Processing Speed and the Relationship Between Trail Making Test-B Performance, Cortical Thinning and White Matter Microstructure in Older Adults
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Edinburgh Research Explorer Processing speed and the relationship between Trail Making Test-B performance, cortical thinning and white matter microstructure in older adults Citation for published version: MacPherson, SE, Cox, SR, Dickie, DA, Karama, S, Starr, JM, Evans, AC, Bastin, ME, Wardlaw, JM & Deary, IJ 2017, 'Processing speed and the relationship between Trail Making Test-B performance, cortical thinning and white matter microstructure in older adults', Cortex, vol. 95, pp. 92-103. https://doi.org/10.1016/j.cortex.2017.07.021 Digital Object Identifier (DOI): 10.1016/j.cortex.2017.07.021 Link: Link to publication record in Edinburgh Research Explorer Document Version: Publisher's PDF, also known as Version of record Published In: Cortex General rights Copyright for the publications made accessible via the Edinburgh Research Explorer is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The University of Edinburgh has made every reasonable effort to ensure that Edinburgh Research Explorer content complies with UK legislation. If you believe that the public display of this file breaches copyright please contact [email protected] providing details, and we will remove access to the work immediately and investigate your claim. Download date: 05. Oct. 2021 cortex 95 (2017) 92e103 Available online at www.sciencedirect.com ScienceDirect Journal homepage: www.elsevier.com/locate/cortex Research report Processing speed and the relationship between Trail Making Test-B performance, cortical thinning and white matter microstructure in older adults * Sarah E. MacPherson a,b, , Simon R. Cox a,b,c, David A. Dickie c,d, Sherif Karama e,f, John M. Starr a,g, Alan C. Evans e, Mark E. Bastin a,c,d, Joanna M. Wardlaw a,c,d and Ian J. Deary a,b a Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, UK b Department of Psychology, University of Edinburgh, UK c Scottish Imaging Network, a Platform for Scientific Excellence (SINAPSE) Collaboration, Edinburgh, UK d Department of Neuroimaging Sciences, Centre for Clinical Brain Sciences, University of Edinburgh, UK e Department of Neurology and Neurosurgery, McConnell Brain Imaging Center, Montreal Neurological Institute, McGill University, Montreal, QC, Canada f Department of Psychiatry, Douglas Mental Health University Institute, McGill University, Verdun, QC, Canada g Alzheimer Scotland Dementia Research Centre, The University of Edinburgh, Edinburgh, UK article info abstract Article history: Part B of the Trail Making Test (TMT-B) is widely used as a quick and easy to administer Received 8 July 2016 measure of executive dysfunction. The current study investigated the relationships be- Reviewed 5 September 2016 tween TMT-B performance, brain volumes, cortical thickness and white matter water Revised 14 January 2017 diffusion characteristics in a large sample of older participants, before and after controlling Accepted 1 August 2017 for processing speed. Four hundred and eleven healthy, community-dwelling older adults Action editor Stefan Schweinberger who were all born in 1936 were assessed on TMT-B, 5 tests of processing speed, and pro- Published online 9 August 2017 vided contemporaneous structural and diffusion MRI data. Significant relationships were found between slower TMT-B completion times and thinner cortex in the frontal, temporal Keywords: and inferior parietal regions as well as the Sylvian fissure/insula. Slower TMT-B completion Aging time was also significantly associated with poorer white matter microstructure of the left Executive function anterior thalamic radiation, and the right uncinate fasciculus. The majority of these as- Neuroimaging sociations were markedly attenuated when additionally controlling for processing speed. Processing speed These data suggest that individual differences in processing speed contribute to the as- Trail Making Test sociations between TMT-B completion time and the grey and white matter structure of older adults. © 2017 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). * Corresponding author. Department of Psychology, PPLS, University of Edinburgh, 7 George Square, Edinburgh EH8 9JZ, UK. E-mail address: [email protected] (S.E. MacPherson). http://dx.doi.org/10.1016/j.cortex.2017.07.021 0010-9452/© 2017 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons. org/licenses/by/4.0/). cortex 95 (2017) 92e103 93 behavioural, cognitive experimental and psychophysical 1. Introduction measures (Deary et al., 2007). In addition, given that some of these processing speed measures might arguably involve The Trail Making Test (TMT) is one of the most commonly more complex decision-making, more akin to executive abil- used tests of executive function in clinical neuropsychological ities, we also derived a simple processing speed factor. We assessment (Delis, Kaplan, & Kramer, 2001; Lezak, 1995; Reitan examine the extent to which these two simple and complex & Wolfson, 1993). Part A is administered as a baseline measure processing speed measures influence the relationship of TMT- of motor and visual search speed, whereas Part B is adminis- B completion time with cortical thickness and white matter tered as a measure of set-shifting and inhibition (Arbuthnott microstructure. & Frank, 2000; Glascher€ et al., 2012; Kortte, Horner, & Windham, 2002; Strauss, Sherman, & Spreen, 2006). Poor performance on TMT-B is often associated with lesions in the 2. Methods dorsolateral prefrontal cortex (Davidson, Gao, Mason, & Winocur, Anderson, 2008; Moll, de Oliveira-Souza, Moll, 2.1. Participants Bramati, & Andreiuolo, 2002; Stuss et al., 2001; Yochim, Baldo, & & Nelson, Delis, 2007; Zakzanis, Mraz, Graham, 2005) and Participants were from the Lothian Birth Cohort 1936 € the anterior cingulate (Glascher et al., 2012), although signifi- (LBC1936), a longitudinal study of aging of individuals all born ' cant differences between frontal and non-frontal patients in 1936 and living mainly in the Edinburgh and Lothians region & TMT-B performance are not always found (Reitan Wolfson, of Scotland, UK (Deary, Gow, Pattie, & Starr, 2012; Deary et al., 1995; Tamez et al., 2011; Chan et al., 2015; see Demakis, 2004, 2007). Participants first had cognitive and other data measured for a meta-analysis). at Wave 1 at age ~70 years between 2004 and 2007. No partic- TMT performance is found to decline, on average, in ipant had a diagnosis of dementia at entry. Wave 2 testing was & healthy aging (Giovagnoli et al., 1996; Hamdan Hamdan, carried out 3 years later. Wave 1 data are not reported as there & 2009; Hashimoto et al., 2006; Hester, Kinsella, Ong, was no neuroimaging at Wave 1, and TMT was not adminis- ~ McGregor, 2005; Perianez et al., 2007; Seo et al., 2006) with tered during Waves 1 or 2. At Wave 3, participants attended performance on TMT-B declining significantly more than cognitive testing and underwent brain MRI at ~76 years. For & TMT-A in older adults (Drane, Yuspeh, Huthwaite, Klingler, the present study, 411 participants (219 males, 192 females) & 2002; Rasmusson, Zonderman, Kawas, Resnick, 1998). Age- were included who had performed the TMT-B, had brain MRI related decline in TMT performance has been associated data, achieved a score of 24 or greater on the Mini-Mental State with poorer grey matter volume in the dorsolateral and Examination (MMSE; Folstein, Folstein, & McHugh, 1975), and ventrolateral prefrontal cortex, medial prefrontal cortex, had a score of less than 11 on the depression subscale of the frontal pole, right inferior frontal gyrus, temporal lobe, insular Hospital Anxiety and Depression Scale (Snaith, 2003)atWave cortex, caudate, globus pallidus, posterior parietal lobe, oc- 3. Cognitive testing and MRI scanning were undertaken on cipital cortex and the cerebellum (Newman, Trivedi, Bendlin, separate occasions with four participants attending their brain & Ries, Johnson, 2007; Pa et al., 2010; Ruscheweyh et al., MRI scan first (lag ¼ 39.40 days, SD ¼ 30.74, range ¼36 to 320). 2013). In terms of white matter microstructural integrity and No participant self-reported a diagnosis of dementia either at TMT performance, while Perry et al. (2009) reported a signifi- entry to LBC1936 or Wave 3 (i.e., their current assessment). No cant association between age and TMT-B performance one had a history of traumatic brain injury, stroke, brain strongly mediated by the effect of age on white matter tumour or other neurological conditions. All participants were microstructure, Koch et al. (2013) found better white matter healthy older adults who were considered able to live inde- microstructure of the body of the corpus callosum was asso- pendently. Study approval was granted by the Lothian ciated with less time needed to complete TMT-A but not Research Ethics Committee (LREC/2003/2/39) and the Multi- TMT-B. Centre Research Ethics Committee for Scotland (MREC/01/0/ Research has shown that processing speed is significantly 56). Written informed consent was obtained from all partici- associated with performance on the TMT-B in older adults pants, and has been kept on file. (Oosterman et al., 2010; Salthouse, 2011a). However, process- ing speed can be assessed in at least three different ways (see 2.2. Cognitive testing Deary, 2000).