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Journal of NeuroEngineering and Rehabilitation
Published in: Journal of NeuroEngineering and Rehabilitation 1/2021

01-12-2021 | Mild Cognitive Impairment | Research

Dynamic changes of region-specific cortical features and scalp-to-cortex distance: implications for transcranial current stimulation modeling

Authors: Hanna Lu, Jing Li, Li Zhang, Sandra Sau Man Chan, Linda Chiu Wa Lam, for the Open Access Series of Imaging Studies

Published in: Journal of NeuroEngineering and Rehabilitation | Issue 1/2021

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Abstract

Background

Transcranial current stimulation in rehabilitation is a fast-growing field featured with computational and biophysical modeling. Cortical features and scalp-to-cortex distance (SCD) are key variables for determining the strength and distribution of the electric field, yet longitudinal studies able to capture these dynamic changes are missing. We sought to investigate and quantify the ageing effect on the morphometry and SCD of left primary motor cortex (M1) and dorsolateral prefrontal cortex (DLPFC) in normal ageing adults and mild cognitive impairment (MCI) converters.

Methods

Baseline, 1-year and 3-year follow-up structural magnetic resonance imaging scans from normal ageing adults (n = 32), and MCI converters (n = 22) were drawn from the Open Access Series of Imaging Studies. We quantified the changes of the cortical features and SCDs of left M1 and DLPFC, including grey matter volume, white matter volume, cortical thickness, and folding. Head model was developed to simulate the impact of SCD on the electric field induced by transcranial current stimulation.

Results

Pronounced ageing effect was found on the SCD of left DLPFC in MCI converters. The SCD change of left DLPFC from baseline to 3-year follow-up demonstrated better performance to discriminate MCI converters from normal ageing adults than the other morphometric measures. The strength of electric field was consequently decreased with SCD in MCI converters.

Conclusion

Ageing has a prominent, but differential effect on the region-specific SCD and cortical features in older adults with cognitive impairments. Our findings suggest that SCD, cortical thickness, and folding of the targeted regions could be used as valuable imaging markers when conducting transcranial brain stimulation in individuals with brain atrophy.
Literature
1.
Cole JH, Franke K. Predicting age using neuroimaging: innovative brain ageing biomarkers. Trends Neurosci. 2017;40:681–90.PubMedCrossRef
2.
Chandra A, Dervenoulas G, Politis M, Alzheimer’s Disease Neuroimaging Initiative, Magnetic resonance imaging in Alzheimer’s disease and mild cognitive impairment. J Neurol. 2019;266:1293–302.PubMedCrossRef
3.
Fjell AM, Westlye LT, Grydeland H, Amlien I, Espeseth T, Reinvang I, Initiative ADN. Accelerating cortical thinning: unique to dementia or universal in aging? Cereb Cortex. 2014;24:919–34.PubMedCrossRef
4.
Madan CR, Kensinger EA. Cortical complexity as a measure of age-related brain atrophy. NeuroImage. 2016;134:617–29.PubMedCrossRef
5.
Fjell AM, Walhovd KB, Fennema-Notestine C, McEvoy LK, Hagler DJ, Holland D, Dale AM. One-year brain atrophy evident in healthy aging. J Neurol. 2009;29:15223–31.
6.
Hogstrom LJ, Westlye LT, Walhovd KB, Fjell AM. The structure of the cerebral cortex across adult life: age-related patterns of surface area, thickness, and gyrification. Cereb Cortex. 2013;23:2521–30.PubMedCrossRef
7.
Salat DH, Kaye JA, Janowsky JS. Prefrontal gray and white matter volumes in healthy aging and Alzheimer disease. Arch Neurol. 1999;56:338–44.PubMedCrossRef
8.
Thompson PM, Hayashi KM, De Zubicaray G, Janke AL, Rose SE, Semple J, Toga AW. Dynamics of gray matter loss in Alzheimer's disease. J Neurol. 2003;23:994–1005.
9.
Dickstein DL, Kabaso D, Rocher AB, Luebke JI, Wearne SL, Hof PR. Changes in the structural complexity of the aged brain. Aging Cell. 2007;6:275–84.PubMedCrossRef
10.
Ruiz de Miras J, Costumero V, Belloch V, Escudero J, Ávila C, Sepulcre J. Complexity analysis of cortical surface detects changes in future Alzheimer's disease converters. Hum Brain Mapp. 2017;38:5905–18.PubMedPubMedCentralCrossRef
11.
Cox SR, Bastin ME, Ritchie SJ, Dickie DA, Liewald DC, Maniega SM, Corley J. Brain cortical characteristics of lifetime cognitive ageing. Brain Struct Funct. 2018;223:509–18.PubMedCrossRef
12.
Douaud G, Groves AR, Tamnes CK, Westlye LT, Duff EP, Engvig A, Matthews PM. A common brain network links development, aging, and vulnerability to disease. Proc Natl Acad Sci U S A. 2014;111:17648–53.PubMedPubMedCentralCrossRef
13.
Wong HL, Chan WC, Wong YL, Wong SN, Yung HY, Wong SMC, Cheng PWC. High-definition transcranial direct current stimulation-An open-label pilot intervention in alleviating depressive symptoms and cognitive deficits in late-life depression. CNS Neurosci Ther. 2019;25:1244–53.PubMedPubMedCentralCrossRef
14.
Lu H, Chan SSM, Chan WC, Lin C, Cheng CPW, Lam LCW. Randomized controlled trial of TDCS on cognition in 201 seniors with mild neurocognitive disorder. Ann Clin Transl Neurol. 2019;6:1938–48.PubMedPubMedCentralCrossRef
15.
Coppens MJ, Staring WH, Nonnekes J, Geurts AC, Weerdesteyn V. Offline effects of transcranial direct current stimulation on reaction times of lower extremity movements in people after stroke: a pilot cross-over study. J Neuroeng Rehabil. 2019;16:1–10.CrossRef
16.
Fox MD, Buckner RL, White MP, Greicius MD, Pascual-Leone A. Efficacy of transcranial magnetic stimulation targets for depression is related to intrinsic functional connectivity with the subgenual cingulate. Biol Psychiatry. 2012;72:595–603.PubMedPubMedCentralCrossRef
17.
McConnell KA, Nahas Z, Shastri A, Lorberbaum JP, Kozel FA, Bohning DE, George MS. The transcranial magnetic stimulation motor threshold depends on the distance from coil to underlying cortex: a replication in healthy adults comparing two methods of assessing the distance to cortex. Biol Psychiatry. 2001;49:454–9.PubMedCrossRef
18.
Lee EG, Duffy W, Hadimani RL, Waris M, Siddiqui W, Islam F, Jiles DC. Investigational effect of brain-scalp distance on the efficacy of transcranial magnetic stimulation treatment in depression. IEEE Trans Magn. 2016;52:1–4.
19.
Huang Y, Liu AA, Lafon B, Friedman D, Dayan M, Wang X, Parra LC. Measurements and models of electric fields in the in vivo human brain during transcranial electric stimulation. Elife. 2017;6:e18834.PubMedPubMedCentralCrossRef
20.
Lu H, Chan SS, Lam LC. Localized analysis of normalized distance from scalp to cortex and personalized evaluation (LANDSCAPE): focusing on age-and dementia-specific changes. J Alzheimers Dis. 2019;67:1331–41.PubMedCrossRef
21.
Lu H, Lam LC, Ning Y. Scalp-to-cortex distance of left primary motor cortex and its computational head model: implications for personalized neuromodulation. CNS Neurosci Ther. 2019;25:1270–6.PubMedPubMedCentralCrossRef
22.
Herbsman T, Forster L, Molnar C, Dougherty R, Christie D, Koola J, Nahas Z. Motor threshold in transcranial magnetic stimulation: the impact of white matter fiber orientation and skull-to-cortex distance. Hum Brain Mapp. 2009;30:2044–55.PubMedCrossRef
23.
Stokes MG, Chambers CD, Gould IC, Henderson TR, Janko NE, Allen NB, Mattingley JB. Simple metric for scaling motor threshold based on scalp-cortex distance: application to studies using transcranial magnetic stimulation. J Neurophysiol. 2005;94:4520–7.PubMedCrossRef
24.
Hanlon CA, Dowdle LT, Moss H, Canterberry M, George MS. Mobilization of medial and lateral frontal-striatal circuits in cocaine users and controls: an interleaved TMS/BOLD functional connectivity study. Neuropsychopharmacology. 2016;41:3032–41.PubMedPubMedCentralCrossRef
25.
Aisen PS, Cummings J, Jack CR, Morris JC, Sperling R, Frölich L, Scheltens P. On the path to 2025: understanding the Alzheimer’s disease continuum. Alzheimers Res Ther. 2017;9:60.PubMedPubMedCentralCrossRef
26.
Marcus DS, Wang TH, Parker J, Csernansky JG, Morris JC, Buckner RL. Open Access Series of Imaging Studies (OASIS): cross-sectional MRI data in young, middle aged, nondemented, and demented older adults. J Cogn Neurosci. 2007;19:1498–507.PubMedCrossRef
27.
Shattuck DW, Mirza M, Adisetiyo V, Hojatkashani C, Salamon G, Narr KL, Toga AW. Construction of a 3D probabilistic atlas of human cortical structures. Neuroimage. 2008;39:1064–80.PubMedCrossRef
28.
Apostolova LG, Thompson PM, Rogers SA, Dinov ID, Zoumalan C, Steiner CA, Cummings JL. Surface feature-guided mapping of cerebral metabolic changes in cognitively normal and mildly impaired elderly. Mol Imaging Biol. 2010;12:218–24.PubMedCrossRef
29.
Lu H, Ma SL, Chan SSM, Lam LCW. The effects of apolipoprotein ε 4 on aging brain in cognitively normal Chinese elderly: a surface-based morphometry study. Int Psychogeriatr. 2016;28:1503–11.PubMedCrossRef
30.
Cendes F, Andermann F, Gloor P, Evans A, Jones-Gotman M, Watson C, Leroux G. MRI volumetric measurement of amygdala and hippocampus in temporal lobe epilepsy. Neurology. 1993;43:719–25.PubMedCrossRef
31.
Cao B, Mwangi B, Passos IC, Wu MJ, Keser Z, Zunta-Soares GB, Soares JC. Lifespan gyrification trajectories of human brain in healthy individuals and patients with major psychiatric disorders. Sci Rep. 2017;7:1–8.CrossRef
32.
Mylius V, Ayache SS, Ahdab R, Farhat WH, Zouari HG, Belke M, Schmidt S. Definition of DLPFC and M1 according to anatomical landmarks for navigated brain stimulation: inter-rater reliability, accuracy, and influence of gender and age. Neuroimage. 2013;78:224–32.PubMedCrossRef
33.
Randazzo MJ, Kondylis ED, Alhourani A, Wozny TA, Lipski WJ, Crammond DJ, Richardson RM. Three-dimensional localization of cortical electrodes in deep brain stimulation surgery from intraoperative fluoroscopy. Neuroimage. 2016;125:515–21.PubMedCrossRef
34.
Huang Y, Datta A, Bikson M, Parra LC. Realistic volumetric-approach to simulate transcranial electric stimulation—ROAST—a fully automated open-source pipeline. J Neural Eng. 2019;16:056006.PubMedPubMedCentralCrossRef
35.
Truong DQ, Hüber M, Xie X, Datta A, Rahman A, Parra LC, Bikson M. Clinician accessible tools for GUI computational models of transcranial electrical stimulation: BONSAI and SPHERES. Brain Stimul. 2014;7:521–4.PubMedPubMedCentralCrossRef
36.
Allen B, Stacey BC, Bar-Yam Y. Multiscale information theory and the marginal utility of information. Entropy. 2017;19:273.CrossRef
37.
Meunier D, Stamatakis EA, Tyler LK. Age-related functional reorganization, structural changes, and preserved cognition. Neurobiol Aging. 2014;35:42–544.PubMedCrossRef
38.
Fjell AM, Westlye LT, Amlien I, Espeseth T, Reinvang I, Raz N, Dale AM. High consistency of regional cortical thinning in aging across multiple samples. Cereb Cortex. 2009;19:2001–122.PubMedPubMedCentralCrossRef
39.
Giorgio A, Santelli L, Tomassini V, Bosnell R, Smith S, De Stefano N, Johansen-Berg H. Age-related changes in grey and white matter structure throughout adulthood. Neuroimage. 2010;51:943–51.PubMedCrossRef
40.
Dotson VM, Szymkowicz SM, Sozda CN, Kirton JW, Green ML, O’Shea A, Woods AJ. Age differences in prefrontal surface area and thickness in middle aged to older adults. Front Aging Neurosci. 2016;7:250.PubMedPubMedCentralCrossRef
41.
Shaw ME, Sachdev PS, Anstey KJ, Cherbuin N. Age-related cortical thinning in cognitively healthy individuals in their 60s: the PATH Through Life study. Neurobiol Aging. 2016;39:202–9.PubMedCrossRef
42.
Yang Z, Wen W, Jiang J, Crawford JD, Reppermund S, Levitan C, Trollor JN. Age-associated differences on structural brain MRI in nondemented individuals from 71 to 103 years. Neurobiol Aging. 2016;40:86–97.PubMedCrossRef
43.
Thambisetty M, Wan J, Carass A, An Y, Prince JL, Resnick SM. Longitudinal changes in cortical thickness associated with normal aging. Neuroimage. 2010;52:1215–23.PubMedCrossRef
44.
Driscoll I, Davatzikos C, An Y, Wu X, Shen D, Kraut M, Resnick S. Longitudinal pattern of regional brain volume change differentiates normal aging from MCI. Neurology. 2009;72:1906–13.PubMedPubMedCentralCrossRef
45.
Terribilli D, Schaufelberger MS, Duran FL, Zanetti MV, Curiati PK, Menezes PR, Busatto GF. Age-related gray matter volume changes in the brain during non-elderly adulthood. Neurobiol Aging. 2011;32:354–68.PubMedPubMedCentralCrossRef
46.
Raz N, Gunning FM, Head D, Dupuis JH, McQuain J, Briggs SD, Acker JD. Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter. Cereb Cortex. 1997;7:268–82.PubMedCrossRef
47.
Van Essen DC. A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature. 1997;385:313–8.PubMedCrossRef
48.
Lu H. Quantifying age-associated cortical complexity of left dorsolateral prefrontal cortex with multiscale measurements. J Alzheimers Dis. 2020;76:505–12.PubMedCrossRef
49.
50.
Bertoux M, Lagarde J, Corlier F, Hamelin L, Mangin JF, Colliot O, Sarazin M. Sulcal morphology in Alzheimer's disease: an effective marker of diagnosis and cognition. Neurobiol Aging. 2019;84:41–9.PubMedCrossRef
Metadata
Title
Dynamic changes of region-specific cortical features and scalp-to-cortex distance: implications for transcranial current stimulation modeling
Authors
Hanna Lu
Jing Li
Li Zhang
Sandra Sau Man Chan
Linda Chiu Wa Lam
for the Open Access Series of Imaging Studies
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Journal of NeuroEngineering and Rehabilitation / Issue 1/2021
Electronic ISSN: 1743-0003
DOI
https://doi.org/10.1186/s12984-020-00764-5

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