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Social behaviour shapes hypothalamic neural ensemble representations of conspecific sex

Remedios, Ryan and Kennedy, Ann and Zelikowsky, Moriel and Grewe, Benjamin F. and Schnitzer, Mark J. and Anderson, David J. (2017) Social behaviour shapes hypothalamic neural ensemble representations of conspecific sex. Nature, 550 (7676). pp. 388-392. ISSN 0028-0836. http://resolver.caltech.edu/CaltechAUTHORS:20171019-073428081

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[img] PDF (Supplementary table 1 - statistical significance testing) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 1: Properties of Esr1+ neuron responses in VMHvl during free social interactions) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 2: Representations of males and females in all individual mice) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 3: Distance dependence of intruder sex representations) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 4: Choice probability histograms and example cells) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 5: Expression of social behaviours across trials and days) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 6: Comparison of the social behaviours and neural representations in example mice that showed and did not show aggression) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 7: Registration of cells across three days of imaging) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 8: Preference changes of Esr1+ neurons during the acquisition of social experience) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 9: Behaviour correlation with male/female PCC) - Supplemental Material
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Abstract

All animals possess a repertoire of innate (or instinctive) behaviours, which can be performed without training. Whether such behaviours are mediated by anatomically distinct and/or genetically specified neural pathways remains unknown. Here we report that neural representations within the mouse hypothalamus, that underlie innate social behaviours, are shaped by social experience. Oestrogen receptor 1-expressing (Esr1+) neurons in the ventrolateral subdivision of the ventromedial hypothalamus (VMHvl) control mating and fighting in rodents. We used microendoscopy to image Esr1+neuronal activity in the VMHvl of male mice engaged in these social behaviours. In sexually and socially experienced adult males, divergent and characteristic neural ensembles represented male versus female conspecifics. However, in inexperienced adult males, male and female intruders activated overlapping neuronal populations. Sex-specific neuronal ensembles gradually separated as the mice acquired social and sexual experience. In mice permitted to investigate but not to mount or attack conspecifics, ensemble divergence did not occur. However, 30 minutes of sexual experience with a female was sufficient to promote the separation of male and female ensembles and to induce an attack response 24 h later. These observations uncover an unexpected social experience-dependent component to the formation of hypothalamic neural assemblies controlling innate social behaviours. More generally, they reveal plasticity and dynamic coding in an evolutionarily ancient deep subcortical structure that is traditionally viewed as a ‘hard-wired’ system.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/nature23885DOIArticle
https://www.nature.com/nature/journal/v550/n7676/full/nature23885.htmlPublisherArticle
http://rdcu.be/wUZsPublisherFree ReadCube access
Additional Information:© 2017 Macmillan Publishers Limited, part of Springer Nature. Received 03 January 2017; Accepted 31 July 2017; Published online 18 October 2017. We thank X. Wang, J. S. Chang and R. Robertson for technical help, H. Lee and P. Kunwar for experimental advice, D. Senyuz for testing behaviour in wild-type mice, D.-W. Kim for pilot experiments, M. McCardle and C. Chiu for genotyping, J.Costanza for mouse colony management, G. Stuber for advice on GCaMP6s expression, Inscopix Inc. for technical support, P. Perona for mouse tracking software, L. Abbott for comments on the manuscript, R. Axel, D. Y. Tsao and M. Meister for critical feedback, X. Da and C. Chiu for laboratory management and G. Mancuso for Administrative Assistance. D.J.A. and M.J.S. are Investigators of the Howard Hughes Medical Institute and Paul G. Allen Distinguished Investigators. This work was supported in part by NIH grant no. R01MH070053, and grants from the Gordon Moore Foundation, Ellison Medical Research Foundation, Simons Foundation and Guggenheim Foundation to D.J.A. A.K. is a fellow of the Helen Hay Whitney Foundation, M.Z. is a recipient of fellowships from the NSF and L’Oréal USA Women in Science. Code availability: Custom code written for the purpose of this study is accessible at https://github.com/DJALab/VMHvl_imaging. Data availability: Imaging and behavioural data will be made available by the corresponding author upon reasonable request. Author Contributions: R.R. designed and performed all imaging experiments, processed the data, contributed to analysis and co-wrote the manuscript; A.K. performed computational analysis, prepared figures and co-wrote the manuscript; M.Z. designed and performed behavioural experiments; M.J.S. and B.F.G. provided training for R.R., guidance on experimental design and data analysis, and critical feedback; D.J.A. supervised the project and co-wrote the manuscript. Competing financial interests: M.J.S. is a scientific co-founder of Inscopix Inc., which produced the miniature fluorescence microscope used in this study. R.R., A.K., M.Z., B.F.G. and D.J.A. declare no competing financial interests.
Funders:
Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Paul G. Allen Family FoundationUNSPECIFIED
NIHR01MH070053
Gordon and Betty Moore FoundationUNSPECIFIED
Ellison Medical Research FoundationUNSPECIFIED
Simons FoundationUNSPECIFIED
John Simon Guggenheim FoundationUNSPECIFIED
Helen Hay Whitney FoundationUNSPECIFIED
NSFUNSPECIFIED
L’Oréal USA Women in ScienceUNSPECIFIED
Subject Keywords:Social behavior; Neural decoding; Neurophysiology; Learning and memory; Inhibition-excitation balance
Record Number:CaltechAUTHORS:20171019-073428081
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20171019-073428081
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:82476
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:19 Oct 2017 16:19
Last Modified:19 Oct 2017 16:19

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