Implicit trustworthiness ratings of self-resembling faces activate brain centers involved in reward

On the basis of Hamilton's (Hamilton, W. D. (1964). The genetical evolution of social behavior I, II. Journal of Theoretical Biology, 7, 17-52) theory of inclusive fitness, self-facial resemblance is hypothesized as a mechanism for self-referent phenotypic matching by which humans can detect kin. To understand the mechanisms underlying pro-sociality toward self-resembling faces, we investigated the neural correlates of implicit trustworthiness ratings for self-resembling faces. Here we show that idiosyncratic trustworthiness ratings of self-resembling faces predict brain activation in the ventral inferior, middle and medial frontal gyri, substrates involved in reward processing. These findings demonstrate that neural reward centers are implicated in evaluating implicit pro-social behaviors toward self-resembling faces. These findings suggest that humans have evolved to use neurocomputational architecture dedicated to face processing and reward evaluation for the differentiation of kin, which drives implicit idiosyncratic affectively regulated social interactions.

[1]  D. Perrett,et al.  Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness , 2003, Neuropsychologia.

[2]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[3]  W. Hamilton The genetical evolution of social behaviour. I. , 1964, Journal of theoretical biology.

[4]  Alan C. Evans,et al.  A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[5]  Thomas E. Myers,et al.  Reactions to children's faces: Males are more affected by resemblance than females are, and so are their brains , 2004 .

[6]  D. Ariely,et al.  Beautiful Faces Have Variable Reward Value fMRI and Behavioral Evidence , 2001, Neuron.

[7]  Colin Camerer,et al.  Neural Systems Responding to Degrees of Uncertainty in Human Decision-Making , 2005, Science.

[8]  V. Quinsey,et al.  Parental Investment and Resemblance: Replications, Refinements, and Revisions , 2007 .

[9]  G. Gallup,et al.  Reactions to children's faces: Resemblance affects males more than females , 2002 .

[10]  E. Rolls,et al.  Abstract reward and punishment representations in the human orbitofrontal cortex , 2001, Nature Neuroscience.

[11]  B. Neff,et al.  Promiscuity Drives Self-Referent Kin Recognition , 2006, Current Biology.

[12]  L. Cosmides,et al.  The architecture of human kin detection , 2007, Nature.

[13]  D. Perrett,et al.  Women's attractiveness judgments of self-resembling faces change across the menstrual cycle , 2005, Hormones and Behavior.

[14]  Stephen M. Smith,et al.  General multilevel linear modeling for group analysis in FMRI , 2003, NeuroImage.

[15]  Andrew D. Engell,et al.  Implicit Trustworthiness Decisions: Automatic Coding of Face Properties in the Human Amygdala , 2007, Journal of Cognitive Neuroscience.

[16]  M. Reuter,et al.  Genetically Determined Differences in Learning from Errors , 2007, Science.

[17]  S. Platek,et al.  The neural basis of facial resemblance , 2008, Neuroscience Letters.

[18]  J. Haxby,et al.  Neural response to the visual familiarity of faces , 2006, Brain Research Bulletin.

[19]  H. Breiter,et al.  Functional Magnetic Resonance Imaging of Brain Reward Circuitry in the Human , 1999, Annals of the New York Academy of Sciences.

[20]  Mark S. Seidenberg,et al.  Neural Systems Underlying the Recognition of Familiar and Newly Learned Faces , 2000, The Journal of Neuroscience.

[21]  T. Chartrand,et al.  THE UNBEARABLE AUTOMATICITY OF BEING , 1999 .

[22]  James M. Kilner,et al.  Brain systems for assessing facial attractiveness , 2007, Neuropsychologia.

[23]  Steven M. Platek,et al.  Facial Resemblance Exaggerates Sex-Specific Jealousy-Based Decisions 1 , 2007 .

[24]  J. M. Smith,et al.  Four Little Books about Evolution@@@Neanderthal, Bandits and Farmers: How Agriculture Really Began@@@Shaping Life: Genes, Embryos and Evolution@@@Divided Labours: An Evolutionary View of Women at Work@@@The Truth about Cinderella: A Darwinian View of Parental Love , 1999 .

[25]  Bernard Tiddeman,et al.  Prototyping and Transforming Facial Textures for Perception Research , 2001, IEEE Computer Graphics and Applications.

[26]  Ellen Leibenluft,et al.  Social and emotional attachment in the neural representation of faces , 2004, NeuroImage.

[27]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[28]  J. Haxby,et al.  Neural systems for recognition of familiar faces , 2007, Neuropsychologia.

[29]  T. Pettigrew,et al.  Energy conservation behavior: The difficult path from information to action. , 1986 .

[30]  Margo Wilson,et al.  Whom are newborn babies said to resemble , 1982 .

[31]  V. Quinsey,et al.  The influence of infant facial cues on adoption preferences , 2002, Human nature.

[32]  Feroze B. Mohamed,et al.  Sex differences in the neural correlates of child facial resemblance: an event-related fMRI study , 2005, NeuroImage.

[33]  Joan Y. Chiao,et al.  Differential responses in the fusiform region to same-race and other-race faces , 2001, Nature Neuroscience.

[34]  L. DeBruine,et al.  Trustworthy but not lust-worthy: context-specific effects of facial resemblance , 2005, Proceedings of the Royal Society B: Biological Sciences.

[35]  Thomas E. Myers,et al.  How much paternal resemblance is enough? Sex differences in hypothetical investment decisions but not in the detection of resemblance , 2003 .

[36]  W. Hamilton The genetical evolution of social behaviour. II. , 1964, Journal of theoretical biology.

[37]  Mark W. Woolrich,et al.  Multilevel linear modelling for FMRI group analysis using Bayesian inference , 2004, NeuroImage.

[38]  D. Perrett,et al.  Social Perception of Facial Resemblance in Humans , 2008, Archives of sexual behavior.

[39]  Samuel M. McClure,et al.  Predictability Modulates Human Brain Response to Reward , 2001, The Journal of Neuroscience.

[40]  J. O'Doherty,et al.  Automatic and intentional brain responses during evaluation of trustworthiness of faces , 2002, Nature Neuroscience.

[41]  Janine Willis,et al.  First Impressions , 2006, Psychological science.