Faculteit Geneeskunde en...

Faculteit Geneeskunde en Gezondheidswetenschappen

Cognitive-motor interference during various upper limb motor tasks in persons

with multiple sclerosis

Joke Raats

Masterproef voorgelegd tot het behalen van de graad van Master of science in de ergotherapeutische wetenschap

Promotor: prof. dr. Feys Peter

Copromotor: dr. Lamers Ilse Academiejaar 2015-2016

MASTER IN DE ERGOTHERAPEUTISCHE WETENSCHAP

Interuniversitaire master in samenwerking met:

UGent, KU Leuven, UHasselt, UAntwerpen, Vives, HoGent, Arteveldehogeschool, AP Hogeschool Antwerpen, HoWest,

Odisee, PXL, Thomas More

ABSTRACT NEDERLANDS

Achtergrond: Het gelijktijdig uitvoeren van twee taken is een frequent voorkomende

gegeven, onder andere het tezamen uitvoeren van een motorische en een cognitieve

taak. Het cognitieve- motorische paradigma bij Multiple Sclerose werd uitgebreid

onderzocht gedurende het wandelen, maar veel minder bij taken van de bovenste

lidmaten.

Doelen: Eerst werd er gekeken of er een cognitief motorische interferentie was bij taken

van het bovenste lidmaat. Vervolgens of deze interferentie verschillend wat voor

personen met MS ten opzichte van gezonde personen. Finaal werd ook de invloed van

de complexiteit van de motorische taak op de DTC bekeken.

Methode: 31 gezonde personen en 37 personen met MS namen deel aan een cross

sectioneel onderzoek, beiden hadden geen beperkingen in de bovenste ledematen. Vijf

motorische taken werden uitgevoerd, enkelvoudig en gecombineerd met een cognitieve

taak. Data werden geanalyseerd met Mann-Withny U testen en een MANOVA.

Resultaten: Voor elke taak en in beide groep werd een interferentie gevonden. De range

van de verschillende motorische DTC ging van 9.97 tot 34.90%. Deze was echter niet

groter voor de personen met MS. De kleinste interferentie werd gezien bij de finger

tapping en de grootste bij de box and Block test.

Conclusie: Er werd een cognitieve motorische interferentie gevonden die gelijkaardig is

voor beide groepen. Deze studie werd uitgevoerd bij personen die op een hoog

motorisch en cognitief niveau functioneerde, wat een verklaring kan zijn waarom er

geen verschil gevonden werd tussen beiden groepen. De complexiteit van de motorische

taak zorgde voor een andere keuze in prioritisering.

“Aantal woorden masterproef: 9147 (exclusief bijlagen en bibliografie)”

ABSTRACT ENGLISH

Background: Executing and performing different tasks at the same time is a common

everyday act, frequently like combining a motor and a cognitive task. The cognitive-

motor paradigm in Multiple Sclerosis (MS) has been examined extensively by cognitive

tasks during walking, but not during upper limb tasks.

Objectives: The primary aim is to see if there is a cognitive- motor inference (CMI)

during upper limb movements. Secondly, to examine whether there is a difference in the

dual task cost (DTC) between PwMS and healthy controls. Finally, the influence of the

complexity of the motor task on the DTC is investigated.

Method: 37 PwMS and 31 HC without marked upper limb dysfunction participated in a

cross-sectional study. They executed five different upper limb tasks, in single condition

and combined with the phonemic word list generation task. Data were analyzed with

Mann-Withny U test and A MANOVA.

Results: For each motor task, and in both groups, a range in the DTC for the motor tasks

between 9.97 and 34.90% was found. However the DTC was similar for the PwMS

compared with the HC in any task. The DTC was smallest during finger-tapping task

and largest in the box and block test.

Conclusion: A CMI is found during upper limb tasks but appeared similarly in PwMS

and HC. The similarity can be explained by the fact that PwMS without marked upper

limb and cognitive dysfunctions has been included. However the degree of difficulty of

the motor task determined a different prioritization over the tasks.

Amount of words: 9147 (exclusive annex and references)

CONTENTS Abstract Nederlands ..................................................................................................... - 1 -

Abstract English ........................................................................................................... - 5 -

Prefaces ......................................................................................................................... - 1 -

Introduction .................................................................................................................. - 3 -

Characteristics of Multiple Sclerosis ........................................................................ - 3 -

The dual task paradigm............................................................................................. - 5 -

Research aims ............................................................................................................... - 7 -

Method .......................................................................................................................... - 8 -

Sample ...................................................................................................................... - 8 -

Design ..................................................................................................................... - 11 -

Experimental procedure and task ........................................................................... - 11 -

Data analyse ............................................................................................................ - 12 -

Results ........................................................................................................................ - 14 -

Discussion ................................................................................................................... - 20 -

Recommendations and implications for future research ............................................ - 25 -

Conclusion .................................................................................................................. - 26 -

Bibliography ............................................................................................................... - 27 -

Annex 1: The different motor tasks ............................................................................ - 33 -

Annex 2: Toelating tot consultatie van de masterproef .............................................. - 34 -

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PREFACES

Het schrijven van deze masterproef is één van de laatste hordes in een zeer verrijkende

opleiding. Achterom kijkend naar dit parcours wil ik dan ook oprecht dank zeggen

tegen enkele mensen. Dit traject leg je immers niet alleen af!

Een eerste dankjewel gaat uit naar de onderzoeksgroep van Reval/ Biomed, UHasselt.

Met een bijzondere dank aan Prof. Dr Peter Feys, Dr. Ilse Lamers, Dr. Ilse Baert en

Drs. Deborah Severijns die met hun kritische kijk mij leidde naar dit eindresultaat.

Dank je wel om mij keer op keer verder te pushen maar me toch steeds net niet te laten

struikelen… De ondersteuning, sturing en discussies die ik met jullie voerde, waren, en

zijn nog steeds, erg verrijkend voor me.

Dank je wel aan elke proefpersoon die tijd maakte voor me. Ik ben hen dankbaar voor

de waardevolle meetgegevens die ik hierdoor kon verzamelen.

Mijn dank gaat ook uit naar alle collega’s van AZ Klina, campus De Mick. Door jullie

was de combinatie van werken en studeren mede mogelijk. Een dikke merci voor de

flexibiliteit waarmee onze ergo’s een extra patiënt in mijn plaats deden, dat jullie je

plan trokken als ik weer een lange tijd achter mijn boeken kroop… Greet, dank je wel

dat je me toe liet om mijn uurrooster niet al te strikt van 8.00 tot 16.00 te laten invullen.

Hoewel Koen hard zijn best deed, zullen computers en ik waarschijnlijk nooit vrienden

worden, toch wil ik hem duizend maal dank zeggen! Een vriendelijke dank u wel aan

de neurologen van het MS Netwerk Antwerpen, dr. B. Willekens, dr. C. deBarsy en dr.

K. Geens, die me steunden bij dit onderzoek. Maar superlatieven schieten tekort om

Marleen te loven voor het werk dat zij leverde voor mij. Zij bood me een schouder

wanneer een virus mijn data had aangetast maar bovenal nog veel meer proefpersonen.

Voor de wijze waarop zij op dat moment me steunde en mij alle moed deed samen

rapen om dit werk af te ronden zal ik haar oneindig dankbaar blijven!

Mijn ouders, jullie niet aflatende steun lijkt echt oneindig te zijn! De voorbije jaren van

werken en studeren zouden onmogelijk geweest zijn als de deuren van dit warm hotel

geen 7/7 dagen en 24/24 uur geopend zouden zijn geweest. Mama en papa, dank je wel

om mij de kans te geven om me te laten doen wat ik graag wil doen!

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Bart, Wendy, Leen en Tom, bedankt voor het luisterend oor en mijn excuses dat ik niet

altijd de vrolijkheid zelve was bij ons thuis. Vanaf nu veranderen hopelijk onze

gespreksonderwerpen weer.

Best friends make the good times better and the hard times easier. Als laatste wil ik hen

dan ook oprecht danken: de bezorgde smsjes, de geïnteresseerde telefoontjes, de

grappige mails… het deed stuk voor stuk deugd. Jullie hielden me te gepaste tijden aan

als weg van mijn bureau. Karen, bedankt om mij steeds bij te praten na een weeral

gemist avondje. Susanne, bedankt voor de uitstapjes waarbij je er op een of andere

wijze wonderwel in slaagt dat ik alles even achter me kan laten. Michael, Bert, Inge…

Het is ontzettend fijn te weten dat er altijd wel iemand naast je staat, die achter je staat!

Bedankt iedereen.

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INTRODUCTION

Executing and performing different tasks at the same time is a common everyday thing

for most of us. In order to execute these tasks, we shouldn’t need to keep our attention

continuously on each single task as performing proceeds natural and automatic. Dual

tasking can be defined as "the concurrent performance of two tasks that can be executed

independently, measured separately and have distinct goals" (McIsaac, Lamberg, &

Muratori, 2015). The most well known and investigated combination of dual tasking is

walking whilst talking. When the dual task becomes more difficult, persons affected

may stop walking when starting up a conversation, due to the specific attention the

walking might demand. A reduced dual task performance could be explained by an

underline concurrence of the cognitive task on physical performance (Hyndman &

Ashburn, 2004). Literatures shows that this combination becomes more difficult when

aging or in neurological diseases like stroke, Parkinson Disease and in Multiple

sclerosis (Lundin-Olsson, Nyberg, & Gustafson, 1997; Hausdorff, Schweiger, Herman,

Yogev-Seligmann, & Giladi, 2008; Strouwen, 2015; Bowen, Wenman, Mickelborough,

Foster, Hill, & Tallis, 2001; Hyndman & Ashburn, 2004; Hamilton, Rochester, Paul,

Rafferty, O'Leary, & Evans, 2009).

CHARACTERISTICS OF MULTIPLE SCLEROSIS

MS is a chronic disease of the central nervous system (CNS) that affects between two

and two and a half million people worldwide (Cameron, Finlayson, & Kesselrinf, 2013).

The disease prevalence is uneven distributed in the world by a north-south and a east-

west gradient (Sindic, 2014). The prevalence rate in Belgium is estimated at 88/100.000

with an incidence rate of 430 newly diagnosed each year. The lifelong implications

physically, cognitively and psychosocially leads to a reduced quality of life,

participation and the ability to maintain employed (Heesen, Böhm, Reich, Kasper,

Goebel, & Gold, 2008).

This neurodegenerative, autoimmune disease is associated with an inflammation and

damage of the myelin in the nerve fibers and the axonal degeneration of the central

nervous system. Specifically because of a loss of oligodendrocytes, which are

responsible for the maintenance of the myelin around the axon, the axonal transmission

becomes more difficult or is not longer possible (Chiaravalloti & DeLuca, 2008). The

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reason of inflammation and plaque formation in MS is unknown. It is thought to be the

result of several immunological, genetic and viral factors (Rumrill, Battersby, & Kaleta,

1996). The clinical signs are heterogeneous, depending on location, amount and the

severity of plaques in the CNS different symptoms may occur (O'Brien, Chiaravalloti,

Goverover, & DeLuca, 2008). Despite the existence of a wide range of symptoms, i.e.

visual, muscular, sensory, bladder... malfunctioning, the focus for this study is only set

on the motor and cognitive malfunctioning.

Motor disorders are the most well know symptoms of MS. Coordination, muscle

strength and tone are commonly affected in PwMS. Consequently weakness, spasticity

and tremor affects most activities of daily life (Bethoux & Sutliff, 2013). These

limitations could hinder voluntary movement of the upper and lower limb and the trunk.

In the context of this study, the focus is on the upper limb. Depending on which

outcome measurement is used, studies shows that 66% of PwMS and up to 81% after 15

years of disease experience impairments of unilateral and bilateral upper limbs (Bertoni,

Lamers, Chen, Feys, & Cattaneo, 2014; Johansson, et al., 2007). These limitations cover

a wide range of disordered functionalities, like precision and force grip, grasping,

releasing, reaching, speed and accuracy and movement patterns are all functions or

activities that could be impaired (Raine, Meadows, & lynch- Ellerington, 2009). PwMS

with Expanded Disability Status Scale (EDSS) score 3.5 or lower present already upper

limb dysfunctions in all the ICF levels (Bertoni et al., 2014).

Cognitive impairment is another common symptom in MS, with prevalence rates

between 43 and 70% (Chiaravalloti & DeLuca, 2008; Patti, 2009; Rao, Leo, Bernadin,

& Unverzagt, 1991). It is an underestimated symptom, particularly in the early phase,

that has a poor correlation with the EDSS (Amato, Zipoli, & Portaccio, 2006). These

disorders can have a major determining impact on many everyday activities, including

social and work-related domains, which is independently of the individual degree of

physical disability (Chiaravalloti & DeLuca, 2008). Memory (54%), mental-processing

speed (50%), executive functions (20%) and visuo-spatial perception (20%) are the

most common impaired functions in PwMS (Ben Ari, Benedict, & LaRocca, 2013).

Difficulties, both with movements of the upper limb and cognition, are known to be

widespread in PwMS. Although there is an increasing evidence for interaction during

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simultaneous execution of these tasks (Wajda & Sosnoff, 2015), in most cases the

different functions are examined independently of each other. Only two published

studies have investigated how these difficulties interact in this particular disease

(D'Esposito, Onishi, Thompson, Robinson, Armstrong, & Grossman, 1996; Learmonth,

Pilutti, & Motl, 2015). Recognizing this interaction can have an impact in analyzing

common daily activities. It can enable clinicians and researches to create more

meaningful outcome measures to identify better real-life performance. The separate

mapping of functions is not a fair representation of everyday activity. A combined

measure of motor and cognitive tasks could increase the validity for measuring real-life

impairment in PwMS. A decrement of one or two tasks could indicate the occurrence of

cognitive-motor interference (Leone, Patti, & Feys, 2015) which can be investigated

with the dual task paradigm.

THE DUAL TASK PARADIGM

During dual tasks, cognitive processes are competing with each other. The precise

manner of the interference during dual task is unknown but two theoretical models are

very frequently put forward: the capacity sharing model and the bottleneck theory (task

switching). Another less known model is the multiple resources theory (Pashler, 1994).

The capacity sharing model is the most commonly accepted method to think about dual

task interference (Plummer, & Eskes, 2015). If tasks are performed simultaneously,

people will have to divide their processing capacity which will result in a reduced

capacity for each individual task and whereby the performance of the dual task in

general will be impaired (McIsaac et al., 2015). It has been suggested that the

interference of the tasks could be caused by an increased use of central resources rather

than an overall reduction in a patient’s processing capacity (Hyndman & Ashburn,

2004). The allocation can be a voluntary choice or influenced by the characteristics of

the task. Difficult tasks will require more focus and the center of attention will be

determining for the other combined task. The brain will be challenged to decide how to

prioritize tasks. In general, prioritization is based on the motivation to minimize danger

and maximize pleasure (Yogev-Seligmann, Hausdorff, & Giladi, 2012). Although this

statement is not always correct. In the DT paradigm of the lower limb an inappropriate

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prioritization strategy is seen. The risk of falling increases when people execute dual

tasks (Wajda & Sosnoff, 2015; Wajda, Motl, & Sosnoff, 2013).

An alternative model is the bottleneck model, which suggests dual tasking is similar to

task switching. In this model it is assumed that it is impossible to run two processes

parallel to each other because they use the same neural pathways. Different processing

bottlenecks could be distinguished in different stages of processing (Pashler, 1994).

During the dual tasks, one or both tasks will have a delay, called a psychological

refractory period effect, which is caused by the bottleneck and the final performance

will be impaired. The bottlenecks are responsible for response selection and decision

making (Tombu & Jolicoeur, 2003). Marois & Ivanoff describes three major bottlenecks

of information processing attention, visual short-term memory and psychological

refractory period phenomena respectively (Marois & Ivanoff, 2005). Consequently,

during dual tasking, the system must always balance between several demands and will

switch attention to the most task-relevant information (McIsaac et al, 2015). By

selecting, there may be a delay in the response. Pashler & Johnston conclude that a

central bottleneck model doesn’t conflict with general observations nor with the idea

that different areas in the brain usually work continuously and concurrently (Pashler &

Johnston, 1998).

The last model is the multiple resources theory. Wickens et al state that there are two

important concepts, namely: the multiple resource model and the mental overload.

Although there is a certain overlap, they also differ from each other. The multiple

resource model is composed of three components which are related to demand, resource

overlap and allocation policy. The mental workload is mainly related to the demands of

the task, the human’s mental resources which are needed for the characteristics of the

demand. Finally Wickens et al. compose a model that suggests that the dual task

paradigm resources competes in four dimensions: the stages of processing, codes of

processing, modalities and responses (Wickens, 2008)

Despite previous exploring theories, the brain-behavior relationship in dual-tasking is

not entirely clear. Several studies show the present of a dual task interference in a

healthy central nervous systems (CNS). Everybody has the ability to select, attend and

process information, but these capacities are limited, which has an influence to the

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preparation and performance of simultaneous tasks. The dual task paradigm is been

investigated in a broad range of cognitive tasks and variances on gait performances (Al-

Yahya, Dawes, Smith, Dennis, Howells, & Cockburn, 2011). The laborious

performance of multitasking changes is apparent in persons with neurodegenerative

diseases. The increased problems in persons with neurodegenerative disease are

explained by Marois & Ivanoff (2005) by three impaired bottlenecks in the CNS.

McIsaac et al. provide three reasons for the declination in performance of dual tasks that

could be linked closely to the theoretical causes of dual task interference. As first the

pathology affects the attention capacity that is needed for a specific task. Secondly,

cortical changes may affect executive function, laid in the frontal lobe. Finally, each

task requires separately more effort in itself, therefore performing tasks simultaneously

brings out a larger effort (McIsaac et al, 2015).

To quantify the cognitive- motor interference (CMI) in experimental studies, the

method of the dual task effect (DTE), a synonym for dual task cost (DTC), is frequently

calculated. A decrement due to dual tasking is represented by a negative result and an

improvement by a positive result. This calculation makes it possible to compare

different tasks with each other.

RESEARCH AIMS

The primary aim of this study was to investigate if there is a difference between PwMS

and healthy controls in performing a motor task combined with a cognitive task.

Additionally, is the dual task cost is determined due to the characteristics of the motor

task.

A higher cognitive cost will be hypothetically associated with some specific motor

tasks, particularly motor tasks that require more precision or manual dexterity. Higher

cognitive cost would indicate more requirement of greater attention for that specific

motor task, under dual-tasking condition.

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METHOD

SAMPLE

The study design and protocol were approved by the ethics committee of the University

Hospital Antwerp, after consulting the local ethics committees of all participating

institutions namely UHasselt en AZ Klina. After the explanation of the study protocol, a

written informed consent was obtained for all participants.

PwMS were recruited through the MS Network of Antwerp. Controls included a

convenience sample of family, friends and colleagues but they were only selected by

age and sex to match the PwMS. Subjects had to be at least 18 years or older and had to

be able to perform the nine hole peg (NHPT) faster than 0.50 peg/ second using their

respective dominant hand (Kierkegaard, Einarsson, Gottberg, van Koch, & Holmqvist,

2012). It was chosen to investigate the impact of MS rather than motor dysfunction in

this pilot study. Only the PwMS were diagnosed according to McDonald's criteria. The

exclusion criteria for both, PwMS and controls, were presence of current major

psychiatric disorder or a history of other neurological disorder or an orthopedic disease

of the upper limb or spine.

All participants had to complete a clinical test-battery. It included several

questionnaires, clinical tests, and descriptive data with regards to their date of birth,

gender, duration of illness and an Expanded Disability Status Scale (EDSS) score as

defined by their neurologist.

The following questionnaires were completed:

The Modified Fatigue Impact Scale (MFIS) is a 21-item structured, self-report

questionnaire with nine ‘physical’ items, ten ‘cognitive’ items and two

‘psychosocial’ items. Participants were asked to score the fatigue they experienced

during the last four weeks. Each item has been rated on a likert-scale (0-4)

indicating how often they have experienced fatigue (Kos, et al., 2003). The total

score for the MFIS is the sum of the scores for the 21 items, subscale scores can also

be generated. The maximum score of 84 indicates an extreme feeling of fatigue, a

minimum score of zero indicates no fatigue.

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The Hospital Anxiety and Depression Scale (HADS) is a two dimension scale to

identify depression and anxiety. It results in a score range from 0-21 for depression

and anxiety scale. High scores indicate more symptoms (Tedman, Young, &

Williams, 1997).

The Edinburgh Handedness Inventory determine the hand dominance (Oldfield,

1971).

The Manual Ability Measure 36 (MAM- 36) assess perceived difficulties in 36

common activity of daily life (ADL) tasks. A four point scale (four = easy, one =

cannot do) on each item led afterwards to sum the score. This score was then

converted into a “manual ability measure” (zero indicates lowest and 100 indicates

perfect manual ability) (Chen & Bode, 2010) .

The dual task questionnaire determines the perceived executing of dual tasks in

daily life. It is a 10-item structured, self-report questionnaire. Participants were

asked to score their perceived difficulties with dual tasks in daily life. Each item is

been rated on a likert-scale (0-4) with four = very often, one = never. The final score

is the average of the filled-items (Evans, Greenfield, & Wilson, 2009).

The following cognitive assessment were executed:

The symbol digit modality test (SDMT) evaluates information processing speed. A

key presenting nine numbers paired with unique symbols was given to the subjects.

Below the key is an array of symbols paired with empty spaces, the patient had to

match the number for each symbol as quickly as possible. The final outcome is the

number of correct responses in 90 seconds (Drake, Weinstock-Guttman, Morrow,

Hojnacki, Munschauer, & Benedict, 2010).

The Stroop color word test (SCWT) is considered to be a general measure of

cognitive flexibility and control. It consists of three subtasks. Each subtask has 100

stimuli, which are distributed evenly in a 10 x 10 matrix. The first subtask shows

color words in random order printed in black ink. Subtask 2 displays solid color

patches in basic colors. The third subtask contains color words printed in an

incongruous ink color. The participants were instructed to read the words, name the

colors, and finally, name the ink color of the printed words as quickly and as

accurately as possible. Finally, the interference is displayed in seconds. This is

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achieved by Stroop III – ((Stroop I + stroop II)/2) (Van der Elst, van Boxtel, Van

Breukelen, & Jolles, 2006).

The Trail Making Test A and B (TMT a, TMT b) measures the cognitive domains of

processing speed, sequencing, mental flexibility and visual–motor skills. The test

contains part A and B. In the first part one has to connect a series of 25 encircled

numbers in numerical order. In part B one is asked to connect 25 encircled numbers

and letters in numerical and alphabetical order, alternating between the numbers and

letters (Tombaugh, 2004; Bowie & Harvey, 2005).

The motor skills were evaluated by the following tests:

The nine Hole Peg Test (NHPT) is developed to assess fine manual dexterity. The

time needed to place and remove nine pegs is recorded and the average of the two

trials was displayed (seconds).

The Semmes-Weinstein monofilaments: Five monofilaments (diameters of 2.83,

3.61, 4.31, 4.56 and 6.65) are used to measure tactile sensitivity in the fingertip and

the thumb:

o 2.83=1, normal sensation

o 3.61=2, diminished light touch

o 4.31=3, diminished protective sensation

o 4.56=4, loss of protective sensation

o 6.65=5, untestable;

The monofilaments are randomly presented in a descending or ascending order to

the thumb and index finger. Each filament is pressed against the skin until it

bends. The participants are instructed to close their eyes and will be asked to give

a response once they sense a touch. All filaments are tested three times. The

filament with the lowest pressure score, which is felt 3/3 times on the fingertip, is

recorded (Cuypers, Levin, Thijs, Swinnen, & Meesen, 2010).

Hand grip strength: an average maximal hand grip strength (kg) was measured for

each hand with the JAMAR® hand-held dynamometer during three repeated trials.

The American Society of Hand Therapists (ASHT) recommends that grip strength

should be measured using the Jamar dynamometer with the handle in the second

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position, whilst the person is in a sitting position, with shoulders adducted, elbows

flexed 90° and forearms in neutral position (Bohannon, Peolsson, Massy-Westropp,

Desrosiers, & Bear-Lehman, 2005).

DESIGN

A cross- sectional design was applied to investigated whether there is a difference

between PwMS and control participants under single and/ or dual- task condition. Data

collection took place between October 2015 and April 2016.

EXPERIMENTAL PROCEDURE AND TASK

The investigation, which lasted slightly more than one hour per subject took place in all

different participating hospitals, included five different motor tasks and one cognitive

task.

Several motor tasks were included, which vary in degree of difficulty, whereby required

attention to a specific motor task was diverse. These varied from almost automatic tasks

to tasks which required more manual dexterity. The motor tasks were performed in a

sitting position, to minimize the postural control as a confounding factor. The five

motor tasks are shown in appendix 1:

1. Finger tapping test: participants were asked to tip the index finger and thumb

together for 30s at their preferred pace. The participants were asked to wear a glove

which contain sensors. The number of contacts between two fingers was measured.

This task was included in the protocol because finger tapping is intended to be a

fairly automatic, coordinated task.

2. Sustained hand grip strength: In the hand grip strength task, subjects were requested

to squeeze isometrically for a maximum of 30 seconds. This was recorded by hand

dynamometer of the E-link device (BIOMETRICS, NL). In the final analysis, the

area under the curve was measured. For an uncomplicated presentation in the table

the number was then divided by 1.000.000.000.

3. The box and block test: participants were asked to move blocks one by one during

30 seconds. This task was chosen because it requires manipulation of an object, the

blocks were 2.5 cm x 2.5 cm and so gross motor skills were required. The number of

blocks that were moved were measured.

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4. The Purdue Pegboard:

a. The Purdue Pegboard unilateral

b. The Purdue Pegboard bimanual

Two particular parts of the Purdue Pegboard test were executed. The original

Purdue Pegboard consists of five different components. In order to reduce

the duration of the research protocol, tests were carried out only unilateral

with the dominant hand, as well as the part where the both hands places the

pegs in the board simultaneously. Each task lasted 30 seconds. The number

of pegs were counted for the final analyses.

The cognitive task was the phonemic word list generation. It is a common used

cognitive task in previous research in DTC in PwMS (Motl R. W., Sosnoff, Dlugonski,

Pilutti, Klaren, & Sandroff, 2014; Kalron, Dvir, & Achiron, 2010; Sosnoff, Boes,

Sandroff, Socie, Pula, & Motl, 2011). Participants were asked to name as many words

as possible beginning with a specific letter during a period of 30 seconds. The total

number of words generated in 30 seconds was used as outcome.

The different tasks (single motor, single cognitive and dual motor-cognitive) were

randomly performed. Based on standardized instructions, each task was executed two

times, one time in a single condition and once in a combined motor-cognitive task

condition. All participants performed a practice trial of each task to get familiarization

of the task. After each test, the subjects were asked to give a score which describes their

feeling of fatigue, by a visual analogue scale (VAS) score. In the dual task condition

subjects were asked to perform the cognitive task and one of the five motor tasks

simultaneously. No instructions were given to the prioritization of the task.

DATA ANALYSE

Thirty-seven PwMS and thirty-one healthy controls participated in the study.

Unfortunately five data files of PwMS were completely lost by an affected laptop. Two

PwMS were excluded because they didn’t match the inclusion criteria of the NHPT

performance. One healthy control was excluded for the research protocol because of

color blindness and inadequate performance on the NHPT, i.e. score of

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All data outcomes were checked for the normality of distribution and appropriate

parametric or non-parametric analyses were performed. Consequently for the

comparison of the descriptive data between the groups a Mann-Whitney U Tests has

been done. To study the differences between the single and dual condition for each task,

a paired samples t-test was used. An independent samples t-test was used to investigate

the differences between PwMS and healthy controls for each task.

The analysis of the experimental data was built up in several steps. First by calculating

the dual task cost for the cognitive and for the motor task separately, as follows:

100

However, the calculation of the DTC separately for each task (cognitive and motor) is

too narrow. We needed to achieve an overall estimation of the performance of the entire

dual task. The DTC must not be seen as an indicator of the dual task performance of a

cognitive task neither of a motor task, but as an interference. In order to take into

account a general performance for a task, a single score for the overall combined change

in cognitive task and motor task performance under dual-task conditions was calculated,

based on the following formula (Hamilton et al., 2009; Baddeley, Della Sala, Gray,

Papagna, & Spinnler, 2005).

To investigate the CMI of all the different dual task, a multivariate analysis of variance

(MANOVA) was used. This was done to avoid separate analyses of each motor task –

and the associated loss of power. The Wilks’ lambda multivariate statistic was used to

determine the significance of the results, and Fischer’s LSD tests for post-hoc testing.

The group variance was used as an independent variable, the different averages of the DTC

as dependent variables and fatigue as a covariate. All the data analyses were performed in

SPSS version 22.0. The significance levels for all tests were set at p < 0.05. To analyze

the different tasks, the mean DTC for each task was compared with another one by

paired sample t-tests.

In addition to the several analyzes of the DTC, there may be a difference in the

prioritizing between the two groups. Despite no task prioritization instructions were

- 14 -

given, it could be possible that PwMS choose the motor task over the cognitive task

because of a possible lesser performance on the motor task in the single condition. If

people made different choices in prioritizing, this would lead to a reduction of the mean

decrement score for the group. On the other hand, it was possible that there were

differences between PwMS and healthy controls. It could be possible that they made

other choices in prioritizing, cognitive versus motor. Therefore, the various DTC are

plotted on charts to get more information.

RESULTS

The basic demographic and descriptive, clinical characteristics of each group are

summarized in table 1. This table shows no significant differences for age or gender.

The EDSS score of the PwMS (mean of 2.3) showed a mild disabled group. PwMS

perceived significantly more fatigue based on the MFIS, just as they experienced a more

anxious and depressed feeling on the HADS. Despite the fact that we recruited on a

good performance of hand dexterity, the PwMS perceived significantly more difficulties

in daily life by the MAM-36. Across the full range of cognitive tests no differences

were found between PwMS and HC. The motor skills of the PwMS were significantly

more impaired. A difference was noted on the NHPT for the non-dominant hand and for

the hand grip strength for both hands. The sensory function of the non dominant hand

was more impaired for the PwMS (Semmes Weinstein non dominant). The dominant

hand wasn’t.

- 15 -

Table 1. Subject characteristics; number, mean and interquartile range

PwMS n= 30 Controls n= 30 P-value

Demographic data

Age (years) 44.1 (33.3-55.4) 43.9 (33.4-55.1) Ns

Gender (M/F) 26/4 26/4 -

Disease-specific data

EDSS score (0-10) 2.3 (1.5-3) - -

Years since diagnosis 9.3 (4.3-12.3) - -

Descriptive data

MFIS (0-57) 38.0 (24.3-48.3) 16.8 (8.5-24.3) P < 0.001

HADS (0-56) 11.1 (5.8-17) 6.8 (3.75-10) P < 0.05

MAM-36 (0-100) 79.7 (67.9-92.5) 97.2 (100-100) P < 0.001

Dual task questionnaire (0-4) 1.4 (0.7-2.1) 1 (0.6 -1.1) P < 0.05

Cognitive testing

SDMT (1-90) 59.8 (49.8-66.8) 61.8 (55-68.5) Ns

SCWT interference 23.6 (20.4-27.7) 26.2 (19.9-30.1) Ns

TMT a (seconds) 24.4 (18.8-28.6) 22.3 (17-26.5) Ns

TMT b (seconds) 53.4 (36.3-57.8) 48.6 (34.9-49.5) Ns

Sensory-Motor testing

NHPT non dominant (seconds) (R/L) 20.8 (17.9- 22.6) (2/28) 18.0 (16.8- 18.6) 3/27) P < 0.001

NHPT dominant (seconds) (R/L) 17.0 (15.8- 18.01) (28/2) 16.2 (14.8-17.6) (27/3) P = 0.08

Semmes Weinstein non dominant 4.1 (4-5) 4.4 (4-5) P < 0.05

Semmes Weinstein dominant 4.1 (4-5) 4.3 (4-5) P = 0.08

Hand grip strength non dominant (kg) 23.0 (18.4-26.2) 29.7 (25.9- 32.4) P < 0.001

Hand grip strength dominant (kg) 27.6 (23.2- 31.9) 33.2 (27.3- 34.3) P < 0.05

Table 2 shows the performance of each group in the single and dual task condition. For

each motor task there was a statistically significant difference between single and dual

task performance. Furthermore, there was a difference in the performance of the motor

tasks in the single condition between PwMS and the healthy controls. No significant

difference was found between PwMS and healthy controls for the cognitive tasks in the

single condition and for the cognitive tasks in the dual task condition combined with the

Purdue Pegboard bimanual, finger tapping and the hand grip strength. On the contrary, a

worse performance was observed between the two groups in the performance for the

cognitive task, while this was combined with the Purdue Pegboard unilateral and the

box and block test.

- 16 -

Table 2. Performance of PwMS and healthy controls for each task (mean ± standard deviation)

Single/

Dual

PwMS Healthy Controls

Finger Tapping (FT) ST 143.23 ± 26.99 158.33 ± 20.15 p

- 17 -

Table 3 shows there were no significant differences for the DTC based on the cognitive

or motor task between PwMS and healthy controls.

Table 3. Dual task cost for each task (%) (mean ± standard deviation)

PwMS Healthy controls p-value

DTC mot FT 20.52 ± 20.26 19.08 ± 12.10 ns

DTC mot HGS 22.41 ± 23.83 21.84 ± 12.35 ns

DTC mot BBT 34.90 ± 19.06 31.17 ± 21.94 ns

DTC mot PP uni 16.00 ± 14.46 10.89 ± 12.18 ns

DTC mot PP bim 9.97 ± 13.18 11.60 ± 11.88 ns

DTC cog, FT -5.19 ± 34.17 -8.26 ± 44.59 ns

DTC cog, HGS 2.21 ± 36.78 0.10 ± 34.49 ns

DTC cog, BBT 3.03 ± 26.69 -1.43 ± 29.97 ns

DTC cog, PP bim 21.72 ± 27.87 11.53 ± 38.19 ns

DTC cog, PPuni 10.77 ± 35.49 -2.36 ± 25.38 ns

Table 4 shows the subsequent analysis. Also here no differences were found for each

task separately. To investigate the CMI of all different tasks, a MANOVA was used.

This multivariate analysis was based on the mean DTC of each task. Finally, it revealed

a non-significant result on the Wilks' Lambda (F=0.829, p=0.535). In summary, no

differences were found between the cognitive-motor interference of PwMS and healthy

controls.

Table 4. A combined dual task cost for each task (%)(mean ± standard deviation)

PwMS Healthy controls p-value

mDTC FT 6.41 ± 21.02 5.4 ± 21.44 ns

mDTC HGS 11.34 ± 19.36 11.04 ± 18.50 ns

mDTC BBT 18.54 ± 14.59 14.87 ± 18.87 ns

mDTC PP uni 13.42 ± 20.38 4.26 ± 14.93 P=0.053

mDTC PP bim 16.51 ± 16.37 11.57 ± 22.13 ns

mDTC= (mean of the motor DTC and the cognitive DTC)

- 18 -

Table 5. A comparison of the mean DTC between the different tasks

mDTC BBT

(16.92 ± 16.82)

mDTC PP bim

(13.71 ± 19.47)

mDTC HGS

(11.19 ± 18.77)

mDTC PP uni

(8.82 ± 18.11)

mDTC FT

(5.90 ± 21.05)

mDTC BBT

(16.92 ± 16.82)

- ns Ns p

- 19 -

Figure 1. Plots of the different motor DTC combined with the cognitive DTC for the five motor

tasks. The mean DTC for each group is shown by a colored line .

- 20 -

D ISCUSSION

The aim of this study was to explore whether there is a difference between PwMS and

healthy controls in performing a motor task combined with a cognitive task, whereby

PwMS without marked upper limb dysfunction were included. We found a cognitive-

motor interference occurred for the executed tasks, independent of the group to which

one belonged. A decline of the performance of one single task while performing two

simultaneous tasks is confirmed by previous research of the CMI in PwMS during

walking (Motl et al., 2014; Leone et al., 2015; Hamilton et al., 2009; Sosnoff et al.,

2011; Wajda & Sosnoff, 2015; Learmonth, Pilutti, & Motl, 2015). Except the research

of Learmonth et al. all studies had applied the dual-task paradigm consisted by tasks

related to the lower limb and walking. Learmonth et al., who conceptualized the dual

task paradigm by using a cognitive task combined with the NHPT, had a DTC for the

PwMS of 20%. These findings are similar with our results, i.e. 17% on the motor DTC

of the Purdue Pegboard unilateral (cf table3). This Purdue Pegboard test for 30 seconds

combined with a cognitive task was also used to explore the dual task paradigm in

Parkinson diseases. Without calculating a specific DTC, they also reached the same

conclusion, i.e. there is a CMI when single and combined condition are compared to

each other (Proud & Morris, 2010). In comparison to our research, Learmonth & Proud

conducted only one dexterity motor task. Each motor task showed a DTC. The result of

this research seems to contribute to the idea that CMI wasn’t present at specific tasks of

the lower limb, but possibly generalized to a larger spectrum of different functions.

In our study we had expected that PwMS would show a greater dual-task interference

compared with healthy controls. Nevertheless, we didn’t found a difference in DTC

between PwMS and healthy controls. A discrepancy in the decrement of the DTC in

PwMS during walking was found in studies of Kalron et al. and Hamilton et al. (Kalron

et al., 2010; Hamilton et al., 2009). Important to note is that in the research of Kalron et

al. a DTC was not calculated and insufficient information about the interference

calculation was given. Similar to this study he selected persons with a low degree of

disability. Although they performed already lower on the single task performance, it is

reasonable to expect a lower performance on the dual task. A DTC is needed to compare

our results with these findings.

- 21 -

The result of our study could be explained by the methodology, the characteristics of the

recruited group, the different motor tasks and cognitive tasks.

CHARACTERISTICS OF THE RECRUITED GROUP

No power analysis has been made in order to estimate an adequate group size. The

absence of research in cognitive- motor interference during dual tasking, specific for

movements of the upper limb, made it not possible to have a reliable effect size. The

study must be seen as a pilot study.

We saw that both groups had no differences in the cognitive performance. So the

outcomes of the Trail Making Test and the SDMT were similar for the PwMS. This

indicated no remarkable cognitive dysfunction for the PwMS. For the motor

functioning, the performance of the NHPT < 18 seconds for the dominant hand

indicated no major upper limb dysfunction. However, the PwMS perceived more

difficulties with the upper limb in their daily life. The outcomes of the motor and

cognitive functions were reflected in the execution of the single motor and cognitive

tasks of the experimental procedure.

According to current literature there is no significant relationship between dual-task

decrement and measures of disease severity (Allali, Laidet, Assal, Armand, & Lalive,

2014; D’Esposito et al., 1996; Hamilton et al., 2009). However, the results of Sosnoff et

al. cannot be refuted or supported (Sosnoff et al., 2011). Sosnoff et al., who examined

the DTC while walking in PwMS with mild, moderate and severe disabilities, found a

difference in the DTC between these three groups of PwMS. In our study only patients

with a mild disability level (mean EDSS of 2.3) were included, so a comparison

between different degrees of disabilities was not possible. We can only conclude that

there was no worse decline in the DTC for the PwMS in a mild stage of the disease

stage.

While the degree of disability (cf EDSS) and the execution of the single motor task are

almost parallel, it is probably more important to look to the performance of the single

task. PwMS scored significantly worse than healthy controls on the performance of the

single motor tasks, which probably is translated to a reduced performance in the dual

task condition. This is confirmed in persons with Parkinson Diseases, specifically

- 22 -

according to Strouwen et al. who stated that the single tasks performance is the

strongest determinant for the dual task ability (Strouwen, 2015). If we make the

analyses based on the capacity sharing model, it would indicate that a final decrement of

the DTC should have been expected, because the motor and cognitive tasks must

compete for resources. Although unexpected, a poorer performance for the DTC was

not observed. Learmonth et al. confirmed this. A poor motor performance doesn’t lead

to a greater DTC. She investigated the cognitive- motor interference by a cognitive task

combined with the NHPT in three different disabled groups of PwMS. She found that an

increase of the disability in PwMS led to a worse performance on the NHPT, but no

increased DTC was found for the severe group of PwMS compared with the mild or

moderated group (Learmonth et al., 2015). Therefore, the capacity sharing model can

not entirely explain why we didn’t found an increased DTC in PwMS compared to

healthy controls. Apparently, the isolated physical status gives no explanation for the

CMI. A possible answer can be found in the multiple resources theory. Specifically, in

spite of a weaker performance on the single tasks by the PwMS, they experienced the

dual task as an easy task and could therefore execute them as good as automatically in

our study. Presumably, some of the chosen tasks were not complex enough to

discriminate. Certainly not for the finger tapping task, which is also reflected by the low

mean DTC FT of 5.9%. Wickens explained that the dual tasks were done in the

“residual capacity” region. Only if an overload is forced by complex tasks, the

performance during dual tasking will fail (Wickens, 2008). There may exist a “residual

capacity”, which is unused in task performance, whereby the reduced dual task

performance was not visible. Despite the fact that D’Esposito and colleagues reported

no relation between the DTC and the disease duration or EDSS score (D'Esposito et al.,

1996), it is expected that the DTC would increase as EDSS severity or upper limb

dysfunction increases further, based on the multiple resources theory.

CHARACTERISTICS OF THE TASKS

The duration of each task was thirty seconds. This might have not been long enough to

establish discriminatory differences between the two subgroups. However, this was a

deliberate choice. On the one hand, by keeping the duration fixed, it was possible to

easily compare the different tasks with each other. On the other hand, although no

correlation has been found between fatigue and DTC (Motl et al., 2014), a different

- 23 -

execution in the single task performance of the sustained hand grip was seen for the

PwMS. Severijns et al. showed a difference in motor fatigability between healthy

controls and PwMS after thirty seconds (Severijns, Lamers, Kerkhofs, & Feys, 2015).

Executing tasks longer by excluding the force grip task could have been more

appropriate to detect differences between PwMS and healthy controls.

Formulating comments on the cognitive task depends strongly on the theoretical model

which is used. Based on the bottleneck theory no DTC could be expected for this

research. It seemed that the neural pathways required for word generation did not

overlap with the motor task of the upper limb. Based on the capacity sharing theory it

was assumable that there were shared complex neural pathways connecting with

different brain regions interlinked with each other. This is effectively showed by MRI

of healthy persons, where the overlapping dual-task situation was compared with the

execution of the single task. An activation in the prefrontal, temporal, parietal, and

occipital cortices was detected (Schubert & Szameitat, 2003). In contrast with the

comments that were given at the section of the characteristics of the recruited group, the

capacity sharing theory gives now a clear explanation. Furthermore, a systematic review

of Al-Yahya et al., concerning CMI in older adults, neurological disorders and healthy

controls during walking, determined a lack of standardization in the dual-task paradigm

for the cognitive task. A great variety of the concurrent cognitive task is seen. Al-Yahya

et al. added that the domain and difficulty level of the cognitive tasks may have an

impact on DT effects during walking. They concluded that cognitive tasks involving

internal interfering factors (e.g. verbal fluency) seem to disturb motor performance

more than tasks based on external interfering factors (e.g. reaction time) (Al-Yahya et

al., 2011). It is assumable that the phonemic word list generation task was not

comprehensive enough to explain the entire cognitive- motor interference paradigm,

because of a low degree of systematic evidence for the cognitive task. It is likely that

the cognitive component is multidimensional and in order to obtain conclusive

information it would be better to select diverse tasks based on different categories of

cognition.

- 24 -

PRIORITIZATION

In this research no task prioritization instructions were given. It allowed persons to

instinctively select which task to prioritize. This seems to match more with situations in

everyday life. Regarding these prioritization, figure 1 shows that both groups made the

same choice in prioritization. Both prioritized the cognitive task over the motor tasks for

the upper limb, exceptionally for the Purdue Pegboard. The motor DTC was

consistently larger than the cognitive DTC. These prioritization could be explained by

both theories. The bottleneck theory argues that a delay on a task is caused by a central

bottleneck. According to Ruthruff et al. it could be a structural limitation, a strategy or

an instruction by the researcher (Ruthruff, Pashler, & Klaasen, 2001). On the other hand

a decline could be explained by the capacity sharing model. A restricted central

processing capacity permitted to do only one task at a time. This delay or decline is also

consistent with the outcomes of table 3 and 5. As illustrated in table 5, the mean DTC of

the box and block test was the highest. In table 3 it is seen that this decline is mainly on

the motor section and hardly noticeable on the cognitive part. This conclusion was also

made by Allali et al. In the four different cognitive tasks that he offered while walking,

the PwMS prioritized consistently the cognitive tasks (Allali et al., 2014). It was

uttermost striking that the same prioritization in the Purdue Pegboard bimanual was not

observed. In the Purdue Pegboard bimanual a prioritization of motor task was seen over

the cognitive task. This means that a greater increase in the DTC of the cognitive task

was seen in comparison with a lower increase for the motor task. This could be

explained due to the complexity of the Purdue Pegboard bimanual test. It seems like this

motor task itself requires more attention. This is contrary to an easy task such as the

finger tapping, where even an improvement for the cognitive task was seen in the

combined condition.

In general the literature shows no consistency in the way people prioritize. In order to

make an overall conclusion regarding the choice in prioritization, there are too few

studies and a too great variability in the types of tasks which are measured (Plummer et

al., 2013). Plummer et al. states that pattern of the CMI likely depends on several

factors, including the types of tasks, levels of difficulty, instructions to prioritize, the

characteristics of the persons… Although the analysis of Plummer was made for the

CMI in stroke patients, it is assumable to conclude this also for PwMS.

- 25 -

RECOMMENDATIONS AND IMPLICATIONS FOR FUTURE RESEARCH

The paradigm of the cognitive- motor interference in general in PwMS is a field that is

not entirely unraveled. It is our opinion that further research should be twofold.

On the one hand, the theoretical frameworks where the methodology is based on, should

be further explored with a more broad variety of tasks that are used to explore the

theories. This would generate a solid basis, which better reflects the everyday life.

Previous research was mainly focused on the cognitive- motor interference while

walking, however, it is important to investigate a larger range of characteristics and

tasks to generalize this phenomenon.

On the other hand, attention must go to specific outcome variables. In view of rigorous

methodology to measure the dual task performance the dual tasks in this research were

conceptualized and reduced in five single motor outcome variables. However, it is clear

that there are more components which influence the execution of the tasks, like postural

control (Boes, Sosnoff, Socie, Pula, & Motl, 2012), reaction time, the variability of

speed during execution… Reducing the executed tasks to only five outcome variables

could be too simple. Recognizing the complexity of the motor skills like a

multidimensional construct, may require extended variances to enable multiple

outcomes for possible further analysis. Using accelerometers for the trunk and for the

arm could be very interesting, just like measuring the reaction time on several cognitive

tasks.

As an important aspect to mention and also like cited above, it appears appropriate to

perform the tasks longer. It may have an effect on the fatigue in PwMS, but on the other

hand this can be a more accurate reflection of the tasks of daily living. This concerns

daily activities such as typing a report at a meeting, making a meal, ironing while

watching television… Eventually, a clear construct of the CMI must be achieved, to

reach the ultimate goal: Provide more targeted interventions, which are based on DTC

assessment. Assessing the DTC could lead us to a more complete and comprehensive

method for detecting effects in daily life. Therapists can take this paradigm into their

therapy by training or compensations. Research of Yogev-Seligman et al and of Kim et

al. about interventional studies suggested the effectiveness of DT training in walking.

The motor and cognitive outcome variables in DT training were better, compared to a

- 26 -

single motor training (Yogev-Seligman, Giladi, Brozgol, & Hausdorff, 2012; Kim, Han,

& Lee, 2014). On the other hand, recent research of Strouwen et al. shows no

differences between consecutive task training and integrated task training. They

suggested that improved DT performance could be explained by an improvement of

carrying out instinctive tasks automatically. However, these studies were only

conducted in other neurological diseases, like Parkinson disease and stroke. Therefore,

it is important to further investigate this unexplored area. As the theory about dual task

paradigm is still underdeveloped, the methodology for future research must be

considered carefully.

CONCLUSION

The current study investigated the differences between PwMS and healthy controls

when performing a motor task of the upper limb combined with a cognitive task. A

cognitive- motor interference was found for tasks performed in single vs. dual

condition, but no differences were found between PwMs and healthy controls in the

dual task cost. The study was executed in PwMS who were functioning on a high level

of performance in the upper limb and in cognition. It is expected that the proper

functioning of these two functions explains why no differences were found between

PwMS and healthy controls in the dual task cost of any different motor task. However,

there is a discrepancy in the DTC for the various motor tasks independent of a specific

group. Depending on the degree of difficulty of the motor task a different prioritization

was given.

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ANNEX 1: THE DIFFERENT MOTOR TASKS

The finger tapping task

The hand grip strength task

The box and Block test

The Purdue Pegboard

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ANNEX 2: TOELATING TOT CONSULTATIE VAN DE MASTERPROEF

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