A neural circuit for male sexual behavior and reward

Daniel W Bayless; Chung-Ha O Davis; Renzhi Yang; Yichao Wei; Vinicius Miessler de Andrade Carvalho; Joseph R Knoedler; Taehong Yang; Oscar Livingston; Akira Lomvardas; Gabriela J Martins; Ana Mafalda Vicente; Jun B Ding; Liqun Luo; Nirao M Shah

doi:10.1016/j.cell.2023.07.021

A neural circuit for male sexual behavior and reward

Cell. 2023 Aug 31;186(18):3862-3881.e28. doi: 10.1016/j.cell.2023.07.021. Epub 2023 Aug 11.

Affiliations

¹ Departments of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA 94305, USA.
² Stanford Neurosciences Graduate Program, Stanford University, Stanford, CA 94305, USA.
³ Allen Institute for Neural Dynamics, Seattle, WA 98109.
⁴ Allen Institute for Neural Dynamics, Seattle, WA 98109; Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY 10027.
⁵ Department of Neurosurgery, Stanford University, Stanford, CA 94305, USA; Departments of Neurology and Neurological Sciences, Stanford University, Stanford, CA 94305, USA.
⁶ Department of Biology, Stanford University, Stanford, CA 94305, USA; Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA; Department of Neurobiology, Stanford University, Stanford, CA 94305, USA.
⁷ Departments of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA 94305, USA; Department of Neurobiology, Stanford University, Stanford, CA 94305, USA; Department of Obstetrics and Gynecology, Stanford University, Stanford, CA 94305, USA. Electronic address: nirao@stanford.edu.

PMID: 37572660
PMCID: PMC10615179 (available on 2024-08-31)
DOI: 10.1016/j.cell.2023.07.021

Abstract

Male sexual behavior is innate and rewarding. Despite its centrality to reproduction, a molecularly specified neural circuit governing innate male sexual behavior and reward remains to be characterized. We have discovered a developmentally wired neural circuit necessary and sufficient for male mating. This circuit connects chemosensory input to BNSTpr^Tac1 neurons, which innervate POA^Tacr1 neurons that project to centers regulating motor output and reward. Epistasis studies demonstrate that BNSTpr^Tac1 neurons are upstream of POA^Tacr1 neurons, and BNSTpr^Tac1-released substance P following mate recognition potentiates activation of POA^Tacr1 neurons through Tacr1 to initiate mating. Experimental activation of POA^Tacr1 neurons triggers mating, even in sexually satiated males, and it is rewarding, eliciting dopamine release and self-stimulation of these cells. Together, we have uncovered a neural circuit that governs the key aspects of innate male sexual behavior: motor displays, drive, and reward.

Keywords: BNST; LTP; POA; Tac1; Tacr1; aggression; bed nucleus of stria terminalis; brain stimulation reward; dopamine; drive; hypothalamic LTP; hypothalamus; libido; male sexual behavior; mating; motivation; preoptic hypothalamus; reinforcement; reward; social behavior network; substance P.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Male
Mice
Neural Pathways*
Neurons / physiology
Reward
Sexual Behavior, Animal* / physiology

A neural circuit for male sexual behavior and reward

Authors

Affiliations

Abstract

Publication types

MeSH terms

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