Functional neuroanatomy of the encoding and retrieval processes of verbal episodic memory in MCI

INTRODUCTION The goal of this study was to explore the association between disease severity and performance on brain activation associated with episodic memory encoding and retrieval in persons with mild cognitive impairment (MCI). METHOD This was achieved by scanning 12 MCI persons and 10 age- and education-matched healthy controls while encoding words and while retrieving them in a recognition test. RESULTS Behaviorally, there was no significant group difference on recognition performance. However, MCI and healthy controls showed different patterns of cerebral activation during encoding. While most of these differences demonstrated reduced activation in the MCI group, there were areas of increased activation in the left ventrolateral prefrontal cortex. Reduced activation was found in brain areas known to be either structurally compromised or hypometabolic in Alzheimer's disease (AD). In contrast, very few group differences were associated with retrieval. Correlation analyses indicated that increased disease severity, as measured with the Mattis Dementia Rating Scale, was associated with smaller activation of the right middle and superior temporal gyri. In contrast, recognition success in MCI persons was associated with larger activation of the left ventrolateral prefrontal cortex during the encoding phase. CONCLUSION Overall, our results indicate that most of the memory-related cerebral network changes in MCI persons occur during the encoding phase. They also suggest that a prefrontal compensatory mechanism could occur in parallel with the disease-associated reduction of cerebral activation in temporal areas.

[1]  F. Craik,et al.  Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[2]  J. Morris,et al.  Current concepts in mild cognitive impairment. , 2001, Archives of neurology.

[3]  C. Jack,et al.  Mild cognitive impairment – beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment , 2004, Journal of internal medicine.

[4]  Lisa T. Eyler,et al.  Verbal paired-associate learning by APOE genotype in non-demented older adults: fMRI evidence of a right hemispheric compensatory response , 2007, Neurobiology of Aging.

[5]  Mark S. Cohen,et al.  Patterns of brain activation in people at risk for Alzheimer's disease. , 2000, The New England journal of medicine.

[6]  Oscar L. Lopez,et al.  Event-related functional magnetic resonance imaging investigation of executive control in very old individuals with mild cognitive impairment , 2005, Biological Psychiatry.

[7]  Vince D. Calhoun,et al.  Alterations in Memory Networks in Mild Cognitive Impairment and Alzheimer's Disease: An Independent Component Analysis , 2006, The Journal of Neuroscience.

[8]  S. Gauthier,et al.  Task switching capacities in persons with Alzheimer's disease and mild cognitive impairment , 2008, Neuropsychologia.

[9]  R. Cabeza Hemispheric asymmetry reduction in older adults: the HAROLD model. , 2002, Psychology and aging.

[10]  J. J. Ryan,et al.  Wechsler Adult Intelligence Scale-III , 2001 .

[11]  Cheuk Y. Tang,et al.  Patterns of cortical activity and memory performance in Alzheimer’s disease , 2001, Biological Psychiatry.

[12]  A. Sack,et al.  Functional activation imaging in aging and dementia , 2005, Psychiatry Research: Neuroimaging.

[13]  S. Belleville Working memory and control of attention in persons with Alzheimer's disease and mild cognitive impairment , 2010, Alzheimer's & Dementia.

[14]  T G Turkington,et al.  Adult age differences in the functional neuroanatomy of verbal recognition memory , 1999, Human brain mapping.

[15]  H. Braak,et al.  Neuropathological stageing of Alzheimer-related changes , 2004, Acta Neuropathologica.

[16]  R. Quirion,et al.  Alzheimer's disease and the basal forebrain cholinergic system: relations to beta-amyloid peptides, cognition, and treatment strategies. , 2002, Progress in neurobiology.

[17]  J. Desrosiers,et al.  Reliability of the revised functional autonomy measurement system (SMAF) for epidemiological research. , 1995, Age and ageing.

[18]  Philip Scheltens,et al.  Medial temporal lobe atrophy on MRI predicts dementia in patients with mild cognitive impairment , 2004, Neurology.

[19]  C. Jack,et al.  Prediction of AD with MRI-based hippocampal volume in mild cognitive impairment , 1999, Neurology.

[20]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[21]  C. Grady,et al.  Neural correlates of incidental memory in mild cognitive impairment: An fMRI study , 2009, Neurobiology of Aging.

[22]  C. Jack,et al.  Usefulness of MRI measures of entorhinal cortex versus hippocampus in AD , 2000, Neurology.

[23]  H. Soininen,et al.  Hippocampus and entorhinal cortex in mild cognitive impairment and early AD , 2004, Neurobiology of Aging.

[24]  M. Erb,et al.  Mild cognitive impairment (MCI) and actual retrieval performance affect cerebral activation in the elderly , 2007, Neurobiology of Aging.

[25]  A. Dale,et al.  Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. , 1998, Science.

[26]  T. Dierks,et al.  Reduced neuronal efficacy in progressive mild cognitive impairment: A prospective fMRI study on visuospatial processing , 2007, Psychiatry Research: Neuroimaging.

[27]  E. Bullmore,et al.  Functional neuroanatomy of successful paired associate learning in Alzheimer's disease. , 2005, The American journal of psychiatry.

[28]  Jemett L. Desmond,et al.  Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  D. A. Bennett,et al.  Natural history of mild cognitive impairment in older persons , 2002, Neurology.

[30]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[31]  Sterling C. Johnson,et al.  Reduced hippocampal activation during episodic encoding in middle-aged individuals at genetic risk of Alzheimer's Disease: a cross-sectional study , 2006, BMC medicine.

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

[33]  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.

[34]  G. E. Alexander,et al.  Activation of brain regions vulnerable to Alzheimer's disease: The effect of mild cognitive impairment , 2006, Neurobiology of Aging.

[35]  R. Cabeza Cognitive neuroscience of aging: contributions of functional neuroimaging. , 2001, Scandinavian journal of psychology.

[36]  C. Jack,et al.  Comparison of memory fMRI response among normal, MCI, and Alzheimer’s patients , 2003, Neurology.

[37]  L. Brusco,et al.  Possible therapeutic value of melatonin in mild cognitive impairment: a retrospective study , 2007, Journal of pineal research.

[38]  J. Kaye,et al.  Brain volume loss in MCI predicts dementia , 2006, Neurology.

[39]  R. Quirion,et al.  Alzheimer’s disease and the basal forebrain cholinergic system: relations to β-amyloid peptides, cognition, and treatment strategies , 2002, Progress in Neurobiology.

[40]  Michael Erb,et al.  Hippocampal activation in patients with mild cognitive impairment is necessary for successful memory encoding , 2007, Journal of Neurology, Neurosurgery & Psychiatry.

[41]  Sterling C. Johnson,et al.  Task-dependent posterior cingulate activation in mild cognitive impairment , 2006, NeuroImage.

[42]  J. Greene Contributions to Neuropsychological Assessment , 1995 .

[43]  Yaakov Stern,et al.  fMRI evidence of compensatory mechanisms in older adults at genetic risk for Alzheimer disease , 2005, Neurology.

[44]  Martial Van der Linden,et al.  L'évaluation des troubles de la mémoire: Présentation de quatre tests de mémoire épisodique (avec leur étalonnage) , 2004 .

[45]  E. Kaplan,et al.  The Boston naming test , 2001 .

[46]  S. Gauthier,et al.  Cognitive complaint in mild cognitive impairment and Alzheimer's disease , 2008, Journal of the International Neuropsychological Society.

[47]  J. Desmond,et al.  Functional Specialization for Semantic and Phonological Processing in the Left Inferior Prefrontal Cortex , 1999, NeuroImage.

[48]  K. Herholz,et al.  Impaired metabolic activation in Alzheimer's disease: A pet study during continuous visual recognition , 1991, Neuropsychologia.

[49]  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.

[50]  G. V. Van Hoesen,et al.  The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimer's disease. , 1991, Cerebral cortex.

[51]  J. Schneider,et al.  Parahippocampal tau pathology in healthy aging, mild cognitive impairment, and early Alzheimer's disease , 2002, Annals of neurology.

[52]  Clifford R. Jack,et al.  3 D maps frommultiple MRI illustrate changing atrophy patterns as subjects progress from mild cognitive impairment to Alzheimer ’ s disease , 2007 .

[53]  R. Gardner,et al.  Mattis Dementia Rating Scale: internal reliability study using a diffusely impaired population. , 1981, Journal of clinical neuropsychology.

[54]  M. Albert,et al.  Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD , 2005, Neurology.

[55]  C. Jack,et al.  3D maps from multiple MRI illustrate changing atrophy patterns as subjects progress from mild cognitive impairment to Alzheimer's disease. , 2007, Brain : a journal of neurology.

[56]  Sylvie Belleville,et al.  Working memory and control of attention in persons with Alzheimer's disease and mild cognitive impairment. , 2007 .

[57]  J. Baron,et al.  FDG-PET measurement is more accurate than neuropsychological assessments to predict global cognitive deterioration in patients with mild cognitive impairment , 2005, Neurocase.

[58]  P. Osterrieth Le test de copie d'une figure complexe , 1944 .

[59]  M. Mesulam,et al.  Cholinergic nucleus basalis tauopathy emerges early in the aging‐MCI‐AD continuum , 2004, Annals of neurology.

[60]  R. Petersen MILD COGNITIVE IMPAIRMENT , 2004, Lancet.

[61]  G. Frisoni,et al.  A voxel based morphometry study on mild cognitive impairment , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[62]  C. Grady,et al.  Encoding and retrieval in aging and memory loss, a fMRI study. , 2002, Brain and cognition.

[63]  Cornelis J. Stam,et al.  Delayed rather than decreased BOLD response as a marker for early Alzheimer's disease , 2005, NeuroImage.

[64]  Thanh-Thu T. Tran,et al.  Cortical deactivation in mild cognitive impairment: high-field-strength functional MR imaging. , 2007, Radiology.

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

[66]  R. Petersen,et al.  Association of Low Plasma Aβ42/Aβ40 Ratios With Increased Imminent Risk for Mild Cognitive Impairment and Alzheimer Disease , 2007 .

[67]  Charles D. Smith,et al.  Neuropathologic substrate of mild cognitive impairment. , 2006, Archives of neurology.

[68]  Maija Pihlajamäki,et al.  Increased fMRI responses during encoding in mild cognitive impairment , 2007, Neurobiology of Aging.

[69]  S. Shergill,et al.  An fMRI study of verbal episodic memory encoding in amnestic mild cognitive impairment , 2008, Cortex.