Toward neuroanatomical and cognitive foundations of macaque social tolerance grades
- Laboratoire de Neurosciences Cognitives et Adaptatives, UMR 7364, France
- Centre de Primatologie de l’Université de Strasbourg, France
- ICube (UMR 7357), Université de Strasbourg-CNRS, France
- Univ Lyon, Université Lyon, Inserm, Stem Cell and Brain Research Institute, U1208, France
- Wellcome Center for Neuroimaging, Dpt of Experimental Psychology, University of Oxford, United Kingdom
Figures
Figure 1 with 3 supplements
Model predictors of the amygdala and hippocampus, and volume predictions across social tolerance grades.
First row (A–D): Model predictors and responses for amygdala volume. The volume ratio is calculated as the amygdala volume divided by the total brain volume (excluding the myelencephalon and cerebellum). (A) Distribution of amygdala volume ratios across social tolerance grades. (B) Distribution of amygdala volume ratios by sex. (C) Distribution of amygdala volume ratios by husbandry condition (enclosed vs. semi-free). (D) Distribution of amygdala volume ratios by the frozen status. (E) Distribution of amygdala volume ratios by age. Second row (F–J): Model predictors and responses for hippocampal volume. The volume ratio is calculated as the hippocampal volume divided by the total brain volume (excluding the myelencephalon and cerebellum). (F) Distribution of hippocampal volume ratios across social tolerance grades. (G) Distribution of hippocampal volume ratios by sex. (H) Distribution of hippocampal volume ratios by husbandry condition (enclosed vs. semi-free). (I) Distribution of hippocampal volume ratios by the frozen status. (I) Distribution of hippocampal volume ratios by age. Panels A-E and F-J share the same y-axis.
Figure 1—figure supplement 1
Total brain volume across macaque species categorized by social grade.
Distribution of total brain volumes (in cm³) across the four social tolerance grades of the Macaca genus. Each dot represents an individual (n=42), and colors indicate social grade: red (grade 1, intolerant), orange (grade 2), olive (grade 3), and green (grade 4, tolerant). Total brain volume was computed from post-mortem MRI scans, excluding the cerebellum and myelencephalon to control for inter-individual variation in preservation quality. While total volume was included as a covariate in the statistical model, this figure provides a complementary descriptive overview of its distribution across social grades.
Figure 1—figure supplement 2
Sequence of dissection steps and MRI acquisition.
(A) Craniotomy step: Position of the cadaver and cut site. (B) Steps of scalp and skull removal using a Dremel tool associated with a flex shaft rotary tool. (C) View of the skull after skull and dura removal. (D) Extraction and formaldehyde fixation of the brain. Right lateral view of the brain after a 7-day formaldehyde fixation. (E) SARM Regions (SARM2) and 3D MRI acquisition with atlas (bottom right). Amygdala (purple; Hartig et al., 2021).
Figure 1—figure supplement 3
Set of photographs of the preparation of the fixed brain for MRI acquisitions.
(A) Air bubble removal stages in a vacuum chamber. The brain is immersed in Fluorinert FC-770 and held in position by the aquarium foam squares. The container is placed in a receptacle to catch any Fluorinert FC-770 that may spill out of the container during the procedure; (B) Placement of the aquarium foam squares inside the container of brain immersed in Fluorinert FC-770 and sealed with parafilm; (C) Placement of the container with a lift foam square to contain the residual air bubble in the top third of the container; (D) Placement of the container in the MRI antenna.
Figure 2
Parameters of the model.
(A) Parameters of the model for the amygdala volume. (B) Parameters of the model for the hippocampal volume. SG [x]: Social Grade [x] vs Social Grade [1]; SG[x]: Age (10 years): Social Grade-Age interaction.
Figure 3
Bayesian hypothesis testing using a Region of Practical Equivalence (ROPE) to assess volume (in mm3) differences between Social Grade 4 (SG4; tolerant) and Social Grade 1 (SG1; intolerant) across age, for the amygdala (left) and hippocampus (right).
Curves represent median posterior estimates, and shaded areas show 90% credible intervals. Gray bands indicate the ROPE (±0.1σ). For the amygdala, the difference is credible until ~19 years. For the hippocampus, a credible effect is observed only between ~13 and 18 years.
Figure 4
Volume predictions across social tolerance grades of the amygdala and hippocampus.
All panels represent the predictions of the multivariate Bayesian linear model, where all the variables are kept constant (including total brain volumes) in order to represent the effect of age only on the volume of amygdala and hippocampus in mm3. First row (A–D): Predicted amygdala volume across social tolerance grades over the lifespan. (A) Predicted amygdala volume as a function of age for grade 1 (intolerant) individuals. (B) Predicted amygdala volume as a function of age for grade 2 individuals. (C) Predicted amygdala volume as a function of age for grade 3 individuals. (D) Predicted amygdala volume as a function of age for grade 4 (tolerant) individuals. Second row (E–H): Predicted hippocampal volume across social tolerance grades over the lifespan. (E) Predicted hippocampal volume as a function of age for grade 1 individuals. (F) Predicted hippocampal volume as a function of age for grade 2 individuals. (G) Predicted hippocampal volume as a function of age for grade 3 individuals. (H) Predicted hippocampal volume as a function of age for grade 4 individuals. In the plots, the solid lines represent the mean predicted values, and the shaded areas indicate the 90% credible intervals, with each social grade shown in a distinct color.
Figure 5
Dataset characteristics relative to the social grade.
In red: social tolerance grade 1, orange: grade 2, olive: grade 3, and green: grade 4. (A) Social tolerance grade distribution, where grade 1 is overrepresented due to the prevalence of Macaca mulatta in laboratories. (B) Sex distribution: There was a significant imbalance in the sample, with females outnumbering males (2:1 ratio). (C) Husbandry distribution of the individuals (enclosed and semi-free ranging conditions) (D) Age distribution: The cohort had a relatively even age distribution with a notable peak in the 20 s. (E) The frozen status distribution. (F) Total brain volume distribution, excluding the myelencephalon and cerebellum due to variation in their preservation.
Tables
Table 1
Cognitive and neuroanatomical categorization of behavioral traits associated with macaque social tolerance.
| Social trait | Underlying social consequences | Cognitive dimension | Neural correlate |
|---|---|---|---|
| Complexity of communication system | Demands in interpreting social signals and adjusting communication to context (Liebal et al., 2014). | Higher socio-cognitive demands | Amygdala volume higher (Bickart et al., 2011; Sallet et al., 2011); Hippocampus volume higher (Kanai et al., 2012; Todorov et al., 2019)9,10 |
| Rate of reconciliation | Demands in recalling social history and regulating affiliation (Thierry and Sapolsky, 2000). | ||
| Male-to-male coalitions | Demands in social knowledge and strategic social decisions (Petit et al., 1997; Silk, 1999). | ||
| Cooperative behaviors | Demands in understanding intentions and coordinating actions during interactions (Demaria and Thierry, 2001; Micheletta et al., 2012). | ||
| Intensity of aggression | Demands in inhibiting impulsive behaviors and regulating emotions (Adams et al., 2015; Loyant et al., 2023). | Better inhibitory control | Amygdala volume lower (Tottenham et al., 2010); Hippocampus volume unchanged (Tottenham et al., 2010). |
| Confidence of social play | Demands in adjusting behavior and inhibiting responses in mutual interactions (Petit et al., 2008; Scopa and Palagi, 2016). | ||
| Resource distribution evenness | Demands in adjusting behavior during competitive interactions and regulating emotions (Thierry, 2007). | ||
| Kin bias (nepotism) | Kin knowledge is less informative to predict social relationships (Silk, 2002; Silk et al., 2003). | Lower predictability of social environment (heightened chronic stress) | Amygdala volume higher (Bickart et al., 2014; Sallet et al., 2011; Tottenham et al., 2010); Hippocampus volume lower (Kim et al., 2015; Lyons et al., 2001; Meyer and Hamel, 2014). |
| Dominance asymmetry | Conflicts are not always won by dominants, leading to greater outcome unpredictability (de Vries et al., 2006; Thierry, 2007). | ||
| Formal submission signals | Communication during conflict is less predictive of outcomes (Flack et al., 2006; Waller et al., 2013). | ||
| Intensity of female rank inheritance | Matrilinear knowledge is less informative to predict social relationships (Hill and Okayasu, 1995; Kutsukake, 2000). | ||
| Rate of affiliative contact | Affiliative networks are denser, reducing predictability (Duboscq et al., 2013; Massen et al., 2010; Silk et al., 2003). | ||
| Rate of counter-aggression | Subordinates are more likely to retaliate, making social outcomes less predictable (Balasubramaniam et al., 2012; Petit et al., 1997). | ||
| Rate of immature interference in mating | Mounting behaviour increases social interactions, producing more erratic social patterns (Petit et al., 2008). | ||
| Centrality of top-ranking males | Low centrality of top-ranking males decreased social network predictability (Sueur et al., 2011). | ||
| Mother protectiveness | Limits how much infants interact with other group members (Maestripieri, 1994). | Unclassified | / |
| Allomothering behavior | Reciprocal benefits for females and infants (Fairbanks, 1990). | ||
| Delayed male dispersal | Limits the range of social networks open to individuals (Thierry, 2007). |
Additional files
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Supplementary file 1
Species and data collection centers in the dataset.
- https://cdn.elifesciences.org/articles/106424/elife-106424-supp1-v1.docx
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Supplementary file 2
Detailed brain extraction procedure.
- https://cdn.elifesciences.org/articles/106424/elife-106424-supp2-v1.docx
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Supplementary file 3
Information relating to the acquisition of anatomical MRI images and the procedures for fixing and preserving post-mortem samples according to the different institutes.
- https://cdn.elifesciences.org/articles/106424/elife-106424-supp3-v1.docx
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MDAR checklist
- https://cdn.elifesciences.org/articles/106424/elife-106424-mdarchecklist1-v1.pdf
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Toward neuroanatomical and cognitive foundations of macaque social tolerance grades
eLife 14:RP106424.
https://doi.org/10.7554/eLife.106424.3
