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Age-related changes in brain activation during a delayed item recognition taskIntroductionBrain areas implicated in working memory maintenance in the youngAge-related changes in the brain mechanisms of verbal WMModels which predict changes in patterns of brain activation with agingModels which predict no change in patterns of brain activation with agingComparing patterns of brain activationMethodsStudy populationBehavioral taskfMRI data acquisitionfMRI data pre-processingfMRI time-series modelingSequential latent root testingSPM voxel-wise intensity testsNeural inefficiencyResultsReaction timeAccuracyDIR task brain activity patterns in young and eldersCompensatory reorganization versus dedifferentiationNeural inefficiency versus capacity limitationAge group comparisons via SPMDiscussionAge effects on brain activation associated with performance of a DIR taskCapacity limitationNeural inefficiencyCompensatory reorganization and dedifferentiationConsideration of population under studyRelationship to previous findingsAlternative explanations of current findingsConclusionsAcknowledgementsReferencesNeurobiology of Aging xxx (2006) xxx–xxxAge-related changes in brain activation duringa delayed item recognition taskEric Zarahn∗, Brian Rakitin, Diane Abela, Joseph Flynn, Yaakov SternCognitive Neuroscience Division, Taub Institute, P and S Box 16, 630 West 168th Street, Columbia University, NY 10032, USAReceived 5 August 2005; received in revised form 9 February 2006; accepted 3 March 2006AbstractTo test competing models of age-related changes in brain functioning (capacity limitation, neural efficiency, compensatory reorganization,and dedifferentiation), young (n = 40; mean age = 25.1 years) and elderly (n = 18; mean age = 74.4 years) subjects performed a delayed itemrecognition task for visually presented letters with three set sizes (1, 3, or 6 letters) while being scanned with BOLD fMRI. Spatial patterns ofbrain activity corresponding to either the slope or y-intercept of fMRI signal with respect to set size during memory set encoding, retentiondelay, or probe stimulus presentation trial phases were compared between elder and young populations. Age effects on fMRI slope duringencoding and on fMRI y-intercept during retention delay were consistent with neural inefficiency; age effects on fMRI slope during retentiondelay were consistent with dedifferentiation. None of the other fMRI signal components showed any detectable age effects. These resultssuggest that, even within the same task, the nature of brain activation changes with aging can vary based on cognitive process engaged.© 2006 Elsevier Inc. All rights reserved.Keywords: Aging; Parietal cortex; Prefrontal cortex; Premotor cortex; Verbal working memory; Working memory; Articulatory loop; Memory load; Compen-satory reorganization; Neural efficiency; Capacity limitation; Dedifferentiation; Canonical variates analysis1. IntroductionFour extant hypotheses concerning changes in brainfunction with aging are compensatory reorganization,dedifferentiation, computational capacity limitation, andneural inefficiency. The purpose of the current paper is totest the ability of these hypotheses to predict age-relatedchanges in brain function associated with various aspectsof cognitive processing, including verbal working memory(WM) maintenance, engaged during performance of adelayed item recognition (DIR) task for letters.1.1. Brain areas implicated in working memorymaintenance in the youngWM is a psychological construct used to describe themaintenance and manipulation of information on a time scale∗Corresponding author. Tel.: +1 212 305 7855; fax: +1 212 342 1838.E-mail address: [email protected] (E. Zarahn).of seconds [7]. WM seems to be divided into verbal, spatial,and object sub-systems [8,37,82,94]. Verbal WM is thoughtto be critical for language comprehension and reasoning [5].Based on neuropsychological dissociations [95,98] and wordlength, phonemic similarity, irrelevant speech, and articu-latory suppression effects [6,11,22,51], the maintenance ofinformation in verbal WM has been modeled as an articu-latory loop in which sub-vocal rehearsal refreshes a phono-logical store. Experimental variation of the amount of infor-mation to be stored in verbal WM (WM load) has yieldedfindings of increases in fMRI signal in premotor, parietal,inferior frontal, and middle frontal areas [55,72,73,76,96].At least some aspects of articulatory loop neural processingvary in intensity with WM load [45,96,106].1.2. Age-related changes in the brain mechanisms ofverbal WMEven in the absence of Alzheimer’s disease (AD) andother recognized brain diseases, aging is associated with0197-4580/$ – see front matter © 2006 Elsevier Inc. All rights reserved.doi:10.1016/j.neurobiolaging.2006.03.002NBA-6507; No. of Pages 152 E. Zarahn et al. / Neurobiology of Aging xxx (2006) xxx–xxximpairment in several different memory variables [78],including WM [9,17,23,49]. In particular, load-dependentdeficits in WM processing have been observed with nor-mal aging [2,23,26,62,64]. Age-related deficits in cognitionare assumed to stem from age-related brain pathology [88].Normal aging is associated with a decrease in neuropil andneuronal number in cortex [12,21,25] and in the subiculumregion of the hippocampus [84,99], an increase in the num-ber of infarcts in cortex, basal ganglia, and white matter [65],an increase in MRI white matter lesions [80], an increase indensity of neurofibrillary tangles in the CA1 region of the hip-pocampus [81], and a global decrease in gray matter volume[31].There is the broad question of whether the functional neu-ral circuitry of the brain remains static in the face of thisneuropathology. Though not exhaustive, four extant hypothe-ses concerning changes in brain function with normal agingare compensatory reorganization, dedifferentiation, compu-tational capacity limitation, and neural inefficiency. The pur-pose of the current study is to test the ability of these hypothe-ses to predict age-related changes in brain function associatedwith load-dependent and load-independent aspects of encod-ing, storage/rehearsal, and recognition/response componentsof a DIR task for letters [90], which is thought to tap verbalWM maintenance. These four hypotheses will now be brieflydescribed, in turn.1.3. Models which predict changes in patterns of brainactivation with agingSome have put forward a hypothesis that the brain is con-structed such that it can


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