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

doi:10.1016/j.neuron.2020.05.028

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^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

40 Scopus citations

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 language	American English
Pages (from-to)	644-655.e7
Journal	Neuron
Volume	107
Issue number	4
DOIs	https://doi.org/10.1016/j.neuron.2020.05.028
State	Published - 19 Aug 2020
Externally published	Yes

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.).

Publisher Copyright:
© 2020 The Author(s)

Keywords

aggression
optogenetics
oxytocin
social behavior
social salience
wireless

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10.1016/j.neuron.2020.05.028

Cite this

Anpilov, S., Shemesh, Y., Eren, N., Harony-Nicolas, H., Benjamin, A., Dine, J., Oliveira, V. E. M., Forkosh, O., Karamihalev, S., Hüttl, R. E., Feldman, N., Berger, R., Dagan, A., Chen, G., Neumann, I. D., Wagner, S., Yizhar, O., & Chen, A. (2020). Wireless Optogenetic Stimulation of Oxytocin Neurons in a Semi-natural Setup Dynamically Elevates Both Pro-social and Agonistic Behaviors. Neuron, 107(4), 644-655.e7. https://doi.org/10.1016/j.neuron.2020.05.028

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

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.",

keywords = "aggression, optogenetics, oxytocin, social behavior, social salience, wireless",

author = "Sergey Anpilov and Yair Shemesh and Noa Eren and Hala Harony-Nicolas and Asaf Benjamin and Julien Dine and Oliveira, {Vin{\'i}cius E.M.} and Oren Forkosh and Stoyo Karamihalev and H{\"u}ttl, {Rosa Eva} and Noa Feldman and Ryan Berger and Avi Dagan and Gal Chen and Neumann, {Inga D.} and Shlomo Wagner and Ofer Yizhar and Alon Chen",

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.). Publisher Copyright: {\textcopyright} 2020 The Author(s)",

year = "2020",

month = aug,

day = "19",

doi = "10.1016/j.neuron.2020.05.028",

language = "American English",

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Anpilov, S, Shemesh, Y, Eren, N, Harony-Nicolas, H, Benjamin, A, Dine, J, Oliveira, VEM, Forkosh, O, Karamihalev, S, Hüttl, RE, Feldman, N, Berger, R, Dagan, A, Chen, G, Neumann, ID, Wagner, S, Yizhar, O & Chen, A 2020, 'Wireless Optogenetic Stimulation of Oxytocin Neurons in a Semi-natural Setup Dynamically Elevates Both Pro-social and Agonistic Behaviors', Neuron, vol. 107, no. 4, pp. 644-655.e7. https://doi.org/10.1016/j.neuron.2020.05.028

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T1 - Wireless Optogenetic Stimulation of Oxytocin Neurons in a Semi-natural Setup Dynamically Elevates Both Pro-social and Agonistic Behaviors

AU - Anpilov, Sergey

AU - Shemesh, Yair

AU - Eren, Noa

AU - Harony-Nicolas, Hala

AU - Benjamin, Asaf

AU - Dine, Julien

AU - Oliveira, Vinícius E.M.

AU - Forkosh, Oren

AU - Karamihalev, Stoyo

AU - Hüttl, Rosa Eva

AU - Feldman, Noa

AU - Berger, Ryan

AU - Dagan, Avi

AU - Chen, Gal

AU - Neumann, Inga D.

AU - Wagner, Shlomo

AU - Yizhar, Ofer

AU - Chen, Alon

N1 - 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)

PY - 2020/8/19

Y1 - 2020/8/19

N2 - 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.

AB - 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.

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KW - optogenetics

KW - oxytocin

KW - social behavior

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U2 - 10.1016/j.neuron.2020.05.028

DO - 10.1016/j.neuron.2020.05.028

M3 - Article

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AN - SCOPUS:85089380100

SN - 0896-6273

VL - 107

SP - 644-655.e7

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ER -

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

Abstract

Bibliographical note

Keywords

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