Cited by 365Olfactory and Sensory Function StudiesNeuroendocrine regulation and behaviorNeurobiology and Insect Physiology Research

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Encoding Pheromonal Signals in the Accessory Olfactory Bulb of Behaving Mice

Luo, Minmin, Fee, Michale S., Katz, Lawrence C.·2003·Science

DOI 10.1126/science.1082133

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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.

Integrity signals

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Crossref · 10.1126/science.1082133

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“particular, rely on pheromonal cues in order to identify their conspecifics (Luo et al., 2003), and hence a crucial role for pheromones has been postulated during mate choice in rats (Beach, 1942; Heimer and Larsson, 1967; Bermant and Taylor, 1969) and mice (Rowe and Edwards, 1972; Rowe and Smith, 1972).”
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BackgroundInfluential
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BackgroundResult
Peripubertal exposure to male odors influences female puberty and adult expression of male-directed odor preference in mice
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Background
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Background
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Background
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Background
α2-Adrenergic receptor activation promotes long-term potentiation at excitatory synapses in the mouse accessory olfactory bulbPreprint
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“In contrast, 10-Hz stimulation, which is within the physiological range of natural neuronal activity (Luo et al. 2003; Leszkowicz et al. 2012), effectively induced LTP.”
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Background
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Background
TRPC2 and the Molecular Biology of Pheromone Detection in Mammals
MD, P. D. (2006) · CRC Press eBooks · doi:10.1201/9781420005844-9 · Cited by 9
A Cellular Mechanism for Main and Accessory Olfactory Integration at the Medial Amygdala
Guthman, E. M., & Vera, J. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.4304-15.2016 · Cited by 9
“The time course of activation of AOS neurons under naturalistic conditions is characterized by a slow increase in firing frequency (in the range of seconds) and a sustained response, without adaptation (Luo et al., 2003).”
Background
Decreased anxiety-like behavior and locomotor/exploratory activity, and modulation in hypothalamus, hippocampus, and frontal cortex redox profile in sexually receptive female rats after short-term exposure to male chemical cues
Behr, G. A., da Motta, L. L., de Oliveira, M. R., Oliveira, M. W. S., Hoff, M. L. M., Silvestrin, R. B., & Moreira, J. C. F. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.11.047 · Cited by 9
Stability and flexibility of the message carried by semiochemical stimuli, as revealed by devaluation of carbon disulfide followed by social transmission of food preference.
Maier, J. X., Blankenship, M. L., Barry, N. C., Richards, S. E. V., & Katz, D. B. (2014) · Behavioral Neuroscience · doi:10.1037/bne0000002 · Cited by 8
Synchronous Infra-Slow Oscillations Organize Ensembles of Accessory Olfactory Bulb Projection Neurons into Distinct Microcircuits
Tsitoura, C., Malinowski, S. T., Mohrhardt, J., Degen, R., DiBenedictis, B. T., Gao, Y., Watznauer, K., Gerhold, K., Nagel, M., Weber, M., et al. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.2925-19.2020 · Cited by 8
“By contrast, rather sparse and Poisson-like discharge has been recorded electrophysiologically from both anesthetized (Hendrickson et al., 2008; Ben-Shaul et al., 2010) and awake behaving mice (Luo et al., 2003).”
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A Nose by Any Other Name (Should Smell as Sweetly)
Choi, G. B., & Anderson, D. J. (2005) · Cell · doi:10.1016/j.cell.2005.11.004 · Cited by 8
“In support of the second explanation, Mandiyan et al. (2005) point out that detection of nonvolatile pheromones by the VNO requires sniffing behavior (Luo et al., 2003), which is strongly reduced in MOE-defective mice.”
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From Reductionism Toward Integration: Understanding How Social Behavior Emerges From Integrated Circuits
Dickinson, S. Y., Kelly, D. A., Padilla, S. L., & Bergan, J. F. (2022) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2022.862437 · Cited by 7
Got milk? A pheromonal message for newborn rabbits
Luo, M. (2003) · BioEssays · doi:10.1002/bies.10391 · Cited by 7
Firing Properties of Accessory Olfactory Bulb Mitral/Tufted Cells in Response to Urine Delivered to the Vomeronasal Organ of Gray Short-Tailed Opossums
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“Our results are similar to the results by Luo et al. (2003) in their recording of excitatory and inhibitory responses from the AOB of behaving mice during natural investigative behaviors.”
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Hypothalamic representation of the imminence of predator threat detected by the vomeronasal organ in micePreprint
Nguyen, Q. A. T., Rocha, A., Chhor, R., Yamashita, Y., Stadler, C., Pontrello, C. G., Yang, H., & Haga‐Yamanaka, S. (2023) · eLife · doi:10.7554/elife.92982 · Cited by 6
“Ethologically relevant chemical cues from different animals, such as pheromones and predator cues, are sucked up into the VNO and activate VNO sensory neurons when animals contact the chemical source ( Luo et al., 2003 ).”
Background
Investigating social communication in mice: A two‐intruders test approach
Morozova, M. V., Boldyreva, L. V., Borisova, M. A., & Kozhevnikova, E. N. (2024) · Journal of Neuroscience Research · doi:10.1002/jnr.25365 · Cited by 6
“…responsible for the basic recognition as it detects volatile odor-ants, whereas AOS detects urinary proteins and is involved in close interactions and is believed to be most critical for the formation and expression of social behaviors (Arakawa et al., 2007; Chamero et al., 2007; Luo et al., 2003).”
Characteristic Response to Chemosensory Signals in GABAergic Cells of Medial Amygdala Is Not Driven by Main Olfactory Input
Westberry, J. M., & Meredith, M. J. (2016) · Chemical Senses · doi:10.1093/chemse/bjw096 · Cited by 6
Assessment of Biostimulation Methods Based on Chemical Communication in Female Doe Reproduction
Villamayor, P., Gullón, J., Yáñez, U., Sánchez, M., Sánchez-Quinteiro, P., Martínez, P., & Quintela, L. (2022) · Animals · doi:10.3390/ani12030308 · Cited by 5
“, lacrimal, mammary, mentonian, Harderian) [9,17,18].”
Accessory Olfactory System
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Associative learning is necessary for airborne pheromones to activate sexual arousal-linked brain areas of female rats
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“In rodents, VOC pheromone detection and sexual behavioral outputs involve the olfactory (main olfactory) system (MOS) and vomeronasal (accessory olfactory) system (AOS) (Leinders-Zufall et al. 2000; Luo et al. 2003; Xu et al. 2005; Brennan and Zufall 2006;Wang et al. 2006; Kang et al. 2009).”
Background
Similar rate of information transfer on stimulus intensity in accessory and main olfactory bulb output neurons
Noguchi, T., Sasajima, H., Miyazono, S., & Kashiwayanagi, M. (2014) · Neuroscience Letters · doi:10.1016/j.neulet.2014.05.058 · Cited by 4
“The firing frequency of MTAOB in vivo gradually increased until reaching a peak after ∼20 s following the initiation of physical contact with the stimulating animal [3].”
Removal of the vomeronasal organ impairs predator odor detection in female golden hamsters
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“, 2005), and an increasing body of literature suggests that the main olfactory and vomeronasal systems combine to detect pheromonal compounds in mice (Sam et al., 2001; Luo et al., 2003; Lin et al., 2005; Xu et al., 2005; Spehr et al., 2006).”
Background
Hypothalamic representation of the imminence of predator threat detected by the vomeronasal organ in mice
Nguyen, Q. A. T., Rocha, A., Chhor, R., Yamashita, Y., Stadler, C., Pontrello, C. G., Yang, H., & Haga‐Yamanaka, S. (2024) · eLife · doi:10.7554/elife.92982.4 · Cited by 4
PHEROMONAL MODULATION OF REPRODUCTIVE FUNCTION IN MAMMALS
Keller, M., Bedos, M., Jouhanneau, M., Martini, M., Retana‐Márquez, S., & Delgadillo, J. A. (2011) · Tropical and Subtropical Agroecosystems · doi:10.56369/tsaes.1359 · Cited by 4
“Luo et al. (2003) have demonstrated, using electrophysiological recordings in behaving animals, that AOB cells are only activated when mice make direct physical contact with the odorant source (for example the ano-genital region of a conspecific), thus giving access to nonvolatile pheromones to the…”
The “scents” of ownership
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“Recent evidence from a study of laboratory mice investigating anaesthetized conspecifics suggests that scent ownership recognition may occur through the vomeronasal system ( Luo et al., 2003 ).”
Background
Memória de reconhecimento social em ratos
de Moura, P. J., & Xavier, G. F. (2010) · Psicologia USP · doi:10.1590/s0103-65642010000200008 · Cited by 4
Male chemosignals inhibit the neural responses of male mice to female chemosignals
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Marking, S., Krosnowski, K. A., Ogura, T., & Lin, W. (2017) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2017.00010 · Cited by 4
“…to the stimuli to facilitate vomeronasal sensing of semiochemicals, especially nonvolatile pheromones that require animals contact the stimuli physically with their nose (Luo et al., 2003; Keverne, 2004; Restrepo et al., 2004; Kang et al., 2009; Martel and Baum, 2009; Slotnick et al., 2010).”
BackgroundInfluential
Olfactory Subsystems
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Have Sexual Pheromones Their Own Reward System in the Brain of Female Mice?
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The Accessory Olfactory System Facilitates the Recovery of the Attraction to Familiar Volatile Female Odors in Male Mice
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TRPC2 and the Molecular Biology of Pheromone Detection in Mammals
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“The broad and variable patterns of MC tuning adds to a growing list of studies indicating that these cells support the encoding of the identity of a chemosignal-emitting animal (Luo et al., 2003; Hendrickson et al., 2008; Ben-Shaul et al., 2010; Tolokh et al., 2013).”
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MHC-Associated Chemosignals and Individual Identity
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“However, strain-specific responses of neurons in the accessory olfactory bulb were recorded during investigation of an anaesthetised animal, and were elicited equally effectively by investigation of the head and the anogenital area (Luo et al. 2003).”
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Application of fMRI in Olfactory Studies of Small Animals*
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Possible Mechanisms of the Influence of Oxytocin and Vasopressin on Perception and Memory of Odors and on Social Behavior
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Biostimulation methods based on chemical communication improve semen quality in male breeder rabbits
Villamayor, P. R., Yáñez, U., Gullón, J., Sánchez‐Quinteiro, P., Peña, A. I., González, J. J. B., Herradón, P. J. G., Martı́nez, P., & Arias, L. Á. Q. (2024) · Theriogenology · doi:10.1016/j.theriogenology.2024.09.016 · Cited by 2

Authors: Luo, M., Fee, M. S., & Katz, L. C.
Affiliations: Howard Hughes Medical Institute (US)
Alcatel-Lucent (France) (FR)
Corresponding author: Luo, Minmin
ORCID: Luo, Minmin
Fee, Michale S.
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2003-02-21
Volume: 299
Issue: 5610
Pages: 1196-1201
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.1082133
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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Encoding Pheromonal Signals in the Accessory Olfactory Bulb of Behaving Mice

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