A neural circuit covarying with social hierarchy in macaques

• Published in: PLoS biology 2014-09, Vol.12 (9), p.e1001940-e1001940
• Main Authors: Noonan, MaryAnn P, Sallet, Jerome, Mars, Rogier B, Neubert, Franz X, O'Reilly, Jill X, Andersson, Jesper L, Mitchell, Anna S, Bell, Andrew H, Miller, Karla L, Rushworth, Matthew F S
• Format: Article
• Language: English
• Subjects: Amygdala - physiology; Animal cognition; Animal communication; Animals; Biology and Life Sciences; Brain Mapping; Corpus Striatum - physiology; Emotions - physiology; Female; Gray Matter - physiology; Hierarchy, Social; Hypothalamus - physiology; Macaca mulatta - physiology; Macaca mulatta - psychology; Macaques; Magnetic Resonance Imaging; Male; Midbrain Raphe Nuclei - physiology; Nerve Net - physiology; Neural circuitry; Neurological research; NMR; Nuclear magnetic resonance; Physiological aspects; Prefrontal Cortex - physiology; Social networks; Temporal Lobe - physiology; Zoological research
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.1001940

Despite widespread interest in social dominance, little is known of its neural correlates in primates. We hypothesized that social status in primates might be related to individual variation in subcortical brain regions implicated in other aspects of social and emotional behavior in other mammals. To examine this possibility we used magnetic resonance imaging (MRI), which affords the taking of quantitative measurements noninvasively, both of brain structure and of brain function, across many regions simultaneously. We carried out a series of tests of structural and functional MRI (fMRI) data in 25 group-living macaques. First, a deformation-based morphometric (DBM) approach was used to show that gray matter in the amygdala, brainstem in the vicinity of the raphe nucleus, and reticular formation, hypothalamus, and septum/striatum of the left hemisphere was correlated with social status. Second, similar correlations were found in the same areas in the other hemisphere. Third, similar correlations were found in a second data set acquired several months later from a subset of the same animals. Fourth, the strength of coupling between fMRI-measured activity in the same areas was correlated with social status. The network of subcortical areas, however, had no relationship with the sizes of individuals' social networks, suggesting the areas had a simple and direct relationship with social status. By contrast a second circuit in cortex, comprising the midsuperior temporal sulcus and anterior and dorsal prefrontal cortex, covaried with both individuals' social statuses and the social network sizes they experienced. This cortical circuit may be linked to the social cognitive processes that are taxed by life in more complex social networks and that must also be used if an animal is to achieve a high social status.