Are Attractive People Rewarding? Sex Differences in the Neural Substrates of Facial Attractiveness

The current study examined the neural substrates of facial attractiveness judgments. Based on the extant behavioral literature, it was hypothesized that brain regions involved in identifying the potential reward value of a stimulus would be more active when men viewed attractive women than when women viewed attractive men. To test this hypothesis, we conducted an event-related functional magnetic resonance imaging experiment during which participants provided explicit attractiveness judgments for faces of the opposite sex. These individual ratings were subsequently used to perform analyses aimed at identifying the brain regions preferentially responsive to attractive faces for both sex groups. The results revealed that brain regions comprising the putative reward circuitry (e.g., nucleus accumbens [NAcc], orbito-frontal cortex [OFC]) showed a linear increase in activation with increased judgments of attractiveness. However, further analysis also revealed sex differences in the recruitment of OFC, which distinguished attractive and unattractive faces only for male participants.

[1]  Timothy E. J. Behrens,et al.  Optimal decision making and the anterior cingulate cortex , 2006, Nature Neuroscience.

[2]  C. N. Macrae,et al.  Finding the Self? An Event-Related fMRI Study , 2002, Journal of Cognitive Neuroscience.

[3]  Alumit Ishai,et al.  Face Perception Is Modulated by Sexual Preference , 2006, Current Biology.

[4]  Philip McGuire,et al.  Brain activity during stimulus independent thought. , 1996 .

[5]  G. Fernández,et al.  Reinforcement Learning Signal Predicts Social Conformity , 2009, Neuron.

[6]  E. Hatfield,et al.  PERSONALITY PROCESSES AND INDIVIDUAL DIFFERENCES Mate Selection Preferences : Gender Differences Examined in a National Sample , 2004 .

[7]  Harold Sigall,et al.  Beauty is talent: Task evaluation as a function of the performer's physical attractiveness. , 1974 .

[8]  J. Swaddle,et al.  Testosterone increases perceived dominance but not attractiveness in human males , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[9]  A. Feingold.  Good-looking people are not what we think. , 1992 .

[10]  Lori A. Roggman,et al.  Facial Diversity and InfantPreferences for Attractive Faces , 1991 .

[11]  G. Glover,et al.  The Role of Ventral Frontostriatal Circuitry in Reward-Based Learning in Humans , 2005, The Journal of Neuroscience.

[12]  Leslie A. Zebrowitz,et al.  Facial Attractiveness: Evolutionary, Cognitive, and Social Perspectives , 2001 .

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

[14]  Aleena Hay,et al.  Attractive men induce testosterone and cortisol release in women , 2009, Hormones and Behavior.

[15]  J. Udry,et al.  Dominant looking male teenagers copulate earlier , 1994 .

[16]  William M. Kelley,et al.  Neuroanatomical Evidence for Distinct Cognitive and Affective Components of Self , 2006, Journal of Cognitive Neuroscience.

[17]  Bryan T. Denny,et al.  Medial prefrontal activity differentiates self from close others. , 2006, Social cognitive and affective neuroscience.

[18]  I. Penton-Voak,et al.  Evolutionary Psychology of Facial Attractiveness , 2002 .

[19]  J. O'Doherty,et al.  Dissociating Valence of Outcome from Behavioral Control in Human Orbital and Ventral Prefrontal Cortices , 2003, The Journal of Neuroscience.

[20]  D. Kenrick,et al.  Sex similarities and differences in preferences for short-term mates: what, whether, and why. , 2006, Journal of personality and social psychology.

[21]  L. Nystrom,et al.  Tracking the hemodynamic responses to reward and punishment in the striatum. , 2000, Journal of neurophysiology.

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

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

[24]  J. Gross,et al.  The cognitive control of emotion , 2005, Trends in Cognitive Sciences.

[25]  Astrid M. Schloerscheidt,et al.  Person Perception Across the Menstrual Cycle: Hormonal Influences on Social-Cognitive Functioning , 2002, Psychological science.

[26]  G. Alexander,et al.  Sex Differences in Adults’ Relative Visual Interest in Female and Male Faces, Toys, and Play Styles , 2009, Archives of sexual behavior.

[27]  J. Parkinson,et al.  Dissociable Contributions of the Human Amygdala and Orbitofrontal Cortex to Incentive Motivation and Goal Selection , 2003, The Journal of Neuroscience.

[28]  John B. Nezlek,et al.  Physical attractiveness in social interaction: II. Why does appearance affect social experience? , 1982 .

[29]  George Bush,et al.  The emotional counting stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division , 1998, Biological Psychiatry.

[30]  C. Senior,et al.  Beauty in the Brain of the Beholder , 2003, Neuron.

[31]  A. Damasio,et al.  Deciding Advantageously Before Knowing the Advantageous Strategy , 1997, Science.

[32]  Adrian R. Willoughby,et al.  The Medial Frontal Cortex and the Rapid Processing of Monetary Gains and Losses , 2002, Science.

[33]  Raymond J. Dolan,et al.  On the neurology of morals , 1999, Nature Neuroscience.

[34]  R. Nebes,et al.  Reliability and validity of some handedness questionnaire items. , 1974, Neuropsychologia.

[35]  T. Heatherton,et al.  Anterior cingulate cortex responds differentially to expectancy violation and social rejection , 2006, Nature Neuroscience.

[36]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

[37]  G. Rhodes.  The evolutionary psychology of facial beauty. , 2006, Annual review of psychology.

[38]  S. Petersen,et al.  Hemispheric Specialization in Human Dorsal Frontal Cortex and Medial Temporal Lobe for Verbal and Nonverbal Memory Encoding , 1998, Neuron.

[39]  S. Hyman,et al.  Acute Effects of Cocaine on Human Brain Activity and Emotion , 1997, Neuron.

[40]  M. Corbetta,et al.  Separating Processes within a Trial in Event-Related Functional MRI II. Analysis , 2001, NeuroImage.

[41]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[42]  Lori A. Roggman,et al.  Infant preferences for attractive faces: Rudiments of a stereotype? , 1987 .

[43]  Michael C. Bailey,et al.  The necessities and luxuries of mate preferences: testing the tradeoffs. , 2002, Journal of personality and social psychology.

[44]  M. L. V. Leeuwen,et al.  IS BEAUTIFUL ALWAYS GOOD? IMPLICIT BENEFITS OF FACIAL ATTRACTIVENESS , 2004 .

[45]  E. Rolls,et al.  The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology , 2004, Progress in Neurobiology.

[46]  Margo Wilson,et al.  Do pretty women inspire men to discount the future? , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[47]  R. Turner,et al.  Characterizing Dynamic Brain Responses with fMRI: A Multivariate Approach , 1995, NeuroImage.

[48]  H. Bekkering,et al.  Modulation of activity in medial frontal and motor cortices during error observation , 2004, Nature Neuroscience.

[49]  R. Dolan,et al.  Psychology: Reward value of attractiveness and gaze , 2001, Nature.

[50]  R. Wise.  Brain Reward Circuitry Insights from Unsensed Incentives , 2002, Neuron.

[51]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

[52]  John B. Nezlek,et al.  Physical attractiveness in social interaction. , 1980 .

[53]  Benjamin Y Hayden,et al.  Economic principles motivating social attention in humans , 2007, Proceedings of the Royal Society B: Biological Sciences.

[54]  E. Rolls.  The orbitofrontal cortex and reward. , 2000, Cerebral cortex.

[55]  Jane F. Banfield,et al.  Medial prefrontal activity predicts memory for self. , 2004, Cerebral cortex.

[56]  David Badre,et al.  Selection, Integration, and Conflict Monitoring Assessing the Nature and Generality of Prefrontal Cognitive Control Mechanisms , 2004, Neuron.

[57]  Salvatore Maria Aglioti,et al.  My face in yours: Visuo-tactile facial stimulation influences sense of identity , 2010, Social neuroscience.

[58]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[59]  Sterling C. Johnson,et al.  Neural correlates of self-reflection. , 2002, Brain : a journal of neurology.

[60]  D. Buss,et al.  Sex differences in human mate preferences: Evolutionary hypotheses tested in 37 cultures , 1989, Behavioral and Brain Sciences.

[61]  Jason P. Mitchell,et al.  Dissociable Medial Prefrontal Contributions to Judgments of Similar and Dissimilar Others , 2006, Neuron.

[62]  M. Ernst,et al.  Orbitofrontal cortex and human drug abuse: functional imaging. , 2000, Cerebral cortex.

[63]  Rebecca Elliott,et al.  Instrumental responding for rewards is associated with enhanced neuronal response in subcortical reward systems , 2004, NeuroImage.

[64]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

[65]  Morten L Kringelbach,et al.  Neural correlates of rapid reversal learning in a simple model of human social interaction , 2003, NeuroImage.

[66]  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.

[67]  David Wypij,et al.  The prevalence of homosexual behavior and attraction in the United States, the United Kingdom and France: Results of national population-based samples , 1995, Archives of sexual behavior.

[68]  Ingrid R Olson,et al.  Facial attractiveness is appraised in a glance. , 2005, Emotion.

[69]  M. Roesch,et al.  Neuronal Activity Related to Reward Value and Motivation in Primate Frontal Cortex , 2004, Science.

[70]  D. Hamermesh,et al.  Beauty and the Labor Market , 1993 .

[71]  Joshua W. Brown,et al.  Learned Predictions of Error Likelihood in the Anterior Cingulate Cortex , 2005, Science.

[72]  C. Keating,et al.  Gender and the physiognomy of dominance and attractiveness. , 1985 .

[73]  John E. Hunter,et al.  Physical attractiveness and intellectual competence : a meta-analytic review , 1995 .

[74]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[75]  A. Dale,et al.  Dorsal anterior cingulate cortex: A role in reward-based decision making , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[76]  Clay B. Holroyd,et al.  Dorsal anterior cingulate cortex shows fMRI response to internal and external error signals , 2004, Nature Neuroscience.

[77]  J. Langlois,et al.  Maxims or myths of beauty? A meta-analytic and theoretical review. , 2000, Psychological bulletin.

[78]  D. Perrett,et al.  Effects of sexual dimorphism on facial attractiveness , 1998, Nature.

[79]  Matthew Flatt,et al.  PsyScope: An interactive graphic system for designing and controlling experiments in the psychology laboratory using Macintosh computers , 1993 .

[80]  J. Simpson,et al.  Changes in women's mate preferences across the ovulatory cycle. , 2007, Journal of personality and social psychology.

[81]  E. Berscheid,et al.  What is beautiful is good. , 1972, Journal of personality and social psychology.

[82]  D. Perrett,et al.  Menstrual cycle alters face preference , 1999, Nature.

[83]  Scott T. Grafton,et al.  Wandering Minds: The Default Network and Stimulus-Independent Thought , 2007, Science.

[84]  P. Blumstein,et al.  Social or evolutionary theories? Some observations on preferences in human mate selection. , 1987 .

[85]  M. Corbetta,et al.  Separating Processes within a Trial in Event-Related Functional MRI I. The Method , 2001, NeuroImage.

[86]  Karl J. Friston,et al.  Characterizing Stimulus–Response Functions Using Nonlinear Regressors in Parametric fMRI Experiments , 1998, NeuroImage.

[87]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[88]  N. Ramnani,et al.  Distinct portions of anterior cingulate cortex and medial prefrontal cortex are activated by reward processing in separable phases of decision-making cognition , 2004, Biological Psychiatry.

[89]  Carl Senior,et al.  The effects of the menstrual cycle on social decision making. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[90]  E. Bora,et al.  Neurobiology of human affiliative behaviour: implications for psychiatric disorders , 2009, Current Opinion in Psychiatry.

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

[92]  D. Buss,et al.  Sexual strategies theory: an evolutionary perspective on human mating. , 1993, Psychological review.

[93]  Andrew L. Alexander,et al.  Contextual Modulation of Amygdala Responsivity to Surprised Faces , 2004, Journal of Cognitive Neuroscience.

[94]  A. Eagly,et al.  What is beautiful is good, but…: A meta-analytic review of research on the physical attractiveness stereotype. , 1991 .

[95]  W. Schultz.  Multiple reward signals in the brain , 2000, Nature Reviews Neuroscience.

[96]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[97]  Andreas Olsson,et al.  The Affective Neuroscience of Emotion: Automatic Activation, Interoception, and Emotion Regulation† , 2009 .

[98]  Michael B. Miller,et al.  Separable Routes to Human Memory Formation: Dissociating Task and Material Contributions in the Prefrontal Cortex , 2004, Journal of Cognitive Neuroscience.

[99]  H. Critchley.  The human cortex responds to an interoceptive challenge. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[100]  T. Robbins,et al.  Defining the Neural Mechanisms of Probabilistic Reversal Learning Using Event-Related Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[101]  Brian Knutson,et al.  Anticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens , 2001, The Journal of Neuroscience.

[102]  J S Fowler,et al.  Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex. , 2000, Cerebral cortex.

[103]  Sabine Landau,et al.  Attribution of social dominance and maleness to schematic faces , 1999 .

[104]  J. Hollerman,et al.  Reward processing in primate orbitofrontal cortex and basal ganglia. , 2000, Cerebral cortex.

[105]  M. Botvinick,et al.  Conflict monitoring and cognitive control. , 2001, Psychological review.

[106]  K. Grammer,et al.  Male facial attractiveness: evidence for hormone-mediated adaptive design , 2001 .

[107]  William L. White,et al.  Addiction as a Disease , 2002 .

[109]  G. Rhodes,et al.  Attractiveness and sexual behavior: Does attractiveness enhance mating success? , 2005 .

[110]  Alumit Ishai,et al.  Sex, beauty and the orbitofrontal cortex. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.