Wireless Optogenetic Stimulation of Oxytocin Neurons in a Semi-natural Setup Dynamically Elevates Both Pro-social and Agonistic Behaviors

Sergey Anpilov, Yair Shemesh, Noa Eren, Hala Harony-Nicolas, Asaf Benjamin, Julien Dine, Vinícius E.M. Oliveira, Oren Forkosh, Stoyo Karamihalev, Rosa Eva Hüttl, Noa Feldman, Ryan Berger, Avi Dagan, Gal Chen, Inga D. Neumann, Shlomo Wagner, Ofer Yizhar, Alon Chen

Research output: Contribution to journalArticlepeer-review

Abstract

Complex behavioral phenotyping techniques are becoming more prevalent in the field of behavioral neuroscience, and thus methods for manipulating neuronal activity must be adapted to fit into such paradigms. Here, we present a head-mounted, magnetically activated device for wireless optogenetic manipulation that is compact, simple to construct, and suitable for use in group-living mice in an enriched semi-natural arena over several days. Using this device, we demonstrate that repeated activation of oxytocin neurons in male mice can have different effects on pro-social and agonistic behaviors, depending on the social context. Our findings support the social salience hypothesis of oxytocin and emphasize the importance of the environment in the study of social neuromodulators. Our wireless optogenetic device can be easily adapted for use in a variety of behavioral paradigms, which are normally hindered by tethered light delivery or a limited environment.

Original languageEnglish
Pages (from-to)644-655.e7
JournalNeuron
Volume107
Issue number4
DOIs
StatePublished - 19 Aug 2020

Bibliographical note

Funding Information:
The authors wish to thank Franck Touboul for assistance with DeepLabCut tracking, Dr. Jessica Keverne for writing and editing support and advice, and Dr. Ron Rotkopf for assistance with statistical analyses. A.C. is the incumbent of the Vera and John Schwartz Family Professorial Chair in Neurobiology at the Weizmann Institute and the head of the Max Planck Society?Weizmann Institute of Science Laboratory for Experimental Neuropsychiatry and Behavioral Neurogenetics gratefully funded by the Max Planck Foundation. This work is supported by an FP7 Grant from the European Research Council (260463, A.C.); a research grant from the Israel Science Foundation (1565/15, A.C.); and the ERANET Program, supported by the Chief Scientist Office of the Israeli Ministry of Health (3-11389, A.C.); the project was funded by the Federal Ministry of Education and Research under the funding code 01KU1501A (A.C.); I-CORE Program of the Planning and Budgeting Committee and The Israel Science Foundation (grant no. 1916/12 to A.C.); Ruhman Family Laboratory for Research in the Neurobiology of Stress (A.C.); research support from Bruno and Simone Licht; the Perlman Family Foundation, founded by Louis L. and Anita M. Perlman (A.C.); the Adelis Foundation (A.C.); and Sonia T. Marschak (A.C.). Conceptualization, S.A. Y.S. and A.C.; Methodology, S.A. Y.S. O.F. H.H.-N. and A.D.; Software, A.B. and O.F.; Investigation, S.A. Y.S. N.E. JD, R.-E.H. V.E.M.O. and G.C.; Validation, S.A. Y.S. N.E. and H.H.-N.; Formal Analysis, S.A. Y.S. N.E. A.B. and J.D. V.E.M.O. S.K. N.F. and R.B.; Writing, N.E. S.A. and Y.S.; Visualization, S.A.; Funding Acquisition, A.C.; Resources, O.Y. and S.W.; Supervision: A.C. O.Y. S.W. and I.D.N. The authors declare no competing interests.

Funding Information:
The authors wish to thank Franck Touboul for assistance with DeepLabCut tracking, Dr. Jessica Keverne for writing and editing support and advice, and Dr. Ron Rotkopf for assistance with statistical analyses. A.C. is the incumbent of the Vera and John Schwartz Family Professorial Chair in Neurobiology at the Weizmann Institute and the head of the Max Planck Society–Weizmann Institute of Science Laboratory for Experimental Neuropsychiatry and Behavioral Neurogenetics gratefully funded by the Max Planck Foundation . This work is supported by an FP7 Grant from the European Research Council ( 260463 , A.C.); a research grant from the Israel Science Foundation ( 1565/15 , A.C.); and the ERANET Program , supported by the Chief Scientist Office of the Israeli Ministry of Health ( 3-11389 , A.C.); the project was funded by the Federal Ministry of Education and Research under the funding code 01KU1501A (A.C.); I-CORE Program of the Planning and Budgeting Committee and The Israel Science Foundation (grant no. 1916/12 to A.C.); Ruhman Family Laboratory for Research in the Neurobiology of Stress (A.C.); research support from Bruno and Simone Licht ; the Perlman Family Foundation , founded by Louis L. and Anita M. Perlman (A.C.); the Adelis Foundation (A.C.); and Sonia T. Marschak (A.C.).

Publisher Copyright:
© 2020 The Author(s)

Keywords

  • aggression
  • optogenetics
  • oxytocin
  • social behavior
  • social salience
  • wireless

ASJC Scopus subject areas

  • Neuroscience (all)

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