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Encoding Pheromonal Signals in the Accessory Olfactory Bulb of Behaving Mice
Abstract
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.
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“This organization suggests that an important transformation of sensory information occurs in the AOB, from a segregated sampling system in the VNO to more integrated codes in the AOB (Luo et al., 2003; Meeks et al., 2010).”
From Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice (2017) · cites this paper as Luo et al., 2003
In the citing paper
“Intriguingly, selective inhibition also shapes social discrimination in the AOB (Luo et al., 2003; Meeks et al., 2010).”
From Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice (2017) · cites this paper as Luo et al., 2003
Citations
Cites
Combinatorial Receptor Codes for Odors
Malnic, B., Hirono, J., Sato, T., & Buck, L. B. (1999) · Cell · doi:10.1016/s0092-8674(00)80581-4 · Cited by 2,302
Visualizing an Olfactory Sensory Map
Mombaerts, P., Wang, F., Dulac, C. G., Chao, S. K., Nemes, A., Mendelsohn, M. M., Edmondson, J., & Axel, R. (1996) · Cell · doi:10.1016/s0092-8674(00)81387-2 · Cited by 1,992
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
Loss 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
An Exteroceptive Block to Pregnancy in the Mouse
Bruce, H. M. (1959) · Nature · doi:10.1038/184105a0 · Cited by 746
The Organization and Function of the Vomeronasal System
Halpern, M. (1987) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.10.030187.001545 · Cited by 732
Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb.
Yokoi, M., Mori, K., & Nakanishi, S. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.8.3371 · Cited by 614
Individual recognition in mice mediated by major urinary proteins
Hurst, J. L., Payne, C. E., Nevison, C. M., Marie, A. D., Humphries, R. E., Robertson, D. H. L., Cavaggioni, A., & Beynon, R. J. (2001) · Nature · doi:10.1038/414631a · Cited by 605
A New Multigene Family of Putative Pheromone Receptors
Ryba, N. J. P., & Tirindelli, R. (1997) · Neuron · doi:10.1016/s0896-6273(00)80946-0 · Cited by 598
Sparse Population Coding of Faces in the Inferotemporal Cortex
Young, M. P., & Yamane, S. (1992) · Science · doi:10.1126/science.1598577 · Cited by 595
Ultrasensitive 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
Altered sexual and social behaviors in trp2 mutant mice
Leypold, B. G., Yu, C., Leinders‐Zufall, T., Kim, M. M., Zufall, F., & Axel, R. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.082127599 · Cited by 572
Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system
Rodriguez, I., Feinstein, P., & Mombaerts, P. (1999) · Cell · doi:10.1016/s0092-8674(00)80730-8 · Cited by 402
Pheromone binding to two rodent urinary proteins revealed by X-ray crystallography
Böcskei, Z., Groom, C. R., Flower, D. R., Wright, C. E., Phillips, S. E. V., Cavaggioni, A., Findlay, J. B. C., & North, A. C. T. (1992) · Nature · doi:10.1038/360186a0 · Cited by 361
Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes
Punta, K. D., Leinders‐Zufall, T., Rodríguez, I., Jukam, D., Wysocki, C. J., Ogawa, S., Zufall, F., & Mombaerts, P. (2002) · Nature · doi:10.1038/nature00955 · Cited by 357
Vomeronasal Organ: Critical Role in Mediating Sexual Behavior of the Male Hamster
Powers, J. B., & Winans, S. S. (1975) · Science · doi:10.1126/science.1145182 · Cited by 351
NEURAL MECHANISMS OF MAMMALIAN OLFACTORY LEARNING
Brennan, P., & Keverne, E. B. (1997) · Progress in Neurobiology · doi:10.1016/s0301-0082(96)00069-x · Cited by 337
Membrane and synaptic properties of identified neurons in the olfactory bulb
Mori, K. (1987) · Progress in Neurobiology · doi:10.1016/0301-0082(87)90024-4 · Cited by 320
Odor Response Properties of Rat Olfactory Receptor Neurons
Duchamp‐Viret, P., Chaput, M. A., & Duchamp, A. (1999) · Science · doi:10.1126/science.284.5423.2171 · Cited by 303
Berghard, A., & Buck, L. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-03-00909.1996 · Cited by 298
Olfactory Bulb Removal Eliminates Mating Behavior in the Male Golden Hamster
Murphy, M. R., & Schneider, G. E. (1970) · Science · doi:10.1126/science.167.3916.302 · Cited by 297
A map of pheromone receptor activation in the mammalian brain
Belluscio, L., Koentges, G., Axel, R., & Dulac, C. (1999) · Cell · doi:10.1016/s0092-8674(00)80731-x · Cited by 293
Mori, K., Kishi, K., & Ojima, H. (1983) · The Journal of Comparative Neurology · doi:10.1002/cne.902190308 · Cited by 286
Medial Nucleus of the Amygdala Mediates Chemosensory Control of Male Hamster Sexual Behavior
Lehman, M. N., Winans, S. S., & Powers, J. B. (1980) · Science · doi:10.1126/science.7423209 · Cited by 282
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
Jia, C., & Halpern, M. (1996) · Brain Research · doi:10.1016/0006-8993(96)00110-2 · Cited by 267
Efferent control of stimulus access to the hamster vomeronasal organ.
Meredith, M. J., & O’Connell, R. J. (1979) · The Journal of Physiology · doi:10.1113/jphysiol.1979.sp012620 · Cited by 260
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
Analysis of Relations between NMDA Receptors and GABA Release at Olfactory Bulb Reciprocal Synapses
Chen, W. R., Xiong, W., & Shepherd, G. M. (2000) · Neuron · doi:10.1016/s0896-6273(00)81065-x · Cited by 235
Scott, J. W., McBride, R. L., & Schneider, S. P. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901940304 · Cited by 234
Access of Urinary Nonvolatiles to the Mammalian Vomeronasal Organ
Wysocki, C. J., Wellington, J. L., & Beauchamp, G. K. (1980) · Science · doi:10.1126/science.7352288 · Cited by 231
Odorants may arouse instinctive behaviours
Sam, M., Vora, S., Malnic, B., Ma, W., Novotný, M. V., & Buck, L. B. (2001) · Nature · doi:10.1038/35084137 · Cited by 221
Mammalian scent gland marking and social behavior.
Thiessen, D. D., & Rice, M. (1976) · Psychological bulletin · doi:10.1037/0033-2909.83.4.505 · Cited by 213
Response Correlation Maps of Neurons in the Mammalian Olfactory Bulb
Luo, M., & Katz, L. C. (2001) · Neuron · doi:10.1016/s0896-6273(01)00537-2 · Cited by 191
Punta, K. D., Puché, A. C., Adams, N. C., Rodríguez, I., & Mombaerts, P. (2002) · Neuron · doi:10.1016/s0896-6273(02)00904-2 · Cited by 182
Miniature motorized microdrive and commutator system for chronic neural recording in small animals
Fee, M. S., & Leonardo, A. M. (2001) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(01)00426-5 · Cited by 181
Dendrodendritic Inhibition: Demonstration with Intracellular Recording
Jahr, C. E., & Nicoll, R. A. (1980) · Science · doi:10.1126/science.7361098 · Cited by 166
Chronic recording of vomeronasal pump activation in awake behaving hamsters
Meredith, M. J. (1994) · Physiology & Behavior · doi:10.1016/0031-9384(94)90205-4 · Cited by 143
Rasmussen, L. E. L., & Schulte, B. A. (1998) · Animal Reproduction Science · doi:10.1016/s0378-4320(98)00124-9 · Cited by 138
Sexual behavior in peripherally anosmic male hamsters
Powers, J. B., & Winans, S. S. (1973) · Physiology & Behavior · doi:10.1016/0031-9384(73)90323-5 · Cited by 99
Imamura, K., Mori, K., Fujita, S. C., & Obata, K. (1985) · Brain Research · doi:10.1016/0006-8993(85)91050-9 · Cited by 81
Kumar, A., Dudley, C. A., & Moss, R. L. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-20-j0003.1999 · Cited by 68
Synaptic Organization and Neurotransmitters in the Rat Accessory Olfactory Bulb
Jia, C., Chen, W. R., & Shepherd, G. M. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.81.1.345 · Cited by 68
Lazar, J., Greenwood, D. R., Rasmussen, L. E. L., & Prestwich, G. D. (2002) · Biochemistry · doi:10.1021/bi0256734 · Cited by 64
Laminar distribution of pheromone‐receptive neurons in rat vomeronasal epithelium
Inamura, K., Matsumoto, Y. M., Kashiwayanagi, M., & Kurihara, K. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.0731s.x · Cited by 57
Reinhardt, W., MacLeod, N. K., Ladewig, J., & Ellendorff, F. (1983) · Neuroscience · doi:10.1016/0306-4522(83)90087-8 · Cited by 27
Booth, W. D. (1972) · Journal of Endocrinology · doi:10.1677/joe.0.0550119 · Cited by 25
Research works printed but not linked: 1
- E. S. Albone Mammalian Semiochemistry: The Investigation of Chemical Signals Between Mammals (Wiley New York 1984).
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“, its neurons respond to molecules other than pheromones, but it remains to be established whether these molecules are physiologically relevant stimul”
BackgroundMolecular 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
“How is pheromonal information encoded in the mitral cells? Using an array of electrodes implanted in the mouse AOB, Luo and colleagues recently recorded mitral cell activity in freely moving mic”
Structure and function of the vomeronasal system: an update
Halpern, M. (2003) · Progress in Neurobiology · doi:10.1016/s0301-0082(03)00103-5 · Cited by 639
MHC Class I Peptides as Chemosensory Signals in the Vomeronasal Organ
Leinders‐Zufall, T., Brennan, P., Widmayer, P., Prashanth Chandramani, S., Maul‐Pavicic, A., Jäger, M., Li, X.-H., Breer, H., Zufall, F., & Boehm, T. L. J. (2004) · Science · doi:10.1126/science.1102818 · Cited by 608
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Chen, P., & Hong, W. (2018) · Neuron · doi:10.1016/j.neuron.2018.02.026 · Cited by 527
“…initial investigation of a conspecific and is maintained for a short period of time after the conspecific has been removed (Hashikawa et al., 2016; Luo et al., 2003), suggesting that activity in the AOB changes with duration of investigation, and is not strictly correlated with the presence of…”
Metadata
- Authors
- Luo, M., Fee, M. S., & Katz, L. C.
- Affiliations
- Howard Hughes Medical Institute (US)
- Alcatel-Lucent (France) (FR)
- Corresponding author
- Luo, Minmin
- Venue
- Science
- Published
- 2003-02-21
- Volume
- 299
- Issue
- 5610
- Pages
- 1196-1201
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2040886375
- Cited by
- 365
- References
- 47
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 15 · 2023: 9 · 2022: 7 · 2021: 10 · 2020: 9 · 2019: 6 · 2018: 16 · 2017: 23 · 2016: 15 · 2015: 18 · 2014: 15 · 2013: 15 · 2012: 12
- FWCI
- 11.36
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- pheromones, vomeronasal system, accessory olfactory bulb, single-unit recording, social communication, reproductive status, sex-specific responses, genetic strain differences, natural behavior
- MeSH terms
- Action Potentials, Animals, Anal Canal, Behavior, Animal, Cues, Electrodes, Implanted, Face, Female, Genitalia, Male, Mice, Inbred BALB C, Mice, Inbred CBA, Mice, Inbred C57BL, Microelectrodes, Mouth, Neural Inhibition, Neurons, Neurons, Afferent, Odorants, Olfactory Bulb, Olfactory Pathways, Pheromones, Sex Characteristics, Smell, Species Specificity, Vomeronasal Organ, Mice
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