Neuroanatomical Markers of Social Hierarchy Recognition in Humans: A Combined ERP/MRI Study

Social hierarchy is an ubiquitous principle of social organization across animal species. Although some progress has been made in our understanding of how humans infer hierarchical identity, the neuroanatomical basis for perceiving key social dimensions of others remains unexplored. Here, we combined event-related potentials and structural MRI to reveal the neuroanatomical substrates of early status recognition. We designed a covertly simulated hierarchical setting in which participants performed a task either with a superior or with an inferior player. Participants showed higher amplitude in the N170 component when presented with a picture of a superior player compared with an inferior player. Crucially, the magnitude of this effect correlated with brain morphology of the posterior cingulate cortex, superior temporal gyrus, insula, fusiform gyrus, and caudate nucleus. We conclude that early recognition of social hierarchies relies on the structural properties of a network involved in the automatic recognition of social identity. SIGNIFICANCE STATEMENT Humans can perceive social hierarchies very rapidly, an ability that is key for social interactions. However, some individuals are more sensitive to hierarchical information than others. Currently, it is unknown how brain structure supports such fast-paced processes of social hierarchy perception and their individual differences. Here, we addressed this issue for the first time by combining the high temporal resolution of event-related potentials (ERPs) and the high spatial resolution of structural MRI. This methodological approach allowed us to unveil a novel association between ERP neuromarkers of social hierarchy perception and the morphology of several cortical and subcortical brain regions typically assumed to play a role in automatic processes of social cognition. Our results are a step forward in our understanding of the human social brain.

[1]  Martin Eimer,et al.  The Face-Sensitivity of the N170 Component , 2011, Front. Hum. Neurosci..

[2]  A. Toga,et al.  Tracking Alzheimer's Disease , 2007, Annals of the New York Academy of Sciences.

[3]  Alan C. Evans,et al.  Where in-vivo imaging meets cytoarchitectonics: The relationship between cortical thickness and neuronal density measured with high-resolution [18F]flumazenil-PET , 2011, NeuroImage.

[4]  Jennifer C. Britton,et al.  Neural correlates of social and nonsocial emotions: An fMRI study , 2006, NeuroImage.

[5]  Matthew D. Lieberman,et al.  Does Rejection Hurt? An fMRI Study of Social Exclusion , 2003, Science.

[6]  C. Zink,et al.  Know Your Place: Neural Processing of Social Hierarchy in Humans , 2008, Neuron.

[7]  N. Kanwisher,et al.  The fusiform face area subserves face perception, not generic within-category identification , 2004, Nature Neuroscience.

[8]  Atle Bjørnerud,et al.  Error-related negativity is mediated by fractional anisotropy in the posterior cingulate gyrus--a study combining diffusion tensor imaging and electrophysiology in healthy adults. , 2009, Cerebral cortex.

[9]  E. Bullmore,et al.  Social intelligence in the normal and autistic brain: an fMRI study , 1999, The European journal of neuroscience.

[10]  A. Todorov,et al.  The functional basis of face evaluation , 2008, Proceedings of the National Academy of Sciences.

[11]  Tom Foulsham,et al.  Gaze allocation in a dynamic situation: Effects of social status and speaking , 2010, Cognition.

[12]  Milos Judas,et al.  Lifespan alterations of basal dendritic trees of pyramidal neurons in the human prefrontal cortex: a layer-specific pattern. , 2008, Cerebral cortex.

[13]  Alan C. Evans,et al.  Positional and surface area asymmetry of the human cerebral cortex , 2009, NeuroImage.

[14]  Jing Yang,et al.  Brain Networks of Explicit and Implicit Learning , 2012, PloS one.

[15]  G. Deco,et al.  'If you are good, I get better': the role of social hierarchy in perceptual decision-making. , 2014, Social cognitive and affective neuroscience.

[16]  R. Sapolsky Social Status and Health in Humans and Other Animals , 2004 .

[17]  Michael G. Hardin,et al.  Attention alters neural responses to evocative faces in behaviorally inhibited adolescents , 2007, NeuroImage.

[18]  D. Amaral,et al.  Role of the Primate Amygdala in Fear-Potentiated Startle: Effects of Chronic Lesions in the Rhesus Monkey , 2007, The Journal of Neuroscience.

[19]  K. Nakamura,et al.  The human amygdala plays an important role in gaze monitoring. A PET study. , 1999, Brain : a journal of neurology.

[20]  Christopher P. Said,et al.  The social evaluation of faces: a meta-analysis of functional neuroimaging studies. , 2013, Social cognitive and affective neuroscience.

[21]  Joseph W. Barter,et al.  Subjective Socioeconomic Status Predicts Human Ventral Striatal Responses to Social Status Information , 2011, Current Biology.

[22]  R. Adolphs,et al.  Toward a Neural Basis for Social Behavior , 2013, Neuron.

[23]  B. de Gelder,et al.  Trait Dominance Promotes Reflexive Staring at Masked Angry Body Postures , 2014, PloS one.

[24]  Kirill V. Nourski,et al.  Processing of Facial Emotion in the Human Fusiform Gyrus , 2012, Journal of Cognitive Neuroscience.

[25]  W. Greenough,et al.  Plasticity of nonneuronal brain tissue: roles in developmental disorders. , 2004, Mental retardation and developmental disabilities research reviews.

[26]  Arthur W. Toga,et al.  A Probabilistic Atlas of the Human Brain: Theory and Rationale for Its Development The International Consortium for Brain Mapping (ICBM) , 1995, NeuroImage.

[27]  Matthew D. Lieberman,et al.  Social cognitive neuroscience: a review of core processes. , 2007, Annual review of psychology.

[28]  B. Fischl,et al.  Cognitive function, P3a/P3b brain potentials, and cortical thickness in aging , 2007, Human brain mapping.

[29]  A. Kling,et al.  Amygdalectomy and social behavior in the caged stump-tailed macaque (Macaca speciosa). , 1971, Folia primatologica; international journal of primatology.

[30]  R. James R. Blair,et al.  Dominance and Submission: The Ventrolateral Prefrontal Cortex and Responses to Status Cues , 2009, Journal of Cognitive Neuroscience.

[31]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[32]  G. Pourtois,et al.  Distributed and interactive brain mechanisms during emotion face perception: Evidence from functional neuroimaging , 2007, Neuropsychologia.

[33]  Alan C. Evans,et al.  A novel quantitative cross-validation of different cortical surface reconstruction algorithms using MRI phantom , 2006, NeuroImage.

[34]  C. Carver,et al.  Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: The BIS/BAS Scales , 1994 .

[35]  Anders M. Dale,et al.  Cortical volume and speed-of-processing are complementary in prediction of performance intelligence , 2005, Neuropsychologia.

[36]  Alan C. Evans,et al.  Automated 3-D extraction and evaluation of the inner and outer cortical surfaces using a Laplacian map and partial volume effect classification , 2005, NeuroImage.

[37]  Amanda V. Utevsky,et al.  Status and the Brain , 2014, PLoS biology.

[38]  S. Roux,et al.  Early visual ERPs are influenced by individual emotional skills. , 2014, Social cognitive and affective neuroscience.

[39]  N. Kanwisher,et al.  The fusiform face area: a cortical region specialized for the perception of faces , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[40]  J. Grèzes,et al.  The role of negative affectivity and social inhibition in perceiving social threat: An fMRI study , 2011, Neuropsychologia.

[41]  W. Boyce,et al.  Social Stratification, Health, and Violence in the Very Young , 2004, Annals of the New York Academy of Sciences.

[42]  Anatol C. Kreitzer,et al.  Plasticity in gray and white: neuroimaging changes in brain structure during learning , 2012, Nature Neuroscience.

[43]  D. Kumaran,et al.  The Emergence and Representation of Knowledge about Social and Nonsocial Hierarchies , 2012, Neuron.

[44]  Peter Hagoort,et al.  The Neural Integration of Speaker and Message , 2008, Journal of Cognitive Neuroscience.

[45]  Wendy Bogers,et al.  Automated subcortical segmentation using FIRST: Test–retest reliability, interscanner reliability, and comparison to manual segmentation , 2013, Human brain mapping.

[46]  Alan C. Evans,et al.  Cortical thickness analysis examined through power analysis and a population simulation , 2005, NeuroImage.

[47]  S. Quartz,et al.  The Right and the Good: Distributive Justice and Neural Encoding of Equity and Efficiency , 2008, Science.

[48]  Stephen M. Smith,et al.  A Bayesian model of shape and appearance for subcortical brain segmentation , 2011, NeuroImage.

[49]  Michael D. Hunter,et al.  Higher or lower? The functional anatomy of perceived allocentric social hierarchies , 2011, NeuroImage.

[50]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[51]  Emily B. Falk,et al.  Social status modulates neural activity in the mentalizing network , 2012, NeuroImage.

[52]  C. Ávila,et al.  The Sensitivity to Punishment and Sensitivity to Reward Questionnaire (SPSRQ) as a measure of Gray's anxiety and impulsivity dimensions. , 2001 .

[53]  S. Dehaene,et al.  Decoding the representation of learned social roles in the human brain , 2013, Cortex.

[54]  Alan C. Evans,et al.  Automated 3-D Extraction of Inner and Outer Surfaces of Cerebral Cortex from MRI , 2000, NeuroImage.

[55]  Pranjal H. Mehta,et al.  The social endocrinology of dominance: basal testosterone predicts cortisol changes and behavior following victory and defeat. , 2008, Journal of personality and social psychology.

[56]  J Leon Kenemans,et al.  Eye Tracking Unconscious Face-to-Face Confrontations , 2011, Psychological science.

[57]  John W. Harwell,et al.  Similar patterns of cortical expansion during human development and evolution , 2010, Proceedings of the National Academy of Sciences.