Cited by 93Neuroendocrine regulation and behaviorNeurobiology and Insect Physiology ResearchHypothalamic control of reproductive hormones

Transformations of neural representations in a social behaviour network

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Yang, Bin, Karigo, Tomomi, Anderson, David J.·2022·Nature

Abstract

Mating and aggression are innate social behaviours that are controlled by subcortical circuits in the extended amygdala and hypothalamus 1-4. The bed nucleus of the stria terminalis (BNSTpr) is a node that receives input encoding sex-specific olfactory cues from the medial amygdala 5,6, and which in turn projects to hypothalamic nuclei that control mating 7-9 (medial preoptic area (MPOA)) and aggression 9-14 (ventromedial hypothalamus, ventrolateral subdivision (VMHvl)), respectively 15. Previous studies have demonstrated that male aromatase-positive BNSTpr neurons are required for mounting and attack, and may identify conspecific sex according to their overall level of activity 16. However, neural representations in BNSTpr, their function and their transformations in the hypothalamus have not been characterized. Here we performed calcium imaging 17,18 of male BNSTpr Esr1 neurons during social behaviours. We identify distinct populations of female- versus male-tuned neurons in BNSTpr, with the former outnumbering the latter by around two to one, similar to the medial amygdala and MPOA but opposite to VMHvl, in which male-tuned neurons predominate 6,9,19. Chemogenetic silencing of BNSTpr Esr1 neurons while imaging MPOA Esr1 or VMHvl Esr1 neurons in behaving animals showed, unexpectedly, that the male-dominant sex-tuning bias in VMHvl was inverted to female-dominant whereas a switch from sniff- to mount-selective neurons during mating was attenuated in MPOA. Our data also indicate that BNSTpr Esr1 neurons are not essential for conspecific sex identification. Rather, they control the transition from appetitive to consummatory phases of male social behaviours by shaping sex- and behaviour-specific neural representations in the hypothalamus.

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  1. [33]Knoedler JR A functional cellular framework for sex and estrous cycle-dependent gene expression and behavior. Cell 185, 654– 671.e22 (2022). 35065713 PMC8956134
  2. [39]Welch JD Single-Cell Multi-omic Integration Compares and Contrasts Features of Brain Cell Identity. Cell 177, 1873– 1887.e17 (2019). 31178122 PMC6716797

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Authors
Yang, B., Karigo, T., & Anderson, D. J.
Affiliations
California Institute of Technology (US)
Corresponding author
Anderson, David J.
Venue
Nature
Published
2022-08-03
Volume
608
Issue
7924
Pages
741-749
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
OpenAlex
W4289637660
Cited by
93
References
45
Citations by year
2026: 17 · 2025: 23 · 2024: 22 · 2023: 30 · 2022: 1
FWCI
17.96
Type
journal article
Language
en
Open access
Locations
  • Nature (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • CaltechAUTHORS (California Institute of Technology) (submittedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
Funders
  • National Institute of Mental Health (R01MH112593, R01MH123612, U19MH114830, R01MH070053)
  • National Institute of Neurological Disorders and Stroke (R01NS123916)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Keywords
neural representations, social behavior, hypothalamus
MeSH terms
Aggression, Amygdala, Animals, Calcium, Female, Hypothalamus, Male, Neurons, Preoptic Area, Sexual Behavior, Animal, Sex Characteristics, Social Behavior

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