Sexual coordination in a whole-brain map of prairie vole pair bonding
- Department of Integrative Biology, The University of Texas at Austin, United States
- Department of Psychology, Western University, Canada
- Cold Spring Harbor Laboratory, Cold Spring Harbor, United States
- Appel Alzheimer's Disease Research Institute, Feil Family Brain and Mind Research Institute, Weill Cornell Medicine, United States
- Institute for Neuroscience, The University of Texas at Austin, United States
Figures
Figure 1 with 1 supplement
Prairie vole reference brain and atlas generation for automatic c-Fos analysis.
(A) Generation of prairie vole (upper row) and mouse (lower row) reference brains was done with light-sheet fluorescence microscopy (LSFM) imaging. Shown is the top view of both prairie vole and …
Figure 1—figure supplement 1
Validation of the prairie vole reference atlas.
Mouse coronal sections (left column) are composed of the mouse reference brain overlaid with atlas boundaries in red on the left and, in the same sections, of tyrosine hydroxylase (TH) …
Figure 2 with 3 supplements
Study design and development of the prairie vole pair bond.
(A) Schematic of the experiment design is shown, where social behaviors (during 1 hr observations, black blocks) and immediate early gene (IEG) expression patterns are compared between mate pairs …
Figure 2—figure supplement 1
Automated tracking of social behavior states.
(A) Long-term tracking of social states was informed by automated measures of the largest body area, pair activity, and pair distance. On the left, body area is plotted against dyad distance from an …
Figure 2—figure supplement 2
Time course of social behaviors during pairing.
Group differences (mean ± standard deviation [SD]) are shown for appetitive behaviors including nose-to-nose touching, anogenital investigation, and close follows. Group differences (mean ± SD) are …
Figure 2—figure supplement 3
Associations between behavioral states and types of social interaction.
Hierarchical clustering of behavioral measures from Pearson correlations is used to group behavioral states and social interactions into three main clusters (n = 190 animals). These clusters involve …
Figure 3 with 4 supplements
A brain-wide functional network is active during pair bond formation.
(A) Map of bonding-associated voxels is shown in coronal sections (rostral to caudal) spanning the vole brain. Brightness indicates significance levels for comparisons of hypothesized and null …
Figure 3—figure supplement 1
Brain-wide patterns of immediate early gene activation during pairing.
(A) Coronal cross-sections (rostral to caudal) from female (top) and male (bottom) mating pairs are shown for the 2.5 hr timepoint group, with brightness corresponding to the mean voxel c-Fos+ cell …
Figure 3—figure supplement 2
Patterns of immediate early gene expression in brain region clusters.
Counts of c-Fos+ cells are shown for regions of interest (ROIs) associated with pair-bond development (n = 68), organized by hierarchical cluster. For each cluster, the total counts are shown on the …
Figure 3—figure supplement 3
Multi-dimensional structure of brain-wide correlation patterns.
Representations of the first three dimensions of a multi-dimensional scaling (MDS) coordinate space based on Pearson correlations between c-Fos+ cell counts in brain regions of interest (ROIs) …
Figure 3—figure supplement 4
Anatomical connectivity in brain regions associated with pairing.
(A) This heatmap shows normalized connection densities (Knox et al., 2019) from projecting to ipsilateral target regions of interest (ROIs) in the mouse brain. These ROIs are the same as, or larger …
Figure 4 with 3 supplements
Bed nucleus of the stria terminalis (BST) emerges as a central hub in the bonding network that is associated with mating success in both sexes.
(A) The first dimension of canonical correlation (CC) scores is compared across experiment groups (mean ± standard deviation [SD], n = 11-12 animals/group). (B) Heatmaps represent correlation …
Figure 4—figure supplement 1
Dimensions of cross-covariance in immediate early gene expression and social behavior.
(A) A schematic of the canonical correlation analysis (CCA) method is shown, where two sets of variables (x and y) are combined linearly to extract latent variates with the strongest correlations …
Figure 4—figure supplement 2
Intra-pair similarity in immediate early gene expression in pairing-associated brain regions.
Heatmaps represent Pearson correlation coefficients, with brain regions on the y-axis (grouped into hierarchical clusters, see Figure 3 for region of interest [ROI] and cluster labels) and …
Figure 4—figure supplement 3
Patterns of association between immediate early gene expression and behavior.
On the top, heatmaps represent Pearson correlation coefficients between selected brain regions of interest (ROIs) in mating pairs (n = 11-12 pairs/timepoint), with female data on the y-axis and male …
Figure 5
Working model for neural systems that shape stages of pair-bond development.
(A) A schematic is shown of the network of regions identified in our study, overlaid with regions involved in rodent mating behavior (Pfaus and Heeb, 1997; Veening et al., 2014; Veening and Coolen, …
Videos
Video 1
Prairie vole reference brain.
The prairie vole reference brain from light-sheet fluorescence microscopy (LSFM) imaging is shown for coronal cross-sections (rostral to caudal) and in a 3D view. Then, coronal cross-sections are …
Video 2
Patterns of whole-brain immediate early gene expression during pairing.
First, coronal cross-sections of immediate early gene (IEG) expression are shown for female (first video) and male (second video) prairie voles across all experiment groups split by partner type …
Additional files
-
Supplementary file 1
Statistical comparisons of absolute and relative brain area volumes between prairie voles and mice.
Absolute and relative area volumes (normalized to total brain volume) are compared between prairie voles (n = 190 voles, 94 males and 96 females) and male mice (n = 108) with negative binomial regression models. Absolute brain area volumes are all statistically significant bigger in the prairie vole compared to the mouse, but none the ratios of area volume (relative to the whole brain) were statistically different between species. Mean, standard deviation (SD), p-values, and false discovery rate (FDR) correction of the p-values are presented for each region.
- https://cdn.elifesciences.org/articles/87029/elife-87029-supp1-v1.xlsx
-
Supplementary file 2
Statistical comparisons of absolute and relative brain area volumes between male and female prairie voles.
Absolute and relative area volumes (normalized to total brain volume) are compared between 94 male and 96 female prairie voles with negative binomial regression models. No statistical differences were found in these sex comparisons. Mean, standard deviation (SD), p-values, and false discovery rate (FDR) correction of the p-values are presented for each region.
- https://cdn.elifesciences.org/articles/87029/elife-87029-supp2-v1.xlsx
-
Supplementary file 3
Prairie vole behavior ethogram.
Descriptions are included for automated, semi-automated, and manually scored behavioral measures.
- https://cdn.elifesciences.org/articles/87029/elife-87029-supp3-v1.xlsx
-
Supplementary file 4
Statistical results from comparisons of generalized linear models across brain regions.
Null generalized linear models (GLMs) and hypothesized (i.e., ‘bonding’) GLMs were compared with analysis of variance (ANOVA) tests for each region of interest (ROI, 824 regions, n = 189 brain samples, 11-12 samples/group). The ANOVA F-statistics are reported alongside p-values computed from permutation tests (10,000 shuffles). The corresponding q-values were computed with the false discovery rate (FDR) method to correct for multiple tests.
- https://cdn.elifesciences.org/articles/87029/elife-87029-supp4-v1.xlsx
-
MDAR checklist
- https://cdn.elifesciences.org/articles/87029/elife-87029-mdarchecklist1-v1.docx
