Connectional architecture of a mouse hypothalamic circuit node controlling social behavior

Type 1 estrogen receptor-expressing neurons in the ventrolateral subdivision of the ventromedial hypothalamus (VMHvlEsr1) play a causal role in the control of social behaviors, including aggression. Here we use six different viral-genetic tracing methods to systematically map the connectional archit...

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Published in:	Proceedings of the National Academy of Sciences - PNAS Vol. 116; no. 15; pp. 7503 - 7512
Main Authors:	Lo, Liching, Yao, Shenqin, Kim, Dong-Wook, Cetin, Ali, Harris, Julie, Zeng, Hongkui, Anderson, David J., Weissbourd, Brandon
Format:	Journal Article
Language:	English
Published:	United States National Academy of Sciences 09-04-2019
Series:	PNAS Plus
Subjects:	Animals Artificial intelligence Behavior, Animal - physiology Biological Sciences Brain Brain architecture Brain Mapping Computer architecture Divergence Estrogen Receptor alpha - biosynthesis Estrogen Receptor alpha - genetics Estrogens Gene mapping Hypothalamus Hypothalamus (ventromedial) Information processing Mapping Mice Mice, Transgenic Nerve Net - cytology Nerve Net - physiology Neurons Neurons - cytology Neurons - metabolism PNAS Plus Sensory integration Social Behavior Subpopulations Target recognition Ventromedial Hypothalamic Nucleus - cytology Ventromedial Hypothalamic Nucleus - physiology aggression connectivity social behavior hypothalamus VMHvl
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Summary:	Type 1 estrogen receptor-expressing neurons in the ventrolateral subdivision of the ventromedial hypothalamus (VMHvlEsr1) play a causal role in the control of social behaviors, including aggression. Here we use six different viral-genetic tracing methods to systematically map the connectional architecture of VMHvlEsr1 neurons. These data reveal a high level of input convergence and output divergence (“fan-in/fan-out”) from and to over 30 distinct brain regions, with a high degree (∼90%) of bidirectionality, including both direct as well as indirect feedback. Unbiased collateralization mapping experiments indicate that VMHvlEsr1 neurons project to multiple targets. However, we identify two anatomically distinct subpopulations with anterior vs. posterior biases in their collateralization targets. Nevertheless, these two subpopulations receive indistinguishable inputs. These studies suggest an overall system architecture in which an anatomically feed-forward sensory-to-motor processing stream is integrated with a dense, highly recurrent central processing circuit. This architecture differs from the “brain-inspired,” hierarchical feed-forward circuits used in certain types of artificial intelligence networks.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Contributed by David J. Anderson, December 12, 2018 (sent for review October 11, 2018; reviewed by Clifford B. Saper and Richard B. Simerly) Author contributions: L.L., D.-W.K., D.J.A., and B.W. designed research; L.L. and D.-W.K. performed research; S.Y., A.C., J.H., and H.Z. contributed new reagents/analytic tools; L.L., D.-W.K., D.J.A., and B.W. analyzed data; and L.L., D.J.A., and B.W. wrote the paper. 1L.L. and S.Y. contributed equally to this work. Reviewers: C.B.S., Harvard Medical School, Beth Israel Deaconess Medical Center; and R.B.S., Vanderbilt University.
ISSN:	0027-8424 1091-6490
DOI:	10.1073/pnas.1817503116