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doi: 10.1097/01.NT.0000457143.22528.34
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Neural Correlates of Social Status Identified in Macaques, Holding Promise for Human Studies

Hurley, Dan

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ARTICLE IN BRIEF

In macaque monkeys, investigators identified brain regions that appear to have a direct relationship with social status.

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For the first time, a team of researchers has identified structural and functional brain correlates of high and low social status in macaques living in experimentally manipulated groups.

Social status was defined in the study as the position macaques held in the hierarchy of the group, influencing access to food and mates and predicting health and reproductive success. The authors observed, for instance, that more dominant macaques tended to make more prosocial choices, or choices that benefitted both themselves and others, as opposed to choices that would only reward the individual.

And although subordinate animals paid attention to social cues provided by animals of any social rank, dominant animals only paid attention to cues provided by other dominant animals, they observed.

The findings, published on Sept. 2 in PLoS Biology, are already guiding US researchers conducting a similar study in humans, and may hold promise for understanding and treating neurologic disorders affecting social functioning, neuroscientists told Neurology Today.

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STUDY METHODOLOGY

Researchers from Oxford University performed a series of structural and functional MRI scans on 25 rhesus macaques, all but three of them male. They observed and recorded the monkeys' interactive behaviors, such as chasing or escaping one another, and used a standard index to rate them as either aggressive or submissive. The monkeys lived in social groups of five, four, three, and two individuals, assigned by the investigators.

An additional 11 macaques, seven of them female, were included in a second analysis of social network size. The social status of these additional animals had not been determined at the time of the study.

Data from the monkeys were used only if at least two isotropic 0.5 mm resolution MRI scans were available. The brains were aligned to a rhesus macaque atlas template, with both positive and negative contrasts used to identify gray matter regions that were larger in more dominant animals, as well as gray matter structures that were larger in subordinate animals.

An earlier study by the Oxford group, published in the journal Science in 2011, identified neural circuits in macaques associated with the size of their social networks. The new study extends those findings to the primates' social status, including the surprising finding that subordinate animals do not simply have smaller brain regions associated with their lower social status — three regions are actually larger than those of dominant animals.

“We found three subcortical regions in the macaque brain that are bigger in the more dominant macaques: the amygdala, the raphe nucleus, and the posterior hypothalamus,” study author MaryAnn Noonan, PhD, a postdoctoral research fellow in the department of experimental psychology at Oxford University, told Neurology Today. “In the subordinates, however, another three regions are bigger: the posterior putamen, the tail of the caudate, and the dorsal septum.”

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EXPERTS COMMENT

The researchers have successfully identified “key regions in macaques that seem to be critical for representing social information,” said Thalia Wheatley, PhD, an associate professor of psychological and brain sciences at Dartmouth University who is conducting similar research but was not involved with the Oxford study.

Dr. Wheatley is studying how social networks covary with neural structure and function in a cohort of MBA students. “We're now going to take a look at these subcortical areas, which we weren't really considering” before the macaque research was published, she said. “We're going to use these findings to constrain our own predictions about where to look for neural correlates of human social status. It tells us where to shine the light.”

“This is a really nice follow-up to the earlier paper the same group published a few years ago,” added Michael Platt, PhD, a neurobiologist at Duke University and co-author of a commentary on the research that was published in the same issue of PLoS One. “In that earlier study, they manipulated the size of the groups the monkeys lived in and found that the structure and function of neural networks, especially in the cortex, co-varied with the size of the social network. That was a pretty amazing result.”

Similar cortical regions in humans have been identified as playing an important role in what Dr. Platt and others call “social cognition.”

“These are processes related to attending to other individuals, determining their states of mind, their intentions, identifying and remembering individuals and their relative ranks,” he said. “Those all require some high-level functioning. But in this new paper, Dr. Noonan and colleagues were able to show that subcortical, brainstem-related regions play a surprisingly strong role strictly related to dominance and subordinance.”

In 2012, a paper by British and Danish researchers published in the Proceedings of the Royal Society B identified a number of cortical areas associated with how many friends people had on Facebook, including the gray matter density of the superior temporal sulcus, the left middle temporal gyrus, and the entorhinal cortex. [See the Neurology Today article, “Status: More Facebook Friends, Larger Brain Structures Important to Social Cognition, Study Finds,” http://bit.ly/brainFB.] The same group published a paper in Current Biology in 2012 showing that lonely individuals have less gray matter in the left posterior superior temporal sulcus.

For now, the study of neural correlates of social cognition remains one of basic science, with no clinical trials planned to test the feasibility of, for instance, manipulating the size or density of selected neural networks through medications, electromagnetic stimulation, or other means in an attempt to alter social functioning. But such randomized trials may be in the offing.

“Understanding these systems might give us information as to how to manipulate them,” said Dr. Wheatley.

Dr. Platt agreed. “The non-human primate research serves as a very strong preclinical [model] for testing various kinds of therapies,” he said. “We can test a noninvasive brain stimulation therapy or a medication, not only for efficacy and safety but also for how it affects underlying neural structures and functions.”

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LINK UP FOR MORE INFORMATION:

•. Noonan MP, Sallet J, Mars RB, et al. A neural circuit covarying with social hierarchy in macaques. PLoS Biol 2014;12(9):e1001940.

Utevsky AV, Platt ML. Status and the brain. PLos Biol 2014; 12(9):e1001941.

Sallet J, Mars RB, Noonan MP, et al. Social network size affects neural circuits in macaques. Science 2011;334(6056):697–700.

Parkinson C, Wheatley T. Old cortex, new contexts: re-purposing spatial perceptions for social cognition. Front Hum Neurosci 2013;7:645.

Kanai R, Bahrami B, Roylance R, et al. Online social network size is reflected in human brain structure. Proc Biol Sci 2012;279(1732):1327–1334.

Kanai R, Bahrami B, Duchaine B, et al. Brain structure links loneliness to social perception. Curr Biol 2012;22(20):1975–1979.

© 2014 American Academy of Neurology

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