Cognitive function and brain structure correlations in healthy elderly East Asians
Introduction
Maintaining optimal cognitive function for as long as possible is a vital element of successful aging (Rowe and Kahn, 1987) and this goal has motivated many cognitive and imaging studies of brain aging. With possibly one exception (Mu et al., 1999) all such studies have been conducted in predominantly Caucasian populations (Carlson et al., 2008, Fotenos et al., 2005, Prins et al., 2002, Raz et al., 1998, Resnick et al., 2003, Scahill et al., 2003).
As the additional resources needed to care for disabled elderly could significantly compound the pressure exerted on global energy and food availability, there is an urgent need for accurate information about brain and cognitive aging among Asians — who constitute the most rapidly aging population grouping in the world. To illustrate, in 1982, adults over the age of 65 years represented only 4.9% of the Chinese population (Liang et al., 1985). This increased to 6.96% of 1.3 billion in 2000 (National Bureau of Statistics People's Republic of China, 2001), and could rise to 23.7% of 1.4 billion in 2050 (Population division of the department of economic and social affairs of the United Nations Secretariat, 2007) i.e. equivalent to the entire United States population in 2006.
The rate of cognitive decline and brain atrophy can be influenced by education (Staff et al., 2004) as well as a variety of cardiovascular risk/fitness factors (Colcombe et al., 2004, Murray et al., 2005, Raz et al., 2003a) in ways that probably generalize across populations. However, diet (Kalmijn et al., 2004, Mattson, 2003), environmental factors and genetic makeup differ across ethnic groups and could affect the aging process (Bamshad, 2005, Kirkwood, 2005). Additionally, culture has been shown to influence cognition (Nisbett and Miyamoto, 2005, Park and Gutchess, 2002) and modulate task-related brain activation (Goh et al., 2007).
Comparing rates of change of brain volume across aging studies requires attention to differences in image acquisition and quality control (Littmann et al., 2006, Preboske et al., 2006), sample size and age span of the cohort (Fotenos et al., 2005, Jernigan and Gamst, 2005), health of volunteers (Resnick et al., 2003), image measurement technique (Gunter et al., 2003) and method of correction for differences in head size (Buckner et al., 2004). The range in findings across studies makes it difficult to assess what is ‘normal’ for a particular group or to judge the benefit of environmental modifiers or the efficacy of interventions that could reduce the impact of age-related change in cognition. These challenges are compounded by the fact that excellent imaging data may not be accompanied by detailed neuropsychological testing or associated health information and vice versa. Such practical realities have motivated the formation of multi-laboratory consortiums to standardize data collection (Jack et al., 2008, Mueller et al., 2005), so as to afford the establishment of baseline data that has robust clinical utility.
In recognition of the methodological issues that could confound the interpretation of contemporary structural imaging studies, we report cross-sectional data originating from a large (248 subjects), single-centre, longitudinal aging study that incorporated recent advancements in image acquisition, quality control (Mallozzi et al., 2006, Mallozzi et al., 2004), image processing (Jovicich et al., 2006) and analysis (Desikan et al., 2006, Fischl et al., 2004) techniques.
We focused on a ‘post-retirement’ age range of 55–86 years, instead of attempting to characterize lifespan changes, because age-related changes in cognition have the greatest economic and societal impact in this segment of the population. In addition to age, we evaluated other factors that could affect cognitive performance (Enzinger et al., 2005). We obtained a number of measures of brain structure and evaluated the effect of age and health variables of interest on these measures. Mindful that pre-existing chronic illness can influence imaging findings (Resnick et al., 2003) we prospectively selected volunteers who met strict health criteria in order that our results would represent a standard an average middle class East Asian individual could benchmark against. Finally, we correlated measures of cognitive performance and brain structure. In view of the increasing automation in brain structure measurement, we made head-to-head comparisons between manual and semi-automated measurements of three commonly reported brain measures as a preface to more extensive data analysis using this methodology. This cross sectional data, while primarily descriptive and comparative in nature, should provide a valuable starting point from which to base future studies concerning brain aging in Asians.
Section snippets
Participants
The volunteers were members of the Singapore Longitudinal Aging Brain Study, a community-based epidemiologic study involving healthy elderly volunteers that sought to characterize age-related brain changes and cognitive performance in persons of Chinese descent resident in Singapore. The study was approved by the Singapore General Hospital Institutional Review Board and participants gave informed consent prior to undergoing evaluation.
349 healthy adults participated in the first wave of the
Characteristics of the study population
The cohort was matched for age and gender (men: mean = 65.9, SD = 6.9 years and women: mean = 65.6, SD = 6.1 years; women 52.8%; Table 1). 84% of participants had at least 10 years of education, substantially higher than that reported in a larger community-based longitudinal aging study conducted in the same city (Feng et al., 2006) but lower than that reported in most studies on Caucasian subjects. For comparison the national average in 1997 for resident non-students > 25 years of age was 8.8 for men
Discussion
The present cross-sectional study is the first sizable combined MRI imaging, neuropsychological and health variable study performed on a cohort of healthy aged volunteers arising from a single, East Asian ethnic group. The study cohort is unique in that most participants were born and grew up in a developing country but aged in a developed one.
We found speed of processing to be the most age-affected cognitive domain. It was associated with commensurate decline in total cerebral hemisphere
Summary
The broad agreement between age-related changes in cognition and brain measures reported here compared to studies based on Caucasian populations argues for the presence of common factors that modulate brain aging across ethnic groups that potentially differ in culture, diet and lifestyle. Total cerebral measures appear to provide adequate brain–cognition correlations with performance on clinical neuropsychological tests in healthy elderly. However, to evaluate the structural neural correlates
Disclosure
The authors have no conflict of interests to disclose. All authors have reviewed the contents of the manuscript being submitted, approve of its contents and validate the accuracy of the data.
Acknowledgments
Arne Littmann provided proprietary homogeneity correction and gradient distortion correction techniques. Jenni Pacheco provided on-site training for the use of FreeSurfer. Cliff Jack provided valuable advice on manual morphometry and the quality control aspects of this study. This work was supported by the Biomedical Research Council, Singapore: BMRC 04/1/36/372 and A⁎STAR: SRP R-913-200-004-304.
References (111)
- et al.
Relationship between body height and dementia
Am. J. Geriatr. Psychiatry
(2005) - et al.
A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume
NeuroImage
(2004) - et al.
Age-related slowing of memory retrieval: contributions of perceptual speed and cerebral white matter integrity
Neurobiol. Aging
(2008) - et al.
Plasma folate concentration and cognitive performance: Rotterdam Scan Study
Am. J. Clin. Nutr.
(2007) - et al.
Measures of brain morphology and infarction in the Framingham Heart Study: establishing what is normal
Neurobiol. Aging
(2005) - et al.
An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest
NeuroImage
(2006) - et al.
Detection of cortical thickness correlates of cognitive performance: reliability across MRI scan sessions, scanners, and field strengths
NeuroImage
(2008) - et al.
Training-induced structural changes in the adult human brain
Behav. Brain Res.
(2008) - et al.
Homocysteine, B vitamin status, and cognitive function in the elderly
Am. J. Clin. Nutr.
(2002) - et al.
Homocysteine, folate, and vitamin B-12 and cognitive performance in older Chinese adults: findings from the Singapore Longitudinal Ageing Study
Am. J. Clin. Nutr.
(2006)
Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain
Neuron
Sequence-independent segmentation of magnetic resonance images
NeuroImage
“Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician
J. Psychiatr. Res.
Imaging cerebral atrophy: normal ageing to Alzheimer's disease
Lancet
Association between blood pressure levels over time and brain atrophy in the elderly
Neurobiol. Aging
Brain tissue volumes in the general elderly population. The Rotterdam Scan Study
Neurobiol. Aging
Effects of age on tissues and regions of the cerebrum and cerebellum
Neurobiol. Aging
Changes in volume with age—consistency and interpretation of observed effects
Neurobiol. Aging
Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data
NeuroImage
Homocysteine versus the vitamins folate, B6, and B12 as predictors of cognitive function and decline in older high-functioning adults: MacArthur Studies of Successful Aging
Am. J. Med.
Understanding the odd science of aging
Cell
Age- and sex-related effects on the neuroanatomy of healthy elderly
NeuroImage
Acquisition-related morphological variability in structural MRI
Acad. Radiol.
Correction for head size in brain-imaging measurements
Psychiatry Res.
The Alzheimer's disease neuroimaging initiative
Neuroimaging Clin. N. Am.
The influence of culture: holistic versus analytic perception
Trends Cogn. Sci.
Aging, cognition, and culture: a neuroscientific perspective
Neurosci. Biobehav. Rev.
Common MRI acquisition non-idealities significantly impact the output of the boundary shift integral method of measuring brain atrophy on serial MRI
NeuroImage
Low folate status is associated with impaired cognitive function and dementia in the Sacramento Area Latino Study on Aging
Am. J. Clin. Nutr.
Brain aging: reorganizing discoveries about the aging mind
Curr. Opin. Neurobiol.
A hybrid approach to the skull stripping problem in MRI
NeuroImage
Generality and specificity in cognitive aging: a volumetric brain analysis
NeuroImage
Height as a marker of childhood development and late-life cognitive function: the Honolulu–Asia Aging Study
Pediatrics
Genetic influences on health: does race matter?
Jama
White matter structural integrity in healthy aging adults and patients with Alzheimer disease: a magnetic resonance imaging study
Arch. Neurol.
Trajectories of brain loss in aging and the development of cognitive impairment
Neurology
Relation of education to brain size in normal aging: implications for the reserve hypothesis
Neurology
Cardiovascular fitness, cortical plasticity and aging
Proc. Natl. Acad. Sci. U. S. A.
Delis-Kaplan Executive Function System
Homocysteine and brain atrophy on MRI of non-demented elderly
Brain
The paradox of low body mass index and high body fat percentage among Chinese, Malays and Indians in Singapore
Int. J. Obes. Relat. Metab. Disord.
Validity of body composition methods across ethnic population groups
Forum Nutr.
An Object and Action Naming Battery
Dehydration confounds the assessment of brain atrophy
Neurology
Total intracranial volume: normative values and lack of association with Alzheimer's disease
Neurology
Homocysteine and cognitive performance in the Framingham offspring study: age is important
Am. J. Epidemiol.
Risk factors for progression of brain atrophy in aging: six-year follow-up of normal subjects
Neurology
Brain volume decline in aging: evidence for a relation between socioeconomic status, preclinical Alzheimer disease, and reserve
Arch. Neurol.
Normative estimates of cross-sectional and longitudinal brain volume decline in aging and AD
Neurology
Age and culture modulate object processing and object–scene binding in the ventral visual area
Cogn. Affect. Behav. Neurosci.
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