Brain functional networks associated with social bonding in monogamous voles

  1. María Fernanda López-Gutiérrez
  2. Zeus Gracia-Tabuenca
  3. Juan J Ortiz
  4. Francisco J Camacho
  5. Larry J Young
  6. Raúl G Paredes
  7. Nestor F Diaz  Is a corresponding author
  8. Wendy Portillo  Is a corresponding author
  9. Sarael Alcauter  Is a corresponding author
  1. Instituto de Neurobiología, Universidad Nacional Autónoma de México, Mexico
  2. Instituto de Neurobiologia, Universidad Nacional Autónoma de México, Mexico
  3. Emory University, United States
  4. Instituto Nacional de Perinatología Isidro Espinosa de los Reyes, Mexico

Abstract

Previous studies have related pair bonding in Microtus ochrogaster, the prairie vole, with plastic changes in several brain regions. However, the interactions between these socially-relevant regions have yet to be described. In this study, we used resting state magnetic resonance imaging to explore bonding behaviors and functional connectivity of brain regions previously associated with pair bonding. Thirty-two male and female prairie voles were scanned at baseline, 24h and 2 weeks after the onset of cohabitation By using network based statistics, we identified that the functional connectivity of a cortico-striatal network predicted the onset of affiliative behavior, while another predicted the amount of social interaction during a partner preference test. Furthermore, a network with significant changes in time was revealed, also showing associations with the level of partner preference. Overall, our findings revealed the association between network-level functional connectivity changes and social bonding.

Data availability

Data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 3 to 6 and supplementary source data has been provided for Figure 2. Code for Figure 5 is an R-based package available at https://cran.r-project.org/web/packages/NBR/index.html

The following data sets were generated

Article and author information

Author details

  1. María Fernanda López-Gutiérrez

    Behavioral and Cognitive Neurobiology, Instituto de Neurobiología, Universidad Nacional Autónoma de México, Querétaro, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  2. Zeus Gracia-Tabuenca

    Behavioral and Cognitive Neurobiology, Instituto de Neurobiologia, Universidad Nacional Autónoma de México, Querétaro, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  3. Juan J Ortiz

    Behavioral and Cognitive Neurobiology, Instituto de Neurobiología, Universidad Nacional Autónoma de México, Querétaro, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  4. Francisco J Camacho

    Behavioral and Cognitive Neurobiology, Instituto de Neurobiología, Universidad Nacional Autónoma de México, Querétaro, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  5. Larry J Young

    Emory University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Raúl G Paredes

    Behavioral and Cognitive Neurobiology, Instituto de Neurobiología, Universidad Nacional Autónoma de México, Querétaro, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  7. Nestor F Diaz

    Fisiología y Desarrollo Celular, Instituto Nacional de Perinatología Isidro Espinosa de los Reyes, Mexico City, Mexico
    For correspondence
    nfdiaz00@yahoo.com.mx
    Competing interests
    The authors declare that no competing interests exist.
  8. Wendy Portillo

    Behavioral and Cognitive Neurobiology, Instituto de Neurobiología, Universidad Nacional Autónoma de México, Querétaro, Mexico
    For correspondence
    portillo@unam.mx
    Competing interests
    The authors declare that no competing interests exist.
  9. Sarael Alcauter

    Behavioral and Cognitive Neurobiology, Instituto de Neurobiología, Universidad Nacional Autónoma de México, Querétaro, Mexico
    For correspondence
    alcauter@inb.unam.mx
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8182-6370

Funding

Consejo Nacional de Ciencia y Tecnología (252756)

  • Wendy Portillo

Consejo Nacional de Ciencia y Tecnología (253631)

  • Raúl G Paredes

Universidad Nacional Autónoma de México (IN202818)

  • Wendy Portillo

Universidad Nacional Autónoma de México (IN212219-3)

  • Sarael Alcauter

Universidad Nacional Autónoma de México (IN203518-3)

  • Raúl G Paredes

Instituto Nacional de Perinatología (2018-1-163)

  • Nestor F Diaz

National Institutes of Health (P50MH100023)

  • Larry J Young

Consejo Nacional de Ciencia y Tecnología (626152)

  • María Fernanda López-Gutiérrez

National Institutes of Health (P51OD011132)

  • Larry J Young

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All surgical, experimental and maintenance procedures were carried out in accordance with the "Reglamento de la Ley General de Salud en Materia de Investigación para la Salud" (Health General Law on Health Research Regulation) of the Mexican Health Ministry which follows the National Institutes of Health's "Guide for the Care and Use of Laboratory Animals" (NIH Publications No. 8023, revised 1978). The animal research protocols were approved by the bioethics committee of the Instituto de Neurobiología, UNAM (Protocol 072). All fMRI scanning sessions were performed under a mixture of isoflurane and dexmedetomidine anesthesia, and all surgery was performed under sevoflurane or a mixture of ketamine/xylazine/saline anesthesia, with every effort to minimize suffering.

Copyright

© 2021, López-Gutiérrez et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. María Fernanda López-Gutiérrez
  2. Zeus Gracia-Tabuenca
  3. Juan J Ortiz
  4. Francisco J Camacho
  5. Larry J Young
  6. Raúl G Paredes
  7. Nestor F Diaz
  8. Wendy Portillo
  9. Sarael Alcauter
(2021)
Brain functional networks associated with social bonding in monogamous voles
eLife 10:e55081.
https://doi.org/10.7554/eLife.55081

Share this article

https://doi.org/10.7554/eLife.55081

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