Risky decision-making in older adults without cognitive deficits: An fMRI study of VMPFC using the Iowa Gambling Task

Some older adults without neurological disease exhibit impaired decision-making in risky, nontransparent situations, like the Iowa Gambling Task (IGT). The prefrontal cortices are particularly vulnerable to age-related decline, and numerous studies implicate the ventromedial prefrontal cortex (VMPFC) in successful IGT performance. However, the relationship between IGT performance and VMPFC function in older adults has not yet been tested by fMRI. In the present study, older adults with seemingly no cognitive impairments performed the IGT and a non-gambling control task during fMRI. Group analyses indicate that in these older adults, regardless of IGT performance level, a right VMPFC subregion is activated during the IGT, while successful IGT performance is correlated with left VMPFC activation, suggesting that bilateral VMPFC during risky, nontransparent situations may contribute to successful decision-making in older adults. Individual subject analyses reveal substantial variation regarding the extent and location of VMPFC activation during the IGT, a finding not captured in the group analysis: There is no correlation between IGT performance and extent of activation in the right VMPFC, although there is such a correlation between left VMPFC activation and IGT performance.

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

[2]  D. Tranel,et al.  Psychophysiological anticipation of positive outcomes promotes advantageous decision-making in normal older persons. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[3]  Fernando Zelaya,et al.  Distinct roles of prefrontal cortical subregions in the Iowa Gambling Task. , 2009, Cerebral cortex.

[4]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[5]  Faith M. Gunning-Dixon,et al.  Neuroanatomical correlates of cognitive aging: evidence from structural magnetic resonance imaging. , 1998, Neuropsychology.

[6]  Takashi Hanakawa,et al.  Functional activity related to risk anticipation during performance of the Iowa gambling task , 2005, NeuroImage.

[7]  Catherine A. Cole,et al.  The Orbitofrontal Cortex, Real‐World Decision Making, and Normal Aging , 2007, Annals of the New York Academy of Sciences.

[8]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[9]  A. Damasio The somatic marker hypothesis and the possible functions of the prefrontal cortex. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[10]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[11]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[12]  Pejman Sehatpour,et al.  Preserved executive function in high‐performing elderly is driven by large‐scale recruitment of prefrontal cortical mechanisms , 2009, Human brain mapping.

[13]  A. Bechara,et al.  Effects of anticipatory stress on decision making in a gambling task. , 2007, Behavioral neuroscience.

[14]  A. Damasio,et al.  Somatic markers and the guidance of behavior: Theory and preliminary testing. , 1991 .

[15]  R. West,et al.  An application of prefrontal cortex function theory to cognitive aging. , 1996, Psychological bulletin.

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

[17]  Monique Ernst,et al.  Decision-making in a Risk-taking Task: A PET Study , 2002, Neuropsychopharmacology.

[18]  D. Schacter,et al.  Ageing and the self-reference effect in memory , 2007, Memory.

[19]  W. Kates,et al.  The relation of worry to prefrontal cortex volume in older adults with and without generalized anxiety disorder , 2009, Psychiatry Research: Neuroimaging.

[20]  M. Delazer,et al.  Normal aging affects decisions under ambiguity, but not decisions under risk. , 2008, Neuropsychology.

[21]  Luke Clark,et al.  The contributions of lesion laterality and lesion volume to decision-making impairment following frontal lobe damage , 2003, Neuropsychologia.

[22]  A. Damasio,et al.  Individuals with sociopathic behavior caused by frontal damage fail to respond autonomically to social stimuli , 1990, Behavioural Brain Research.

[23]  Peter Boesiger,et al.  Affective judgment and beneficial decision making: Ventromedial prefrontal activity correlates with performance in the Iowa Gambling Task , 2006, Human brain mapping.

[24]  Arnaud D'Argembeau,et al.  The Iowa Gambling Task in fMRI images , 2009, Human brain mapping.

[25]  A. Damasio,et al.  Failure to respond autonomically to anticipated future outcomes following damage to prefrontal cortex. , 1996, Cerebral cortex.

[26]  D. Schacter,et al.  See Blockindiscussions, Blockinstats, Blockinand Blockinauthor Blockinprofiles Blockinfor Blockinthis Blockinpublication Aging, Blockinself-referencing, Blockinand Blockinmedial Blockinprefrontal Cortex , 2022 .

[27]  A. Dale,et al.  One-Year Brain Atrophy Evident in Healthy Aging , 2009, The Journal of Neuroscience.

[28]  H. Markowitsch,et al.  Mechanisms Contributing to Decision-Making Difficulties in Late Adulthood: Theoretical Approaches, Speculations and Empirical Evidence , 2010, Gerontology.

[29]  Daniel L Schacter,et al.  Effects of emotion on memory specificity in young and older adults. , 2007, The journals of gerontology. Series B, Psychological sciences and social sciences.

[30]  R. Cabeza,et al.  Task-independent and task-specific age effects on brain activity during working memory, visual attention and episodic retrieval. , 2004, Cerebral cortex.

[31]  E. Tolosa,et al.  Neuroanatomical correlates of impaired decision‐making and facial emotion recognition in early Parkinson’s disease , 2009, The European journal of neuroscience.

[32]  Daniel Tranel,et al.  Asymmetric Functional Roles of Right and Left Ventromedial Prefrontal Cortices in Social Conduct, Decision-Making, and Emotional Processing , 2002, Cortex.

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

[34]  D. Tranel,et al.  The ability to decide advantageously declines prematurely in some normal older persons , 2005, Neuropsychologia.

[35]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[36]  Lesley K Fellows,et al.  The human ventromedial frontal lobe is critical for learning from negative feedback. , 2008, Brain : a journal of neurology.

[37]  T. Robbins,et al.  Specific cognitive deficits in mild frontal variant frontotemporal dementia. , 1999, Brain : a journal of neurology.

[38]  George Fein,et al.  Older adults make less advantageous decisions than younger adults: Cognitive and psychological correlates , 2007, Journal of the International Neuropsychological Society.

[39]  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.

[40]  Potential Mechanisms Contributing to Decision-Making Difficulties in Late Adulthood , 2010, Gerontology.

[41]  P. Fox,et al.  Age-related differences in neural activities during risk taking as revealed by functional MRI , 2007, Social cognitive and affective neuroscience.

[42]  Jens C. Pruessner,et al.  Regional Frontal Cortical Volumes Decrease Differentially in Aging: An MRI Study to Compare Volumetric Approaches and Voxel-Based Morphometry , 2002, NeuroImage.

[43]  A. Peters,et al.  The effects of aging on layer 1 in area 46 of prefrontal cortex in the rhesus monkey. , 1998, Cerebral cortex.

[44]  H. Damasio,et al.  Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. , 2000, Brain : a journal of neurology.

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

[46]  A. Damasio,et al.  Insensitivity to future consequences following damage to human prefrontal cortex , 1994, Cognition.

[47]  K I Bolla,et al.  Cerebral Cortex Advance Access published May 13, 2004 Sex-related Differences in a Gambling Task and Its Neurological Correlates , 2022 .

[48]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[49]  H. Markowitsch,et al.  Aging and Decision-Making: A Neurocognitive Perspective , 2009, Gerontology.