Changes in male brain responses to emotional faces from adolescence to middle age

Facial emotion perception is fundamental to human social behaviour, and changes with age. Nevertheless, age-related differences in the relative activation of components of emotion processing networks are poorly understood. Thus we measured brain activity with event-related fMRI in 40 right handed healthy male controls, age range 8-50 years, during implicit processing of fearful, disgusted, and a control condition of neutral facial expressions. There was a significant negative correlation between increasing age and neural response to fearful and disgusted expressions in dorsomedial prefrontal cortex (BA 10), and middle frontal gyri (BA 6). Hence, in healthy subjects, the functional anatomy of facial emotion processing is not 'hard-wired', but undergoes progressive change into adulthood. Possible explanations for the age-related changes in dorsomedial and middle frontal cortical activity may include a reduction in the attentional demands of appraising facial expressions as perceptual skill increases, or changes in processing the self-relevance of facial expressions during social and cognitive development.

[1]  F. Craik,et al.  In search of the emotional self: an fMRI study using positive and negative emotional words. , 2003, The American journal of psychiatry.

[2]  L. Carstensen,et al.  Emotional experience in everyday life across the adult life span. , 2000, Journal of personality and social psychology.

[3]  Margot J. Taylor,et al.  Children recruit distinct neural systems for implicit emotional face processing , 2006, Neuroreport.

[4]  David I. Perrett,et al.  Amygdala response to facial expressions in children and adults , 2000, NeuroImage.

[5]  C. Frith,et al.  “Hey John”: Signals Conveying Communicative Intention toward the Self Activate Brain Regions Associated with “Mentalizing,” Regardless of Modality , 2003, The Journal of Neuroscience.

[6]  T. H. Joffe,et al.  Social pressures have selected for an extended juvenile period in primates. , 1997, Journal of human evolution.

[7]  William D S Killgore,et al.  Sex-specific developmental changes in amygdala responses to affective faces , 2001, Neuroreport.

[8]  Christina Gloeckner,et al.  Modern Applied Statistics With S , 2003 .

[9]  L. Carstensen,et al.  Taking time seriously. A theory of socioemotional selectivity. , 1999, The American psychologist.

[10]  R. Schultz.  Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area , 2005, International Journal of Developmental Neuroscience.

[11]  David I. Perrett,et al.  Facial expressions of emotion: Stimuli and tests (FEEST) , 2002 .

[12]  N. Sadato,et al.  Age‐related differences in the medial temporal lobe responses to emotional faces as revealed by fMRI , 2002, Hippocampus.

[13]  Debra A. Gusnard,et al.  Being a self: Considerations from functional imaging , 2005, Consciousness and Cognition.

[14]  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.

[15]  K. Kendler,et al.  A typological model of schizophrenia based on age at onset, sex and familial morbidity , 1994, Acta psychiatrica Scandinavica.

[16]  Leanne M Williams,et al.  The Mellow Years?: Neural Basis of Improving Emotional Stability over Age , 2006, The Journal of Neuroscience.

[17]  J. Haxby,et al.  Human neural systems for face recognition and social communication , 2002, Biological Psychiatry.

[18]  S. Rauch,et al.  Neurobiology of emotion perception I: the neural basis of normal emotion perception , 2003, Biological Psychiatry.

[19]  Joshua D. Greene,et al.  How (and where) does moral judgment work? , 2002, Trends in Cognitive Sciences.

[20]  Istvan Molnar-Szakacs,et al.  Watching social interactions produces dorsomedial prefrontal and medial parietal BOLD fMRI signal increases compared to a resting baseline , 2004, NeuroImage.

[21]  Evelyn C. Ferstl,et al.  The Anterior Frontomedian Cortex and Evaluative Judgment: An fMRI Study , 2002, NeuroImage.

[22]  G. McCarthy,et al.  Dissociable prefrontal brain systems for attention and emotion , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Frank Schneider,et al.  Dependence of amygdala activation on echo time: Results from olfactory fMRI experiments , 2006, NeuroImage.

[24]  William N. Venables,et al.  Modern Applied Statistics with S , 2010 .

[25]  Michael J. Brammer,et al.  A preferential increase in the extrastriate response to signals of danger , 2003, NeuroImage.

[26]  Robin M. Chan,et al.  Age-related differences in brain activation during emotional face processing , 2003, Neurobiology of Aging.

[27]  G. Fink,et al.  Neural activation during selective attention to subjective emotional responses , 1997, Neuroreport.

[28]  Corinna E Löckenhoff,et al.  Socioemotional selectivity theory, aging, and health: the increasingly delicate balance between regulating emotions and making tough choices. , 2004, Journal of personality.

[29]  F. Craik,et al.  Cognition through the lifespan: mechanisms of change , 2006, Trends in Cognitive Sciences.

[30]  Kevin N. Ochsner,et al.  For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion , 2004, NeuroImage.

[31]  Andrew N. Meltzoff,et al.  Brain Activation during Face Perception: Evidence of a Developmental Change , 2005, Journal of Cognitive Neuroscience.

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

[33]  R. Blair,et al.  Facial expressions, their communicatory functions and neuro-cognitive substrates. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[34]  M. Phillips,et al.  Annotation: Development of facial expression recognition from childhood to adolescence: behavioural and neurological perspectives. , 2004, Journal of child psychology and psychiatry, and allied disciplines.

[35]  Ellen Leibenluft,et al.  Adolescent immaturity in attention-related brain engagement to emotional facial expressions , 2003, NeuroImage.

[36]  Tammy English,et al.  Amygdala Responses to Emotionally Valenced Stimuli in Older and Younger Adults , 2004, Psychological science.

[37]  Mara Mather,et al.  Aging and Attentional Biases for Emotional Faces , 2003, Psychological science.

[38]  R. Dolan,et al.  Distant influences of amygdala lesion on visual cortical activation during emotional face processing , 2004, Nature Neuroscience.

[39]  C. Frith,et al.  Development and neurophysiology of mentalizing. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[40]  G. Fink,et al.  Cerebral Representation of One’s Own Past: Neural Networks Involved in Autobiographical Memory , 1996, The Journal of Neuroscience.

[41]  F. Bermpohl,et al.  Cortical midline structures and the self , 2004, Trends in Cognitive Sciences.

[42]  S. Rauch,et al.  Neurobiology of emotion perception II: implications for major psychiatric disorders , 2003, Biological Psychiatry.