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Thinning of the Cerebral Cortex in Aging

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Cerebral Cortex V 14 N 7 © Oxford University Press 2004; all rights reserved Cerebral Cortex July 2004;14:721–730; DOI: 10.1093/cercor/bhh032Thinning of the Cerebral Cortex in AgingDavid H. Salat1, Randy L. Buckner2,3,5, Abraham Z. Snyder3,4, Douglas N. Greve1, Rahul S.R. Desikan1, Evelina Busa1, John C. Morris4, Anders M. Dale1 and Bruce Fischl11MGH/MIT/HMS Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA, USA, 2Departments of Psychology, Anatomy and Neurobiology, Washington University, St Louis, MO, USA, 3Department of Radiology, Washington University, St Louis, MO, USA, 4Department of Neurology, Washington University, St Louis, MO, USA and 5Howard Hughes Medical InstituteThe thickness of the cerebral cortex was measured in 106 non-demented participants ranging in age from 18 to 93 years. For eachparticipant, multiple acquisitions of structural T1-weighted magneticresonance imaging (MRI) scans were averaged to yield high-resolu-tion, high-contrast data sets. Cortical thickness was estimated as thedistance between the gray/white boundary and the outer corticalsurface, resulting in a continuous estimate across the corticalmantle. Global thinning was apparent by middle age. Men andwomen showed a similar degree of global thinning, and did not differin mean thickness in the younger or older groups. Age-associateddifferences were widespread but demonstrated a patchwork ofregional atrophy and sparing. Examination of subsets of the data fromindependent samples produced highly similar age-associatedpatterns of atrophy, suggesting that the specific anatomic patternswithin the maps were reliable. Certain results, including prominentatrophy of prefrontal cortex and relative sparing of temporal andparahippocampal cortex, converged with previous findings. Otherresults were unexpected, such as the finding of prominent atrophy infrontal cortex near primary motor cortex and calcarine cortex nearprimary visual cortex. These findings demonstrate that cortical thin-ning occurs by middle age and spans widespread cortical regionsthat include primary as well as association cortex.Keywords: aging, atrophy, calcarine cortex, cortical thickness, dementia, executive function, magnetic resonance imaging, MRI, prefrontal cortexIntroductionAge-related changes in brain morphology are apparent in bothpostmortem histological and in vivo magnetic resonanceimaging (MRI) studies (for reviews, see Kemper, 1994; Raz,2000). The majority of post-mortem studies report age-relatedalteration of global morphometric properties including declinein total brain weight, cortical thinning and gyral atrophy that isparticularly accelerated during the sixth and seventh decades(Kemper, 1994). Questions remain as to how early suchchanges begin and whether specific cortical regions are prefer-entially vulnerable to the morphologic changes associated withaging. In the present study, age-associated cortical atrophy wasmapped as the thinning of cortex across the entire corticalmantle, allowing visualization of regional cortical atrophypatterns.Previous neuronal counting studies have suggested thatdegenerative changes are accelerated in specific areas of thecortex, including frontal pole and premotor cortex (Kemper,1994). Comparisons across species led to speculation that age-related cortical changes follow a gradient, with greatest andearliest changes occurring in association areas and lesserchanges occurring later in primary sensory regions (Flood andColeman, 1988). Although early studies postulated this atrophyto be due to neurodegeneration, several recent studies suggestthat neuron number is relatively preserved in the healthy agingbrain of both humans and nonhuman primates (Morrison andHof, 1997; Peters et al., 1998), although alterations in neuronalmorphology are evident.Contemporary in vivo neuroimaging studies have confirmedthat there are alterations in global brain morphologic proper-ties (Jernigan et al., 1991, 2001; Pfefferbaum et al., 1994;Blatter et al., 1995; Raz et al., 1997; Good et al., 2001; Sowell etal., 2003). These studies additionally support the view thatmorphological alterations may be accelerated in particularareas of the cortex — described by Raz (2000) as a ‘patchworkpattern of differential declines and relative preservation’. Pref-erential vulnerability of prefrontal cortex, in particular, hasbeen demonstrated across studies, prefrontal change beinggreater than changes in other regions (Jernigan et al., 1991; Razet al., 1997; Sowell et al., 2003). Although this preferentialvulnerability has been statistically demonstrated in certainstudies (e.g. Raz et al., 1997), the majority of MRI studies ofbrain aging have not directly compared regional effects todescribe patterns of regional selectivity.The specific patterns of regional change place importantconstraints on what may underlie cortical atrophy and howatrophy may relate to the complex constellation of cognitivechanges associated with aging. One idea, originally proposedin the context of developmental myelination, is that age-associ-ated changes are characteristic of association cortex asopposed to primary cortex (reviewed by Kemper, 1994).Consistent with this possibility, Raz (2000) recently reported astrong relation between order of developmental myelinationand degree of age-associated volumetric atrophy, with regionsdeveloping late showing the strongest age-related atrophy.Maps of cortical atrophy, as produced in the present study,provide a test of this idea, in so far as it applies to corticalatrophy patterns. More broadly construed, maps of age-associ-ated cortical thinning provide constraints on hypothesesconcerning regionally specific processes related to atrophy.In the present study, we measured the thickness of the cere-bral cortex from MR images (Dale and Sereno, 1993; Dale et al.,1999; Fischl et al., 1999a, 2001; Fischl and Dale, 2000), using atechnique that has been validated via histological (Rosas et al.,2002) as well as manual measurements (Kuperberg et al.,2003), to examine the regional patterns of age-associatedcortical thinning. As a secondary question, we explored the722Age-associated Cortical Thinning • Salat et al.lower age limit at which reliable effects are demonstrable. Allolder participants were clinically characterized to minimizethe contribution of potential common medical comorbiditiesthat could confound the interpretation of the data. We


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