Brain functional networks associated with social bonding in monogamous voles

  1. M Fernanda López-Gutiérrez
  2. Zeus Gracia-Tabuenca
  3. Juan J Ortiz
  4. Francisco J Camacho
  5. Larry J Young
  6. Raúl G Paredes
  7. Néstor F Díaz  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. Silvio O Conte Center for Oxytocin and Social Cognition, Center for Translational Social Neuroscience, Yerkes National Primate Research Center, Department of Psychiatry and Behavioral Sciences, Emory University, United States
  3. Escuela Nacional de Estudios Superiores, Unidad Juriquilla, Universidad Nacional Autónoma de México, Mexico
  4. Instituto Nacional de Perinatología Isidro Espinosa de los Reyes, Mexico
6 figures, 1 table and 1 additional file

Figures

Figure 1 with 5 supplements
Experimental design and brain regions of interest.

(A) Sequence of experiments during a 30 day period: Female voles were bilaterally ovariectomized before MR and behavioral protocols. After being allowed to recover from surgery for 10 days, silastic …

Figure 1—figure supplement 1
Representative rsfMRI time series.

(a–p) Representative rsfMRI time series of regions of interest (ROIs). For each ROI, the time series are shown before (Raw) and after pre-processing (Pre-processed). ACC: anterior cingulate cortex. …

Figure 1—figure supplement 2
Average functional connectivity correlation matrices between ROIs in all subjects shown by MR acquisition sessions: baseline, 24 hr, and 2 weeks.

(A) Pearson’s correlation values of rsfMRI time-series connectivity matrices. (B) Partial-correlation values of rsfMRI time-series connectivity matrices. (C) Fisher z-transformed, rsfMRI time-series …

Figure 1—figure supplement 3
Representative rsfMRI and anatomical raw data and examples of the registration steps.

(a) Raw SE-EPI rsfMRI image; (b) raw anatomic image; (c) brain extraction and bias field correction of the anatomic image; (d) registration of the anatomic data (grayscale) to the prairie vole brain …

Figure 1—figure supplement 4
Average seed-based functional connectivity maps for each of the 16 ROIs here explored.

For every subject, session, and ROI, the average time series from the ROI is extracted and the functional connectivity with every voxel of the brain is estimated as the Pearson’s correlation. Then …

Figure 1—figure supplement 5
Vole temperature during acquisition, discarded images and signal-to-noise ratio.

(A) Prairie vole temperatures during MR acquisition sessions. A separate sub-sample was used to evaluate the design of the anesthesia protocol on physiological data in both male (n = 3) and female …

Relationships between baseline functional connectivity and affiliative behavior (huddling) during cohabitation with mating in male and female prairie voles.

(A) Representation of a prairie vole brain with regions (nodes) that constitute the network with a significant negative association with huddling latency. Scatter-plot graphs (B–J) of the …

Figure 2—source data 1

Functional connectivity values of edges that correlate significantly with huddling latencies in prairie voles.

https://cdn.elifesciences.org/articles/55081/elife-55081-fig2-data1-v2.xlsx
Figure 3 with 1 supplement
Partner preference test.

(A) Representative figure showing the design of the arena in which voles were tested for partner preference test. (B) Between 48 and 72 hr of cohabitation, partner preference was evaluated on each …

Figure 3—source data 1

Values of parter preference index obtained from the proportion of time spent on social incentive areas related to the partner and stranger voles.

https://cdn.elifesciences.org/articles/55081/elife-55081-fig3-data1-v2.csv
Figure 3—figure supplement 1
Partner preference indexes at two different time points.

No significant differences were found between Partner preference indexes obtained 48 hr after the onset of cohabitation (N = 16) in male (n = 7) and female (n = 9) prairie voles, with Partner …

Figure 3—figure supplement 1—source data 1

Partner preference index comparison at different PPT test times (48 vs 72 hr) from the onset of cohabitation.

https://cdn.elifesciences.org/articles/55081/elife-55081-fig3-figsupp1-data1-v2.csv
Figure 4 with 1 supplement
Relationships between functional connectivity 24 hr after the onset of cohabitation and social interaction during partner preference test in male and female prairie voles.

(A) Representation of a prairie vole brain with regions (nodes) that constitute the network with a significant negative association with the amount of social interaction during the PPT. Scatter-plot …

Figure 4—source data 1

Values of percentage of time spent on social incentive areas related to the partner and stranger voles.

https://cdn.elifesciences.org/articles/55081/elife-55081-fig4-data1-v2.xlsx
Figure 4—figure supplement 1
Relationships between social behaviors in the prairie vole.

Huddling latency was measured during the first hours of cohabitation, while percentage of time on social incentive areas and partner preference index were calculated from the partner preference test …

Figure 5 with 2 supplements
Network-wide changes in time in brain functional connectivity of female and male prairie voles.

(A) NBR analysis via Linear mixed models (LMM) analysis results represented in a prairie vole brain with regions (nodes) comprising the brain network that undergoes significant changes in functional …

Figure 5—source data 1

Functional connectivity values that changed significantly across sessions (Ses; 1, 2, and 3) in male and female prairie voles (females: F; males: M).

NA: data not available.

https://cdn.elifesciences.org/articles/55081/elife-55081-fig5-data1-v2.csv
Figure 5—source data 2

Estimated marginal means (EMM) post hoc comparisons values obtained from the longitudinal analysis of functional connectivity data (edge), via linear mixed models with NBR.

Values are corrected for a false discovery rate (FDR) of q < 0.05 (PH_pFDR).

https://cdn.elifesciences.org/articles/55081/elife-55081-fig5-data2-v2.csv
Figure 5—figure supplement 1
Control regions for the longitudinal analysis of rsfMRI data.

3D views of the nine control region masks embedded within the prairie vole template: primary auditory area (AUDp), the cerebellar cortex (CBX), forceps minor of the corpus callosum (fmi), …

Figure 5—figure supplement 2
Ten components gICA.

(a) Sensory/motor components, including motor cortex (IC01, IC07), somatosensory cortex (IC06), parietal cortex (IC01), colliculi (IC08), and olfactory bulb (IC09). (b) Default-mode network (IC04). …

Relationships between relevant network connections and partner preference index during cohabitation with mating in male and female prairie voles.

Scatterplots (A–C) that show significant correlations (with best line fit) between functional connectivity (Fisher z-transformed partial-correlation values) and partner preference index in network …

Figure 6—source data 1

Functional connectivity values of edges that correlate significantly with partner preference index of prairie voles in each session: session 1 (s01), session 2 (s02), and session 3 (s03), which correspond to baseline, 24 hr, and 2 weeks after the onset of cohabitation, respectively.

https://cdn.elifesciences.org/articles/55081/elife-55081-fig6-data1-v2.xlsx

Tables

Key resources table
Reagent type
(species) or resource
DesignationSource or referenceIdentifiersAdditional information
Software, algorithmNetwork-Based Statistic ToolboxPMID:20600983RRID:SCR_002454
Software, algorithmNetwork-Based R-Statisticsdoi: 10.1101/2020.11.07.373019RRID:SCR_019114
Software, algorithmnlmeCRANRRID:SCR_015655
Software, algorithmFSLPMID:21979382RRID:SCR_002823
Software, algorithmANTS – Advanced Normalization ToolSPMID:20851191RRID:SCR_004757
Software, algorithmggplot2CRANRRID:SCR_014601
Software, algorithmGraphPad PrismGraphPadRRID:SCR_002798
Software, algorithmMATLABMathWorksRRID:SCR_001622
Chemical compound, drugDexmedetomidineZoetisPubChem CID:
5311068
s.c. bolus dose:0.05 mg/kg
Chemical compound, drugIsofluranePiSAPubChem CID: 3763
Chemical compound, drugβ-Estradiol 3-benzoateSigmaPubChem CID: 222757Dose: 0.5 mg/mL dissolved in corn oil
OtherDow Corning Silastic Laboratory TubingThermoFisher ScientificLength of tubing for capsule: 1.7 cm

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