Elsevier

NeuroImage

Volume 52, Issue 4, 1 October 2010, Pages 1667-1676
NeuroImage

Effects of memory training on cortical thickness in the elderly

https://doi.org/10.1016/j.neuroimage.2010.05.041Get rights and content

Abstract

The brain's ability to alter its functional and structural architecture in response to experience and learning has been extensively studied. Mental stimulation might serve as a reserve mechanism in brain aging, but macrostructural brain changes in response to cognitive training have been demonstrated in young participants only. We examined the short-term effects of an intensive memory training program on cognition and brain structure in middle-aged and elderly healthy volunteers. The memory trainers completed an 8-week training regimen aimed at improving verbal source memory utilizing the Method of Loci (MoL), while control participants did not receive any intervention. Both the memory trainers and the controls underwent magnetic resonance imaging (MRI) scans and memory testing pre and post 8 weeks of training or no training, respectively. Cortical thickness was automatically measured across the cortical mantle, and data processing and statistical analyses were optimized for reliable detection of longitudinal changes. The results showed that memory training improved source memory performance. Memory trainers also showed regional increases in cortical thickness compared with controls. Furthermore, thickness change in the right fusiform and lateral orbitofrontal cortex correlated positively with improvement in source memory performance, suggesting a possible functional significance of the structural changes. These findings demonstrate that systematic mental exercise may induce short-term structural changes in the aging human brain, indicating structural brain plasticity in elderly. The present study included short-term assessments, and follow-up studies are needed in order to assess whether such training indeed alters the long-term structural trajectories.

Introduction

Plasticity and reorganization of neural systems have recently been studied in both animals and humans (Buonomano and Merzenich, 1998, DeFelipe, 2006, Jones et al., 2006, Martin et al., 2000). Advances in neuroimaging techniques have enabled tracking of behavioral changes to alterations in specific brain regions in vivo (Draganski et al., 2006, Haier et al., 2009). Accumulating evidence suggests that the brain's potential to adapt and change is life-long (Johansson, 2004, Pascual-Leone et al., 2005). However, the mechanisms by which such alterations are effectuated are poorly understood, and little is known about their functional specificity. Structural grey matter (GM) changes measured by MRI have been reported in young subjects from days to months after learning to juggle (Draganski and May, 2008, Driemeyer et al., 2008). This finding was also replicated in older subjects, suggesting intact neuroplasticity in advanced age (Boyke et al., 2008). The same group also reported structural alterations in students in response to extensive studying (Draganski et al., 2006). Thus, training visuo-motor skills and learning abstract information seems to induce structural brain changes in both young and older subjects.

To answer questions of domain specificity, it is important to address different functional domains. Memory, a spectrum of cognitive functions inextricably coupled to everyday function, is associated with increasing concern among the aging population (Anderson and McConnell, 2007, National Council on the Aging, 2000), and memory complaints are reported by up to 50% of adults aged 64 and over (Reid and MacLullich, 2006). Furthermore, aging is associated with both progressive structural alterations (Fjell et al., 2009b, Jernigan et al., 2001, Raz et al., 2004, Raz et al., 2007, Salat et al., 2004, Walhovd et al., 2005, Walhovd et al., 2009, Westlye et al., 2009, Westlye et al., in press-aa, Westlye et al., in press-bb) and functional decline across multiple cognitive domains (Mahncke et al., 2006, Raz and Rodrigue, 2006). Population studies have indicated that mental exercise may slow the rate of cognitive decline (Valenzuela and Sachdev, 2006a) and decrease the risk of dementia (Valenzuela and Sachdev, 2006b). Hence, the role of mental exercise has gained much attention in preventive aging research (Rebok et al., 2007). However, knowledge about protective effects of mental exercise is sparse, and it is not known whether engaging in cognitively stimulating activities changes aging-related structural cerebral trajectories.

Most behavioral studies of memory improvement have been strategy-based, focusing on learning a specific mnemonic technique known as the MoL (Bower, 1970). Studies employing this technique have found associated changes in brain activation and neurochemistry (Kondo et al., 2005, Nyberg et al., 2003, Valenzuela and Sachdev, 2006a). However, no experimental study so far has been conducted to investigate whether such memory training can induce macro-structural changes in the brain. Further, visuo-motor training has been shown to induce macro-structural changes in elderly, but for cognitive training this has been demonstrated in young only. The aim of the present MRI study was to determine whether engaging in an 8-week memory training program would improve memory performance and induce regional changes in longitudinal cortical thickness trajectories in middle aged and older adults.

Section snippets

Sample

Table 1 summarizes baseline demographic and neuropsychological characteristics of the participants included in the analyses. Fig. 1 gives an overview of the recruitment and group assignment process. Volunteers were recruited through a local newspaper ad and screened by a structured interview before inclusion. All included participants reported to be right-handed, native Norwegian speakers, not concerned about their own memory function, not using medications known to interfere with cognitive

Memory performance changes

Table 1 summarizes neuropsychological characteristics and results from independent samples t-tests comparing the two groups at tp1. No significant group differences were found at tp1. The mean source memory task scores for the training and control group were 0.52 (Standard Error (SE) = 0.03) and 0.57 (SE = 0.02), respectively, at tp1, and 0.73 (SE = 0.03) and 0.62 (SE = 0.03), respectively, at tp2. Repeated measures ANOVA revealed a significant group × time interaction (Greenhouse–Geisser corrected, F

Discussion

There were three main findings in the present study: (1) Intensive source memory training specifically improved memory performance on a source memory task, (2) memory training induced longitudinal short-term regional effects on cortical thickness, indicating that the intervention influenced the age-related trajectories, and (3) regional cortical thickening was positively correlated with memory improvement. Thus, degree of cortical change was directly related to improvement rate in source memory

Acknowledgments

The Norwegian Research Council (177404/W50) to K.B.W., (175066/D15) to A.M.F. The Medical student research program to A.E. We thank the participants, and Håkon Grydeland and Inge Amlien for help with data acquisition.

References (88)

  • D.J. Hagler et al.

    Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data

    Neuroimage

    (2006)
  • X. Han et al.

    Reliability of MRI-derived measurements of human cerebral cortical thickness: the effects of field strength, scanner upgrade and manufacturer

    Neuroimage

    (2006)
  • S. Hayasaka et al.

    Validating cluster size inference: random field and permutation methods

    Neuroimage

    (2003)
  • T.L. Jernigan et al.

    Effects of age on tissues and regions of the cerebrum and cerebellum

    Neurobiol Aging

    (2001)
  • S. Jones et al.

    Cognitive and neural plasticity in aging: general and task-specific limitations

    Neurosci Biobehav Rev

    (2006)
  • J. Jovicich et al.

    Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data

    Neuroimage

    (2006)
  • J. Jovicich et al.

    MRI-derived measurements of human subcortical, ventricular and intracranial brain volumes: Reliability effects of scan sessions, acquisition sequences, data analyses, scanner upgrade, scanner vendors and field strengths

    NeuroImage

    (2009)
  • Y. Kondo et al.

    Changes in brain activation associated with use of a memory strategy: a functional MRI study

    Neuroimage

    (2005)
  • H.W. Mahncke et al.

    Brain plasticity and functional losses in the aged: scientific bases for a novel intervention

  • N. Raz et al.

    Differential aging of the brain: patterns, cognitive correlates and modifiers

  • D.H. Salat et al.

    Age-associated alterations in cortical gray matter and subjacent white matter signal intensity

    Neuroimage

    (2009)
  • A.J. van der Kouwe et al.

    On-line automatic slice positioning for brain MR imaging

    Neuroimage

    (2005)
  • K.B. Walhovd et al.

    Effects of age on volumes of cortex, white matter and subcortical structures

    Neurobiol Aging

    (2005)
  • L.T. Westlye et al.

    Increased sensitivity to effects of normal aging and Alzheimer's disease on cortical thickness by adjustment for local variability in gray/white contrast: a multi-sample MRI study

    Neuroimage

    (2009)
  • J.A. Yesavage et al.

    Development and validation of a geriatric depression screening scale: a preliminary report

    J Psychiatr Res

    (1983)
  • K. Ball et al.

    Effects of cognitive training interventions with older adults: a randomized controlled trial

    JAMA

    (2002)
  • T. Benner et al.

    Comparison of manual and automatic section positioning of brain MR images

    Radiology

    (2006)
  • G.H. Bower

    Analysis of a mnemonic device

    Am Sci

    (1970)
  • J. Boyke et al.

    Training-induced brain structure changes in the elderly

    J Neurosci

    (2008)
  • D.V. Buonomano et al.

    CORTICAL PLASTICITY: from synapses to maps

    Annu Rev Neurosci

    (1998)
  • A.D. Craig

    How do you feel—now? The anterior insula and human awareness

    Nat Rev Neurosci

    (2009)
  • A.M. Dale et al.

    Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach

    J Cogn Neurosci

    (1993)
  • J. DeFelipe

    Brain plasticity and mental processes: Cajal again

    Nat Rev Neurosci

    (2006)
  • D.C. Delis et al.

    California Verbal Learning Test—Second Edition (CVLT-II)

    (2000)
  • N.U.F. Dosenbach et al.

    Distinct brain networks for adaptive and stable task control in humans

    Proc Natl Acad Sci

    (2007)
  • B. Draganski et al.

    Neuroplasticity: changes in grey matter induced by training

    Nature

    (2004)
  • B. Draganski et al.

    Temporal and spatial dynamics of brain structure changes during extensive learning

    J Neurosci

    (2006)
  • J. Driemeyer et al.

    Changes in gray matter induced by learning—revisited

    PLoS ONE

    (2008)
  • B. Fischl et al.

    Measuring the thickness of the human cerebral cortex from magnetic resonance images

    Proc Natl Acad Sci U S A

    (2000)
  • B. Fischl et al.

    High-resolution intersubject averaging and a coordinate system for the cortical surface

    Hum Brain Mapp

    (1999)
  • A.M. Fjell et al.

    One-year brain atrophy evident in healthy aging

    J Neurosci

    (2009)
  • A.M. Fjell et al.

    High consistency of regional cortical thinning in aging across multiple samples

    Cereb Cortex

    (2009)
  • S. Forman et al.

    Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold

    Magn Reson Med

    (1995)
  • A.F. Fotenos et al.

    Normative estimates of cross-sectional and longitudinal brain volume decline in aging and AD

    Neurology

    (2005)
  • Cited by (272)

    View all citing articles on Scopus
    View full text