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Sex differences in neural representations of social and nonsocial reward in the medial prefrontal cortex

Author

Listed:
  • Jennifer Isaac

    (Emory University
    Emory University)

  • Sonia Corbett Karkare

    (Emory University
    Emory University)

  • Hymavathy Balasubramanian

    (Emory University
    Emory University)

  • Nicholas Schappaugh

    (Emory University)

  • Jarildy Larimar Javier

    (Emory University
    Emory University)

  • Maha Rashid

    (Emory University
    Emory University)

  • Malavika Murugan

    (Emory University
    Emory University)

Abstract

The reinforcing nature of social interactions is necessary for the maintenance of appropriate social behavior. However, the neural substrates underlying social reward processing and how they might differ based on the sex and internal state of the animal remains unknown. It is also unclear whether these neural substrates are shared with those involved in nonsocial rewarding processing. We developed a fully automated, two choice (social-sucrose) operant assay in which mice choose between social and nonsocial rewards to directly compare the reward-related behaviors associated with two competing stimuli. We performed cellular resolution calcium imaging of medial prefrontal cortex (mPFC) neurons in male and female mice across varying states of water restriction and social isolation. We found that mPFC neurons maintain largely non-overlapping, flexible representations of social and nonsocial reward that vary with internal state in a sex-dependent manner. Additionally, optogenetic manipulation of mPFC activity during the reward period of the assay disrupted reward-seeking behavior across male and female mice. Thus, using a two choice operant assay, we have identified sex-dependent, non-overlapping neural representations of social and nonsocial reward in the mPFC that vary with internal state and that are essential for appropriate reward-seeking behavior.

Suggested Citation

  • Jennifer Isaac & Sonia Corbett Karkare & Hymavathy Balasubramanian & Nicholas Schappaugh & Jarildy Larimar Javier & Maha Rashid & Malavika Murugan, 2024. "Sex differences in neural representations of social and nonsocial reward in the medial prefrontal cortex," Nature Communications, Nature, vol. 15(1), pages 1-27, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52294-6
    DOI: 10.1038/s41467-024-52294-6
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    References listed on IDEAS

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    1. Ryan Remedios & Ann Kennedy & Moriel Zelikowsky & Benjamin F. Grewe & Mark J. Schnitzer & David J. Anderson, 2017. "Social behaviour shapes hypothalamic neural ensemble representations of conspecific sex," Nature, Nature, vol. 550(7676), pages 388-392, October.
    2. Joshua H. Jennings & Christina K. Kim & James H. Marshel & Misha Raffiee & Li Ye & Sean Quirin & Sally Pak & Charu Ramakrishnan & Karl Deisseroth, 2019. "Interacting neural ensembles in orbitofrontal cortex for social and feeding behaviour," Nature, Nature, vol. 565(7741), pages 645-649, January.
    3. Ofer Yizhar & Lief E. Fenno & Matthias Prigge & Franziska Schneider & Thomas J. Davidson & Daniel J. O’Shea & Vikaas S. Sohal & Inbal Goshen & Joel Finkelstein & Jeanne T. Paz & Katja Stehfest & Roman, 2011. "Neocortical excitation/inhibition balance in information processing and social dysfunction," Nature, Nature, vol. 477(7363), pages 171-178, September.
    4. Ben Engelhard & Joel Finkelstein & Julia Cox & Weston Fleming & Hee Jae Jang & Sharon Ornelas & Sue Ann Koay & Stephan Y. Thiberge & Nathaniel D. Daw & David W. Tank & Ilana B. Witten, 2019. "Specialized coding of sensory, motor and cognitive variables in VTA dopamine neurons," Nature, Nature, vol. 570(7762), pages 509-513, June.
    5. Elizabeth A. Amadei & Zachary V. Johnson & Yong Jun Kwon & Aaron C. Shpiner & Varun Saravanan & Wittney D. Mays & Steven J. Ryan & Hasse Walum & Donald G. Rainnie & Larry J. Young & Robert C. Liu, 2017. "Dynamic corticostriatal activity biases social bonding in monogamous female prairie voles," Nature, Nature, vol. 546(7657), pages 297-301, June.
    6. Gül Dölen & Ayeh Darvishzadeh & Kee Wui Huang & Robert C. Malenka, 2013. "Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin," Nature, Nature, vol. 501(7466), pages 179-184, September.
    7. Mattia Rigotti & Omri Barak & Melissa R. Warden & Xiao-Jing Wang & Nathaniel D. Daw & Earl K. Miller & Stefano Fusi, 2013. "The importance of mixed selectivity in complex cognitive tasks," Nature, Nature, vol. 497(7451), pages 585-590, May.
    8. James M. Otis & Vijay M. K. Namboodiri & Ana M. Matan & Elisa S. Voets & Emily P. Mohorn & Oksana Kosyk & Jenna A. McHenry & J. Elliott Robinson & Shanna L. Resendez & Mark A. Rossi & Garret D. Stuber, 2017. "Prefrontal cortex output circuits guide reward seeking through divergent cue encoding," Nature, Nature, vol. 543(7643), pages 103-107, March.
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