The effects of dual-task cognitive interference on gait and turning in Huntington’s disease
Autoři:
Nicollette L. Purcell aff001; Jennifer G. Goldman aff002; Bichun Ouyang aff004; Yuanqing Liu aff004; Bryan Bernard aff004; Joan A. O’Keefe aff001
Působiště autorů:
Department of Cell and Molecular Medicine, Rush University Medical Center, Chicago, IL, United States of America
aff001; Shirley Ryan Ability Lab, Chicago, IL, United States of America
aff002; Northwestern University-Feinberg School of Medicine, Chicago, IL, United States of America
aff003; Department of Neurological Sciences, Section of Parkinson Disease and Movement Disorders, Rush University Medical Center, Chicago, IL, United States of America
aff004
Vyšlo v časopise:
PLoS ONE 15(1)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0226827
Souhrn
Huntington’s disease (HD) is characterized by motor, cognitive, and psychiatric dysfunction. HD progression causes loss of automaticity, such that previously automatic tasks require greater attentional resources. Dual-task (DT) paradigms and fast-paced gait may stress the locomotor system, revealing deficits not seen under single-task (ST). However, the impact of gait “stress tests” on HD individuals needs further investigation. Therefore, the aims of this study were to investigate whether: 1) fast-paced and dual-task walking uncover deficits in gait and turning not seen under single-task, 2) cognitive and gait outcomes relate to fall incidence, and 3) gait deficits measured with wearable inertial sensors correlate with motor symptom severity in HD as measured by the Unified Huntington’s disease Rating Scale-total motor score (UHDRS-TMS). Seventeen HD (55 ± 9.7 years) and 17 age-matched controls (56.5 ± 9.3 years) underwent quantitative gait testing via a 25m, two-minute walk test with APDMTM inertial sensors. Gait was assessed under a 1) ST, self-selected pace, 2) fast-as-possible (FAP) pace, and 3) verbal fluency DT. The UHDRS-TMS and a cognitive test battery were administered, and a retrospective fall history was obtained. During ST, DT, and FAP conditions, HD participants demonstrated slower gait, shorter stride length, and greater lateral step and stride length variability compared to controls (p<0.00001 to 0.034). Significant dual-task costs (DTC) were observed for turns; HD participants took more time (p = 0.013) and steps (p = 0.028) to complete a turn under DT compared to controls. Higher UHDRS-TMS correlated with greater stride length variability, less double-support, and more swing-phase time under all conditions. Decreased processing speed was associated with increased gait variability under ST and FAP conditions. Unexpectedly, participant’s self-reported falls did not correlate with any gait or turn parameters. HD participants demonstrated significantly greater DTC for turning, which is less automatic than straight walking, requiring coordination of body segments, anticipatory control, and cortical regulation. Turn complexity likely makes it more susceptible to cognitive interference in HD.
Klíčová slova:
Animal cognition – Cognition – Cognitive impairment – Cognitive neurology – Cognitive psychology – Gait analysis – Huntington disease – Walking
Zdroje
1. Clabough EB. Huntington's disease: the past, present, and future search for disease modifiers. Yale J Biol Med. 2013;86: 217–233. 23766742
2. Canals JM, Pineda JR, Torres-Peraza JF, Bosch M, Martin-Ibanez R, Munoz MT, et al. Brain-derived neurotrophic factor regulates the onset and severity of motor dysfunction associated with enkephalinergic neuronal degeneration in Huntington's disease. J Neurosci. 2004;24: 7727–7739. doi: 10.1523/JNEUROSCI.1197-04.2004 15342740
3. Ross CA, Aylward EH, Wild EJ, Langbehn DR, Long JD, Warner JH, et al. Huntington disease: natural history, biomarkers and prospects for therapeutics. Nat Rev Neurol. 2014;10: 204–216. doi: 10.1038/nrneurol.2014.24 24614516
4. Rao AK, Muratori L, Louis ED, Moskowitz CB, Marder KS. Spectrum of gait impairments in presymptomatic and symptomatic Huntington's disease. Mov Disord. 2008;23: 1100–1107. doi: 10.1002/mds.21987 18412252
5. Aron AR, Watkins L, Sahakian BJ, Monsell S, Barker RA, Robbins TW. Task-set switching deficits in early-stage Huntington's disease: implications for basal ganglia function. J Cogn Neurosci. 2003;15: 629–642. doi: 10.1162/089892903322307357 12965037
6. Maurage P, Heeren A, Lahaye M, Jeanjean A, Guettat L, Verellen-Dumoulin C, et al. Attentional impairments in Huntington's disease: A specific deficit for the executive conflict. Neuropsychology. 2017;31: 424–436. doi: 10.1037/neu0000321 28240935
7. Thompson JC, Poliakoff E, Sollom AC, Howard E, Craufurd D, Snowden JS. Automaticity and attention in Huntington's disease: when two hands are not better than one. Neuropsychologia. 2010;48: 171–178. doi: 10.1016/j.neuropsychologia.2009.09.002 19747497
8. Delval A, Krystkowiak P, Delliaux M, Dujardin K, Blatt JL, Destee A, et al. Role of attentional resources on gait performance in Huntington's disease. Mov Disord. 2008;23: 684–689. doi: 10.1002/mds.21896 18175353
9. Kloos AD, Kegelmeyer DA, Fritz NE, Daley AM, Young GS, Kostyk SK. Cognitive Dysfunction Contributes to Mobility Impairments in Huntington's Disease. J Huntingtons Dis. 2017;6: 363–370. doi: 10.3233/JHD-170279 29254103
10. Paulsen JS. Cognitive impairment in Huntington disease: diagnosis and treatment. Curr Neurol Neurosci Rep. 2011;11: 474–483. doi: 10.1007/s11910-011-0215-x 21861097
11. Amboni M, Barone P, Iuppariello L, Lista I, Tranfaglia R, Fasano A, et al. Gait patterns in Parkinsonian patients with or without mild cognitive impairment. Mov Disord. 2012;27: 1536–1543. doi: 10.1002/mds.25165 23032876
12. Fritz NE, Hamana K, Kelson M, Rosser A, Busse M, Quinn L. Motor-cognitive dual-task deficits in individuals with early-mid stage Huntington disease. Gait Posture. 2016;49: 283–289. doi: 10.1016/j.gaitpost.2016.07.014 27474949
13. Hamilton F, Rochester L, Paul L, Rafferty D, O'Leary CP, Evans JJ. Walking and talking: an investigation of cognitive-motor dual tasking in multiple sclerosis. Mult Scler. 2009;15: 1215–1227. doi: 10.1177/1352458509106712 19667011
14. Purcell NL, Goldman JG, Ouyang B, Bernard B, O'Keefe JA. The Effects of Dual-Task Cognitive Interference and Environmental Challenges on Balance in Huntington's Disease. Mov Disord Clin Pract. 2019;6: 202–212. doi: 10.1002/mdc3.12720 30949551
15. Vaportzis E, Georgiou-Karistianis N, Churchyard A, Stout JC. Dual Task Performance May be a Better Measure of Cognitive Processing in Huntington's Disease than Traditional Attention Tests. J Huntingtons Dis. 2015;4: 119–130. doi: 10.3233/JHD-140131 26397893
16. Callisaya ML, Blizzard L, McGinley JL, Srikanth VK. Risk of falls in older people during fast-walking—the TASCOG study. Gait Posture. 2012;36: 510–515. doi: 10.1016/j.gaitpost.2012.05.003 22682610
17. Comber L, Galvin R, Coote S. Gait deficits in people with multiple sclerosis: A systematic review and meta-analysis. Gait Posture. 2017;51: 25–35. doi: 10.1016/j.gaitpost.2016.09.026 27693958
18. Bilney B, Morris ME, Churchyard A, Chiu E, Georgiou-Karistianis N. Evidence for a disorder of locomotor timing in Huntington's disease. Mov Disord. 2005;20: 51–57. doi: 10.1002/mds.20294 15390128
19. Huntington SG. Unified Huntington's Disease Rating Scale: reliability and consistency. Mov Disord. 1996;11: 136–142. doi: 10.1002/mds.870110204 8684382
20. Hart EP, Marinus J, Burgunder JM, Bentivoglio AR, Craufurd D, Reilmann R, et al. Better global and cognitive functioning in choreatic versus hypokinetic-rigid Huntington's disease. Mov Disord. 2013;28: 1142–1145. doi: 10.1002/mds.25422 23495076
21. Mancini M, King L, Salarian A, Holmstrom L, McNames J, Horak FB. Mobility Lab to Assess Balance and Gait with Synchronized Body-worn Sensors. J Bioeng Biomed Sci. 2011;Suppl 1: 007–9538.S1-007.
22. Bohannon RW, Wang YC, Gershon RC. Two-minute walk test performance by adults 18 to 85 years: normative values, reliability, and responsiveness. Arch Phys Med Rehabil. 2015;96: 472–477. doi: 10.1016/j.apmr.2014.10.006 25450135
23. Gijbels D, Eijnde BO, Feys P. Comparison of the 2- and 6-minute walk test in multiple sclerosis. Mult Scler. 2011;17: 1269–1272. doi: 10.1177/1352458511408475 21642370
24. Schwenk M, Zieschang T, Oster P, Hauer K. Dual-task performances can be improved in patients with dementia: a randomized controlled trial. Neurology. 2010;74: 1961–1968. doi: 10.1212/WNL.0b013e3181e39696 20445152
25. Freitas S, Simoes MR, Alves L, Santana I. Montreal cognitive assessment: validation study for mild cognitive impairment and Alzheimer disease. Alzheimer Dis Assoc Disord. 2013;27: 37–43. doi: 10.1097/WAD.0b013e3182420bfe 22193353
26. Wechsler D. Wechsler Adult Intelligence Scale WAIS-IV; Technical and Interpretive Manual: Pearson; 2008.
27. Smith A. The symbol-digit modalities test: a neuropsychologic test of learning and other cerebral disorders. Special Child Publications. 1968;83.
28. Seo EH, Lee DY, Lee JH, Choo IH, Kim JW, Kim SG, et al. Total scores of the CERAD neuropsychological assessment battery: validation for mild cognitive impairment and dementia patients with diverse etiologies. Am J Geriatr Psychiatry. 2010;18: 801–809. doi: 10.1097/JGP.0b013e3181cab764 20220577
29. Gullett JM, Price CC, Nguyen P, Okun MS, Bauer RM, Bowers D. Reliability of three Benton Judgment of Line Orientation short forms in idiopathic Parkinson's disease. Clin Neuropsychol. 2013;27: 1167–1178. doi: 10.1080/13854046.2013.827744 23957375
30. Kertesz A. Western Aphasia Battery. San Antonio, TX: The Psychological Corporation; 1982.
31. Berg K, Wood-Dauphinee S, Williams JI. The Balance Scale: reliability assessment with elderly residents and patients with an acute stroke. Scand J Rehabil Med. 1995;27: 27–36. 7792547
32. Powell LE, Myers AM. The Activities-specific Balance Confidence (ABC) Scale. J Gerontol A Biol Sci Med Sci. 1995;50A: M28–34. doi: 10.1093/gerona/50a.1.m28 7814786
33. Herman T, Giladi N, Hausdorff JM. Properties of the 'timed up and go' test: more than meets the eye. Gerontology. 2011;57: 203–210. doi: 10.1159/000314963 20484884
34. King LA, Mancini M, Priest K, Salarian A, Rodrigues-de-Paula F, Horak F. Do clinical scales of balance reflect turning abnormalities in people with Parkinson's disease? J Neurol Phys Ther. 2012;36: 25–31. doi: 10.1097/NPT.0b013e31824620d1 22333919
35. Pal G, O'Keefe J, Robertson-Dick E, Bernard B, Anderson S, Hall D. Global cognitive function and processing speed are associated with gait and balance dysfunction in Parkinson's disease. J Neuroeng Rehabil. 2016;13: 94. doi: 10.1186/s12984-016-0205-y 27793167
36. Grimbergen YA, Knol MJ, Bloem BR, Kremer BP, Roos RA, Munneke M. Falls and gait disturbances in Huntington's disease. Mov Disord. 2008;23: 970–976. doi: 10.1002/mds.22003 18381643
37. Bloem BR, Grimbergen YA, van Dijk JG, Munneke M. The "posture second" strategy: a review of wrong priorities in Parkinson's disease. J Neurol Sci. 2006;248: 196–204. doi: 10.1016/j.jns.2006.05.010 16806270
38. Nocera JR, Roemmich R, Elrod J, Altmann LJ, Hass CJ. Effects of cognitive task on gait initiation in Parkinson disease: evidence of motor prioritization? J Rehabil Res Dev. 2013;50: 699–708. doi: 10.1682/jrrd.2012.06.0114 24013917
39. de Souza Fortaleza AC, Mancini M, Carlson-Kuhta P, King LA, Nutt JG, Chagas EF, et al. Dual task interference on postural sway, postural transitions and gait in people with Parkinson's disease and freezing of gait. Gait Posture. 2017;56: 76–81. doi: 10.1016/j.gaitpost.2017.05.006 28521148
40. Lord S, Galna B, Coleman S, Yarnall A, Burn D, Rochester L. Cognition and gait show a selective pattern of association dominated by phenotype in incident Parkinson's disease. Front Aging Neurosci. 2014;6: 249. doi: 10.3389/fnagi.2014.00249 25374538
41. Yogev G, Giladi N, Peretz C, Springer S, Simon ES, Hausdorff JM. Dual tasking, gait rhythmicity, and Parkinson's disease: which aspects of gait are attention demanding? Eur J Neurosci. 2005;22: 1248–1256. doi: 10.1111/j.1460-9568.2005.04298.x 16176368
42. Maki BE. Gait changes in older adults: predictors of falls or indicators of fear. J Am Geriatr Soc. 1997;45: 313–320. doi: 10.1111/j.1532-5415.1997.tb00946.x 9063277
43. Vuong K, Canning CG, Menant JC, Loy CT. Gait, balance, and falls in Huntington disease. Handb Clin Neurol. 2018;159: 251–260. doi: 10.1016/B978-0-444-63916-5.00016-1 30482318
44. Hausdorff JM, Cudkowicz ME, Firtion R, Wei JY, Goldberger AL. Gait variability and basal ganglia disorders: stride-to-stride variations of gait cycle timing in Parkinson's disease and Huntington's disease. Mov Disord. 1998;13: 428–437. doi: 10.1002/mds.870130310 9613733
45. Kwon MS, Kwon YR, Park YS, Kim JW. Comparison of gait patterns in elderly fallers and non-fallers. Technol Health Care. 2018;26: 427–436. doi: 10.3233/THC-174736 29758966
46. Wajda DA, Motl RW, Sosnoff JJ. Dual task cost of walking is related to fall risk in persons with multiple sclerosis. J Neurol Sci. 2013;335: 160–163. doi: 10.1016/j.jns.2013.09.021 24090757
47. Mielke MM, Roberts RO, Savica R, Cha R, Drubach DI, Christianson T, et al. Assessing the temporal relationship between cognition and gait: slow gait predicts cognitive decline in the Mayo Clinic Study of Aging. J Gerontol A Biol Sci Med Sci. 2013;68: 929–937. doi: 10.1093/gerona/gls256 23250002
48. Beckmann H, Bohlen S, Saft C, Hoffmann R, Gerss J, Muratori L, et al. Objective assessment of gait and posture in premanifest and manifest Huntington disease—A multi-center study. Gait Posture. 2018;62: 451–457. doi: 10.1016/j.gaitpost.2018.03.039 29660633
49. Pyo SJ, Kim H, Kim IS, Park YM, Kim MJ, Lee HM, et al. Quantitative Gait Analysis in Patients with Huntington's Disease. J Mov Disord. 2017;10: 140–144. doi: 10.14802/jmd.17041 28851209
50. Pistacchi M, Gioulis M, Sanson F, De Giovannini E, Filippi G, Rossetto F, et al. Gait analysis and clinical correlations in early Parkinson's disease. Funct Neurol. 2017;32: 28–34. doi: 10.11138/FNeur/2017.32.1.028 28380321
51. O'Keefe JA, Robertson-Dick EE, Hall DA, Berry-Kravis E. Gait and Functional Mobility Deficits in Fragile X-Associated Tremor/Ataxia Syndrome. Cerebellum. 2016;15: 475–482. doi: 10.1007/s12311-015-0714-4 26298472
52. Cruz-Jimenez M. Normal Changes in Gait and Mobility Problems in the Elderly. Phys Med Rehabil Clin N Am. 2017;28: 713–725. doi: 10.1016/j.pmr.2017.06.005 29031338
53. Cromwell RL, Newton RA. Relationship between balance and gait stability in healthy older adults. J Aging Phys Act. 2004;12: 90–100. doi: 10.1123/japa.12.1.90 15211023
54. Termsarasab P, Frucht SJ. The "Stutter-Step": A Peculiar Gait Feature in Advanced Huntington's Disease and Chorea-Acanthocytosis. Mov Disord Clin Pract. 2018;5: 223–224. doi: 10.1002/mdc3.12586 30746406
Článek vyšel v časopise
PLOS One
2020 Číslo 1
- Pomohou nám s detekcí karcinomu plic i včely?
- Duševní onemocnění se u teenagerů přenáší v rámci školní třídy
- Od kostiček k lidské kůži. Jak si postavit 3D biotiskárnu?
- Řekněte mi, co jíte, a já vám řeknu, jaká je úroveň vaší kognice
- Umělá inteligence v mozkovém implantátu pomáhá muži po mrtvici s dvojjazyčnou konverzací
Nejčtenější v tomto čísle
- Severity of misophonia symptoms is associated with worse cognitive control when exposed to misophonia trigger sounds
- Chemical analysis of snus products from the United States and northern Europe
- Calcium dobesilate reduces VEGF signaling by interfering with heparan sulfate binding site and protects from vascular complications in diabetic mice
- Effect of Lactobacillus acidophilus D2/CSL (CECT 4529) supplementation in drinking water on chicken crop and caeca microbiome
Zvyšte si kvalifikaci online z pohodlí domova
Všechny kurzy