A centrifugal pathway to the mouse accessory olfactory bulb from the medial amygdala conveys gender-specific volatile pheromonal signals

We previously found that female mice exhibited Fos responses in the accessory olfactory bulb (AOB) after exposure to volatile opposite‐sex, but not same‐sex, urinary odours. This effect was eliminated by lesioning the main olfactory epithelium, raising the possibility that the AOB receives informati...

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Published inThe European journal of neuroscience Vol. 29; no. 2; pp. 368 - 376
Main Authors Martel, Kristine L., Baum, Michael J.
Format Journal Article
LanguageEnglish
Published Oxford, UK Blackwell Publishing Ltd 01.01.2009
Subjects
Online AccessGet full text
ISSN0953-816X
1460-9568
1460-9568
DOI10.1111/j.1460-9568.2008.06564.x

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Abstract We previously found that female mice exhibited Fos responses in the accessory olfactory bulb (AOB) after exposure to volatile opposite‐sex, but not same‐sex, urinary odours. This effect was eliminated by lesioning the main olfactory epithelium, raising the possibility that the AOB receives information about gender via centrifugal inputs originating in the main olfactory system instead of from the vomeronasal organ. We asked which main olfactory forebrain targets send axonal projections to the AOB, and whether these input neurons express Fos in response to opposite‐sex urinary volatiles. Female mice received bilateral injections of the retrograde tracer cholera toxin B (CTB), into the AOB, and were exposed to either same‐ or opposite‐sex volatile urinary odours 1 week later. We found CTB‐labeled cell bodies in several forebrain sites including the bed nucleus of the accessory olfactory tract, the rostral portion of the medial amygdala (MeA) and the posteromedial cortical nucleus of the amygdala. A significant increase in the percentage of CTB/Fos co‐labeled cells was seen only in the MeA of female subjects exposed to male but not to female urinary volatiles. In Experiment 2, CTB‐injected females were later exposed to volatile odours from male mouse urine, food, or cat urine. Again, a significant increase in the percentage of CTB/Fos co‐labeled cells was seen in the MeA of females exposed to male mouse urinary volatiles but not to food or predator odours. Main olfactory–MeA–AOB signaling may motivate approach behaviour to opposite‐sex pheromonal signals that ensure successful reproduction.
AbstractList We previously found that female mice exhibited Fos responses in the accessory olfactory bulb (AOB) after exposure to volatile opposite-sex, but not same-sex, urinary odours. This effect was eliminated by lesioning the main olfactory epithelium, raising the possibility that the AOB receives information about gender via centrifugal inputs originating in the main olfactory system instead of from the vomeronasal organ. We asked which main olfactory forebrain targets send axonal projections to the AOB, and whether these input neurons express Fos in response to opposite-sex urinary volatiles. Female mice received bilateral injections of the retrograde tracer cholera toxin B (CTB), into the AOB, and were exposed to either same- or opposite-sex volatile urinary odours 1 week later. We found CTB-labeled cell bodies in several forebrain sites including the bed nucleus of the accessory olfactory tract, the rostral portion of the medial amygdala (MeA) and the posteromedial cortical nucleus of the amygdala. A significant increase in the percentage of CTB/Fos co-labeled cells was seen only in the MeA of female subjects exposed to male but not to female urinary volatiles. In Experiment 2, CTB-injected females were later exposed to volatile odours from male mouse urine, food, or cat urine. Again, a significant increase in the percentage of CTB/Fos co-labeled cells was seen in the MeA of females exposed to male mouse urinary volatiles but not to food or predator odours. Main olfactory-MeA-AOB signaling may motivate approach behaviour to opposite-sex pheromonal signals that ensure successful reproduction.
We previously found that female mice exhibited Fos responses in the accessory olfactory bulb (AOB) after exposure to volatile opposite-sex, but not same-sex, urinary odours. This effect was eliminated by lesioning the main olfactory epithelium, raising the possibility that the AOB receives information about gender via centrifugal inputs originating in the main olfactory system instead of from the vomeronasal organ. We asked which main olfactory forebrain targets send axonal projections to the AOB, and whether these input neurons express Fos in response to opposite-sex urinary volatiles. Female mice received bilateral injections of the retrograde tracer cholera toxin B (CTB), into the AOB, and were exposed to either same- or opposite-sex volatile urinary odours 1 week later. We found CTB-labeled cell bodies in several forebrain sites including the bed nucleus of the accessory olfactory tract, the rostral portion of the medial amygdala (MeA) and the posteromedial cortical nucleus of the amygdala. A significant increase in the percentage of CTB/Fos co-labeled cells was seen only in the MeA of female subjects exposed to male but not to female urinary volatiles. In Experiment 2, CTB-injected females were later exposed to volatile odours from male mouse urine, food, or cat urine. Again, a significant increase in the percentage of CTB/Fos co-labeled cells was seen in the MeA of females exposed to male mouse urinary volatiles but not to food or predator odours. Main olfactory-MeA-AOB signaling may motivate approach behaviour to opposite-sex pheromonal signals that ensure successful reproduction.We previously found that female mice exhibited Fos responses in the accessory olfactory bulb (AOB) after exposure to volatile opposite-sex, but not same-sex, urinary odours. This effect was eliminated by lesioning the main olfactory epithelium, raising the possibility that the AOB receives information about gender via centrifugal inputs originating in the main olfactory system instead of from the vomeronasal organ. We asked which main olfactory forebrain targets send axonal projections to the AOB, and whether these input neurons express Fos in response to opposite-sex urinary volatiles. Female mice received bilateral injections of the retrograde tracer cholera toxin B (CTB), into the AOB, and were exposed to either same- or opposite-sex volatile urinary odours 1 week later. We found CTB-labeled cell bodies in several forebrain sites including the bed nucleus of the accessory olfactory tract, the rostral portion of the medial amygdala (MeA) and the posteromedial cortical nucleus of the amygdala. A significant increase in the percentage of CTB/Fos co-labeled cells was seen only in the MeA of female subjects exposed to male but not to female urinary volatiles. In Experiment 2, CTB-injected females were later exposed to volatile odours from male mouse urine, food, or cat urine. Again, a significant increase in the percentage of CTB/Fos co-labeled cells was seen in the MeA of females exposed to male mouse urinary volatiles but not to food or predator odours. Main olfactory-MeA-AOB signaling may motivate approach behaviour to opposite-sex pheromonal signals that ensure successful reproduction.
We previously found that female mice exhibited Fos responses in the accessory olfactory bulb (AOB) after exposure to volatile opposite-, but not same-sex, urinary odours. This effect was eliminated by lesioning the main olfactory epithelium, raising the possibility that the AOB receives information about gender via centrifugal inputs originating in the main olfactory system instead of from the vomeronasal organ . We asked which main olfactory forebrain targets send axonal projections to the AOB, and whether these input neurons express Fos in response to opposite-sex urinary volatiles. Female mice received bilateral injections of the retrograde tracer, cholera toxin B (CTB), into the AOB, and were exposed to either same- or opposite-sex volatile urinary odours one week later. We found CTB- labeled cell bodies in several forebrain sites including the bed nucleus of the accessory olfactory tract, the rostral portion of the medial amygdala (MeA), and the posteromedial cortical nucleus of the amygdala. A significant increase in the percentage of CTB/Fos co-labeled cells was seen only in the MeA of female subjects exposed to male but not to female urinary volatiles. In Experiment 2, CTB-injected females were later exposed to volatile odours from male mouse urine, food, or cat urine. Again, a significant increase in the percentage of CTB/Fos co-labeled cells was seen in the MeA of females exposed to male mouse urinary volatiles but not to food or predator odours. Main olfactory - MeA -AOB signaling may motivate approach behaviour to opposite-sex pheromonal signals that ensure successful reproduction.
AbstractWe previously found that female mice exhibited Fos responses in the accessory olfactory bulb (AOB) after exposure to volatile opposite-sex, but not same-sex, urinary odours. This effect was eliminated by lesioning the main olfactory epithelium, raising the possibility that the AOB receives information about gender via centrifugal inputs originating in the main olfactory system instead of from the vomeronasal organ. We asked which main olfactory forebrain targets send axonal projections to the AOB, and whether these input neurons express Fos in response to opposite-sex urinary volatiles. Female mice received bilateral injections of the retrograde tracer cholera toxin B (CTB), into the AOB, and were exposed to either same- or opposite-sex volatile urinary odours 1week later. We found CTB-labeled cell bodies in several forebrain sites including the bed nucleus of the accessory olfactory tract, the rostral portion of the medial amygdala (MeA) and the posteromedial cortical nucleus of the amygdala. A significant increase in the percentage of CTB/Fos co-labeled cells was seen only in the MeA of female subjects exposed to male but not to female urinary volatiles. In Experiment2, CTB-injected females were later exposed to volatile odours from male mouse urine, food, or cat urine. Again, a significant increase in the percentage of CTB/Fos co-labeled cells was seen in the MeA of females exposed to male mouse urinary volatiles but not to food or predator odours. Main olfactory-MeA-AOB signaling may motivate approach behaviour to opposite-sex pheromonal signals that ensure successful reproduction.
Author Baum, Michael J.
Martel, Kristine L.
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  surname: Baum
  fullname: Baum, Michael J.
  organization: Department of Biology, Boston University, Boston, MA 02215, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/19077123$$D View this record in MEDLINE/PubMed
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Muroi, Y., Ishii, T., Komori, S., Kitamura, N. & Nishimura, M. (2006) Volatile female odors activate the accessory olfactory system of male mice without physical contact. Neuroscience, 141, 551-558.
Larriva-Sahd, J. (2008) The accessory olfactory bulb in the adult rat: a cytological study of its cell types, neuropil, neuronal modules, and interactions with the main olfactory system. J. Comp. Neurol., 510, 309-350.
Spehr, M., Kelliher, K.R., Li, X.H., Boehm, T., Leinders-Zufall, T. & Zufall, F. (2006) Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. J. Neurosci., 26, 1961-1970.
Keller, M., Douhard, Q., Baum, M.J. & Bakker, J. (2006a) Destruction of the main olfactory epithelium reduces female sexual behavior and olfactory investigation in female mice. Chem. Senses, 31, 315-323.
Shipley, M.T., Halloran, F.J. & De La Torre, J. (1985) Surprisingly rich projection from locus coeruleus to the olfactory bulb in the rat. Brain Res., 329, 294-299.
Kang, N., Baum, M.J. & Cherry, J.A. (2008) Opposite-Sex Volatile Pheromones Activate a Novel Main Olfactory Bulb-Medial Amygdala Projection and Downstream Forebrain Targets in Mice. Society for Neuroscience Annual Meeting, Washington DC, p. 866.24.
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Meredith, M., Marques, D.M., O'Connell, R.O. & Stern, F.L. (1980) Vomeronasal pump: significance for male hamster sexual behavior. Science, 207, 1224-1226.
Ma, D., Allen, N.D., Van Bergen, Y.C., Jones, C.M., Baum, M.J., Keverne, E.B. & Brennan, P.A. (2002) Selective ablation of olfactory receptor neurons without functional impairment of vomeronasal receptor neurons in OMP-ntr transgenic mice. Eur. J. Neurosci., 16, 2317-2323.
Martel, K.L. & Baum, M.J. (2007) Sexually dimorphic activation of the accessory, but not the main, olfactory bulb in mice by urinary volatiles. Eur. J. Neurosci., 26, 463-475.
Brennan, P.A. & Zufall, F. (2006) Pheromonal communication in vertebrates. Nature, 444, 308-315.
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Novotny, M.V. (2003) Pheromones, binding proteins and receptor responses in rodents. Biochem. Soc. Trans., 31, 117-122.
Pankevich, D.E., Baum, M.J. & Cherry, J.A. (2004) Olfactory sex discrimination persists, whereas the preference for urinary odorants from estrous females disappears in male mice after vomeronasal organ removal. J. Neurosci., 24, 9451-9457.
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Chess, A., Buck, L., Dowling, M.M., Axel, R. & Ngai, J. (1992) Molecular biology of smell: expression of the multigene family encoding putative odorant receptors. Cold Spring Harb. Symp. Quant. Biol., 57, 505-516.
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Schaefer, M.L., Young, D.A. & Restrepo, D. (2001) Olfactory fingerprints for major histocompatibility complex-determined body odors. J. Neurosci., 21, 2481-2487.
Lin, D.Y., Zhang, S.Z., Block, E. & Katz, L.C. (2005) Encoding social signals in the mouse main olfactory bulb. Nature, 434, 470-477.
Baum, M.J. & Keverne, E.B. (2002) Sex difference in attraction thresholds for volatile odors from male and estrous female mouse urine. Horm. Behav., 41, 213-219.
Keller, M., Pierman, S., Douhard, Q., Baum, M.J. & Bakker, J. (2006b) The vomeronasal organ is required for the expression of lordosis behaviour, but not sex discrimination in female mice. Eur. J. Neurosci., 23, 521-530.
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Kevetter, G.A. & Winans, S.S. (1981) Connections of the corticomedial amygdala in the golden hamster. I. Efferents of the "vomeronasal amygdala". J. Comp. Neurol., 197, 81-98.
Beauchamp, G.K., Martin, I.G., Wysocki, C.J. & Wellington, J.L. (1982) Chemoinvestigatory and sexual behavior of male guinea pigs following vomeronasal organ removal. Physiol. Behav., 29, 329-336.
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Snippet We previously found that female mice exhibited Fos responses in the accessory olfactory bulb (AOB) after exposure to volatile opposite‐sex, but not same‐sex,...
We previously found that female mice exhibited Fos responses in the accessory olfactory bulb (AOB) after exposure to volatile opposite-sex, but not same-sex,...
AbstractWe previously found that female mice exhibited Fos responses in the accessory olfactory bulb (AOB) after exposure to volatile opposite-sex, but not...
We previously found that female mice exhibited Fos responses in the accessory olfactory bulb (AOB) after exposure to volatile opposite-, but not same-sex,...
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SubjectTerms Amygdala - cytology
Amygdala - physiology
Animals
Brain Mapping
Cholera Toxin
Efferent Pathways - cytology
Efferent Pathways - physiology
Female
Fos
Male
Mice
Neurons - metabolism
Odorants
Olfactory Bulb - cytology
Olfactory Bulb - physiology
Olfactory Pathways - cytology
Olfactory Pathways - physiology
ovariectomy
pheromone
Proto-Oncogene Proteins c-fos - metabolism
retrograde
Sex Attractants - physiology
Sex Characteristics
Sexual Behavior, Animal - physiology
Signal Transduction - physiology
Smell - physiology
Staining and Labeling
volatile
Title A centrifugal pathway to the mouse accessory olfactory bulb from the medial amygdala conveys gender-specific volatile pheromonal signals
URI https://api.istex.fr/ark:/67375/WNG-THLPV3QH-P/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fj.1460-9568.2008.06564.x
https://www.ncbi.nlm.nih.gov/pubmed/19077123
https://www.proquest.com/docview/20334884
https://www.proquest.com/docview/66900956
https://pubmed.ncbi.nlm.nih.gov/PMC2754263
Volume 29
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