Comparative connectomics of the primate social brain

Abstract

Social interaction is thought to provide a selection pressure for human intelligence, yet little is known about its neurobiological basis and evolution throughout the primate lineage. Recent advances in neuroimaging have enabled whole brain investigation of brain structure, function, and connectivity in humans and non-human primates (NHPs), leading to a nascent field of comparative connectomics. However, linking social behavior to brain organization across the primates remains challenging. Here, we review the current understanding of the macroscale neural mechanisms of social behaviors from the viewpoint of system neuroscience. We first demonstrate an association between the number of cortical neurons and the size of social groups across primates, suggesting a link between neural information-processing capacity and social capabilities. Moreover, by capitalizing on recent advances in species-harmonized functional MRI, we demonstrate that portions of the mirror neuron system and default-mode networks, which are thought to be important for representation of the other's actions and sense of self, respectively, exhibit similarities in functional organization in macaque monkeys and humans, suggesting possible homologies. With respect to these two networks, we describe recent developments in the neurobiology of social perception, joint attention, personality and social complexity. Together, the Human Connectome Project (HCP)-style comparative neuroimaging, hyperscanning, behavioral, and other multi-modal investigations are expected to yield important insights into the evolutionary foundations of human social behavior.

Keywords: Comparative connectomics; Cross-species; Neuroimaging; Primate; Social behavior.

Fig. 1.

Non-human primate (NHP) cortical neuron count is associated with social group size. The red vertical line indicates 95% confidence interval of human group size, predicted from the regression line of NHPs. Cortical neuron counts of monkeys (blue circle, species N = 11) were taken from Herculano-Houzel et al. (2015), and that of chimpanzee (red circle) from Collins et al. (2016). Social group sizes were based on DeCasien et al. (2017) except for Microcebus and Callimico (Eberle and Kappeler, 2006; Kappeler and Heymann, 1996; Nash and Harcourt, 1986). The black line indicates the regression line fitted to the logarithm of cortical neuron count and social group size. Regression slope was 0.66, which indicates that doubling social group size is associated with ~3 times more cortical neurons (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.).

Fig. 2.

Two contrasting brain network homologs in the primate cortex. Putative homologs of functional networks in the left hemispheres of macaque (top) and human (bottom) cerebral cortices. (A) Dense functional connectivity (FC) seeded from the left ventral premotor (vPM) cortex (areas F5a and 6r in macaque and human, respectively) reveals a fronto-parietal network mostly localized near to the primary sensory cortex. Note that positive FC extends over premotor, inferior parietal and insular cortices whereas anticorrelation extends over temporal and prefrontal cortices. (B) FC seeded from the left posterior cingulate cortex/precuneus (pC/PCC) reveals another fronto-parieto-temporal association network that exhibits positive FC in the angular gyrus (parietal area G inferior, PGi), parietal area G superior (PGs) and medial prefrontal cortices. Interestingly, the vPM and pC/PCC FC are spatially anticorrelated in both species. Annotations of cortical areas and boundaries (gray color) are according to M132 (Markov et al., 2014) and the Young Adult Human Connectome Project (YA-HCP) (Glasser et al., 2016b) parcellations in macaque and human, respectively. Human data is from the YA-HCP S1200 Release whereas the macaque data (N = 30) was obtained using standardized HCP-style data acquisition and preprocessing (Autio et al., 2020a; Glasser et al., 2013; Hayashi et al., 2021, ) and standardized in a CIFTI greyordinate space in each species (see Section 4.3). Fig. 2b was reproduced from Hayashi et al. (2021). Note that while the human HCP_MMP cortical parcellation was created based on multimodal MRI data including functional connectome, the macaque parcellation is created based on neuroanatomy but often disagrees with functional maps in some of the areas, e.g., posterior cingulate cortex (Vogt et al., 1987,2006). Data at https://balsa.wustl.edu/MxZ8N (A, Macaque), https://balsa.wustl.edu/qNG6m (A, Human), https://balsa.wustl.edu/B45Zp (B, Macaque), https://balsa.wustl.edu/lLV2K (B, Human).

Fig. 3.

Face-selective patches in marmosets, macaques, and humans. (A) Face-selective areas overlaid on the marmoset cortical surface (reproduced from Hung et al., 2015) and (B) the macaque inflated cortical surface (reproduced from Hesse and Tsao, 2020). (C) The contrast of face stimuli minus average of all stimulus classes in the working memory task in the Young-Adult Human Connectome Project S1200 (Glasser et al., 2016a). Upper: lateral view; lower: ventral view of right hemisphere. Abbreviations: AD, anterior dorsal; AF, anterior fundus; AL, anterior lateral; MF, middle fundus; ML, middle lateral; PL, posterior lateral are the six canonical face patches in the inferotemporal cortex of macaque monkey. AD, anterior dorsal; MD, middle dorsal; MV, middle ventral; O, occipital; PA, prefrontal pre-arcuate; PD, posterior dorsal; PO, prefrontal orbital; PR, perirhinal; PV, posterior ventral; PVL, prefrontal ventrolateral; TP, temporal pole are additional face related regions. Data of panel C available at https://balsa.wustl.edu/Vj9mN.

Fig. 4.

Cortical myelin flat-maps and inferior lateral parietal areal boundaries for (A) macaque and (B) human. Black labels: same areas in both species. White labels: Proposed modular differentiation, more in human than macaque. Yellow labels: Areas emergent in human but not macaque via hypothesized areal duplication or de novo areal evolution. Data available at https://balsa.wusd.edu/Z4LMz (panel A) and https://balsa.wustl.edu/VjXD9 (panel B) (For interpretation of the references to color in this figure, the reader is referred to the web version of this article.).