see citing works
“B (2005) in sex and identity recognition (Dulac & Torello 2003; Luo et al. 2003; Brennan & Keverne 2004).”
Background
Ucn3 and CRF-R2 in the medial amygdala regulate complex social dynamics
Shemesh, Y., Forkosh, O., Mahn, M., Anpilov, S., Sztainberg, Y., Manashirov, S., Shlapobersky, T., Elliott, E., Tabouy, L., Ezra, G., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4346 · Cited by 99 · see citing works
What Is a Pheromone? Mammalian Pheromones Reconsidered
Stowers, L., & Marton, T. F. (2005) · Neuron · doi:10.1016/j.neuron.2005.04.032 · Cited by 100 · see citing works
“While it is true that the MOE responds to odorants and VNO neurons respond to pheromones (reviewed in Dulac and Torello, 2003, and Brennan and Keverne, 2004), it appears that the converse may also occur.”
Background
Genes, odours and the recognition of parasitized individuals by rodents.
Kavaliers, M., Choleris, E., & Pfaff, D. (2005) · Trends in Parasitology · doi:10.1016/j.pt.2005.07.008 · Cited by 101 · see citing works
Decoding an olfactory mechanism of kin recognition and inbreeding avoidance in a primate
Boulet, M., Charpentier, M. J. E., & Drea, C. M. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-281 · Cited by 96 · see citing works
“The lipocalin family includes MUPs, a group of binding proteins functioning as semiochemical transporters [63] and notably linked to inbreeding avoidance in mice [23].”
Background
Ultrasonic vocalizations as a fundamental tool for early and adult behavioral phenotyping of Autism Spectrum Disorder rodent models
Caruso, A., Ricceri, L., & Scattoni, M. L. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.06.011 · Cited by 85 · see citing works
The role of pheromones in freshwater fishes
Burnard, D., Gozlan, R. E., & Griffiths, S. W. (2008) · Journal of Fish Biology · doi:10.1111/j.1095-8649.2008.01872.x · Cited by 87 · see citing works
Encoding pheromonal signals in the mammalian vomeronasal system
Luo, M., & Katz, L. C. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.07.001 · Cited by 82 · see citing works
Cells in the vomeronasal organ express odorant receptors but project to the accessory olfactory bulb
Lévai, O., Feistel, T., Breer, H., & Strotmann, J. M. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21067 · Cited by 80 · see citing works
“…fluids and are commonly received by direct contact (Luo et al., 2003); such molecules carry specific information concerning species, gender, and identity of an animal and are commonly termed pheromones (for recent reviews, see Brennan and Keverne, 2004; Dulac and Torello, 2003; Rodriguez, 2004).”
Background
A niche for adult neurogenesis in social behavior
Gheusi, G., Ortega‐Pérez, I., Murray, K., & Lledo, P. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.02.006 · Cited by 77 · see citing works
Central role of G protein Gαi2 and Gαi2 + vomeronasal neurons in balancing territorial and infant-directed aggression of male mice
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
A centrifugal pathway to the mouse accessory olfactory bulb from the medial amygdala conveys gender‐specific volatile pheromonal signals
Martel, K. L., & Baum, M. J. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06564.x · Cited by 70 · see citing works
“Recent studies have shown that the functions of the main and accessory olfactory systems may complement each other (Brennan & Keverne, 2004; Brennan & Zufall, 2006; Shepherd, 2006).”
Background
Identification of urinary sex pheromones in female buffaloes and their influence on bull reproductive behaviour
Rajanarayanan, S., & Archunan, G. (2011) · Research in Veterinary Science · doi:10.1016/j.rvsc.2010.12.005 · Cited by 70 · see citing works
Integration and sensory experience‐dependent survival of newly‐generated neurons in the accessory olfactory bulb of female mice
Oboti, L., Savalli, G., Giachino, C., Marchis, S. D., Panzica, G., Fasolo, A., & Peretto, P. M. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06614.x · Cited by 71 · see citing works
High-speed odor sensing using miniaturized electronic nose
Dennler, N., Drix, D., Warner, T. P. A., Rastogi, S., Casa, C. D., Ackels, T., Schaefer, A. T., André, V. S., & Schmuker, M. (2024) · Science Advances · doi:10.1126/sciadv.adp1764 · Cited by 76 · see citing works
Chemosensory communication of gender through two human steroids in a sexually dimorphic manner.
Zhou, W., Yang, X.-Y., Chen, K.-P., Cai, P., He, S., & Jiang, Y. (2014) · Current Biology · doi:10.1016/j.cub.2014.03.035 · Cited by 67 · see citing works
“Pheromones are chemical signals that convey information between members of the same species [3, 4].”
Background
The Social Environment and Neurogenesis in the Adult Mammalian Brain
Lieberwirth, C., & Wang, Z. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00118 · Cited by 66 · see citing works
“For example, pheromones are involved in modulating rodent mating and reproductive behaviors (Dulac and Torello, 2003; Brennan and Keverne, 2004) and also play a role in human social behavior, such as attraction (Cowley and Brooksbank, 1991).”
Background
Mouse Models of Autism: Testing Hypotheses About Molecular Mechanisms
Roullet, F., & Crawley, J. N. (2011) · Current topics in behavioral neurosciences · doi:10.1007/7854_2010_113 · Cited by 65 · see citing works
“Social olfactory tasks for mice generally measure sniffing of urinary pheronomones (Humphries et al. 1999; Hurst et al. 2001; Bakker 1994; Brennan and Keverne 2004; Hurst and Beynon 2004; Hurst et al. 2005; Arakawa et al. 2007; Yang and Crawley 2009) and behavioral responses toward scent marks…”
Background
Neural systems that facilitate the representation of social rank
Dwortz, M. F., Curley, J. P., Tye, K. M., & Padilla-Coreano, N. (2022) · Philosophical Transactions of the Royal Society B · doi:10.1098/rstb.2020.0444 · Cited by 64 · see citing works
Kisspeptin Signaling Is Required for the Luteinizing Hormone Response in Anestrous Ewes following the Introduction of Males
Bond, J. P. D., Li, Q., Millar, R. P., Clarke, I. J., & Smith, J. T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057972 · Cited by 64 · see citing works
“The effect of pheromones on mammalian reproduction is well recognized [39,40], but the precise neuroanatomical pathways to the relevant hypothalamic centers and/or GnRH neurons are not defined.”
Background
Seasonal and reproductive variation in chemical constituents of scent signals in wild giant pandas
Zhou, W., Nie, Y., Hu, Y., Swaisgood, R. R., Zhang, Y., Liu, D., & Wei, F. (2019) · Science China Life Sciences · doi:10.1007/s11427-018-9388-9 · Cited by 63 · see citing works
Sexually mature European eels (Anguilla anguilla L.) stimulate gonadal development of neighbouring males: possible involvement of chemical communication.
Huertas, M., Scott, A., Hubbard, P., Canário, A., & Cerdà, J. (2006) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2006.01.017 · Cited by 62 · see citing works
“The presence of pheromones has been described in invertebrates and vertebrates (Brennan and Keverne, 2004; Kikuyama et al., 2002; Stacey, 2003; Sorensen and Stacey, 2004; Tillman et al., 1999), but in teleosts, although a wide variety of chemicals have been proposed to function as pheromones, only for certain gonadal…”
Background
Significance of inoculation density and carbon source on the mycelial growth and Tuber polysaccharides production by submerged fermentation of Chinese truffle Tuber sinense
Ya-jie Tang, A., Zhu, L., Li, D.-S., Mi, Z., & Li, H. (2008) · Process Biochemistry · doi:10.1016/j.procbio.2008.01.021 · Cited by 59 · see citing works
Male quality and conspecific scent preferences in the house finch, Carpodacus mexicanus
Amo, L., López‐Rull, I., Pagán, I., & Garcı́a, C. M. (2012) · Animal Behaviour · doi:10.1016/j.anbehav.2012.09.021 · Cited by 54 · see citing works
Comparative Anatomy and Physiology of Chemical Senses in Aquatic Mammals
Pihlström, H. (2008) · University of California Press eBooks · doi:10.1525/california/9780520252783.003.0007 · Cited by 54 · see citing works
Divergence of odorant signals within and between the two European subspecies of the house mouse
Smadja, C. M., & Ganem, G. (2007) · Behavioral Ecology · doi:10.1093/beheco/arm127 · Cited by 53 · see citing works
“1976; Pillay et al. 1995; Theiler and Blanco 1996), and to our knowledge, no study has investigated specifically geographical patterns of odorant signal divergence, possibly because the chemical characteristics of such signals are difficult to analyze (Novotny 2003; Todrank and Heth 2003; Brennan and Keverne 2004; Hur…”
Pyrazine Analogues Are Active Components of Wolf Urine That Induce Avoidance and Freezing Behaviours in Mice
Osada, K., Kurihara, K., Izumi, H., & Kashiwayanagi, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061753 · Cited by 51 · see citing works
“The rodent vomeronasal system plays a crucial role in mediating pheromone-evoked social and sexual behaviours [41].”
Background
Contrasting responses within a single neuron class enable sex-specific attraction in Caenorhabditis elegans
Narayan, A., Venkatachalam, V., Durak, O., Reilly, D. K., Bose, N., Schroeder, F. C., Samuel, A. D. T., Srinivasan, J., & Sternberg, P. W. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1600786113 · Cited by 51 · see citing works
“Proc Natl Acad Sci USA 94(7):3384–3387.”
BackgroundInfluential
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 50 · see citing works
Sex and the nose: human pheromonal responses
Bhutta, M. (2007) · Journal of the Royal Society of Medicine · doi:10.1177/014107680710000612 · Cited by 48 · see citing works
The TRPC2 ion channel and pheromone sensing in the accessory olfactory system
Zufall, F. (2005) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-005-1028-8 · Cited by 45 · see citing works
“comparison of the two studies (McCarthy and Auger 2002; Keverne 2002; Brennan and Keverne 2004 ).”
BackgroundResult
Patch-Clamp Analysis of Gene-Targeted Vomeronasal Neurons Expressing a Defined V1r or V2r Receptor: Ionic Mechanisms Underlying Persistent Firing
Ukhanov, K., Leinders‐Zufall, T., & Zufall, F. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00642.2007 · Cited by 45 · see citing works
Comparative Analysis of Volatile Constituents from Mice and their Urine
Röck, F., Mueller, S., Weimar, U., Rammensee, H., & Overath, P. (2006) · Journal of Chemical Ecology · doi:10.1007/s10886-006-9091-2 · Cited by 44 · see citing works
“These compounds are perceived either through the main or the accessory olfactory organ (reviewed in Brennan and Keverne, 2004; Stowers and Marton, 2005).”
Background
1-Iodo-2methylundecane, a putative estrus-specific urinary chemo-signal of female mouse (Mus musculus)
Achiraman, S., & Archunan, G. (2006) · Theriogenology · doi:10.1016/j.theriogenology.2006.05.010 · Cited by 43 · see citing works
“Chemical olfaction is vital for inter-individual communication among the same species for several functions including reproductive behaviour, such as, sexual attraction [1–4], interference with puberty, estrus cycle and pregnancy [5,6], as well as social behaviour like territorial marking [7,8], individual identificat…”
Background
Cladistic Analysis of Olfactory and Vomeronasal Systems
Úbeda‐Bañón, I., Pró-Sistiaga, P., Mohedano‐Moriano, A., Saiz‐Sánchez, D., de la Rosa‐Prieto, C., Gutiérrez‐Castellanos, N., Lanuza, E., Martínez‐Garciá, F., & Martı́nez-Marcos, A. (2011) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2011.00003 · Cited by 43 · see citing works
“neurons to higher processing centers and, ultimately, to behavior (Buck, 1995, 1996, 2000, 2004; Mombaerts, 1996, 1999a,b, 2004; Mombaerts et al., 1996; Dulac, 1997, 2000; Dulac and Torello, 2003; Brennan and Keverne, 2004; Brennan and Zufall, 2006; Dulac and Wagner, 2006; Cleland, 2010).”
Proteomic Analysis of Pig (Sus scrofa) Olfactory Soluble Proteome Reveals O-Linked-N-Acetylglucosaminylation of Secreted Odorant-Binding Proteins
Meillour, P. N., Vercoutter‐Edouart, A., Hilliou, F., Danvic, C. L., & Lévy, F. (2014) · Frontiers in Endocrinology · doi:10.3389/fendo.2014.00202 · Cited by 41 · see citing works
“Contrary to OBP isoforms of short size, VEG isoforms of short size are never labeled by RL2, suggesting that the modification occurs on the N-terminal part that is missing in these forms (peptide [1–16]).”
Background
Chemosensory Selectivity of Output Neurons Innervating an Identified, Sexually Isomorphic Olfactory Glomerulus
Reisenman, C. E., Christensen, T. A., & Hildebrand, J. G. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1314-05.2005 · Cited by 41 · see citing works
“The second subsystem, analogous to the “accessory” OB of many vertebrates (for review, see Brennan and Keverne, 2004), comprises three sexually dimorphic glomeruli (Rospars and Hildebrand, 1992).”
Background
The scent of wolves: pyrazine analogs induce avoidance and vigilance behaviors in prey
Osada, K., Miyazono, S., & Kashiwayanagi, M. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00363 · Cited by 39 · see citing works
“In addition to the primary olfactory system, most mammals have a vomeronasal system; this system contributes to the detection of certain conspecific pheromones, and it also perceives common volatile odorants (Trinh and Storm, 2003; Brennan and Keverne, 2004).”
Background
Co-evolution of a primordial peptide-presentation system and cellular immunity
Boehm, T. L. J. (2006) · Nature reviews. Immunology · doi:10.1038/nri1749 · Cited by 38 · see citing works
“Previous work had shown that the Bruce effect depends on an intact vomeronasal organ that forms part of the olfactory system in mic”
Background
The Microevolution of V1r Vomeronasal Receptor Genes in Mice
Park, S. H., Podlaha, O., Grus, W. E., & Zhang, J. (2011) · Genome Biology and Evolution · doi:10.1093/gbe/evr039 · Cited by 37 · see citing works
“In the genome of the laboratory mouse, ª The Author(s) 2011.”
Background
Aluminum trichloride-induced hippocampal inflammatory lesions are associated with IL-1β-activated IL-1 signaling pathway in developing rats
Zhang, H., Wang, P., Yu, H., Yu, K., Cao, Z., Xu, F., Yang, X., Song, M., & Li, Y. (2018) · Chemosphere · doi:10.1016/j.chemosphere.2018.03.162 · Cited by 36 · see citing works
Electrophysiological Properties and Modeling of Murine Vomeronasal Sensory Neurons in Acute Slice Preparations
Shimazaki, R. (2006) · Chemical Senses · doi:10.1093/chemse/bjj047 · Cited by 37 · see citing works
“…in the brain (for reviews on the vomeronasal system see Døving and Trotier, 1998; Jacobson et al., 1998; Keverne, 2002; Zufall et al., 2002, 2005; Dulac and Torello, 2003; Halpern and Martinez-Marcos, 2003; Rodriguez, 2003, 2004; Brennan and Keverne, 2004; Luo and Katz, 2004; Bigiani et al., 2005).”
Background
Biomarkers of fitness and welfare in dairy animals: healthy living
de Almeida, A. D., Zachut, M., Hernández-Castellano, L., Šperanda, M., Gabai, G., & Mobasheri, A. (2019) · Journal of Dairy Research · doi:10.1017/s0022029919000803 · Cited by 29 · see citing works
Natural ligands of hamster aphrodisin.
Briand, L., Blon, F., Trotier, D., & Pernollet, J. (2004) · Chemical Sensors · doi:10.1093/chemse/bjh044 · Cited by 38 · see citing works
“In many species, in contrast with the large number of well-documented sex attractants in insects, mammal pheromones are still poorly identified chemical cues (Dulac and Torello, 2003; Schaal et al., 2003; Brennan and Keverne, 2004).”
Background
Volatile female odors activate the accessory olfactory system of male mice without physical contact
Muroi, Y., Ishii, T., Komori, S., Kitamura, N., & Nishimura, M. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.04.026 · Cited by 35 · see citing works
“proteins act as transporters and reservoirs of volatile pheromones ( Brennan and Keverne, 2004 ).”
Background
Both olfactory epithelial and vomeronasal inputs are essential for activation of the medial amygdala and preoptic neurons of male rats
Dhungel, S., Masaoka, M., Rai, D., Kondo, Y., & Sakuma, Y. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.09.051 · Cited by 32 · see citing works
“VNO and OE inputs may complement each other (Brennan and Keverne, 2004; Brennan and Zufall, 2006).”
Background
α1A‐Adrenergic regulation of inhibition in the olfactory bulb
Zimnik, N. C., Treadway, T., Smith, R. S., & Araneda, R. C. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.248591 · Cited by 31 · see citing works
“…a region involved in the processing of chemosignals that trigger aggressive and reproductive behaviours, noradrenaline (NA) is thought to promote synaptic changes that underlie a female mouse’s ability to learn a stud’s odour during mating, also known as the Bruce effect (Brennan & Keverne, 2004).”
Background
Asymmetrical cache pilfering between yellow pine chipmunks and golden-mantled ground squirrels
Wall, S. B. V., Enders, M. S., & Waitman, B. A. (2009) · Animal Behaviour · doi:10.1016/j.anbehav.2009.05.030 · Cited by 31 · see citing works
Chapter 8 Neurobiology of Maternal Behavior in Sheep
Lévy, F., & Keller, M. (2008) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)00008-9 · Cited by 31 · see citing works
The vomeronasal system in mice: From the nose to the hypothalamus- and back!
Boehm, U. (2006) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2006.04.013 · Cited by 31 · see citing works
Heterogeneities of size and sexual dimorphism between the subdomains of the lateral-innervated accessory olfactory bulb (AOB) of Octodon degus (Rodentia: Hystricognathi)
Suárez, R., & Mpodozis, J. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.11.009 · Cited by 31 · see citing works
Genomic Imprinting and the Evolution of Sex Differences in Mammalian Reproductive Strategies
Keverne, E. B. (2007) · Advances in genetics · doi:10.1016/s0065-2660(07)59008-5 · Cited by 30 · see citing works
Self-citation
Factors That Can Influence Animal Research
Baker, D. G., & Lipman, N. S. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-409527-4.00033-x · Cited by 30 · see citing works
Pregnancy block by MHC class I peptides is mediatedviathe production of inositol 1,4,5-trisphosphate in the mouse vomeronasal organ
Thompson, R. N., McMillon, R., Napier, A., & Wekesa, K. S. (2007) · Journal of Experimental Biology · doi:10.1242/jeb.02753 · Cited by 29 · see citing works
“Clear phenotypic discrepancies have been observed between genetically modified mice and those with surgical VNO lesions (McCarthy and Auger, 2002; Brennan and Keverne, 2004; Pankevich et al., 2004).”
Background
Involvement of the oxytocin gene in the recognition and avoidance of parasitized males by female mice
Kavaliers, M., Choleris, E., Ågmo, A., Muglia, L. J., Ogawa, S., & Pfaff, D. W. (2005) · Animal Behaviour · doi:10.1016/j.anbehav.2004.12.016 · Cited by 28 · see citing works
Induction of c-Fos Expression in Mouse Vomeronasal Neurons by Sex-specific Non-volatile Pheromone(s)
Kimoto, H. (2005) · Chemical Senses · doi:10.1093/chemse/bjh156 · Cited by 28 · see citing works
“Since numerous studies have described that urine or urine-derived compounds cause several pheromonal effects including male–male aggression, puberty acceleration and pregnancy block (Dulac and Torello, 2003; Brennan and Keverne, 2004), our observation that the stimulant(s) is non-volatile and not urine-originated is l…”
Background
Dynamic evolution of V1R putative pheromone receptors between Mus musculus and Mus spretus
Kurzweil, V. C., Getman, M., Program, N. C. S., Green, E. D., & Lane, R. P. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-74 · Cited by 25 · see citing works
“The vomeronasal organ (VNO) of terrestrial vertebrates is responsible for pheromonal responses that evoke social and reproductive behaviors, including male territorial aggression, sexual preference, and sexual maturity (reviewed in [1]).”
Background
Chemosensory cues affect amygdaloid neurogenesis and alter behaviors in the socially monogamous prairie vole
Liu, Y., Lieberwirth, C., Jia, X., Curtis, J. T., Meredith, M. J., & Wang, Z. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12531 · Cited by 25 · see citing works
“Although there are various definitions, pheromones are commonly defined as chemosensory stimuli conveying information among conspecifics (Dulac & Torello, 2003; Brennan & Keverne, 2004).”
Background
Odor Perception and the Variability in Natural Odor Scenes
Wright, G. A., & Thomson, M. G. A. (2005) · Recent advances in phytochemistry · doi:10.1016/s0079-9920(05)80009-7 · Cited by 25 · see citing works
“Pheromones are often produced in specific glandular tissues specialized for their production,(24,25) but they may also arise from other scent sources such as body tissues.(26) Volatile compounds, such as ethylene and methyl jasmonate, are produced by plants during herbivorous attack and have been shown to act as signa…”
Background

Authors: Brennan, P. A., & Keverne, E. B.
Affiliations: University of Cambridge (GB)
ORCID: Brennan, Peter A.
Venue: Current Biology
Publisher: Elsevier BV
Published: 2004-01
Volume: 14
Issue: 2
Pages: R81-R89
ISSN: 0960-9822 (ISSN-L)
DOI: 10.1016/j.cub.2003.12.052
OpenAlex: W2110523906
Semantic Scholar: e0cc580358f9277e8f24797630d7e7ff00834142
Cited by: 236
References: 77
Citations by year: 2026: 2 · 2025: 3 · 2024: 9 · 2023: 4 · 2022: 5 · 2021: 1 · 2020: 5 · 2019: 8 · 2018: 11 · 2017: 5 · 2016: 6 · 2015: 7 · 2014: 11 · 2013: 7 · 2012: 19
FWCI: 2.52
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 3485 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Current Biology (publishedVersion)
PubMed (publishedVersion)
Funders: Medical Research Council
Biotechnology and Biological Sciences Research Council
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 system, vomeronasal receptors, olfactory receptors, chemosensory communication, vomeronasal organ, sex pheromone, genetic identity, chemosignals, olfactory system
MeSH terms: Afferent Pathways, Animals, Animal Communication, Chemoreceptor Cells, Mammals, Olfactory Bulb, Pheromones, Sex Factors, Smell, Vomeronasal Organ

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Something in the Air? New Insights into Mammalian Pheromones

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