Aging and electrocortical response to error feedback during a spatial learning task.

Event-related potentials were collected as older and younger adults responded to error feedback in an adaptation of the Groton Maze Learning Test, an age-sensitive measure of spatial learning and executive skills expected to maximally involve anterior cingulate cortex (ACC). Older adults made more errors and produced smaller feedback-related negativities (FRNs) than young controls. LORETA source localization revealed that, for young adults, neural activation associated with the FRN was focused in ACC and was stronger to negative feedback. Older adults responded with less intense and less differentiated ACC activation, but FRN amplitudes did relate to error rate for the most difficult mazes. The feedback P3 was sensitive to negative feedback but played no role in the prediction of error for either group. These data reflect the selective age-related decline of ACC response but also its continued contribution to performance monitoring in aging.

[1]  M. C. Newman,et al.  Spatial Memory and Aging: Performance on a Human Analog of the Morris Water Maze , 2000 .

[2]  R. Knight,et al.  Prefrontal–cingulate interactions in action monitoring , 2000, Nature Neuroscience.

[3]  P. Snyder,et al.  Spatial learning efficiency and error monitoring in normal aging: an investigation using a novel hidden maze learning test. , 2007, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[4]  B. Richmond,et al.  Anterior Cingulate: Single Neuronal Signals Related to Degree of Reward Expectancy , 2002, Science.

[5]  Stimulus-Response Compatibility and Psychophysiology , 1991 .

[6]  D. Lehmann,et al.  Functional imaging with low-resolution brain electromagnetic tomography (LORETA): a review. , 2002, Methods and findings in experimental and clinical pharmacology.

[7]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

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

[9]  J. Hohnsbein,et al.  Changes of error-related ERPs with age , 2001, Experimental Brain Research.

[10]  Timothy E. J. Behrens,et al.  Learning the value of information in an uncertain world , 2007, Nature Neuroscience.

[11]  Jonathan D. Cohen,et al.  Decision making, the P3, and the locus coeruleus-norepinephrine system. , 2005, Psychological bulletin.

[12]  D. Meyer,et al.  A Neural System for Error Detection and Compensation , 1993 .

[13]  S. Kalinin,et al.  Noradrenaline deficiency in brain increases β-amyloid plaque burden in an animal model of Alzheimer's disease , 2007, Neurobiology of Aging.

[14]  Michael G. H. Coles,et al.  What if I told you: "You were wrong"? Brain potentials and behavioral adjustments elicited by feedback in a time-estimation task , 2004 .

[15]  M. Herrmann,et al.  Source localization (LORETA) of the error-related-negativity (ERN/Ne) and positivity (Pe). , 2004, Brain research. Cognitive brain research.

[16]  P. Snyder,et al.  A method for determining the magnitude of change across different cognitive functions in clinical trials: the effects of acute administration of two different doses alprazolam , 2005, Human psychopharmacology.

[17]  Wouter Hulstijn,et al.  Altered Response Evaluation Monitoring of Late Responses After Administration of D-Amphetamine , 2005 .

[18]  Clay B. Holroyd,et al.  The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. , 2002, Psychological review.

[19]  Laura L. Boles Ponto,et al.  Aging, grey matter, and blood flow in the anterior cingulate cortex , 2007, NeuroImage.

[20]  Naomi Hasegawa,et al.  Thalamocortical and intracortical connections of monkey cingulate motor areas , 2003, The Journal of comparative neurology.

[21]  Sander Nieuwenhuis,et al.  Mediofrontal negativities in the absence of responding. , 2005, Brain research. Cognitive brain research.

[22]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[23]  C. Braun,et al.  Event-Related Brain Potentials Following Incorrect Feedback in a Time-Estimation Task: Evidence for a Generic Neural System for Error Detection , 1997, Journal of Cognitive Neuroscience.

[24]  T. Shirokawa,et al.  Involvement of neurotrophic factors in aging of noradrenergic innervations in hippocampus and frontal cortex , 2006, Neuroscience Research.

[25]  K. Rommelfanger,et al.  Norepinephrine: The redheaded stepchild of Parkinson's disease. , 2007, Biochemical pharmacology.

[26]  M. Posner,et al.  Localization of a Neural System for Error Detection and Compensation , 1994 .

[27]  E. Procyk,et al.  Reward encoding in the monkey anterior cingulate cortex. , 2006, Cerebral cortex.

[28]  Karen J. Mathewson,et al.  Brain bases of error-related ERPs as influenced by age and task , 2005, Biological Psychology.

[29]  N C Andreasen,et al.  Age-related changes in regional cerebral blood flow among young to mid-life adults. , 1999, Neuroreport.

[30]  Nathan Herrmann,et al.  The role of norepinephrine in the behavioral and psychological symptoms of dementia. , 2004, The Journal of neuropsychiatry and clinical neurosciences.

[31]  Brenda Milner,et al.  Visually-guided maze learning in man: effects of bilateral hippocampal, bilateral frontal, and unilateral cerebral lesions , 1965 .

[32]  Manuel Rodriguez,et al.  Aging of the rat mesostriatal system: Differences between the nigrostriatal and the mesolimbic compartments , 2007, Experimental Neurology.

[33]  R. Simons,et al.  To err is autonomic: error-related brain potentials, ANS activity, and post-error compensatory behavior. , 2003, Psychophysiology.

[34]  Carolyn C. Meltzer,et al.  Verbal and spatial working memory in older individuals: A positron emission tomography study , 2006, Brain Research.

[35]  Clay B. Holroyd,et al.  Knowing good from bad: differential activation of human cortical areas by positive and negative outcomes , 2005, The European journal of neuroscience.

[36]  J. Tanji,et al.  Role for cingulate motor area cells in voluntary movement selection based on reward. , 1998, Science.

[37]  N. Volkow,et al.  Association between age-related decline in brain dopamine activity and impairment in frontal and cingulate metabolism. , 2000, The American journal of psychiatry.

[38]  David Goodman,et al.  Performance Monitoring in the Anterior Cingulate is Not All Error Related: Expectancy Deviation and the Representation of Action-Outcome Associations , 2007, Journal of Cognitive Neuroscience.

[39]  Lars Farde,et al.  Age-related dopamine D2/D3 receptor loss in extrastriatal regions of the human brain , 2000, Neurobiology of Aging.

[40]  Clay B. Holroyd,et al.  The feedback-related negativity reflects the binary evaluation of good versus bad outcomes , 2006, Biological Psychology.

[41]  S. Nakai,et al.  Age-dependent interactive changes in serotonergic and noradrenergic cortical axon terminals in F344 rats , 2006, Neuroscience Research.

[42]  N. Raz,et al.  Extrahippocampal contributions to age differences in human spatial navigation. , 2007, Cerebral cortex.

[43]  M. Coles,et al.  Performance monitoring in a confusing world: error-related brain activity, judgments of response accuracy, and types of errors. , 2000, Journal of experimental psychology. Human perception and performance.

[44]  T. Paus,et al.  Regional differences in the effects of task difficulty and motor output on blood flow response in the human anterior cingulate cortex: a review of 107 PET activation studies , 1998, Neuroreport.

[45]  J. Polich.  Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.

[46]  Clay B. Holroyd,et al.  ERP correlates of feedback and reward processing in the presence and absence of response choice. , 2005, Cerebral cortex.

[47]  G. Band,et al.  Age effects on response monitoring in a mental-rotation task , 2000, Biological Psychology.

[48]  Mark D'Esposito,et al.  Region-specific changes in prefrontal function with age: a review of PET and fMRI studies on working and episodic memory. , 2005, Brain : a journal of neurology.

[49]  K. R. Ridderinkhof,et al.  A computational account of altered error processing in older age: Dopamine and the error-related negativity , 2002, Cognitive, affective & behavioral neuroscience.

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

[51]  R. Sutherland,et al.  The aging hippocampus: cognitive, biochemical and structural findings. , 2003, Cerebral cortex.

[52]  A. Rodríguez-Fornells,et al.  Brain potentials related to self-generated and external information used for performance monitoring , 2005, Clinical Neurophysiology.

[53]  A. Ferrandez,et al.  Does cerebral activity change in middle-aged adults in a visual discrimination task? , 2001, Neurobiology of Aging.

[54]  A. Sanfey,et al.  Independent Coding of Reward Magnitude and Valence in the Human Brain , 2004, The Journal of Neuroscience.

[55]  Nora D. Volkow,et al.  Dr. Volkow and Colleagues Reply , 1987 .

[56]  S. Reeves,et al.  Ageing and the nigrostriatal dopaminergic system , 2002, International journal of geriatric psychiatry.

[57]  Ulman Lindenberger,et al.  Environmental topography and postural control demands shape aging-associated decrements in spatial navigation performance. , 2005, Psychology and aging.

[58]  Sidney J. Segalowitz,et al.  The effects of uncertainty in error monitoring on associated ERPs , 2004, Brain and Cognition.

[59]  S. Resnick,et al.  Age differences in the neural systems supporting human allocentric spatial navigation , 2006, Neurobiology of Aging.

[60]  S. Ishii,et al.  Resolution of Uncertainty in Prefrontal Cortex , 2006, Neuron.

[61]  F. Yasuno,et al.  Age-related decline of dopamine synthesis in the living human brain measured by positron emission tomography with l-[β-11C]DOPA , 2006 .

[62]  Clay B. Holroyd,et al.  Why is there an ERN/Ne on correct trials? Response representations, stimulus-related components, and the theory of error-processing , 2001, Biological Psychology.

[63]  A. Kok.  Age-related changes in involuntary and voluntary attention as reflected in components of the event-related potential (ERP) , 2000, Biological Psychology.

[64]  Cheryl L. Dickter,et al.  Strategic control and medial frontal negativity: beyond errors and response conflict. , 2005, Psychophysiology.