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Transformations of neural representations in a social behaviour network

Yang, Bin and Karigo, Tomomi and Anderson, David J. (2022) Transformations of neural representations in a social behaviour network. Nature . ISSN 0028-0836. doi:10.1038/s41586-022-05057-6. (In Press) https://resolver.caltech.edu/CaltechAUTHORS:20220803-535873000

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Image (JPEG) (Extended Data Fig. 1: Chemogenetic and optogenetic silencing of BNSTp^(rEsr1) neurons disrupts aggression and mating) - Supplemental Material
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Image (JPEG) (Extended Data Fig. 2: Optogenetic silencing of BNSTpr^(Esr1) terminals in MPOA or VMHvl during male-male/ male-female interactions) - Supplemental Material
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Image (JPEG) (Extended Data Fig. 3: Performance of 0.85 mm Ø prism coupled GRIN lens compared to 0.6 mm Ø GRIN lens for imaging BNSTpr) - Supplemental Material
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Image (JPEG) (Extended Data Fig. 4: Miniscope imaging analysis of BNSTpr neurons) - Supplemental Material
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Image (JPEG) (Extended Data Fig. 5: ChemoScope imaging of MPOA and VMHvl across multiple days) - Supplemental Material
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Image (JPEG) (Extended Data Fig. 6: ChemoScope imaging of MPOA and VMHvl) - Supplemental Material
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Image (JPEG) (Extended Data Fig. 7: Tracking changes to MPOA and VMHvl single-unit responses before and after silencing BNSTpr) - Supplemental Material
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Image (JPEG) (Extended Data Fig. 8: Effect of BNSTpr silencing on VMHvl behavior representations and female / male preference) - Supplemental Material
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Image (JPEG) (Extended Data Fig. 9: Retrograde tracing and imaging of BNSTpr projection neurons) - Supplemental Material
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Abstract

Mating and aggression are innate social behaviours that are controlled by subcortical circuits in the extended amygdala and hypothalamus. The bed nucleus of the stria terminalis (BNSTpr) is a node that receives input encoding sex-specific olfactory cues from the medial amygdala, and which in turn projects to hypothalamic nuclei that control mating (medial preoptic area (MPOA)) and aggression (ventromedial hypothalamus, ventrolateral subdivision (VMHvl)), respectively15. 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. However, neural representations in BNSTpr, their function and their transformations in the hypothalamus have not been characterized. Here we performed calcium imaging of male BNSTprEsr1 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. 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.


Item Type:Article
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https://doi.org/10.1038/s41586-022-05057-6DOIArticle
https://rdcu.be/cS3n9PublisherFree ReadCube access
ORCID:
AuthorORCID
Karigo, Tomomi0000-0002-5370-3274
Anderson, David J.0000-0001-6175-3872
Additional Information:© 2022 Springer Nature. Received 26 March 2021. Accepted 29 June 2022. Published 03 August 2022. We thank A. Kennedy and A. Nair for advice on miniscope data analysis; M. Hui and C. Kim for assistance with animal surgery and behaviour experiments; M. Zelikowsky for advice on statistical analysis; W. Hong for pilot experiments performed on BNSTpr; X. Da, J. Chang and X. Wang for histology; Y. Huang for genotyping; Caltech OLAR staff for animal care; J. Costanza for mouse colony management; M. Schnitzer, A. Vinograd and B. Weissbourd for constructive comments on the manuscript; C. Chiu for laboratory management; G. Mancuso for administrative assistance; and members of the Anderson laboratory for helpful comments on this project. This paper was supported by NIH grant nos. MH070053, MH112593 and NS123916 and by the Simons Collaboration on the Global Brain. D.J.A. is an investigator of the Howard Hughes Medical Institute. Contributions. B.Y. performed experiments, analysed data and prepared figures. T.K. performed retrograde tracing experiments. B.Y. and D.J.A. designed the study and wrote the paper. Data availability. The data on which this study is based are available on reasonable request. Code availability. The custom MATLAB and Python codes used to analyse the data in this study are available on request. Reporting summary. Further information on research design is available in the Nature Research Reporting Summary linked to this paper. The authors declare no competing interests. Peer review information. Nature thanks the anonymous reviewers for their contribution to the peer review of this work. Peer reviewer reports are available.
Group:Tianqiao and Chrissy Chen Institute for Neuroscience
Funders:
Funding AgencyGrant Number
NIHMH070053
NIHMH112593
NIHNS123916
Simons FoundationUNSPECIFIED
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
DOI:10.1038/s41586-022-05057-6
Record Number:CaltechAUTHORS:20220803-535873000
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220803-535873000
Official Citation:Yang, B., Karigo, T. & Anderson, D.J. Transformations of neural representations in a social behaviour network. Nature (2022). https://doi.org/10.1038/s41586-022-05057-6
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:116070
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:09 Aug 2022 15:03
Last Modified:09 Aug 2022 15:03

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