The effect of prioritization over cognitive-motor interference in people with relapsing-remitting multiple sclerosis and healthy controls

Autoři: Barbara Postigo-Alonso aff001;  Alejandro Galvao-Carmona aff001;  Cristina Conde-Gavilán aff003;  Ana Jover aff003;  Silvia Molina aff003;  María A. Peña-Toledo aff003;  Roberto Valverde-Moyano aff003;  Eduardo Agüera aff003
Působiště autorů: Department of Psychology, Universidad Loyola Andalucía. Seville, Spain aff001;  Human Neuroscience Lab (HNL), Universidad Loyola Andalucía, Seville, Spain aff002;  Neurology Service, Reina Sofía University Hospital, Cordoba, Spain aff003;  Maimonides Institute for Research in Biomedicine of Cordoba, (IMIBIC), Cordoba, Spain aff004
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article


The cognitive-motor interference (CMI) produced by simultaneous performance of a cognitive and a motor task has been proposed as a marker of real-life impairment of people with Multiple Sclerosis (pwMS), yet there is no consensus on the dual task (DT) procedure. This study aimed to compare DT performance of pwMS and healthy controls (HC) under different instructions and to examine its association with neuropsychological and clinical variables. PwMS (N = 23; relapsing-remitting course) and HC (N = 24) completed the cognitive (Verbal Fluency) and motor (walking) tasks under three conditions: independently or as single task (ST), both tasks simultaneously at best capacity or double prioritization (DT-DP), and only the cognitive task at best capacity while walking at preferred speed or cognitive prioritization (DT-CP). Compared to HC, pwMS walked significantly slower and produced less correct words under all conditions. The distance walked by pwMS and HC significantly differed between conditions (DT-CP< DT-DP< ST). PwMS produced more words during ST respective to DT-DP and DT-CP, with no difference between both DT conditions. HC showed no differences in cognitive performance between conditions. Motor and cognitive dual-task costs (DTC) were similar between groups. Only in pwMS, the cognitive DTC of DT-DP was different from zero. CMI measures correlated with neuropsychological, symptomatic, physiological (cognitive event-related potentials) and clinical variables. These results suggest that cognitive performance while walking is impaired in pwMS, but not in HC. CMI over cognitive performance might be a potential early marker of cognitive decline in pwMS, which may be enhanced by the instruction to prioritize both tasks in DT.

Klíčová slova:

Cognition – Cognitive impairment – Cognitive psychology – Memory recall – Multiple sclerosis – Neuropsychological testing – Neuropsychology – Walking


1. Chiaravalloti ND, DeLuca J. Cognitive impairment in multiple sclerosis. Lancet Neurol. 2008;7: 1139–1151. doi: 10.1016/S1474-4422(08)70259-X 19007738

2. Rocca MA, Amato MP, De Stefano N, Enzinger C, Geurts JJ, Penner I-K, et al. Clinical and imaging assessment of cognitive dysfunction in multiple sclerosis. Lancet Neurol. 2015;14: 302–317. doi: 10.1016/S1474-4422(14)70250-9 25662900

3. Cameron MH, Nilsagard Y. Balance, gait, and falls in multiple sclerosis. In: Day BL, Lord SR, editors. Handbook of Clinical Neurology. 3rd ed. Elsevier B.V.; 2018. pp. 237–250. doi: 10.1016/B978-0-444-63916-5.00015-X 30482317

4. Leone C, Patti F, Feys P. Measuring the cost of cognitive-motor dual tasking during walking in multiple sclerosis. Mult Scler J. 2015;21: 123–131. doi: 10.1177/1352458514547408 25178543

5. Woollacott M, Shumway-Cook A. Attention and the control of posture and gait: A review of an emerging area of research. Gait Posture. 2002;16: 1–14. doi: 10.1016/s0966-6362(01)00156-4 12127181

6. Amato MP, Ponziani G, Siracusa G, Sorbi S. Cognitive dysfunction in early-onset multiple sclerosis: A reappraisal after 10 years. Arch Neurol. 2001;58: 1602–1606. doi: 10.1001/archneur.58.10.1602 11594918

7. Achiron A, Barak Y. Cognitive impairment in probable multiple sclerosis. J Neurol Neurosurg Psychiatry. 2003;74: 443–6. doi: 10.1136/jnnp.74.4.443 12640060

8. Montero-Odasso MM, Sarquis-Adamson Y, Speechley M, Borrie MJ, Hachinski VC, Wells J, et al. Association of Dual-Task Gait With Incident Dementia in Mild Cognitive Impairment: Results From the Gait and Brain Study. JAMA Neurol. 2017;74: 857–865. doi: 10.1001/jamaneurol.2017.0643 28505243

9. Learmonth YC, Ensari I, Motl RW. Cognitive Motor Interference in Multiple Sclerosis: Insights From a Systematic Quantitative Review. Arch Phys Med Rehabil. 2017;98: 1229–1240. doi: 10.1016/j.apmr.2016.07.018 27543046

10. Postigo-Alonso B, Galvao-Carmona A, Benítez I, Conde-Gavilán C, Jover A, Molina S, et al. Cognitive-motor interference during gait in patients with Multiple Sclerosis: a mixed methods Systematic Review. Neurosci Biobehav Rev. 2018;94: 126–148. doi: 10.1016/j.neubiorev.2018.08.016 30189226

11. Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology. 1983;33: 1444–1452. doi: 10.1212/wnl.33.11.1444 6685237

12. Polman CH, Reingold SC, Edan G, Filippi M, Hartung H-P, Kappos L, et al. Diagnostic criteria for multiple sclerosis: 2005 revisions to the “McDonald Criteria.” Ann Neurol. 2005;58: 840–846. doi: 10.1002/ana.20703 16283615

13. Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, et al. Diagnostic criteria for multiple sclerosis: 2010 Revisions to the McDonald criteria. Ann Neurol. 2011;69: 292–302. doi: 10.1002/ana.22366 21387374

14. Beck AT, Steer RA, Brown GK. Manual. BDI-II. Inventario de Depresión de Beck-II (Adaptación española: Sanz, J., y Vázquez, C.). Madrid: Pearson; 2011.

15. Beck AT, Steer RA, Brown GK. Manual for the Beck Depression Inventory-II. 2nd ed. San Antonio, TX: Psychological Corporation; 1996.

16. Verghese J, Kuslansky G, Holtzer R, Katz M, Xue X, Buschke H, et al. Walking While Talking: Effect of Task Prioritization. Arch Phys Med Rehabil. 2007;88: 50–53. doi: 10.1016/j.apmr.2006.10.007 17207675

17. Peña-Casanova J, Quiñones-Ubeda S, Gramunt-Fombuena N, Quintana-Aparicio M, Aguilar M, Badenes D, et al. Spanish Multicenter Normative Studies (NEURONORMA Project): Norms for Verbal Fluency Tests. Arch Clin Neuropsychol. 2009;24: 395–411. doi: 10.1093/arclin/acp042 19648583

18. Baddeley AD, Della Sala S, Gray C, Papagno C, Spinnler H. Testing central executive functioning with a pencil-and-paper test. In: Rabbitt P, editor. Methodology of frontal and executive functions. Hove: Psychology Press; 1997. pp. 61–80.

19. Smith A. Symbol Digit Modalities Test: Manual. Los Angeles, CA: Western Psychological Services; 1982.

20. Benedict RH, DeLuca J, Phillips G, LaRocca N, Hudson LD, Rudick R. Validity of the Symbol Digit Modalities Test as a cognition performance outcome measure for multiple sclerosis. Mult Scler J. 2017;23: 721–733. doi: 10.1177/1352458517690821 28206827

21. Sedó MA. “5 digit test”: a multilinguistic non-reading alternative to the Stroop test. Rev Neurol. 2004;38: 824–828. doi: 10.33588/rn.3809.2003545 15152349

22. Delis DC, Kramer JH, Kaplan E, Ober BA. California Verbal Learning Test. New York: Psychological Corporation; 1987.

23. Benedet MJ, Alejandre MA. TAVEC. Test de aprendizaje verbal España-Complutense. Madrid: TEA Ediciones; 1998.

24. Aymerich M, Guillamón I, Perkal G, Nos C, Porcel J, Berra S, et al. Adaptación al español del cuestionario específico MSQOL-54 para pacientes con esclerosis múltiple. Neurologia. 2006;21: 181–187. 16832772

25. Vickrey BG, Hays RD, Harooni R, Myers LW, Ellison GW. A health-related quality of life measure for multiple sclerosis. Qual Life Res. 1995;4: 187–206. doi: 10.1007/bf02260859 7613530

26. Fisk JD, Doble SE. Construction and validation of a fatigue impact scale for daily administration (D-FIS). Qual Life Res. 2002;11: 263–272. doi: 10.1023/a:1015295106602 12074263

27. Benito-León J, Martínez-Martín P, Frades B, Martínez-Ginés ML, de Andrés C, Meca-Lallana JE, et al. Impact of fatigue in multiple sclerosis: The fatigue Impact Scale for Daily Use (D-FIS). Mult Scler. 2007;13: 645–651. doi: 10.1177/1352458506073528 17548445

28. Jurcak V, Tsuzuki D, Dan I. 10/20, 10/10, and 10/5 systems revisited: Their validity as relative head-surface-based positioning systems. Neuroimage. 2007;34: 1600–1611. doi: 10.1016/j.neuroimage.2006.09.024 17207640

29. Cohen J. Statistical power analysis for the behavioral sciences. 2nd ed. New York: L. Erlbaum Associates; 1988.

30. Faust ME, Balota DA. Inhibition of return and visuospatial attention in healthy older adults and individuals with dementia of the Alzheimer type. Neuropsychology. 1997;11: 13–29. doi: 10.1037//0894-4105.11.1.13 9055266

31. Wajda DA, Roeing KL, Mcauley E, Motl RW, Sosnoff JJ. The relationship between balance confidence and cognitive motor interference in individuals with multiple sclerosis. J Mot Behav. 2016;48: 66–71. doi: 10.1080/00222895.2015.1040110 25988565

32. Downer MB, Kirkland MC, Wallack EM, Ploughman M. Walking impairs cognitive performance among people with multiple sclerosis but not controls. Hum Mov Sci. 2016;49: 124–131. doi: 10.1016/j.humov.2016.06.010 27371919

33. Etemadi Y. Dual task cost of cognition is related to fall risk in patients with multiple sclerosis: a prospective study. Clin Rehabil. 2017;31: 278–284. doi: 10.1177/0269215516637201 26951347

34. Saleh S, Sandroff BM, Vitiello T, Owoeye O, Hoxha A, Hake P, et al. The Role of Premotor Areas in Dual Tasking in Healthy Controls and Persons With Multiple Sclerosis: An fNIRS Imaging Study. Front Behav Neurosci. 2018;12: 1–11. doi: 10.3389/fnbeh.2018.00001

35. Hamilton F, Rochester L, Paul L, Rafferty D, O’Leary C, Evans J. Walking and talking: an investigation of cognitive—motor dual tasking in multiple sclerosis. Mult Scler J. 2009;15: 1215–1227. doi: 10.1177/1352458509106712 19667011

36. Plummer P, Grewal G, Najafi B, Ballard A. Instructions and skill level influence reliability of dual-task performance in young adults. Gait Posture. 2015;41: 964–967. doi: 10.1016/j.gaitpost.2015.03.348 25891529

37. Decavel P, Moulin T, Sagawa Y. Gait tests in multiple sclerosis: Reliability and cut-off values. Gait Posture. 2019;67: 37–42. doi: 10.1016/j.gaitpost.2018.09.020 30269001

38. Bethoux F, Bennett S. Evaluating Walking in Patients with Multiple Sclerosis. Int J MS Care. 2011;13: 4–14. doi: 10.7224/1537-2073-13.1.4 24453700

39. 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

40. Sandroff BM, Benedict RH, Motl RW. Nonsignificant Associations between Measures of Inhibitory Control and Walking while Thinking in Persons with Multiple Sclerosis. Arch Phys Med Rehabil. 2015;96: 1518–1524. doi: 10.1016/j.apmr.2015.04.015 25944499

41. Wajda DA, Motl RW, Sosnoff JJ. Correlates of dual task cost of standing balance in individuals with multiple sclerosis. Gait Posture. 2014;40: 352–356. doi: 10.1016/j.gaitpost.2014.04.209 24909581

42. Motl RW, Sosnoff JJ, Dlugonski D, Pilutti LA, Klaren R, Sandroff BM. Walking and cognition, but not symptoms, correlate with dual task cost of walking in multiple sclerosis. Gait Posture. 2014;39: 870–874. doi: 10.1016/j.gaitpost.2013.11.023 24378281

43. Learmonth YC, Sandroff BM, Pilutti LA, Klaren RE, Ensari I, Riskin BJ, et al. Cognitive motor interference during walking in multiple sclerosis using an alternate-letter alphabet task. Arch Phys Med Rehabil. 2014;95: 1498–1503. doi: 10.1016/j.apmr.2014.03.007 24681387

44. Vázquez-Marrufo M, González-Rosa JJ, Galvao-Carmona A, Hidalgo-Muñoz A, Borges M, Peña JLR, et al. Retest Reliability of Individual P3 Topography Assessed by High Density Electroencephalography. PLoS One. 2013;8: 1–8. doi: 10.1371/journal.pone.0062523

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