Effects of cognitive training on gray matter volumes in memory clinic patients with subjective memory impairment.

Subjective memory impairment (SMI) is a common risk factor for Alzheimer's disease, with few established options for treatment. Here we investigate the effects of two months episodic memory training on regional brain atrophy in 19 memory clinic patients with SMI. We used a sensitive longitudinal magnetic resonance imaging protocol and compared the patients with 42 matched healthy volunteers randomly assigned to a group performing the same training, or a no-training control group. Following intervention, the SMI sample exhibited structural gray matter volume increases in brain regions encompassing the episodic memory network, with cortical volume expansion of comparable extent as healthy training participants. Further, we found significant hippocampal volume increases in the healthy training group but not in the SMI group. Still, individual differences in left hippocampal volume change in the patient group were related to verbal recall improvement following training. The present results reinforce earlier studies indicating intact brain plasticity in aging, and further suggest that training-related brain changes can be evident also in the earliest form of cognitive impairment.

[1]  M. Bennett,et al.  The prefrontal–limbic network in depression: A core pathology of synapse regression , 2011, Progress in Neurobiology.

[2]  E. McAuley,et al.  Exercise training increases size of hippocampus and improves memory , 2011, Proceedings of the National Academy of Sciences.

[3]  R. Mayeux,et al.  Hippocampal and entorhinal atrophy in mild cognitive impairment , 2007, Neurology.

[4]  U. Lindenberger,et al.  A theoretical framework for the study of adult cognitive plasticity. , 2010, Psychological bulletin.

[5]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[6]  A. Dale,et al.  Regional rates of neocortical atrophy from normal aging to early Alzheimer disease , 2009, Neurology.

[7]  D. Delis,et al.  The California Verbal Learning Test--second edition: test-retest reliability, practice effects, and reliable change indices for the standard and alternate forms. , 2006, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[8]  O. Almkvist,et al.  Identifying Patients at High and Low Risk of Cognitive Decline Using Rey Auditory Verbal Learning Test among Middle-Aged Memory Clinic Outpatients , 2006, Dementia and Geriatric Cognitive Disorders.

[9]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[10]  Hans-Jochen Heinze,et al.  Experience-dependent plasticity of white-matter microstructure extends into old age , 2010, Neuropsychologia.

[11]  Steve Iliffe,et al.  Subjective memory problems , 2010, BMJ : British Medical Journal.

[12]  Louise M. Reid,et al.  Subjective Memory Complaints and Cognitive Impairment in Older People , 2006, Dementia and Geriatric Cognitive Disorders.

[13]  F. Jessen,et al.  Prediction of dementia by subjective memory impairment: effects of severity and temporal association with cognitive impairment. , 2010, Archives of general psychiatry.

[14]  Anders M. Dale,et al.  Six-month atrophy in MTL structures is associated with subsequent memory decline in elderly controls , 2010, NeuroImage.

[15]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[16]  Jonas Persson,et al.  Longitudinal structure-function correlates in elderly reveal MTL dysfunction with cognitive decline. , 2012, Cerebral cortex.

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

[18]  Daniel Fürth,et al.  Working memory plasticity modulated by dopamine transporter genotype , 2009, Neuroscience Letters.

[19]  A. Dale,et al.  CSF Biomarkers in Prediction of Cerebral and Clinical Change in Mild Cognitive Impairment and Alzheimer's Disease , 2010, The Journal of Neuroscience.

[20]  Wesley K. Thompson,et al.  Bias in tensor based morphometry Stat-ROI measures may result in unrealistic power estimates , 2011, NeuroImage.

[21]  C. Jonker,et al.  Are memory complaints predictive for dementia? A review of clinical and population‐based studies , 2000, International journal of geriatric psychiatry.

[22]  N. Raz,et al.  Shrinkage of the Entorhinal Cortex over Five Years Predicts Memory Performance in Healthy Adults , 2004, The Journal of Neuroscience.

[23]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[24]  Andreas Engvig,et al.  Effects of memory training on cortical thickness in the elderly , 2010, NeuroImage.

[25]  Andreas Engvig,et al.  Hippocampal subfield volumes correlate with memory training benefit in subjective memory impairment , 2012, NeuroImage.

[26]  Thomas E. Nichols,et al.  Validating cluster size inference: random field and permutation methods , 2003, NeuroImage.

[27]  S. Ryu,et al.  Multistrategic Memory Training with the Metamemory Concept in Healthy Older Adults , 2011, Psychiatry investigation.

[28]  A. Dale,et al.  Subregional neuroanatomical change as a biomarker for Alzheimer's disease , 2009, Proceedings of the National Academy of Sciences.

[29]  Daniel Fürth,et al.  Preliminary evidence that allelic variation in the LMX1A gene influences training-related working memory improvement , 2011, Neuropsychologia.

[30]  T. Shallice,et al.  Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis. , 1999, Brain : a journal of neurology.

[31]  G. Bower Analysis of a mnemonic device , 1970 .

[32]  S. Naismith,et al.  Early intervention for cognitive decline: can cognitive training be used as a selective prevention technique? , 2010, International Psychogeriatrics.

[33]  A. Sunderland,et al.  Memory failures in everyday life following severe head injury. , 1984, Journal of clinical neuropsychology.

[34]  Christian Büchel,et al.  Training-Induced Brain Structure Changes in the Elderly , 2008, The Journal of Neuroscience.

[35]  S. Gauthier,et al.  Training-related brain plasticity in subjects at risk of developing Alzheimer's disease. , 2011, Brain : a journal of neurology.

[36]  Hans-Jochen Heinze,et al.  Article Title : Performance-related Increases in Hippocampal N-acetylaspartate (naa) Induced by Spatial Navigation Training Are Restricted to Bdnf Val Homozygotes First Author : Martin Lö Vdé N Article Title : Performance-related Increases in Hippocampal N-acetylaspartate (naa) Induced by Spatial Na , 2022 .

[37]  Hans-Jochen Heinze,et al.  Spatial navigation training protects the hippocampus against age-related changes during early and late adulthood , 2012, Neurobiology of Aging.

[38]  Sylvie Belleville,et al.  Improvement of Episodic Memory in Persons with Mild Cognitive Impairment and Healthy Older Adults: Evidence from a Cognitive Intervention Program , 2006, Dementia and Geriatric Cognitive Disorders.

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

[40]  Martin van Boxtel,et al.  Cognitive interventions in healthy older adults and people with mild cognitive impairment: A systematic review , 2013, Ageing Research Reviews.

[41]  R. Stewart,et al.  Subjective cognitive impairment , 2012, Current opinion in psychiatry.

[42]  A. Saykin,et al.  Older adults with cognitive complaints show brain atrophy similar to that of amnestic MCI , 2006, Neurology.

[43]  R. Stewart,et al.  Neuroimaging correlates of subjective memory deficits in a community population , 2008, Neurology.

[44]  Knut Engedal,et al.  The Memory Clinic--outpatient assessment when dementia is suspected. , 2011, Tidsskrift for den Norske laegeforening : tidsskrift for praktisk medicin, ny raekke.

[45]  John O. Willis,et al.  Wechsler Abbreviated Scale of Intelligence , 2014 .

[46]  Wei Zhu,et al.  Outcome over seven years of healthy adults with and without subjective cognitive impairment , 2010, Alzheimer's & Dementia.

[47]  C. Sherbourne,et al.  The MOS 36-Item Short-Form Health Survey (SF-36) , 1992 .

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

[49]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[50]  A. Dale,et al.  Brain Changes in Older Adults at Very Low Risk for Alzheimer's Disease , 2013, The Journal of Neuroscience.

[51]  Prabha Siddarth,et al.  The memory fitness program: cognitive effects of a healthy aging intervention. , 2012, The American journal of geriatric psychiatry : official journal of the American Association for Geriatric Psychiatry.

[52]  G. Finnerty,et al.  Sensory Experience and Cortical Rewiring , 2010, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[53]  V. Leirer,et al.  Development and validation of a geriatric depression screening scale: a preliminary report. , 1982, Journal of psychiatric research.

[54]  Hans-Jochen Heinze,et al.  Cortical thickness changes following spatial navigation training in adulthood and aging , 2012, NeuroImage.

[55]  F. Jessen,et al.  Volume Loss of the Medial Temporal Lobe Structures in Subjective Memory Impairment , 2010, Dementia and Geriatric Cognitive Disorders.

[56]  A. Dale,et al.  Unbiased comparison of sample size estimates from longitudinal structural measures in ADNI , 2012, Human brain mapping.

[57]  Ayse Pinar Saygin,et al.  Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data , 2006, NeuroImage.

[58]  Andreas Engvig,et al.  Memory training impacts short‐term changes in aging white matter: A Longitudinal Diffusion Tensor Imaging Study , 2012, Human brain mapping.

[59]  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.

[60]  D. Delis,et al.  California Verbal Learning Test--Second Edition , 2016 .

[61]  F. Jessen,et al.  Glucose metabolism, gray matter structure and memory decline in subjective memory impairment , 2012, Alzheimer's & Dementia.

[62]  Anders M. Dale,et al.  Nonlinear registration of longitudinal images and measurement of change in regions of interest , 2011, Medical Image Anal..

[63]  B. Reisberg,et al.  The pre–mild cognitive impairment, subjective cognitive impairment stage of Alzheimer’s disease , 2008, Alzheimer's & Dementia.

[64]  H. Christensen,et al.  Memory complaints in a community sample aged 60–64 years: associations with cognitive functioning, psychiatric symptoms, medical conditions, APOE genotype, hippocampus and amygdala volumes, and white-matter hyperintensities , 2004, Psychological Medicine.

[65]  H. Walter,et al.  Evidence of neuronal compensation during episodic memory in subjective memory impairment. , 2011, Archives of general psychiatry.