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Published in: BMC Geriatrics 1/2009

Open Access 01-12-2009 | Research article

Maximum (prior) brain size, not atrophy, correlates with cognition in community-dwelling older people: a cross-sectional neuroimaging study

Authors: Susan D Shenkin, Carly S Rivers, Ian J Deary, John M Starr, Joanna M Wardlaw

Published in: BMC Geriatrics | Issue 1/2009

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Abstract

Background

Brain size is associated with cognitive ability in adulthood (correlation ~ .3), but few studies have investigated the relationship in normal ageing, particularly beyond age 75 years. With age both brain size and fluid-type intelligence decline, and regional atrophy is often suggested as causing decline in specific cognitive abilities. However, an association between brain size and intelligence may be due to the persistence of this relationship from earlier life.

Methods

We recruited 107 community-dwelling volunteers (29% male) aged 75–81 years for cognitive testing and neuroimaging. We used principal components analysis to derived a 'general cognitive factor' (g) from tests of fluid-type ability. Using semi-automated analysis, we measured whole brain volume, intracranial area (ICA) (an estimate of maximal brain volume), and volume of frontal and temporal lobes, amygdalo-hippocampal complex, and ventricles. Brain atrophy was estimated by correcting WBV for ICA.

Results

Whole brain volume (WBV) correlated with general cognitive ability (g) (r = .21, P < .05). Statistically significant associations between brain areas and specific cognitive abilities became non-significant when corrected for maximal brain volume (estimated using ICA), i.e. there were no statistically significant associations between atrophy and cognitive ability. The association between WBV and g was largely attenuated (from .21 to .03: i.e. attenuating the variance by 98%) by correcting for ICA. ICA accounted for 6.2% of the variance in g in old age, whereas atrophy accounted for < 1%.

Conclusion

The association between brain regions and specific cognitive abilities in community dwelling people of older age is due to the life-long association between whole brain size and general cognitive ability, rather than atrophy of specific regions. Researchers and clinicians should therefore be cautious of interpreting global or regional brain atrophy on neuroimaging as contributing to cognitive status in older age without taking into account prior mental ability and brain size.
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Literature
1.
go back to reference Mann DMA: Neurobiology of Aging. Geriatric medicine and gerontology. Edited by: Tallis R, Fillit H, Brocklehurst JC. 1998, Edinburgh: Churchill Livingstone, 385-422. 5 Mann DMA: Neurobiology of Aging. Geriatric medicine and gerontology. Edited by: Tallis R, Fillit H, Brocklehurst JC. 1998, Edinburgh: Churchill Livingstone, 385-422. 5
2.
go back to reference Witelson SF, Beresh H, Kigar DL: Intelligence and brain size in 100 postmortem brains: sex, lateralization and age factors. Brain. 2006, 129: 386-398. 10.1093/brain/awh696.CrossRefPubMed Witelson SF, Beresh H, Kigar DL: Intelligence and brain size in 100 postmortem brains: sex, lateralization and age factors. Brain. 2006, 129: 386-398. 10.1093/brain/awh696.CrossRefPubMed
3.
go back to reference Resnick SM, Pham DL, Kraut MA, Zonderman AB, Davatzikos C: Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain. J Neurosci. 2003, 23: 3295-3301.PubMed Resnick SM, Pham DL, Kraut MA, Zonderman AB, Davatzikos C: Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain. J Neurosci. 2003, 23: 3295-3301.PubMed
4.
go back to reference Fotenos AF, Snyder AZ, Girton LE, Morris JC, Buckner RL: Normative estimates of cross-sectional and longitudinal brain volume decline in aging and AD. Neurology. 2005, 64: 1032-1039.CrossRefPubMed Fotenos AF, Snyder AZ, Girton LE, Morris JC, Buckner RL: Normative estimates of cross-sectional and longitudinal brain volume decline in aging and AD. Neurology. 2005, 64: 1032-1039.CrossRefPubMed
5.
go back to reference Deary IJ, Whalley LJ, Lemmon H, Crawford JR, Starr JM: The stability of individual differences in mental ability from childhood to old age: follow-up of the 1932 Scottish Mental Survey. Intelligence. 2000, 28: 49-55. 10.1016/S0160-2896(99)00031-8.CrossRef Deary IJ, Whalley LJ, Lemmon H, Crawford JR, Starr JM: The stability of individual differences in mental ability from childhood to old age: follow-up of the 1932 Scottish Mental Survey. Intelligence. 2000, 28: 49-55. 10.1016/S0160-2896(99)00031-8.CrossRef
6.
go back to reference Wickett JC, Vernon P, Lee DH: Relationships between factors of intelligence and brain volume. Personality and Individual Differences. 2000, 29: 1095-1122. 10.1016/S0191-8869(99)00258-5.CrossRef Wickett JC, Vernon P, Lee DH: Relationships between factors of intelligence and brain volume. Personality and Individual Differences. 2000, 29: 1095-1122. 10.1016/S0191-8869(99)00258-5.CrossRef
7.
go back to reference Gale CR, Walton S, Martyn CN: Foetal and postnatal head growth and risk of cognitive decline in old age. Brain. 2003, 126: 2273-2278. 10.1093/brain/awg225.CrossRefPubMed Gale CR, Walton S, Martyn CN: Foetal and postnatal head growth and risk of cognitive decline in old age. Brain. 2003, 126: 2273-2278. 10.1093/brain/awg225.CrossRefPubMed
8.
go back to reference Reynolds MD, Johnston JM, Dodge HH, DeKosky ST, Ganguli M: Small head size is related to low Mini-Mental State Examination scores in a community sample of nondemented older adults. Neurology. 1999, 53: 228-229.CrossRefPubMed Reynolds MD, Johnston JM, Dodge HH, DeKosky ST, Ganguli M: Small head size is related to low Mini-Mental State Examination scores in a community sample of nondemented older adults. Neurology. 1999, 53: 228-229.CrossRefPubMed
9.
go back to reference Tisserand DJ, Bosma H, Van Boxtel MPJ, Jolles J: Head size and cognitive ability in nondemented older adults are related. Neurology. 2001, 56: 969-971.CrossRefPubMed Tisserand DJ, Bosma H, Van Boxtel MPJ, Jolles J: Head size and cognitive ability in nondemented older adults are related. Neurology. 2001, 56: 969-971.CrossRefPubMed
10.
go back to reference McDaniel MA: Big-brained people are smarter: a meta-analysis of the relationship between in vivo brain volume and intelligence. Intelligence. 2005, 33: 337-346. 10.1016/j.intell.2004.11.005.CrossRef McDaniel MA: Big-brained people are smarter: a meta-analysis of the relationship between in vivo brain volume and intelligence. Intelligence. 2005, 33: 337-346. 10.1016/j.intell.2004.11.005.CrossRef
11.
go back to reference van Petten C: Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: review and meta-analysis. Neuropsychologia. 2004, 42: 1394-1413. 10.1016/j.neuropsychologia.2004.04.006.CrossRefPubMed van Petten C: Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: review and meta-analysis. Neuropsychologia. 2004, 42: 1394-1413. 10.1016/j.neuropsychologia.2004.04.006.CrossRefPubMed
12.
go back to reference Raz N, Rodrigue KM: Differential aging of the brain: Patterns, cognitive correlates and modifiers. Neurosci Biobehav Rev. 2006, 30: 730-748. 10.1016/j.neubiorev.2006.07.001.CrossRefPubMed Raz N, Rodrigue KM: Differential aging of the brain: Patterns, cognitive correlates and modifiers. Neurosci Biobehav Rev. 2006, 30: 730-748. 10.1016/j.neubiorev.2006.07.001.CrossRefPubMed
13.
go back to reference Ferguson KJ, Wardlaw JM, Edmond CL, Deary IJ, MacLullich AM: Intracranial area: a validated method for estimating intracranial volume. J Neuroimaging. 2005, 15: 76-78. 10.1177/1051228404270243.CrossRefPubMed Ferguson KJ, Wardlaw JM, Edmond CL, Deary IJ, MacLullich AM: Intracranial area: a validated method for estimating intracranial volume. J Neuroimaging. 2005, 15: 76-78. 10.1177/1051228404270243.CrossRefPubMed
14.
go back to reference MacLullich A, Ferguson K, Deary I, Seckl J, Starr J, Wardlaw J: Intracranial capacity and brain volumes are associated with cognition in healthy elderly men. Neurology. 2002, 59: 169-174.CrossRefPubMed MacLullich A, Ferguson K, Deary I, Seckl J, Starr J, Wardlaw J: Intracranial capacity and brain volumes are associated with cognition in healthy elderly men. Neurology. 2002, 59: 169-174.CrossRefPubMed
15.
go back to reference Christensen H, Anstey KJ, Parslow RA, Maller J, Mackinnon A, Sachdev P: The brain reserve hypothesis, brain atrophy and aging. Gerontology. 2007, 53: 82-95. 10.1159/000096482.CrossRefPubMed Christensen H, Anstey KJ, Parslow RA, Maller J, Mackinnon A, Sachdev P: The brain reserve hypothesis, brain atrophy and aging. Gerontology. 2007, 53: 82-95. 10.1159/000096482.CrossRefPubMed
16.
go back to reference Staff RT, Murray AD, Deary IJ, Whalley LJ: What provides cerebral reserve?. Brain. 2004, 127: 1191-1199. 10.1093/brain/awh144.CrossRefPubMed Staff RT, Murray AD, Deary IJ, Whalley LJ: What provides cerebral reserve?. Brain. 2004, 127: 1191-1199. 10.1093/brain/awh144.CrossRefPubMed
17.
go back to reference Lye TC, Piguet O, Grayson DA, Creasey H, Ridley LJ, Bennett HP, Broe GA: Hippocampal size and memory function in the ninth and tenth decades of life: the Sydney Older Persons Study. J Neurol Neurosurg Psychiatry. 2004, 75: 548-554. 10.1136/jnnp.2003.010223.CrossRefPubMedPubMedCentral Lye TC, Piguet O, Grayson DA, Creasey H, Ridley LJ, Bennett HP, Broe GA: Hippocampal size and memory function in the ninth and tenth decades of life: the Sydney Older Persons Study. J Neurol Neurosurg Psychiatry. 2004, 75: 548-554. 10.1136/jnnp.2003.010223.CrossRefPubMedPubMedCentral
18.
go back to reference Staff RT, Murray AD, Deary IJ, Whalley LJ: Generality and specificity in cognitive aging: a volumetric brain analysis. Neuroimage. 2006, 30: 1433-1440. 10.1016/j.neuroimage.2005.11.004.CrossRefPubMed Staff RT, Murray AD, Deary IJ, Whalley LJ: Generality and specificity in cognitive aging: a volumetric brain analysis. Neuroimage. 2006, 30: 1433-1440. 10.1016/j.neuroimage.2005.11.004.CrossRefPubMed
19.
go back to reference Deary IJ, Whiteman MC, Starr JM, Whalley LJ, Fox HC: The impact of childhood intelligence on later life: following up the Scottish mental surveys of 1932 and 1947. J Pers Soc Psychol. 2004, 86: 130-147. 10.1037/0022-3514.86.1.130.CrossRefPubMed Deary IJ, Whiteman MC, Starr JM, Whalley LJ, Fox HC: The impact of childhood intelligence on later life: following up the Scottish mental surveys of 1932 and 1947. J Pers Soc Psychol. 2004, 86: 130-147. 10.1037/0022-3514.86.1.130.CrossRefPubMed
20.
go back to reference Shenkin SD, Bastin ME, MacGillivray TJ, Deary IJ, Starr JM, Rivers CS, Wardlaw JM: Cognitive correlates of cerebral white matter lesions and water diffusion tensor parameters in community-dwelling older people. Cerebrovasc Dis. 2005, 20: 310-318. 10.1159/000087930.CrossRefPubMed Shenkin SD, Bastin ME, MacGillivray TJ, Deary IJ, Starr JM, Rivers CS, Wardlaw JM: Cognitive correlates of cerebral white matter lesions and water diffusion tensor parameters in community-dwelling older people. Cerebrovasc Dis. 2005, 20: 310-318. 10.1159/000087930.CrossRefPubMed
21.
go back to reference Folstein MF, Folstein SE, McHugh PR: "Mini-mental state." A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975, 12: 189-198. 10.1016/0022-3956(75)90026-6.CrossRefPubMed Folstein MF, Folstein SE, McHugh PR: "Mini-mental state." A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975, 12: 189-198. 10.1016/0022-3956(75)90026-6.CrossRefPubMed
22.
go back to reference Lezak MD: Neuropsychological Assessment. 1995, New York, Oxford: Oxford University Press Lezak MD: Neuropsychological Assessment. 1995, New York, Oxford: Oxford University Press
23.
go back to reference The Scottish Council For Research in Education: The Intelligence of Scottish Children. A National Survey of an Age Group. 1933, London: University of London Press The Scottish Council For Research in Education: The Intelligence of Scottish Children. A National Survey of an Age Group. 1933, London: University of London Press
24.
go back to reference Raven JC, Court JH, Raven J: Manual for Raven's Progressive Matrices and Vocabulary Scales. 1977, London: HK Lewis & Co Raven JC, Court JH, Raven J: Manual for Raven's Progressive Matrices and Vocabulary Scales. 1977, London: HK Lewis & Co
25.
go back to reference Wechsler D: Wechsler Memory Scale – Revised (WMS-R). 1987, New York: Psychological Corporation Wechsler D: Wechsler Memory Scale – Revised (WMS-R). 1987, New York: Psychological Corporation
26.
go back to reference Hofer SM, Berg S, Era P: Evaluating the interdependence of aging-related changes in visual and auditory acuity, balance, and cognitive functioning. Psychol Aging. 2003, 18: 285-305. 10.1037/0882-7974.18.2.285.CrossRefPubMed Hofer SM, Berg S, Era P: Evaluating the interdependence of aging-related changes in visual and auditory acuity, balance, and cognitive functioning. Psychol Aging. 2003, 18: 285-305. 10.1037/0882-7974.18.2.285.CrossRefPubMed
27.
go back to reference Staff RT, Murray AD, Deary IJ, Whalley LJ: What provides cerebral reserve?. Brain. 2004, 127: 1191-1199. 10.1093/brain/awh144.CrossRefPubMed Staff RT, Murray AD, Deary IJ, Whalley LJ: What provides cerebral reserve?. Brain. 2004, 127: 1191-1199. 10.1093/brain/awh144.CrossRefPubMed
28.
go back to reference Stern Y: Cognitive reserve and Alzheimer Disease. Alzheimer Dis Assoc Disord. 2006, 20 (3 Suppl 2): S69-S74. 10.1097/01.wad.0000213815.20177.19.CrossRefPubMed Stern Y: Cognitive reserve and Alzheimer Disease. Alzheimer Dis Assoc Disord. 2006, 20 (3 Suppl 2): S69-S74. 10.1097/01.wad.0000213815.20177.19.CrossRefPubMed
29.
go back to reference Stern Y, Zarahn E, Habeck C, Holtzer R, Rakitin BC, Kumar A, Flynn J, Steffener J, Brown T: A common neural network for cognitive reserve in verbal and object working memory in young but not old. Cereb Cortex. 2008, 18 (4): 959-967. 10.1093/cercor/bhm134.CrossRefPubMed Stern Y, Zarahn E, Habeck C, Holtzer R, Rakitin BC, Kumar A, Flynn J, Steffener J, Brown T: A common neural network for cognitive reserve in verbal and object working memory in young but not old. Cereb Cortex. 2008, 18 (4): 959-967. 10.1093/cercor/bhm134.CrossRefPubMed
30.
go back to reference Richards M, Sacker A: Lifetime antecedents of cognitive reserve. J Clin Exp Neuropsychol. 2003, 25: 614-624. 10.1076/jcen.25.5.614.14581.CrossRefPubMed Richards M, Sacker A: Lifetime antecedents of cognitive reserve. J Clin Exp Neuropsychol. 2003, 25: 614-624. 10.1076/jcen.25.5.614.14581.CrossRefPubMed
31.
go back to reference Walhovd KB, Fjell AM, Reinvang I, Lundervold A, Dale AM, Quinn BT, Salat D, Makris N, Fischl B: Neuroanatomical aging: Universal but not uniform. Neurobiol Aging. 2005, 26: 1279-1282. 10.1016/j.neurobiolaging.2005.05.018.CrossRef Walhovd KB, Fjell AM, Reinvang I, Lundervold A, Dale AM, Quinn BT, Salat D, Makris N, Fischl B: Neuroanatomical aging: Universal but not uniform. Neurobiol Aging. 2005, 26: 1279-1282. 10.1016/j.neurobiolaging.2005.05.018.CrossRef
32.
go back to reference Brickman AM, Habeck C, Zarahn E, Flynn J, Stern Y: Structural MRI covariance patterns associated with normal aging and neuropsychological functioning. Neurobiol Aging. 2007, 28: 284-295. 10.1016/j.neurobiolaging.2005.12.016.CrossRefPubMed Brickman AM, Habeck C, Zarahn E, Flynn J, Stern Y: Structural MRI covariance patterns associated with normal aging and neuropsychological functioning. Neurobiol Aging. 2007, 28: 284-295. 10.1016/j.neurobiolaging.2005.12.016.CrossRefPubMed
33.
go back to reference Lupien SJ, Maheu F, Tu M, Fiocco A, Schramek TE: The effects of stress and stress hormones on human cognition: Implications for the field of brain and cognition. Brain Cogn. 2007, 65 (3): 209-237. 10.1016/j.bandc.2007.02.007.CrossRefPubMed Lupien SJ, Maheu F, Tu M, Fiocco A, Schramek TE: The effects of stress and stress hormones on human cognition: Implications for the field of brain and cognition. Brain Cogn. 2007, 65 (3): 209-237. 10.1016/j.bandc.2007.02.007.CrossRefPubMed
34.
go back to reference Tisserand DJ, van Boxtel MP, Pruessner JC, Hofman P, Evans AC, Jolles J: A Voxel-based Morphometric Study to Determine Individual Differences in Gray Matter Density Associated with Age and Cognitive Change Over Time. Cerebral Cortex. 2004, 14: 966-973. 10.1093/cercor/bhh057.CrossRefPubMed Tisserand DJ, van Boxtel MP, Pruessner JC, Hofman P, Evans AC, Jolles J: A Voxel-based Morphometric Study to Determine Individual Differences in Gray Matter Density Associated with Age and Cognitive Change Over Time. Cerebral Cortex. 2004, 14: 966-973. 10.1093/cercor/bhh057.CrossRefPubMed
35.
go back to reference Gale CR, O'Callaghan FJ, Godfrey KM, Law CM, Martyn CN: Critical periods of brain growth and cognitive function in children. Brain. 2004, 127: 321-329. 10.1093/brain/awh034.CrossRefPubMed Gale CR, O'Callaghan FJ, Godfrey KM, Law CM, Martyn CN: Critical periods of brain growth and cognitive function in children. Brain. 2004, 127: 321-329. 10.1093/brain/awh034.CrossRefPubMed
36.
go back to reference Shenkin SD, Starr JM, Deary IJ: Birth weight and cognitive ability in childhood: a systematic review. Psychol Bull. 2004, 130: 989-1013. 10.1037/0033-2909.130.6.989.CrossRefPubMed Shenkin SD, Starr JM, Deary IJ: Birth weight and cognitive ability in childhood: a systematic review. Psychol Bull. 2004, 130: 989-1013. 10.1037/0033-2909.130.6.989.CrossRefPubMed
37.
go back to reference Callen DJ, Black SE, Gao F, Caldwell CB, Szalai JP: Beyond the hippocampus: MRI volumetry confirms widespread limbic atrophy in AD. Neurology. 2001, 57: 1669-1674.CrossRefPubMed Callen DJ, Black SE, Gao F, Caldwell CB, Szalai JP: Beyond the hippocampus: MRI volumetry confirms widespread limbic atrophy in AD. Neurology. 2001, 57: 1669-1674.CrossRefPubMed
38.
go back to reference Devanand DP, Mayeux R, Liu X, Khandji A, De Santi S, Segal S, Rusinek H, Pelton GH, Honig LS, Mayeux R, et al: Hippocampal and entorhinal atrophy in mild cognitive impairment: prediction of Alzheimer disease. Neurology. 2007, 68: 828-836. 10.1212/01.wnl.0000256697.20968.d7.CrossRefPubMed Devanand DP, Mayeux R, Liu X, Khandji A, De Santi S, Segal S, Rusinek H, Pelton GH, Honig LS, Mayeux R, et al: Hippocampal and entorhinal atrophy in mild cognitive impairment: prediction of Alzheimer disease. Neurology. 2007, 68: 828-836. 10.1212/01.wnl.0000256697.20968.d7.CrossRefPubMed
Metadata
Title
Maximum (prior) brain size, not atrophy, correlates with cognition in community-dwelling older people: a cross-sectional neuroimaging study
Authors
Susan D Shenkin
Carly S Rivers
Ian J Deary
John M Starr
Joanna M Wardlaw
Publication date
01-12-2009
Publisher
BioMed Central
Published in
BMC Geriatrics / Issue 1/2009
Electronic ISSN: 1471-2318
DOI
https://doi.org/10.1186/1471-2318-9-12

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