MaryAnn P. Noonan; Jerome Sallet; Rogier B. Mars; Franz X. Neubert; Jill X. O'Reilly; Jesper L. Andersson; Anna S. Mitchell; Andrew H. Bell; Karla L. Miller; Matthew F. S. Rushworth

“ We obtained structural and fMRI scans of 25 macaques living in groups of five, four, three, and two individuals (five, twelve, one, and seven animals in each case) after assigning each animal a cardinal index of dominance on the basis of its behavioral interactions (based on [16] ) . Deformation-based morphometric (DBM) analysis was used to identify regions in the left hemisphere where GM covaried with social status. This analysis specifies the expansion/contraction required at each voxel in the group average templates scan to deform the brain to an individuals' brain. ”

“ Unlike in some other cortical regions, these neurons' activity encoded both choices that the monkey and the competitor made and activity depended on whether the monkey was engaged in a genuinely social situation, playing against another monkey, or against an inanimate computer. Being able to track another individual's behavior as well as one's own would obviously be an advantage in a social setting, and this may be why these areas increase as an individual experiences larger social network sizes ”

“ We were unable to find a relationship between dominance and cortisol metabolite regardless of whether or not effects of social network size, age, and weight were partialled out. We did, however, find evidence for a significant relationship between epiandrosterone and dominance after partialling out effects of age, weight, and social network size (r = −0.703, p = 0.023) . This pattern of results suggests that stress, at least as indexed by cortisol metabolite levels, is unlikely to mediate the relationship between the brain areas in Figures 1–8 and social status. ”

“ In order to examine how variations in the strength of interareal coupling across individuals are related to dominance, the next analysis was conducted at the “group level”—on data from all individuals. At the group level, the resulting partial correlation values were Fisher-transformed and entered into a correlation with the residual variance of individual social status values after controlling for age, weight, and sex. This analysis indexes interareal BOLD coupling between areas in individuals and the individuals' dominance statuses. ”

“ Social rank is likely to be an important determinant of such self-values. Activity in some of the regions we identified, such as parts of the striatum, is known to encode many parameters that determine the values of choices [25] , and our results suggest the same regions may also encode longer term valuation signals reflecting each individual's status. Recently neurons have been reported in the caudate that track a monkey's own social status during an interactive food-grab game with a competitor. ”

“ Furthermore, an additional test showed that the strength of coupling between fMRI-measured activity in different parts of the subcortical network changed as a function of social status.
Whether neural activity in these brain regions determines or is determined by dominance is still to be ascertained. In theory, to address this question, animals could be repeatedly assigned and reassigned from one social group to another, and an attempt could be made to carry out a longitudinal analysis of dominance effects. ”

“ In our colony, in line with national guidelines, emphasis is placed on the welfare benefits of stable group housing. Another potentially interesting approach is to test whether incidental changes in dominance that occur spontaneously can be ascribed to prior neural changes. For such an approach to work, however, it is necessary for dominance changes over time to be sufficiently substantial that successive dominance measures are uncorrelated with one another. ”

“ DS (D) coupling and dominance. Individual dominant (red) and subdominant (blue) animals in which interregional coupling was significantly positive (in subdominant animals) and negative (in dominant animals) are also shown. All other animals, where the interregional correlation was not significant at the individual subject level, are shown in black. In general, a subordinate social status was associated with positive coupling between activity levels in pairs of the areas, but as social status rose, there was more likely to be negative coupling between areas. ”

“ We examine effects in predefined ROIs using a threshold of p<0.05 and correction for multiple comparisons across all voxels in the ROI. As noted above, there are a priori reasons for thinking that dominance may be associated with the amygdala and the serotonergic system. We cannot, with a non-invasive approach such as MRI, selectively examine neurons identified as serotonergic, but we can examine whether the brainstem nuclei containing many serotonergic nuclei have any association with dominance. ”

“ The convention adopted in these studies in recent years has been to focus on effects that extend over 10 voxels [14] and so we have adopted the same approach in our study.
In addition to the whole brain approach, we also adopted a hypothesis-driven region of interest (ROI) approach widely used in human neuroimaging. ”

“ PS, principal sulcus; AS, arcuate sulcus; LOS, lateral occipital sulcus; STS, superior temporal sulcus. Hormone Metabolite Levels and Dominance
It has been suggested that some hormone levels correlate with dominance in monkeys, but the relationship is complex and influenced by numerous factors and perhaps is only clear when very large group sizes are investigated [22] , [23] . We measured two hormone-related metabolites in 13 of the male macaques participating in the second study of dominance (see Table S3) . ”

“ Note the coordinates refer to the macaque MNI atlas [56] . Each mask was first registered to F99 space and then individually registered from F99 space to each monkey structural scan. The ROI masks were 166.375 mm3 in size. We also restricted our analyses to contrasts that reflect the expected direction of effect—that is, positive correlation for AMY, PH, and RN and negative for CAUD, DS, and PPUT. The results of this analysis are shown in Figure 7. ”

“ 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.==Abstract== Author SummarySocial status is an important feature of group life in many primates. ”

“ Gadian, DG & Friston, KJ, “Detecting bilateral abnormalities with voxel-based morphometry”, Hum Brain Mapp 11: 223–232, [ [pmid:11098800 SalmondCHAshburnerJVargha-KhademFGadianDGFristonKJ] ] ↑ Watkins, KE ”

“ Watson, SJ & Yates, BJ, “Brainstem substrates of sympatho-motor circuitry identified using trans-synaptic tracing with pseudorabies virus recombinants”, J Neurosci 23: 4657–4666, [ [pmid:12805305 KermanIAEnquistLWWatsonSJYatesBJ] ] ↑ Izquierdo, A; Newman, TK; Higley, JD & Murray, EA, “Genetic modulation of cognitive flexibility and socioemotional behavior in rhesus monkeys”, Proc Natl Acad Sci U S A 104: 14128–14133, [ [pmid:17715054 IzquierdoANewmanTKHigleyJDMurrayEA] ] ↑ Dolen, G ”