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Current Alzheimer Research

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ISSN (Print): 1567-2050
ISSN (Online): 1875-5828

Research Article

Functional Connectivity, Physical Activity, and Neurocognitive Performances in Patients with Vascular Cognitive Impairment, No Dementia

Author(s): Ya-Ting Chang*, Chun-Ting Liu, Shih-Wei Hsu, Chen-Chang Lee and Pei-Ching Huang

Volume 19, Issue 1, 2022

Published on: 27 January, 2022

Page: [56 - 67] Pages: 12

DOI: 10.2174/1567205019666220127103852

Price: $65

Abstract

Background: Vascular Cognitive Impairment, No Dementia (VCIND) is a key stage at which early intervention will delay or prevent dementia. The pathophysiology of VCIND posits that a lesion in a single location in the brain has the ability to disrupt brain networks, and the subsequent abnormal Functional Connectivity (FC) of brain networks leads to deficits in corresponding neurobehavioral domains. In this study, we tested the hypothesis that disrupted anterior cingulate cortex and striatal networks mediated the effects of Physical Activity (PA) on neurobehavioral function.

Methods: In 27 patients with VCIND, FC within the brain networks and neurobehavioral dysfunction were assessed. The relationship between the cognitive scores, FC, and PA was studied. The Fitbit Charge 2 was used to measure step counts, distance, and calories burned. In patients with VCIND, a cross-sectional Spearman’s correlation to analyze the relationship among patient-level measures of PA, cognitive function scores, and FC strength within the brain networks.

Results: Average step counts and average distance were associated with Trail Making Test B (TMB) time to completion (seconds) and Instrumental Activities of Daily Living (IADL) score (P < 0.05). The average calories burned were associated with IADL score (P = 0.009). The FC within the brain networks anchored by left caudal Anterior Cingulate Cortex (ACC) seeds (x= -5, y= 0, z= 36) and (x= -5, y= -10, z= 47) were positively correlated with average step counts and average distance, were negatively correlated with TMB time to completion (seconds), and were positively correlated with IADL score (P < 0.05). The FC within the brain networks anchored by left subgenual ACC seed (x= -5, y= 25, z= -10) were negatively correlated with average step counts and average distance were positively correlated with TMB time to completion (seconds), and were negatively correlated with IADL score (P < 0.05). The FC within the striatal networks was positively correlated with average calories burned and IADL score (P < 0.05).

Conclusion: FC within the brain networks anchored by caudal ACC seeds was positively correlated with more average step counts/average distance and better IADL score; negatively correlated with longer TMB time to completion (seconds), whereas FC of subgenual ACC seed was negatively correlated with the same parameters. FC within the brain networks anchored by putamen rather than caudate or pallidum was positively correlated with average calories burned and IADL score.

Keywords: Actigraphy, brain network, cognition, executive function, functional connectivity, physical activity.

[1]
Dichgans M, Leys D. Vascular cognitive impairment. Circ Res 2017; 120(3): 573-91.
[http://dx.doi.org/10.1161/CIRCRESAHA.116.308426] [PMID: 28154105]
[2]
van der Flier WM, Skoog I, Schneider JA, et al. Vascular cognitive impairment. Nat Rev Dis Primers 2018; 4: 18003.
[http://dx.doi.org/10.1038/nrdp.2018.3] [PMID: 29446769]
[3]
Snyder HM, Corriveau RA, Craft S, et al. Vascular contributions to cognitive impairment and dementia including Alzheimer’s disease. Alzheimers Dement 2015; 11(6): 710-7.
[http://dx.doi.org/10.1016/j.jalz.2014.10.008] [PMID: 25510382]
[4]
Wu YT, Fratiglioni L, Matthews FE, et al. Dementia in western Europe: epidemiological evidence and implications for policy making. Lancet Neurol 2016; 15(1): 116-24.
[http://dx.doi.org/10.1016/S1474-4422(15)00092-7] [PMID: 26300044]
[5]
Rockwood K, Wentzel C, Hachinski V, Hogan DB, MacKnight C, McDowell I. Prevalence and outcomes of vascular cognitive impairment. Neurology 2000; 54(2): 447-51.
[http://dx.doi.org/10.1212/WNL.54.2.447] [PMID: 10668712]
[6]
Jia J, Zhou A, Wei C, et al. The prevalence of mild cognitive impairment and its etiological subtypes in elderly Chinese. Alzheimers Dement 2014; 10(4): 439-47.
[http://dx.doi.org/10.1016/j.jalz.2013.09.008] [PMID: 24418053]
[7]
Tang Y, Xing Y, Zhu Z, et al. The effects of 7-week cognitive training in patients with vascular cognitive impairment, no dementia (the Cog-VACCINE study): A randomized controlled trial. Alzheimers Dement 2019; 15(5): 605-14.
[http://dx.doi.org/10.1016/j.jalz.2019.01.009] [PMID: 30894299]
[8]
Corbetta M, Ramsey L, Callejas A, et al. Common behavioral clusters and subcortical anatomy in stroke. Neuron 2015; 85(5): 927-41.
[http://dx.doi.org/10.1016/j.neuron.2015.02.027] [PMID: 25741721]
[9]
Alstott J, Breakspear M, Hagmann P, Cammoun L, Sporns O. Modeling the impact of lesions in the human brain. PLOS Comput Biol 2009; 5(6): e1000408.
[http://dx.doi.org/10.1371/journal.pcbi.1000408] [PMID: 19521503]
[10]
Siegel JS, Ramsey LE, Snyder AZ, et al. Disruptions of network connectivity predict impairment in multiple behavioral domains after stroke. Proc Natl Acad Sci USA 2016; 113(30): E4367-76.
[http://dx.doi.org/10.1073/pnas.1521083113] [PMID: 27402738]
[11]
Ihara M, Okamoto Y, Hase Y, Takahashi R. Association of physical activity with the visuospatial/executive functions of the montreal cognitive assessment in patients with vascular cognitive impairment. J Stroke Cerebrovasc Dis 2013; 22(7): e146-51.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2012.10.007] [PMID: 23153550]
[12]
Boraxbekk CJ, Salami A, Wåhlin A, Nyberg L. Physical activity over a decade modifies age-related decline in perfusion, gray matter volume, and functional connectivity of the posterior default-mode network-A multimodal approach. Neuroimage 2016; 131: 133-41.
[http://dx.doi.org/10.1016/j.neuroimage.2015.12.010] [PMID: 26702778]
[13]
Bento-Torres J, Bento-Torres NVO, Stillman CM, et al. Associations between cardiorespiratory fitness, physical activity, intraindividual variability in behavior, and cingulate cortex in younger adults. J Sport Health Sci 2019; 8(4): 315-24.
[http://dx.doi.org/10.1016/j.jshs.2019.03.004] [PMID: 31333884]
[14]
Maddock RJ, Casazza GA, Fernandez DH, Maddock MI. Acute modulation of cortical glutamate and GABA content by physical activity. J Neurosci 2016; 36(8): 2449-57.
[http://dx.doi.org/10.1523/JNEUROSCI.3455-15.2016] [PMID: 26911692]
[15]
Marais L, Stein DJ, Daniels WM. Exercise increases BDNF levels in the striatum and decreases depressive-like behavior in chronically stressed rats. Metab Brain Dis 2009; 24(4): 587-97.
[http://dx.doi.org/10.1007/s11011-009-9157-2] [PMID: 19844781]
[16]
Verstynen TD, Lynch B, Miller DL, et al. Caudate nucleus volume mediates the link between cardiorespiratory fitness and cognitive flexibility in older adults. J Aging Res 2012; 2012: 939285.
[http://dx.doi.org/10.1155/2012/939285] [PMID: 22900181]
[17]
Najar J, Östling S, Gudmundsson P, et al. Cognitive and physical activity and dementia: A 44-year longitudinal population study of women. Neurology 2019; 92(12): e1322-30.
[http://dx.doi.org/10.1212/WNL.0000000000007021] [PMID: 30787164]
[18]
Case MA, Burwick HA, Volpp KG, Patel MS. Accuracy of smartphone applications and wearable devices for tracking physical activity data. JAMA 2015; 313(6): 625-6.
[http://dx.doi.org/10.1001/jama.2014.17841] [PMID: 25668268]
[19]
Straiton N, Alharbi M, Bauman A, et al. The validity and reliability of consumer-grade activity trackers in older, community-dwelling adults: A systematic review. Maturitas 2018; 112: 85-93.
[http://dx.doi.org/10.1016/j.maturitas.2018.03.016] [PMID: 29704922]
[20]
Takacs J, Pollock CL, Guenther JR, Bahar M, Napier C, Hunt MA. Validation of the Fitbit One activity monitor device during treadmill walking. J Sci Med Sport 2014; 17(5): 496-500.
[http://dx.doi.org/10.1016/j.jsams.2013.10.241] [PMID: 24268570]
[21]
Evenson KR, Goto MM, Furberg RD. Systematic review of the validity and reliability of consumer-wearable activity trackers. Int J Behav Nutr Phys Act 2015; 12: 159.
[http://dx.doi.org/10.1186/s12966-015-0314-1] [PMID: 26684758]
[22]
Stahl ST, Insana SP. Caloric expenditure assessment among older adults: criterion validity of a novel accelerometry device. J Health Psychol 2014; 19(11): 1382-7.
[http://dx.doi.org/10.1177/1359105313490771] [PMID: 23818504]
[23]
Skrobot OA, Attems J, Esiri M, et al. Vascular cognitive impairment neuropathology guidelines (VCING): the contribution of cerebrovascular pathology to cognitive impairment. Brain 2016; 139(11): 2957-69.
[http://dx.doi.org/10.1093/brain/aww214] [PMID: 27591113]
[24]
Hachinski V, Iadecola C, Petersen RC, et al. National institute of neurological disorders and stroke-canadian stroke network vascular cognitive impairment harmonization standards. Stroke 2006; 37(9): 2220-41.
[http://dx.doi.org/10.1161/01.STR.0000237236.88823.47] [PMID: 16917086]
[25]
Scheltens P, Leys D, Barkhof F, et al. Atrophy of medial temporal lobes on MRI in “probable” Alzheimer’s disease and normal ageing: diagnostic value and neuropsychological correlates. J Neurol Neurosurg Psychiatry 1992; 55(10): 967-72.
[http://dx.doi.org/10.1136/jnnp.55.10.967] [PMID: 1431963]
[26]
Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol 1987; 149(2): 351-6.
[http://dx.doi.org/10.2214/ajr.149.2.351] [PMID: 3496763]
[27]
Roalf DR, Moberg PJ, Xie SX, Wolk DA, Moelter ST, Arnold SE. Comparative accuracies of two common screening instruments for classification of Alzheimer’s disease, mild cognitive impairment, and healthy aging. Alzheimers Dement 2013; 9(5): 529-37.
[http://dx.doi.org/10.1016/j.jalz.2012.10.001] [PMID: 23260866]
[28]
Chang CC, Kramer JH, Lin KN, et al. Validating the Chinese version of the verbal learning test for screening Alzheimer’s disease. J Int Neuropsychol Soc 2010; 16(2): 244-51.
[http://dx.doi.org/10.1017/S1355617709991184] [PMID: 20003579]
[29]
Lezak MD. Neuropsychological assessment. 4th ed. New York: Oxford University Press 2004.
[30]
Rey A. L’examen psychologique dans les cas d’encéphalopathie traumatique. Arch Psychol 1941; 28: 286-340.
[31]
Warrington EK, James M. The visual object and space perception battery. Bury St Edmunds, England: Thames Valley Test Company 1991.
[32]
Weintraub S, Salmon D, Mercaldo N, et al. The Alzheimer’s Disease Centers’ Uniform Data Set (UDS): the neuropsychologic test battery. Alzheimer Dis Assoc Disord 2009; 23(2): 91-101.
[http://dx.doi.org/10.1097/WAD.0b013e318191c7dd] [PMID: 19474567]
[33]
Reitan RM. The relation of the trail making test to organic brain damage. J Consult Psychol 1955; 19(5): 393-4.
[http://dx.doi.org/10.1037/h0044509] [PMID: 13263471]
[34]
Lawton MP, Brody EM. Assessment of older people: self-maintaining and instrumental activities of daily living. Gerontologist 1969; 9(3): 179-86.
[http://dx.doi.org/10.1093/geront/9.3_Part_1.179] [PMID: 5349366]
[35]
Whitfield-Gabrieli S, Nieto-Castanon A. Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect 2012; 2(3): 125-41.
[http://dx.doi.org/10.1089/brain.2012.0073] [PMID: 22642651]
[36]
Chang YT, Mori E, Suzuki M, et al. APOE-MS4A genetic interactions are associated with executive dysfunction and network abnormality in clinically mild Alzheimer’s disease. Neuroimage Clin 2019; 21: 101621.
[http://dx.doi.org/10.1016/j.nicl.2018.101621] [PMID: 30528368]
[37]
Chang YT, Hsu SW, Huang SH, et al. ABCA7 polymorphisms correlate with memory impairment and default mode network in patients with APOEε4-associated Alzheimer’s disease. Alzheimers Res Ther 2019; 11(1): 103.
[http://dx.doi.org/10.1186/s13195-019-0563-3] [PMID: 31831047]
[38]
Margulies DS, Kelly AM, Uddin LQ, Biswal BB, Castellanos FX, Milham MP. Mapping the functional connectivity of anterior cingulate cortex. Neuroimage 2007; 37(2): 579-88.
[http://dx.doi.org/10.1016/j.neuroimage.2007.05.019] [PMID: 17604651]
[39]
Kelly AM, Di Martino A, Uddin LQ, et al. Development of anterior cingulate functional connectivity from late childhood to early adulthood. Cereb Cortex 2009; 19(3): 640-57.
[http://dx.doi.org/10.1093/cercor/bhn117] [PMID: 18653667]
[40]
Di Martino A, Scheres A, Margulies DS, et al. Functional connectivity of human striatum: a resting state FMRI study. Cereb Cortex 2008; 18(12): 2735-47.
[http://dx.doi.org/10.1093/cercor/bhn041] [PMID: 18400794]
[41]
Behzadi Y, Restom K, Liau J, Liu TT. A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 2007; 37(1): 90-101.
[http://dx.doi.org/10.1016/j.neuroimage.2007.04.042] [PMID: 17560126]
[42]
Ferguson T, Rowlands AV, Olds T, Maher C. The validity of consumer-level, activity monitors in healthy adults worn in free-living conditions: a cross-sectional study. Int J Behav Nutr Phys Act 2015; 12: 42.
[http://dx.doi.org/10.1186/s12966-015-0201-9] [PMID: 25890168]
[43]
Nachev P, Kennard C, Husain M. Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci 2008; 9(11): 856-69.
[http://dx.doi.org/10.1038/nrn2478] [PMID: 18843271]
[44]
Correia S, Ahern DC, Rabinowitz AR, et al. Lowering the floor on trail making test part B: Psychometric evidence for a new scoring metric. Arch Clin Neuropsychol 2015; 30(7): 643-56.
[http://dx.doi.org/10.1093/arclin/acv040] [PMID: 26164816]
[45]
Sánchez-Cubillo I, Periáñez JA, Adrover-Roig D, et al. Construct validity of the trail making test: role of task-switching, working memory, inhibition/interference control, and visuomotor abilities. J Int Neuropsychol Soc 2009; 15(3): 438-50.
[http://dx.doi.org/10.1017/S1355617709090626] [PMID: 19402930]
[46]
Amieva H, Lafont S, Rouch-Leroyer I, et al. Evidencing inhibitory deficits in Alzheimer’s disease through interference effects and shifting disabilities in the Stroop test. Arch Clin Neuropsychol 2004; 19(6): 791-803.
[http://dx.doi.org/10.1016/j.acn.2003.09.006] [PMID: 15288332]
[47]
Jefferson AL, Paul RH, Ozonoff A, Cohen RA. Evaluating elements of executive functioning as predictors of instrumental activities of daily living (IADLs). Arch Clin Neuropsychol 2006; 21(4): 311-20.
[http://dx.doi.org/10.1016/j.acn.2006.03.007] [PMID: 16814980]
[48]
van Veen V, Cohen JD, Botvinick MM, Stenger VA, Carter CS. Anterior cingulate cortex, conflict monitoring, and levels of processing. Neuroimage 2001; 14(6): 1302-8.
[http://dx.doi.org/10.1006/nimg.2001.0923] [PMID: 11707086]
[49]
Fan J, Hof PR, Guise KG, Fossella JA, Posner MI. The functional integration of the anterior cingulate cortex during conflict processing. Cereb Cortex 2008; 18(4): 796-805.
[http://dx.doi.org/10.1093/cercor/bhm125] [PMID: 17652463]
[50]
Petit L, Courtney SM, Ungerleider LG, Haxby JV. Sustained activity in the medial wall during working memory delays. J Neurosci 1998; 18(22): 9429-37.
[http://dx.doi.org/10.1523/JNEUROSCI.18-22-09429.1998] [PMID: 9801381]
[51]
Fan J, McCandliss BD, Fossella J, Flombaum JI, Posner MI. The activation of attentional networks. Neuroimage 2005; 26(2): 471-9.
[http://dx.doi.org/10.1016/j.neuroimage.2005.02.004] [PMID: 15907304]
[52]
Qin Q, Tang Y, Dou X, et al. Default mode network integrity changes contribute to cognitive deficits in subcortical vascular cognitive impairment, no dementia. Brain Imaging Behav 2021; 15(1): 255-65.
[http://dx.doi.org/10.1007/s11682-019-00252-y] [PMID: 32125614]
[53]
Salas-Gomez D, Fernandez-Gorgojo M, Pozueta A, et al. Physical activity is associated with better executive function in university students. Front Hum Neurosci 2020; 14: 11.
[http://dx.doi.org/10.3389/fnhum.2020.00011] [PMID: 32132908]
[54]
Prakash RS, Voss MW, Erickson KI, et al. Cardiorespiratory fitness and attentional control in the aging brain. Front Hum Neurosci 2011; 4: 229.
[http://dx.doi.org/10.3389/fnhum.2010.00229] [PMID: 21267428]
[55]
Chapman SB, Aslan S, Spence JS, et al. Shorter term aerobic exercise improves brain, cognition, and cardiovascular fitness in aging. Front Aging Neurosci 2013; 5: 75.
[http://dx.doi.org/10.3389/fnagi.2013.00075] [PMID: 24282403]
[56]
Colcombe SJ, Erickson KI, Scalf PE, et al. Aerobic exercise training increases brain volume in aging humans. J Gerontol A Biol Sci Med Sci 2006; 61(11): 1166-70.
[http://dx.doi.org/10.1093/gerona/61.11.1166] [PMID: 17167157]
[57]
Burdette JH, Laurienti PJ, Espeland MA, et al. Using network science to evaluate exercise-associated brain changes in older adults. Front Aging Neurosci 2010; 2: 23.
[http://dx.doi.org/10.3389/fnagi.2010.00023] [PMID: 20589103]
[58]
Farr OM, Mantzoros CS. Obese individuals with more components of the metabolic syndrome and/or prediabetes demonstrate decreased activation of reward-related brain centers in response to food cues in both the fed and fasting states: a preliminary fMRI study. Int J Obes 2017; 41(3): 471-4.
[http://dx.doi.org/10.1038/ijo.2016.231] [PMID: 28017966]
[59]
Trigiani LJ, Lacalle-Aurioles M, Bourourou M, et al. Benefits of physical exercise on cognition and glial white matter pathology in a mouse model of vascular cognitive impairment and dementia. Glia 2020; 68(9): 1925-40.
[http://dx.doi.org/10.1002/glia.23815] [PMID: 32154952]
[60]
Lyu F, Wu D, Wei C, Wu A. Vascular cognitive impairment and dementia in type 2 diabetes mellitus: An overview. Life Sci 2020; 254: 117771.
[http://dx.doi.org/10.1016/j.lfs.2020.117771] [PMID: 32437791]
[61]
Brunt A, Albines D, Hopkins-Rosseel D. The effectiveness of exercise on cognitive performance in individuals with known vascular disease: A systematic review. J Clin Med 2019; 8(3): 8.
[http://dx.doi.org/10.3390/jcm8030294] [PMID: 30832238]
[62]
Al Jerdi S, Aleyadeh R, Imam Y. Management of cognitive impairment after stroke. Curr Treatment Options Neurol 2020; 22: 7-DOI:10.1007/s11940-020-00627-3.

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