A labeled-line neural circuit for pheromone-mediated sexual behaviors in mice
Open accessAbstract
In mice, various instinctive behaviors can be triggered by olfactory input. Despite growing knowledge of the brain regions involved in such behaviors, the organization of the neural circuits that convert olfactory input into stereotyped behavioral output remains poorly understood. Here, we mapped the neural circuit responsible for enhancing sexual receptivity of female mice by a male pheromone, exocrine gland-secreting peptide 1 (ESP1). We revealed specific neural types and pathways by which ESP1 information is conveyed from the peripheral receptive organ to the motor-regulating midbrain via the amygdala-hypothalamus axis. In the medial amygdala, a specific type of projection neurons gated ESP1 signals to the ventromedial hypothalamus (VMH) in a sex-dependent manner. In the dorsal VMH, which has been associated with defensive behaviors, a selective neural subpopulation discriminately mediated ESP1 information from a predator cue. Together, our data illuminate a labeled-line organization for controlling pheromone-mediated sexual behavioral output in female mice.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
These regions have distinct roles in socio-sexual behavior in adulthood, often driven by distinct, separable cell type-specific and projection-specific mechanisms.
“These regions have distinct roles in socio-sexual behavior in adulthood as well, often driven by distinct, separable cell type-specific and projection-specific mechanisms (Unger et al., 2015; Wong et al., 2016; Ishii et al., 2017; Kohl et al., 2018).”
From Social play experience in juvenile rats is indispensable for appropriate socio-sexual behavior in adulthood in males but not females (2023) · cites this paper as Ishii et al., 2017
Cites
Functional identification of an aggression locus in the mouse hypothalamus
Lin, D., Boyle, M. P., Dollar, P., Lee, H., Lein, E. S., Perona, P., & Anderson, D. J. (2011) · Nature · doi:10.1038/nature09736 · Cited by 914 · see citing works
Viral-genetic tracing of the input-output organization of a central noradrenaline circuit
Schwarz, L. A., Miyamichi, K., Gao, X. J., Beier, K. T., Weissbourd, B., DeLoach, K. E., Ren, J., Ibanes, S., Malenka, R. C., Kremer, E. J., et al. (2015) · Nature · doi:10.1038/nature14600 · Cited by 744 · see citing works
Self-citationMolecular organization of vomeronasal chemoreception
Isogai, Y., Si, S., Pont-Lezica, L., Tan, T., Kapoor, V., Murthy, V. N., & Dulac, C. (2011) · Nature · doi:10.1038/nature10437 · Cited by 317 · 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
Lindberg, D., Chen, P., & Li, C. (2013) · Journal of Comparative Neurology · doi:10.1002/cne.23338 · Cited by 125 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Neural circuit mechanisms of social behavior
Chen, P., & Hong, W. (2018) · Neuron · doi:10.1016/j.neuron.2018.02.026 · Cited by 527 · see citing works
Multimodal analysis of cell types in a hypothalamic node controlling social behavior
Kim, D.-W., Yao, Z., Graybuck, L. T., Kim, T. K., Nguyen, T. N., Smith, K. A., Fong, O., Yi, L., Koulena, N., Pierson, N., et al. (2019) · Cell · doi:10.1016/j.cell.2019.09.020 · Cited by 259 · see citing works
An amygdala-to-hypothalamus circuit for social reward
Hu, R. K., Zuo, Y., Ly, T., Wang, J., Meera, P., Wu, Y. E., & Hong, W. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00828-2 · Cited by 174 · 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
Stimulus-specific hypothalamic encoding of a persistent defensive state
Kennedy, A., Kunwar, P. S., Li, L.-Y., Stagkourakis, S., Wagenaar, D. A., & Anderson, D. J. (2020) · Nature · doi:10.1038/s41586-020-2728-4 · Cited by 144 · see citing works
Shared song detector neurons in Drosophila male and female brains drive sex-specific behaviors
Deutsch, D., Clemens, J., Thiberge, S. Y., Guan, G., & Murthy, M. (2019) · Current Biology · doi:10.1016/j.cub.2019.08.008 · Cited by 67 · see citing works
Recording and manipulation of the maternal oxytocin neural activities in mice
Yukinaga, H., Hagihara, M., Tsujimoto, K., Chiang, H.-L., Kato, S., Kobayashi, K., & Miyamichi, K. (2022) · Current Biology · doi:10.1016/j.cub.2022.06.083 · Cited by 33 · see citing works
Self-citationMarquardt, A. E., VanRyzin, J. W., Fuquen, R. W., & McCarthy, M. M. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1076765 · Cited by 31 · see citing works
“These regions have distinct roles in socio-sexual behavior in adulthood as well, often driven by distinct, separable cell type-specific and projection-specific mechanisms (Unger et al., 2015; Wong et al., 2016; Ishii et al., 2017; Kohl et al., 2018).”
Dynamics of pulsatile activities of arcuate kisspeptin neurons in aging female mice
Goto, T., Hagihara, M., & Miyamichi, K. (2023) · eLife · doi:10.7554/elife.82533 · Cited by 27 · see citing works
Self-citationHearing, touching, and multisensory integration during mate choice
Lenschow, C., Mendes, A. R. P., & Lima, S. Q. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.943888 · Cited by 17 · see citing works
- Authors
- Ishii, K. K., Osakada, T., Mori, H., Miyasaka, N., Yoshihara, Y., Miyamichi, K., & Touhara, K.
- Affiliations
- Japan Science and Technology Agency (JP)
- RIKEN Center for Brain Science (JP)
- Corresponding author
- Miyamichi, Kazunari
- Touhara, Kazushige
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2017-07
- Volume
- 95
- Issue
- 1
- Pages
- 123-137.e8
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2646486909
- Cited by
- 185
- References
- 5
- Citations by year
- 2026: 13 · 2025: 33 · 2024: 15 · 2023: 23 · 2022: 24 · 2021: 25 · 2020: 20 · 2019: 16 · 2018: 14 · 2017: 2
- FWCI
- 8.73
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Funders
- JSPS
- ERATO Touhara Chemosensory Signal Project (JST ERATO (JPMJER1202)
- JSPS Kakenhi (16K20963)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- female receptivity, medial amygdala, ventromedial hypothalamus, dorsal hypothalamus, olfactory input, mice
- MeSH terms
- Amygdala, Animals, Cues, Female, Hypothalamus, Male, Mesencephalon, Mice, Transgenic, Nerve Net, Neurons, Predatory Behavior, Proteins, Sex Attractants, Sexual Behavior, Animal, Sex Characteristics, Intercellular Signaling Peptides and Proteins, Mice
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
