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.

Metrics

  • 3,197
    views
  • 320
    downloads
  • 24
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Neuroscience
    Sven Ohl, Martin Rolfs
    Research Article

    Detecting causal relations structures our perception of events in the world. Here, we determined for visual interactions whether generalized (i.e. feature-invariant) or specialized (i.e. feature-selective) visual routines underlie the perception of causality. To this end, we applied a visual adaptation protocol to assess the adaptability of specific features in classical launching events of simple geometric shapes. We asked observers to report whether they observed a launch or a pass in ambiguous test events (i.e. the overlap between two discs varied from trial to trial). After prolonged exposure to causal launch events (the adaptor) defined by a particular set of features (i.e. a particular motion direction, motion speed, or feature conjunction), observers were less likely to see causal launches in subsequent ambiguous test events than before adaptation. Crucially, adaptation was contingent on the causal impression in launches as demonstrated by a lack of adaptation in non-causal control events. We assessed whether this negative aftereffect transfers to test events with a new set of feature values that were not presented during adaptation. Processing in specialized (as opposed to generalized) visual routines predicts that the transfer of visual adaptation depends on the feature similarity of the adaptor and the test event. We show that the negative aftereffects do not transfer to unadapted launch directions but do transfer to launch events of different speeds. Finally, we used colored discs to assign distinct feature-based identities to the launching and the launched stimulus. We found that the adaptation transferred across colors if the test event had the same motion direction as the adaptor. In summary, visual adaptation allowed us to carve out a visual feature space underlying the perception of causality and revealed specialized visual routines that are tuned to a launch’s motion direction.

    1. Neuroscience
    Gergely F Turi, Sasa Teng ... Yueqing Peng
    Research Article

    Synchronous neuronal activity is organized into neuronal oscillations with various frequency and time domains across different brain areas and brain states. For example, hippocampal theta, gamma, and sharp wave oscillations are critical for memory formation and communication between hippocampal subareas and the cortex. In this study, we investigated the neuronal activity of the dentate gyrus (DG) with optical imaging tools during sleep-wake cycles in mice. We found that the activity of major glutamatergic cell populations in the DG is organized into infraslow oscillations (0.01–0.03 Hz) during NREM sleep. Although the DG is considered a sparsely active network during wakefulness, we found that 50% of granule cells and about 25% of mossy cells exhibit increased activity during NREM sleep, compared to that during wakefulness. Further experiments revealed that the infraslow oscillation in the DG was correlated with rhythmic serotonin release during sleep, which oscillates at the same frequency but in an opposite phase. Genetic manipulation of 5-HT receptors revealed that this neuromodulatory regulation is mediated by Htr1a receptors and the knockdown of these receptors leads to memory impairment. Together, our results provide novel mechanistic insights into how the 5-HT system can influence hippocampal activity patterns during sleep.