Brain functional networks associated with social bonding in monogamous voles
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
-
Data from: Brain functional networks associated with social bonding in monogamous volesDryad Digital Repository, 10.5061/dryad.1rn8pk0q9.
Article and author information
Author details
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
-
- 3,215
- views
-
- 322
- downloads
-
- 24
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
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)
Further reading
-
- Neuroscience
Cerebellar dysfunction leads to postural instability. Recent work in freely moving rodents has transformed investigations of cerebellar contributions to posture. However, the combined complexity of terrestrial locomotion and the rodent cerebellum motivate new approaches to perturb cerebellar function in simpler vertebrates. Here, we adapted a validated chemogenetic tool (TRPV1/capsaicin) to describe the role of Purkinje cells — the output neurons of the cerebellar cortex — as larval zebrafish swam freely in depth. We achieved both bidirectional control (activation and ablation) of Purkinje cells while performing quantitative high-throughput assessment of posture and locomotion. Activation modified postural control in the pitch (nose-up/nose-down) axis. Similarly, ablations disrupted pitch-axis posture and fin-body coordination responsible for climbs. Postural disruption was more widespread in older larvae, offering a window into emergent roles for the developing cerebellum in the control of posture. Finally, we found that activity in Purkinje cells could individually and collectively encode tilt direction, a key feature of postural control neurons. Our findings delineate an expected role for the cerebellum in postural control and vestibular sensation in larval zebrafish, establishing the validity of TRPV1/capsaicin-mediated perturbations in a simple, genetically tractable vertebrate. Moreover, by comparing the contributions of Purkinje cell ablations to posture in time, we uncover signatures of emerging cerebellar control of posture across early development. This work takes a major step towards understanding an ancestral role of the cerebellum in regulating postural maturation.
-
- Neuroscience
When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.