Bimanual Simultaneous Motor Performance and Impaired Ability to Shift Attention in Parkinson's Disease

Journal ofNeurology, Neurosurgery, and Psychiatry 1990;53:685-690 685 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.8.685 on 1 August 1990. Downloaded from Bimanual simultaneous motor performance and impaired ability to shift attention in Parkinson's disease

M W I M Horstink, H J C Berger, K P M van Spaendonck, J H L van den Bercken, A R Cools

Abstract sharing time and shifting attention. To our The ability to share time and to shift knowledge, time-sharing during repetitive attention between bimanual simultan- simultaneous movements has not been studied eous motor tasks were studied in 18 in PD. As far as the ability to shift attention is patients with Parkinson's disease (PD) concerned, several authors reported that PD and 19 age- and intelligence-matched patients have problems with shifting set;7 11-19 controls. The task consisted of drawing set being defined as a process of focussed and triangles with the dominant hand and sustained attention predisposing a subject to squeezing a rubber bulb with the non- respond in one way when several alternatives dominant hand. Motor performance was are available.718 Such shifting deficiency is measured using the variables: amplitude associated with hypofunctioning of the of squeezing, frequency of squeezing and dopaminergic system." velocity of drawing triangles. After In this study, a simplified test of Schwab eliminating variance due to baseline et aP9 was used to evaluate both time sharing differences in single-handed perfor- and shifting attention. The dominant hand mance, the bimanual simultaneous per- drew triangles, while the non-dominant hand formance of PD and controls turned out at the same time repeatedly squeezed a rubber to be similar to the frequency of squeez- bulb. Drawing fixed triangles is strongly ing and the velocity of drawing triangles. determined by external cues, while squeezing The amplitude of squeezing, however, of a rubber bulb almost entirely depends on differed between the two groups: it was internal control. We therefore expected that significantly reduced in PD. Arguably squeezing in PD patients would be more the disturbance in the bimanual perfor- impaired than drawing triangles, since PD mance of PD patients was not due to a patients are impaired when they have to rely disorder of time sharing, but to a upon internal control for regulating attention, decreased ability to shift attention from but are relatively unimpaired when external the visually cued task to the non visually cues or guidance are given.6 19 21 cued task. The results agree with current evidence that PD patients are more

impaired when they have to rely upon Subjects http://jnnp.bmj.com/ internal control for the regulation of Eighteen patients with idiopathic PD (without shifting attention than when external thalamotomy) and nineteen controls were cues are available. studied. All patients regularly attended the outpatient department of movement disorders and gave their informed consent. The patients Temporal and spatial processing is involved in had been clinically stable for at least one the simultaneous performance of two separate month before the examination. Relevant data on September 30, 2021 by guest. Protected copyright. University of single-handed tasks. The timing of bimanual and disease factors are summarised in table 1. Nijmegen, Nijmegen, simultaneous tasks is a function of one gen- PD patients and controls were well matched The Netherlands Department of eralised time-programme,'-5 a phenomenon for age, intelligence and attention. Five sub- Neurology also referred to as time-sharing.4 The spatial tests of the WAIS were used to assess M W I M Horstink performance of both tasks is executed by two intelligence (score (SD)): Vocabulary (PD: Department of separate concurrently running motor- 36-12 (9 74); controls: 41-05 (9 02)), Medical Psychology programmes that are controlled by shifting Similarities (PD: 16-33 (5-34); controls: 17-47 H J C Berger one to K P M van Spaendonck attention from task the other.46 (4-17)), Picture Completion (PD: 1050 (3 09); Department of Special Patients with Parkinson's disease (PD) are controls: 11-37 (3-51)), Block Design (PD: Education known to have much more difficulty than 10-67 (4 43); controls: 12-16 (5-19)) and Digit J H L van den Bercken controls when simultaneously performing two Span (PD: 11-78 (2 73); controls: 12 32 Department of separate single-handed tasks, even though (3-84)). Deficits in attention were assessed Pharmacology they can perform each of these tasks with the Stroop Colour Word Test by sub- R A Cools separately."'0 Their performance turns out to tracting the duration of Stroop Colour Word Correspondence to: Dr M W (PD: I M Horstink, Department be task dependent: separate single movements Test-2 from that of the Stroop Test-322 23 of Neurology, University are executed simultaneously in PD,610 but 58-83 (20 70); controls: 49-32 (17-00)). The Hospital, PO Box 9101, 6500 means were not HB Nijmegen, The repetitive movements sequentially.9 PD differences between the group Netherlands. patients are apparently disabled when simul- significant (MANOVA, SPSSX: F = 0-85, df Received 23 September 1988 taneous repetitive movements are involved. - 6 and 30; p > 0-05). Depression was and in final revised form 7 and November 1989. Correct performance of such repetitive simul- excluded by clinical examination Accepted 11 December 1989 taneous tasks depends on the capability of enquiries among family members. 686 Horstink, Berger, van Spaendonck, van den Bercken, Cools J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.8.685 on 1 August 1990. Downloaded from Table 1 Demographic data and diseasefactors in Parkinson's disease (PD) Webster Hypokin Levodopa Antichol Pat Age PD R L R L H-Y nr yrs yrs yrs mg/d yrs mgld arm arm arm arm stage 1 63 5 5 025 400' 45 i4 2 5 1 2 3 2 66 3 0 - * 25 1503 4 4 2 2 3 3 70 40 - - - - 3 2 1 1 1 4 69 1 5 025 400' - - 6 2 2 1 2 5 67 4 5 - * 25 1503 2 3 1 1 3 6 71 60 1-5 400' - - 4 3 1 1 2 7 47 5s0 - * 25 1503 1 1 1 1 1 8 50 6 5 2.0 300' 2 5 1503 2 2 1 1 2 9 51 5 0 - * 2-5 1503 6 2 2 1 2 10 59 1.5 - * 15 2003 5 5 2 2 2 11 41 55 - - - - 3 4 1 1 2 12 47 6 5 5 5 16002 - - 3 4 2 2 3 13 58 7-5 5 0 400' 6-5 150' 7 3 3 1 3 14 70 14 5 6 0 32002 13 0 3003 5 4 2 2 3 15 63 50 30 200' - - 5 7 2 2 3 16 67 4 0 3 0 200' 3-5 14 2 7 1 2 2 17 68 11.5 6-0 35002 90 45 5 7 2 2 4 18 64 7 0 5 0 600' 6 0 1503 2 2 1 1 1 mean 608 58 33 3-7 3-7 15 14 23 SD 9-3 3-1 2 3 16 1-8 0-6 0 5 0-8 Abbreviations: Webster: sum of tremor, hypokinesia and rigidity scores of upper extremity according to Webster rating scale. Hypokin: Webster hypokinesia score of the upper extremity. R: right side, L: left side. H-Y: Hoehn-Yahr scale. mg/d: mg/day; antichol: anticholinergics. 1 Levodopa plus decarboxylase inhibitor; ': levodopa; 3: orphenadrine-HCI; 4: dexetimide; ': benzatropine; *: amantadine 200 mg.

Methods with only the experimenter present. The Single-handed performance was assessed by experimenter first demonstrated the standard means of two tasks: squeezing with the non- procedure, after which the subjects practised dominant hand (Sq) and drawing triangles each test twice, each trial lasting about lOs. with the dominant hand (Tr). Bimanual This appeared to be sufficient for familiarising simultaneous performance was assessed by them with the technical equipment. There two tests: simultaneously squeezing and draw- was a 60s break between the performances. ing triangles (Sq + Tr) and simultaneously Characteristic performance by controls and squeezing and writing the letter e (Sq+ee). PD patients are shown in figs 1A, B. The single-handed and the bimanual tests lasted 15s each. Design and data analysis The tests were administered in the follow- The following three variables were studied: 1) ing constant order: 1 Squeezing with non- Amplitude of Sq, that is, mean excursion of dominant hand (Sq): subjects were instructed the recording pen in cm. 2) Frequency of Sq, as 5s. to squeeze the bulb repeatedly and quickly that is, number of squeezes per 3) Velocity http://jnnp.bmj.com/ as possible by fully opening and closing the of drawing triangles, that is, trajectory of the hand. This task served as the baseline squeez- recording pen in cm/5s. The recordings did ing performance. not allow for accurate measurements of the 2 Drawing triangles with dominant hand velocity of writing the lower case e's. Perfor- (Tr): subjects were instructed to connect mance during each test was analysed from the without interruption, and as quickly as possi- first recorded movement and not from the ble, the fixed angle points of a triangle with 9 moment at which subjects were instructed to cm sides. This task served as the baseline start. on September 30, 2021 by guest. Protected copyright. triangle performance. The data were collected according to a 3 Sq and Tr simultaneously (Sq + Tr): design, in which we focussed on differences subjects squeezed (Sq) with the non-dominant between PD patients and controls for biman- hand while the dominant hand simultaneously ual simultaneous motor performance. By con- drew triangles (Tr). trasting bimanual with single-handed perfor- 4 Sq and ee simultaneously (Sq + ee): to mance confounding baseline differences in ensure that a decrease in performance was not single-handed performance were eliminated. due to the complexity of the tasks, subjects In our paradigm there was one between- also performed a simpler test (Bloxham subjects factor with two levels: controls and et aP4). In this test the dominant hand wrote a PD. Motor performance was a within-subjects series of lower case e's while the non-domin- factor also with two levels: single-handed per- ant hand was squeezing. formance and bimanual simultaneous perfor- All ergograms were recorded with an electr- mance. The analysis of variance of the result- owriter which transformed the two-dimen- ing repeated measures design was based on a sional movements of the dominant hand into multivariate approach in which bimanual per- the one-dimensional movements of the recor- formance was compared with single-handed ding pen. The recorded distance was propor- performance by means of difference scores.25 tional to the actual performance. Only a min- Since motor performance was measured by a imal effort was required for squeezing the number of variables, there were several bulb. Subjects were seated in a quiet room difference scores for the contrast of single- Bimanual simultaneous motor performance and impaired ability to shift attention in Parkinson's disease 687

handed and bimanual performance. Both mul- J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.8.685 on 1 August 1990. Downloaded from g tivariate and univariate statistics are reported. \ \ Pearson correlation coefficients were used to assess the correlations between the variables of motor performance. The analysis was performed by the SPSSX procedure MAN- ~ee OVA.26

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Results Correlations between amplitude of Sq,frequency of Sq and velocity of Tr. Performance Sq was measured with two variables: amplitude and frequency. During single- handed Sq these variables were not significan- I'll tly correlated in PD (r = 0-13, p > 0-05). In controls the amplitude of Sq was inversely proportional to the frequency of Sq (r = -046, p < 0105). In the Sq+ee and Sq+Tr |'nC- tests, there was no correlation between 'IlS __ _ amplitude and frequency of Sq in either PD r = 0 > :? (Sq+ee: 37, p 0-05; Sq+Tr; r =

.. i. .. -. .. ;.- -- i. ...-.... - -- -0-25, p > 0-05) or controls (Sq+ee: r = -0-25, p > 0-05; Sq+Tr: r = -0-38, p > 0105). In both groups the amplitudes of Sq in Sq + ee and Sq + Tr were correlated (PD: r = 0179, p < 01001; controls: r = 0 59, p < 0-01). The same held true for the frequencies of Sq in Sq+ee and Sq+Tr (PD: r = 049, p < 0105; controls: r = 0-85, p < 0-001). In Sq+Tr velocity of Tr correlated with frequency of Sq in both PD (r = 0A43, p < 0105) and controls (r = 0173, p < 0-001). There was no correlation T I eee between the amplitude of Sq and the velocity of |- 'I an3i nlsb Tr in either group. (PD: r = 0-16, p > 0105; controls: r = -0-22, p > 0105). Single-handed performance The results of single-handed performance in PD and controls are shown in table 2. Both groups differed significantly as shown by a multivariate test (Wilks' Lambda = 0-31, F = http://jnnp.bmj.com/ SqueezinE. 11, df = 3 and 33, p < 01001). During single- handed Sq the amplitude of Sq in PD equalled IL 90% of the amplitude of Sq in controls (F = 4 90, df = 1 and 35, p < 0105). The difference in frequency of Sq was greater: frequency of Sq 5s in PD equalled 62% of the frequency found in

controls (F = 17T27, df = 1 and 35, p < 01001). on September 30, 2021 by guest. Protected copyright. * ' ' ;. ; r/ ;, Finally, the difference in the velocity of drawing Tr was most striking: velocity in PD only equalled 51% of that displayed by the controls (F = 20-80, df = 1 and 35, p < 0-001). Bimanual simultaneous performance of PD patients versus controls Bimanual simultaneous performance of PD patients was compared with that of controls (table 2, fig 2). Our main interest was in differences in bimanual motor performance over and above differences in baseline performance. This was achieved by using difference scores between variables of single-handed and bimanual performance as dependent variables in the analysis of variance (see design and data analysis). The Figure 2 Mean and SD of amplitude of squeezing (Sq),frequency of Sq and velocity data are shown in table 3. PD patients and of drawing triangles (Tr) during single-handed (SHMP) and bimanual simultaneous motor performance (BSMP) in patients with Parkinson's disease (PD) and controls appeared to differ significantly for the controls (CS). set of difference scores as a whole (Wilks' 688 Horstink, Berger, van Spaendonck, van den Bercken, Cools

Table 2 Motor performance of PD patients and controls in single-handed and opinion, the latter differences also reflected J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.8.685 on 1 August 1990. Downloaded from bimanual simultaneous tasks well-known difficulties in executing a motor P ofF plan in PD.2>3 Task Variable CS mean (SD) PD mean (SD) PD vs CS Bimanual simultaneous performance Single-handed: Sq ampl Sq (cm/5s) 9-9 (0 2) 8-9 (1 9) <0-05 Controls usually cannot perform two tasks Sq freq Sq (n/5s) 7-3 (2-4) 4-5 (1 4) <0-001 together as well as they can separately because Tr vel Tr (cm/5s) 38-5 (10-4) 19 8 (9 3) <0-001 the tasks may interfere with each other.4 Given Bimanual simultaneous: Sq + Tr ampl Sq (cm/5s) 9-6 (0 6) 6-1(3-3) * previous reports on impaired bimanual simul- Sq + Tr freq Sq (n/5s) 6 7 (2 2) 3 3 (1-2) * taneous performance in PD,`'0 it is most strik- Sq + Tr vel Tr (cm/5s) 33-4 (10-3) 15 6 (8-0) * Sq + ee ampl Sq (cm/5s) 8-5 (1 2) 4-9 (2 5) * ing that PD patients in Sq + ee and in Sq + Tr Sq + ee freq Sq (n/5s) 7-5 (2 0) 4-8 (1-9) * showed the same changes in the frequencies of Sq as controls. The same is true for the velocity Abbreviations: PD: Parkinson's disease; CS: controls; Sq: squeezing; Tr: drawing triangles; ee: writing e's; ampl: amplitude; freq: frequency; vel: velocity. *See table 3. of Tr in Sq + Tr. In PD patients only the reduction in the amplitude of Sq exceeded the range of interference in controls, both in Table 3 Difference scores between single-handed and bimanual simultaneous Sq + ee and in Sq + Tr (table 3, fig 2). performance of PD patients versus controls Our model comprises the concepts of a Pof F generalised time-programme and of separate Task Variable CS mean (SD) PD mean (SD) PD vs CS concurrently running motor-programmes. are charac- Sq vs Sq + Tr ampl Sq (cm/5s) -0 3 (0-6) -2-8 (2-5) <0-05 Bilaterally generalised programmes Sq vs Sq + Tr freq Sq (n/5s) -0-6 (1-3) -1 2 (1 4) ns terised by an invariant interlimb ratio of the Sq vs Sq + Tr vel Tr (cm/5s) -51 (9 9) -4 2 (7 3) ns On the contrary, if a Sq vs Sq + ee ampl Sq (cm/5s) -1 4 (1 2) -4 0 (2-1) <0-001 pertinent variable.634 Sq vs Sq + ee freq Sq (n/5s) 0 2 (1 7) 0 3 (1-8) ns variable has a variant interlimb ratio, then the pertinent aspect of movement is supposedly Legends: see table 2. executed by separate concurrent programmes.634 In the latter case, performance depends Lambda = 0 53,F = 6-97,df = 5and31,p < on the ability to shift attention from one task to 0-001). The univariate statistics revealed that the other while carrying them out.4 In both the effect resided in a reduction of the groups the frequency of Tr in Sq + Tr (the amplitude of Sq: this reduction was much frequency which with sides were drawn being greater in PD patients than in controls, both in naturally proportional to the velocity of Tr) Sq+Tr (F = 21-34, df = I and 35, p < 0-001) correlated with the frequency of simultaneous and in Sq+ ee (F =5 95, df = 1 and 35, p < Sq. This may indicate an intrasubject invariant 005). The difference scores of the frequencies interlimb ratio and, hence, a generalised time- of Sq and the velocities of Tr did not differ programme. On the other hand, since the significantly between patients and controls. In correlation existed between subjects this might both groups the frequency of Sq in Sq+ee have reflected that the frequency with which tended to increase with respect to single-han- individuals simultaneously performed ded squeezing (fig 2). Although this phen- squeezes and triangles depended on whether omenon did not show statistical significance, it they were fast or slow types, irrespective of remained remarkable because it was present in interlimb linkage. The fact that the ratio of the http://jnnp.bmj.com/ both groups. frequency of Sq to the frequency of drawing sides ofTr (that is, velocity ofTr) did not differ Discussion significantly between PD ( =4 7) and controls Single-handed performance (=4 9) suggested task specific invariant As the main purpose of this study was to focus interlimb linkage. Moreover, the frequency of on bimanual performance, we will not give a Sq varied with the type of task carried out by lengthy discussion on single-handed perfor- the dominant hand in both groups: frequency

mance. The PD patients clearly had hypokin- of Sq tended to increase in Sq + ee and on September 30, 2021 by guest. Protected copyright. esia, showing a significantly lower frequency decreased in Sq + Tr. Apparently, in both PD and amplitude of Sq than controls (table 2). In and controls the type of task of the dominant other patients with extreme hypokinesia, hand determined the pace of Sq. These results curves of comparable bulb ergograms showed not only suggest that both groups adapted the fatigue,27 which is defined as gradually decreas- timing of the one hand to the other, but also ing amplitude with successive movements.27 28 that both groups adapted it in the same way, However, in our patients fatigue did not play a indicating that PD patients constructed a gen- major role: random variations in amplitude eralised time-programme as controls sup- were much more striking than successive drops posedly do.'-5 in amplitude (fig 1). The relatively low levels of Such a bilaterally generalised time- disability in our PD patients could be one programme in Sq + Tr indicates that Sq and Tr explanation for our results (table 1). The PD were executed simultaneously in PD. In fact, patients also showed bradykinesia, as manifes- most of our patients drew continuously: their ted by a reduced velocity in their single-handed ergograms of ee and Tr showed hardly any Tr. When the variables of single-handed gaps. Gaps would be obvious if the bimanual movements are considered, the velocity of tasks were executed sequentially in Sq + ee and movement was most profoundly affected in Sq + Tr. This observation is contrary to those PD. There were not only clear differences of Schwab et aP that PD patients do not between PD and controls in the means of the perform repetitive movements simultaneously, variables, but also in the variances. In our but sequentially. However, it must be noted Bimanual simultaneous motor performance and impaired ability to shift attention in Parkinson's disease 689 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.8.685 on 1 August 1990. Downloaded from that our drawing test was less difficult than the that of the patients and controls, the greater one used by Schwab et al; the instruction to part of squeezing resulted from isotonic muscle draw perpendicular lines in the triangle being contraction. But, what is more important, the omitted. Their observations probably hold true main purpose of this study was to evaluate the for more complex tasks. ability to shift attention between two simultan- During bimanual simultaneous perfor- eous motor tasks. The question of whether the mance, the frequency and the amplitude of Sq amplitude of Sq represented spatial perfor- did not correlate in either group. This indicates mance or force did not influence our con- that these variables represented independent clusions in that respect: in both cases an processes. The observation that in controls impairment of shifting of attention will both variables were negatively correlated dur- produce a lower amplitude of Sq. ing single-handed Sq only indicates that time The deficit in bimanual simultaneous perfor- constraints did induce mutual dependency.5 mance in Sq + Tr did not correspond to the These results agree with our frame ofreference complexity of the task: the amplitude of Sq in that both variables corresponded to distinct Sq + ee was also affected (fig 2) despite the fact processes in the brain, that is, frequency corre- that PD patients performed ee more easily than sponded to time-sharing and amplitude to Tr (Bloxham et al 24). Nor could simple spatial performance. fatigue27 account for this impairment. Iffatigue In Sq + Tr the amplitude of Sq did not played a prominent role in the performance of correlate with the spatial performance of Tr: the bimanual tasks, the velocity of Tr would although all subjects did in fact draw Tr also be affected. Certainly, the velocity of Tr accurately according to the fixed scheme, was reduced in Sq + Tr in PD patients, but amplitudes of Sq varied clearly (table 2, fig 2). only to the same degree as seen in controls This variant interlimb ratio agrees with the (table 3, fig 2). conclusions of Keele5 and Poulton4 that the We conclude that in PD the disturbance of spatial performances of separate bimanual bimanual simultaneous performance of the simultaneous tasks are not executed by one present tasks was not due to a decreased ability generalised motor programme, but by two to share time between the two tasks. The deficit concurrent motor programmes. Correct per- in bimanual simultaneous performance was, formance of such concurrent motor program- however, apparently caused by the fact that PD mes relies on the ability to shift attention patients were unable to shift their attention between both tasks.46 Because in both Sq + ee sufficiently from one of the simultaneous tasks and in Sq + Tr the reduction in the amplitude to the other. These experiments yield further of Sq was significantly greater in PD than in evidence that PD patients are more impaired in controls, we conclude that the PD patients had the regulation oftheir attention when they have a diminished capacity to shift their attention to to rely upon internal control than when exter- Sq. nal visual cues or guidance are available. The question remains as to why there was no significant difference between PD and controls in the reduction of velocity of Tr during Sq + Tr, compared with single-handed Tr 1 Peters M. Simultaneous performance of two motor activities: the factor of timing. Neuropsychol 1977;15: (table 3, fig 2). PD patients apparently concen- 461-4. http://jnnp.bmj.com/ trated on Tr and did not shift attention to Sq, 2 Kelso JAS, Southard DL, Goodman D. On the coordination oftwo-handed movements. J Exp Psychol 1979;5:229-38. presumably because visual cues or guidance, as 3 Klapp ST. Doing two things at once: the role of temporal present in Tr, take priority over non-visual, compatibility. Memory and Cognition 1979;7:375-81. 4 Poulton EC. Human Manual Control. In: Brookhart JM, that is, sensory ones, as present in Sq.4"5 Such a Mountcastle VB, Geiger SR, eds. Handbook ofPhysiology, procedure yields further evidence that PD section I The Nervous System vol II, part 2. Bethesda: American Physiological Society 1981:1337-90. patients depend on external cues or guidance to 5 Keele SW. Behavioral analysis of movement. 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