Anterior Cingulate Activation Is Related to a Positivity Bias and Emotional Stability in Successful Aging

BACKGROUND Behavioral studies consistently reported an increased preference for positive experiences in older adults. The socio-emotional selectivity theory explains this positivity effect with a motivated goal shift in emotion regulation, which probably depends on available cognitive resources. The present study investigates the neurobiological mechanism underlying this hypothesis. METHODS Functional magnetic resonance imaging data were acquired in 21 older and 22 young subjects while performing a spatial-cueing paradigm that manipulates attentional load on emotional face distracters. We focused our analyses on the anterior cingulate cortex as a key structure of cognitive control of emotion. RESULTS Elderly subjects showed a specifically increased distractibility by happy faces when more attentional resources were available for face processing. This effect was paralleled by an increased engagement of the rostral anterior cingulate cortex, and this frontal engagement was significantly correlated with emotional stability. CONCLUSIONS The current study highlights how the brain might mediate the tendency to preferentially engage in positive information processing in healthy aging. The finding of a resource-dependency of this positivity effect suggests demanding self-regulating processes that are related to emotional well-being. These findings are of particular relevance regarding implications for the understanding, treatment, and prevention of nonsuccessful aging like highly prevalent late-life depression.

[1]  M. Whisman,et al.  Neuroticism as a common feature of the depressive and anxiety disorders: a test of the revised integrative hierarchical model in a national sample. , 2006, Journal of abnormal psychology.

[2]  R. Hales,et al.  J Neuropsychiatry Clin Neurosci , 1992 .

[3]  T. Egner,et al.  Dissociable neural systems resolve conflict from emotional versus nonemotional distracters. , 2008, Cerebral cortex.

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

[5]  Christian Büchel,et al.  The influence of directed covert attention on emotional face processing , 2010, NeuroImage.

[6]  E. Holmes,et al.  The modification of attentional bias to emotional information: A review of the techniques, mechanisms, and relevance to emotional disorders , 2010, Cognitive, affective & behavioral neuroscience.

[7]  Remco J. Renken,et al.  Neuroticism modulates amygdala—prefrontal connectivity in response to negative emotional facial expressions , 2010, NeuroImage.

[8]  Sarah E. MacPherson,et al.  Age, executive function, and social decision making: a dorsolateral prefrontal theory of cognitive aging. , 2002, Psychology and aging.

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

[10]  E. Phelps,et al.  Neural mechanisms mediating optimism bias , 2007, Nature.

[11]  Kevin N. Ochsner,et al.  Neural Systems Supporting the Control of Affective and Cognitive Conflicts , 2009, Journal of Cognitive Neuroscience.

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

[13]  A. Bowling,et al.  What is successful ageing and who should define it? , 2005, BMJ : British Medical Journal.

[14]  G. Glover,et al.  Reflecting upon Feelings: An fMRI Study of Neural Systems Supporting the Attribution of Emotion to Self and Other , 2004, Journal of Cognitive Neuroscience.

[15]  D. Johnson,et al.  Goal-directed attentional deployment to emotional faces and individual differences in emotional regulation , 2009 .

[16]  M. Eysenck,et al.  Personality and Individual Differences: A Natural Science Approach , 1985 .

[17]  D. Pandya,et al.  Cingulate cortex of the rhesus monkey: II. Cortical afferents , 1987, The Journal of comparative neurology.

[18]  Roberto Cabeza,et al.  Aging Gracefully: Compensatory Brain Activity in High-Performing Older Adults , 2002, NeuroImage.

[19]  Anthony R. McIntosh,et al.  Task-related activity in prefrontal cortex and its relation to recognition memory performance in young and old adults , 2005, Neuropsychologia.

[20]  D. Derryberry,et al.  Attentional interference effects of emotional pictures: threat, negativity, or arousal? , 2005, Emotion.

[21]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[22]  C. Büchel,et al.  Ventromedial Prefrontal Cortex Processing During Emotional Evaluation in Late-Life Depression: A Longitudinal Functional Magnetic Resonance Imaging Study , 2008, Biological Psychiatry.

[23]  L. Carstensen The Influence of a Sense of Time on Human Development , 2006, Science.

[24]  M. Reuter,et al.  Personality and emotion: test of Gray's personality theory by means of an fMRI study. , 2004, Behavioral neuroscience.

[25]  R. Dolan,et al.  The neural basis of mood-congruent processing biases in depression. , 2002, Archives of general psychiatry.

[26]  M. Posner,et al.  Attention and the detection of signals. , 1980, Journal of experimental psychology.

[27]  M. Mather,et al.  Aging and motivated cognition: the positivity effect in attention and memory , 2005, Trends in Cognitive Sciences.

[28]  L. Pessoa How do emotion and motivation direct executive control? , 2009, Trends in Cognitive Sciences.

[29]  Faith M. Gunning-Dixon,et al.  Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume , 2004, Neurobiology of Aging.

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

[31]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[32]  Gereon R Fink,et al.  Cerebral correlates of alerting, orienting and reorienting of visuospatial attention: an event-related fMRI study , 2004, NeuroImage.

[33]  J. Duncan,et al.  Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli , 2004, Nature Neuroscience.

[34]  Mara Mather,et al.  Aging and goal-directed emotional attention: distraction reverses emotional biases. , 2007, Emotion.

[35]  H. Barbas,et al.  Synapses with Inhibitory Neurons Differentiate Anterior Cingulate from Dorsolateral Prefrontal Pathways Associated with Cognitive Control , 2009, Neuron.

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

[37]  G. Miller,et al.  Regret intensity, diurnal cortisol secretion, and physical health in older individuals: evidence for directional effects and protective factors. , 2007, Psychology and aging.

[38]  Hiroko H Dodge,et al.  Depressive symptoms and cognitive decline in late life: a prospective epidemiological study. , 2006, Archives of general psychiatry.

[39]  H. Mayberg Limbic-cortical dysregulation: a proposed model of depression. , 1997, The Journal of neuropsychiatry and clinical neurosciences.

[40]  L. Leyman,et al.  The Karolinska Directed Emotional Faces: A validation study , 2008 .

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

[42]  Susanne Scheibe,et al.  Emotional aging: recent findings and future trends. , 2010, The journals of gerontology. Series B, Psychological sciences and social sciences.

[43]  L. Carstensen,et al.  Selective attention to emotion in the aging brain. , 2009, Psychology and aging.

[44]  Mara Mather,et al.  Goal-directed memory: the role of cognitive control in older adults' emotional memory. , 2005, Psychology and aging.