Healthy aging is associated with increased neural processing of positive valence but attenuated processing of emotional arousal: an fMRI study

Arousal and valence play key roles in emotional perception, with normal aging leading to changes in the neural substrates supporting valence processing. The objective of this study was to investigate normal age-related changes in the neural substrates of emotional arousal processing. Twenty-three young and 23 older, healthy women underwent functional magnetic resonance imaging as they viewed images which were neutral or positive in valence and which varied in arousal level from low to high. Using a parametric modulation approach, we examined how the blood oxygen-level dependent signal varied with single trial subjective ratings of valence and arousal, and whether this differed with age. In accordance with previous studies we found that the older group showed greater activation in response to positive valence, in the left amygdala, left middle temporal gyrus and right lingual gyrus. In contrast however, they showed reduced reactivity to emotional arousal, in occipital and temporal visual cortices bilaterally, the left inferior parietal cortex, and the supplementary motor area bilaterally. This study represents the first of its kind to clearly dissociate how aging affects the neural correlates of emotional arousal and valence. The changes in arousal processing may in part be mediated by the functional reorganization evident in the aging brain, such as reduced activation of the posterior cortices as described by the posterior-anterior shift in ageing (PASA) effect.

[1]  J. Morris,et al.  The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part I. Clinical and neuropsychological assesment of Alzheimer's disease , 1989, Neurology.

[2]  Burton H Singer,et al.  Diverse pathways to positive and negative affect in adulthood and later life: an integrative approach using recursive partitioning. , 2008, Developmental psychology.

[3]  Cheryl L Grady,et al.  The effects of encoding task on age-related differences in the functional neuroanatomy of face memory. , 2002, Psychology and aging.

[4]  M. Bradley,et al.  Neuroanatomical correlates of pleasant and unpleasant emotion , 1997, Neuropsychologia.

[5]  Susanne Scheibe,et al.  Replicating the positivity effect in picture memory in Koreans: evidence for cross-cultural generalizability. , 2009, Psychology and aging.

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

[7]  R. Mohs,et al.  Consortium to establish a registry for Alzheimer's disease (CERAD) clinical and neuropsychological assessment of Alzheimer's disease. , 2002, Psychopharmacology bulletin.

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

[9]  Anthony R. McIntosh,et al.  The Effects of Divided Attention on Encoding- and Retrieval-Related Brain Activity: A PET Study of Younger and Older Adults , 2000, Journal of Cognitive Neuroscience.

[10]  Michael Davis,et al.  The amygdala: vigilance and emotion , 2001, Molecular Psychiatry.

[11]  Simon Finnigan,et al.  ERP measures indicate both attention and working memory encoding decrements in aging. , 2011, Psychophysiology.

[12]  Florin Dolcos,et al.  Effects of Aging on Functional Connectivity of the Amygdala for Subsequent Memory of Negative Pictures , 2009, Psychological science.

[13]  J L McGaugh,et al.  Amygdala activity at encoding correlated with long-term, free recall of emotional information. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[14]  S. Wiens,et al.  Age effects to negative arousal differ for self-report and electrodermal activity. , 2007, Psychophysiology.

[15]  Mara Mather,et al.  The Role of Motivation in the Age-Related Positivity Effect in Autobiographical Memory , 2004, Psychological science.

[16]  R. Cabeza,et al.  Effects of aging on transient and sustained successful memory encoding activity , 2007, Neurobiology of Aging.

[17]  E. Glisky.  Changes in Cognitive Function in Human Aging , 2007 .

[18]  Daniel Tranel,et al.  Evidence for preserved emotional memory in normal older persons. , 2003, Emotion.

[19]  Riddle Dr,et al.  Changes in Cognitive Function in Human Aging -- Brain Aging: Models, Methods, and Mechanisms , 2007 .

[20]  C. Reynolds,et al.  Age-related differences and change in positive and negative affect over 23 years. , 2001, Journal of personality and social psychology.

[21]  L. Carstensen,et al.  Socioemotional Selectivity Theory and the Regulation of Emotion in the Second Half of Life , 2003 .

[22]  K. Luan Phan,et al.  Subjective rating of emotionally salient stimuli modulates neural activity , 2003, NeuroImage.

[23]  J. Desmond,et al.  An fMRI study of personality influences on brain reactivity to emotional stimuli. , 2001, Behavioral neuroscience.

[24]  E. Tangalos,et al.  Mild Cognitive Impairment Clinical Characterization and Outcome , 1999 .

[25]  A. Henik,et al.  Orienting of attention, pupil size, and the norepinephrine system , 2011, Attention, perception & psychophysics.

[26]  N Butters,et al.  Detection of abnormal memory decline in mild cases of Alzheimer's disease using CERAD neuropsychological measures. , 1991, Archives of neurology.

[27]  Á. Pascual-Leone,et al.  How do we modulate our emotions? Parametric fMRI reveals cortical midline structures as regions specifically involved in the processing of emotional valences. , 2005, Brain research. Cognitive brain research.

[28]  Terry E. Goldberg,et al.  Age-related Alterations in Simple Declarative Memory and the Effect of Negative Stimulus Valence , 2009, Journal of Cognitive Neuroscience.

[29]  H. Flor,et al.  Gender differences in the processing of standardized emotional visual stimuli in humans: a functional magnetic resonance imaging study , 2003, Neuroscience Letters.

[30]  J. Leppänen.  Emotional information processing in mood disorders: a review of behavioral and neuroimaging findings , 2006, Current opinion in psychiatry.

[31]  R. Dolan,et al.  Encoding of emotional memories depends on amygdala and hippocampus and their interactions , 2004, Nature Neuroscience.

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

[33]  Daniel L. Schacter,et al.  Neural Processes Supporting Young and Older Adults' Emotional Memories , 2008, Journal of Cognitive Neuroscience.

[34]  P. Bertolucci,et al.  The paradox of age: an analysis of responses by aging Brazilians to International Affective Picture System (IAPS). , 2010, Revista brasileira de psiquiatria.

[35]  Leslie G. Ungerleider,et al.  Dissociation of object and spatial visual processing pathways in human extrastriate cortex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[36]  A. Kleinschmidt,et al.  Effects of arousing emotional scenes on the distribution of visuospatial attention: changes with aging and early subcortical vascular dementia , 2005, Journal of the Neurological Sciences.

[37]  Daniel L Schacter,et al.  Amygdala Activity Is Associated with the Successful Encoding of Item, But Not Source, Information for Positive and Negative Stimuli , 2006, The Journal of Neuroscience.

[38]  M. Bradley,et al.  Affective Normsfor English Words (ANEW): Stimuli, instruction manual and affective ratings (Tech Report C-1) , 1999 .

[39]  J. Mazziotta,et al.  Modulating emotional responses: effects of a neocortical network on the limbic system , 2000, Neuroreport.

[40]  T. Braver,et al.  A theory of cognitive control, aging cognition, and neuromodulation , 2002, Neuroscience & Biobehavioral Reviews.

[41]  H. Critchley,et al.  Neural correlates of processing valence and arousal in affective words. , 2006, Cerebral cortex.

[42]  Turhan Canli,et al.  Functional brain mapping of extraversion and neuroticism: learning from individual differences in emotion processing. , 2004, Journal of personality.

[43]  R. Cabeza,et al.  Interaction between the Amygdala and the Medial Temporal Lobe Memory System Predicts Better Memory for Emotional Events , 2004, Neuron.

[44]  P. Baltes,et al.  No aging bias favoring memory for positive material: evidence from a heterogeneity-homogeneity list paradigm using emotionally toned words. , 2005, Psychology and aging.

[45]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[46]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[47]  Jennifer C. Britton,et al.  Neural correlates of individual ratings of emotional salience: a trial-related fMRI study , 2004, NeuroImage.

[48]  M. Bradley,et al.  Affective Norms for English Words (ANEW): Instruction Manual and Affective Ratings , 1999 .

[49]  N Butters,et al.  Detection and staging of dementia in Alzheimer's disease. Use of the neuropsychological measures developed for the Consortium to Establish a Registry for Alzheimer's Disease. , 1992, Archives of neurology.

[50]  A. Schleicher,et al.  Cytoarchitectonic identification and probabilistic mapping of two distinct areas within the anterior ventral bank of the human intraparietal sulcus , 2006, The Journal of comparative neurology.

[51]  M. Mather,et al.  Angry faces get noticed quickly: threat detection is not impaired among older adults. , 2006, The journals of gerontology. Series B, Psychological sciences and social sciences.

[52]  P. Vuilleumier,et al.  How brains beware: neural mechanisms of emotional attention , 2005, Trends in Cognitive Sciences.

[53]  Elizabeth G. Kehoe,et al.  Personality modulates the effects of emotional arousal and valence on brain activation. , 2012, Social cognitive and affective neuroscience.

[54]  Vladimir V. Frolkis,et al.  Neurobiology of Aging , 2019, Psychobiology of Behaviour.

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

[56]  H. Wilson,et al.  Is there an age-related positivity effect in visual attention? A comparison of two methodologies. , 2006, Emotion.

[57]  W. D. O'Neill,et al.  Neurologial Interpretations and the Information in the Cognitive Pupillary Response , 2000, Methods of Information in Medicine.

[58]  Steven G. Potkin,et al.  Sex-Related Difference in Amygdala Activity during Emotionally Influenced Memory Storage , 2001, Neurobiology of Learning and Memory.

[59]  M. Bradley,et al.  Emotion and motivation II: sex differences in picture processing. , 2001, Emotion.

[60]  D. Mroczek,et al.  The effect of age on positive and negative affect: a developmental perspective on happiness. , 1998, Journal of personality and social psychology.

[61]  P. Lang.  International affective picture system (IAPS) : affective ratings of pictures and instruction manual , 2005 .

[62]  Leslie G. Ungerleider,et al.  Distributed representation of objects in the human ventral visual pathway. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[63]  Elizabeth A. Phelps,et al.  How arousal modulates memory: Disentangling the effects of attention and retention , 2004, Cognitive, affective & behavioral neuroscience.

[64]  L. Carstensen,et al.  Emotion and aging: experience, expression, and control. , 1997, Psychology and aging.

[65]  R. Cabeza,et al.  Que PASA? The posterior-anterior shift in aging. , 2008, Cerebral cortex.

[66]  Danielle M. Williams,et al.  Novel fearful faces activate the amygdala in healthy young and elderly adults , 2006, Neurobiology of Aging.

[67]  K. Luan Phan,et al.  Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging , 2003, NeuroImage.

[68]  Emiliano Ricciardi,et al.  Beyond sensory images: Object-based representation in the human ventral pathway. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[69]  James L. McGaugh,et al.  Make mild moments memorable: add a little arousal , 2006, Trends in Cognitive Sciences.

[70]  Daniel Grühn,et al.  Age-related differences in valence and arousal ratings of pictures from the International Affective Picture System (IAPS): Do ratings become more extreme with age? , 2008, Behavior research methods.

[71]  David R. Riddle,et al.  Brain aging : models, methods, and mechanisms , 2007 .

[72]  R. Todd Constable,et al.  Stop the sadness: Neuroticism is associated with sustained medial prefrontal cortex response to emotional facial expressions , 2008, NeuroImage.

[73]  Arnaud D'Argembeau,et al.  PHENOMENAL CHARACTERISTICS OF AUTOBIOGRAPHICAL MEMORIES FOR EMOTIONAL AND NEUTRAL EVENTS IN OLDER AND YOUNGER ADULTS , 2005, Experimental aging research.

[74]  S. Corkin,et al.  Two routes to emotional memory: distinct neural processes for valence and arousal. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[75]  M. Bradley,et al.  Emotion, Motivation, and Anxiety: Brain Mechanisms and Psychophysiology the Motivational Organization of Emotion Patterns of Human Emotion Emotion and Perception the Psychophysiology of Picture Processing Neural Imaging: Motivation in the Visual Cortex Motivational Circuits in the Brain , 2022 .

[76]  Daniel L. Schacter,et al.  How Negative Emotion Enhances the Visual Specificity of a Memory , 2007, Journal of Cognitive Neuroscience.

[77]  Abraham Z. Snyder,et al.  Altered Emotional Interference Processing in Affective and Cognitive-Control Brain Circuitry in Major Depression , 2008, Biological Psychiatry.

[78]  E. Kensinger,et al.  Effects of age on detection of emotional information. , 2008, Psychology and aging.

[79]  M. Bradley,et al.  Activation of the visual cortex in motivated attention. , 2003, Behavioral neuroscience.

[80]  Elizabeth A. Kensinger,et al.  There are age-related changes in neural connectivity during the encoding of positive, but not negative, information , 2010, Cortex.

[81]  M. Mather,et al.  Aging and emotional memory: the forgettable nature of negative images for older adults. , 2003, Journal of experimental psychology. General.

[82]  J. Gollan,et al.  Deficits in sustaining reward responses in subsyndromal and syndromal major depression , 2011, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[83]  E. Fox,et al.  Do threatening stimuli draw or hold visual attention in subclinical anxiety? , 2001, Journal of experimental psychology. General.

[84]  Murray Grossman,et al.  Age-Related Changes in Working Memory during Sentence Comprehension: An fMRI Study , 2002, NeuroImage.

[85]  Janaina Mourão Miranda,et al.  Contributions of stimulus valence and arousal to visual activation during emotional perception , 2003, NeuroImage.

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