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Published August 20, 2020 | Published
Journal Article Open

A Neuro-hormonal Circuit for Paternal Behavior Controlled by a Hypothalamic Network Oscillation

Abstract

Parental behavior is pervasive throughout the animal kingdom and essential for species survival. However, the relative contribution of the father to offspring care differs markedly across animals, even between related species. The mechanisms that organize and control paternal behavior remain poorly understood. Using Sprague-Dawley rats and C57BL/6 mice, two species at opposite ends of the paternal spectrum, we identified that distinct electrical oscillation patterns in neuroendocrine dopamine neurons link to a chain of low dopamine release, high circulating prolactin, prolactin receptor-dependent activation of medial preoptic area galanin neurons, and paternal care behavior in male mice. In rats, the same parameters exhibit inverse profiles. Optogenetic manipulation of these rhythms in mice dramatically shifted serum prolactin and paternal behavior, whereas injecting prolactin into non-paternal rat sires triggered expression of parental care. These findings identify a frequency-tuned brain-endocrine-brain circuit that can act as a gain control system determining a species' parental strategy.

Additional Information

© 2020 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). Received 29 October 2018, Revised 21 October 2019, Accepted 9 July 2020, Available online 6 August 2020. The authors thank Dr. G. Spigolon for advice regarding experiments and Dr. K. Ampatzis for advice regarding illustrations. Members of the Broberger laboratory are thanked for discussions during preparation of this manuscript and Drs. N.G. Larsson and O. Kiehn for sharing the DAT-Cre and floxed-tdTomato mice, respectively. This study was supported by grants from the European Research Council (261286-ENDOSWITCH to C.B. and ERC-AdG-2015-695136 to T.H.); the Swedish Research Council (2018-02480), Strategic Research Program in Diabetes at Karolinska Institutet and StratNeuro, Hjärnfonden (Swedish Brain Foundation), Novo Nordisk Fonden, and internal funds from Karolinska Institutet (to C.B.), and EMBO ALTF 736-2018 (to S.S.). Author Contributions: S.S., P.W., S.K., and K.Z. designed, performed, and analyzed experiments. K.O.S., R.S.E.B., and D.R.G. collaborated on data involving the prolactin receptor floxed mouse. J.B. and T.H. collaborated on data involving the Gal-Cre mice. C.B. designed experiments. S.S. and C.B. wrote the manuscript. All authors reviewed the manuscript. The authors declare no competing interests.

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Created:
August 22, 2023
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October 20, 2023