Behavioural Brain Research 102 (1999) 115 – 127

Research report

Motor learning by imagery is differentially affected in Parkinson’s and Huntington’s diseases Lidia Ya´gu¨ez a,b,*, Anthony G.M. Canavan a, Herwig W. Lange a, Vo¨lker Ho¨mberg a b

a Neurological Therapy Centre, Uni6ersity of Du¨sseldorf, Dusseldorf, Germany Institute of Psychiatry, Department of Psychology, Uni6ersity of London, London, UK

Received 10 August 1998; received in revised form 21 December 1998; accepted 21 December 1998

Abstract Studies of motor imagery and motor learning have thus far been concerned only with its effects on healthy subjects. Therefore, in order to investigate the possible involvement of the basal ganglia, the effectiveness of motor imagery in the acquisition of motor constants in a graphomotor trajectorial learning task was examined in 11 non-demented mildly affected Huntington’s disease (HD) patients and 12 non-demented Parkinson’s disease (PD) patients. The patients received, after baseline, 10 min of motor imagery training, followed by a motor practice phase. Additionally, a test battery for visual imagery abilities was administered in order to investigate possible relations between visual and motor imagery. The results showed that imagery training alone enabled the HD patients to achieve a significant approach to movement isochrony, whereas the PD patients showed no marked improvements, either with motor imagery or with motor practice. Furthermore, the PD patients had more difficulties than the HD patients in solving the visual imagery tasks. Subsequent correlational analysis revealed significant relationships between the degree of caudate atrophy in the HD patients and their performance in the visual imagery tasks. However, there were no substantial correlations between the performance on the visual imagery tasks and the improvement of motor performance through motor imagery, which indicates that visual and motor imagery are independent processes. It is suggested that the dopaminergic input to the basal ganglia plays an important role in the translation of motor representations into motor performance, whereas the caudate nucleus atrophy of the HD patients does not seem to affect motor imagery, but only the visual imagery process. Furthermore, the deficits found in PD patients might also be related to their limited attentional resources and difficulties in employing predictive motor strategies. © 1999 Elsevier Science B.V. All rights reserved. Keywords: Motor imagery; Motor learning; Parkinson’s disease; Huntington’s disease

1. Introduction There is no general agreement about what exactly motor imagery is, and therefore not about how it can influence motor behaviour. Nevertheless, one particular aspect of motor imagery, which does not cause too much controversy, is that it is a conscious process. That is, motor imagery refers to the capability of imagining

* Corresponding author. Present address: Department of Psychology, Institute of Psychiatry, De Crespigny Park, Denmark Hill, London SE5 8AF, UK. Tel.: +44-171-919-3522; fax: + 44-171-9192473. E-mail address: [email protected] (L. Ya´gu¨ez)

performing a given motor action or motor skill. The debate is as to whether this conscious imagining is directly or indirectly related to the motor process per se. There is ample evidence that during the imagination of movements, the neurophysiological activity that occurs resembles strongly the activity seen during the actual execution of the movement (for example, [6– 8,17,25,29,33,38]). Given these similarities between imagining and executing movements, the next logical step would be to assume that the central changes occurring during motor imagery should also affect subsequent movement performance. Thus far, several studies confirm this assumption (for example, [27,30,37,42,43]).

0166-4328/99/$ - see front matter © 1999 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 6 - 4 3 2 8 ( 9 9 ) 0 0 0 0 5 - 4

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Accepting the view put forward by Jeannerod [19,20] that motor imagery involves motor images, which are indeed conscious motor representations, and as such have the same properties as the corresponding motor representations, i.e. share common neurophysiological substrates, then the question arises as to whether patients with basal ganglia disorders have access to such conscious motor representations. There is indeed at least one experiment with Parkinson’s disease (PD) patients that supports this assumption: Dominey et al. [10] demonstrated similar asymmetries between the affected and non-affected limb in patients with hemiparkinsonism during the execution and the imagination of motor sequences. These results suggest, first, that PD patients are generally able to create conscious motor representations, and second, that these representations share similar neurophysiological substrates with actual motor representations, since they are both similarly affected in PD. Hence, the next question is as to whether imagining a motor task can facilitate the acquisition of invariant features of a motor skill in patients with basal ganglia disorders. Most published reports on motor performance in PD have been concerned with the issue of normality, i.e. whether the performance pattern in patients with PD differs from that of matched normal subjects. However, an important question that arises is one of specificity, i.e. whether the particular pattern of deficits is specific to PD or is also present in other disorders of the basal ganglia [18]. Patients with Huntington’s disease (HD) have not yet been assessed, and yet the selective loss of intrinsic striatal neurones with relatively well preserved nigrostriatal tract and dopaminergic nerve cells in the early stages of the illness [12,15,21,36], offers an excellent chance to study basal ganglia function disruption, without decreased dopaminergic input. Therefore, in order to find out whether or not motor imagery training improves the acquisition of the spatio-temporal characteristics of graphomotor trajectories in patients with basal ganglia disorders, the paradigm described by Ya´gu¨ez et al. [42] was employed in patients with PD and HD. Ya´gu¨ez et al. [42] investigated, in healthy subjects, the effects of motor imagery training upon the acquisition of the spatio-temporal features of a movement skill, namely trajectorial learning, and showed that imagery training alone enabled the subjects to achieve a significant approach to movement isochrony. In contrast, a control group that did not receive the imagery training did not show this effect. Thus, the present study can be regarded as a sequel of the previous experiment with healthy subjects reported by Ya´gu¨ez et al. [42] The invariance of movement time over differing movement amplitudes is a typical feature of certain automatic voluntary movements, especially handwriting [13]. This isochrony principle [40] is a useful criterion to establish whether a motor skill, such

as ideogram drawing, has been learned, and is already approaching the automatised level. Isochrony is achieved by systematically scaling up movement velocity in relation to the required amplitude of the movement. Isochrony, or the tendency towards isochrony, was employed in the present experiment, as in Ref. [42], to determine whether or not a certain level of motor learning could be achieved by motor imagery. In addition, the effect of the combination of previous mental training with physical practice in PD and HD patients was compared. The ability to achieve visual imagery effectively is likely to be a major determinant of motor imagery. Therefore, in order to investigate possible mechanisms involved in the contribution of motor imagery to motor learning, the test battery for visual imagery abilities described in Ref. [42] was also administered to the patients in the present study.

2. Patients and methods

2.1. Patients with HD The HD patient group consisted of 11 non-demented HD patients (six males and five females) with a mean age of 47.6 years (S.D., 10.0; range, 29–68). Three patients were under medication (see Table 1) at the time of the experiment. The years of formal education ranged from 8 to 13 (mean, 10.4; S.D., 2.1). Their mean verbal IQ (MWT-B [24]) was 114.5 (S.D., 13.6; range, 93–136). The mean score obtained on the APM-Set I (Raven’s Advanced Progressive Matrices [28]) was 6.9 points (S.D., 2.6; range, 4–11). The HD diagnosis was established for all HD patients by an experienced neurologist (HWL), and a positive family history of HD was documented for all (see Table 1). Quantitative neurological examination was carried out in all HD patients: “ The degree of choreatic movement disorder was assessed with a clinical rating scale [23] (0, without chorea; 1, mild chorea; 2, moderate chorea; 3, severe chorea). “ Functional ratings were obtained with a German adaptation [23] of the Shoulson and Fahn scale [34] for the abilities of the patients in daily tasks. “ Computed tomography (CT) scans were carried out using a CGR ND 8000 Scanner in the University Clinic of Du¨sseldorf. A neuroradiologist, who had no access to the clinical or neuropsychological data, estimated the degree of cortical and subcortical atrophy. The distances between the left and right caudate nuclei (CC) and the inner table of the skull (IT) were measured at the level of the interventricular foramen. The CC/IT was calculated and multiplied by 100, to obtain a percentage value of caudate atrophy. Values

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Table 1 Description of the Huntington’s disease (HD) patient samplea Patient

Age

Gen

Edu

IQ

APM

Han

Dur

Psy

Mot

S&F

HCG

AtC (%)

AtF

AtP

Med

HD1 HD2 HD3 HD4 HD5 HD6 HD7 HD8 HD9 HD10 HD11

38 44 53 54 44 42 68 61 30 43 29

M F M M F F M M M F F

12 8 8 13 10 8 9 10 10 8 13

136 101 100 129 118 104 124 118 101 124 112

11 5 7 10 6 4 7 5 9 6 6

R L R R L R R R R R R

0.5 1.0 1.0 2.0 4.0 5.0 7.0 0.5 1.0 0.5 3.0

8 9 12 5 12 5 8 9 0 3 5

8 5 1 13 4 6 7 1 2 3 4

0.7 1.5 0.7 0.9 0.7 0.4 0.2 0.0 0.0 1.0 0.5

1.0 1.0 1.0 2.0 2.0 1.0 0.5 1.0 0.5 1.5 1.0

12.4 15.6 15.6 18.3 19.4 19.5 14.5 16.5 – 17.6 19.5

1.0 0.5 0.5 0.5 2.0 1.5 1.0 1.0 – 1.0 1.0

0.0 1.0 1.0 1.0 2.0 0.5 1.0 1.0 – 1.5 0.5

2 0 0 1 0 0 0 0 0 0 0

a Gen: gender (M, male; F, female); Edu: years of formal education; IQ: verbal IQ; APM: advanced progressive matrices (scores: B6, ‘dull’; between 6 and 10, ‘average’; \10, ‘bright’); Han: handedness (R, right-handed; L, left-handed); Dur: number of years since diagnosis; Psy: number of years since the first psychiatric symptoms; Mot: number of years since the first motor symptoms; S&F: Shoulson and Fahn (1979) scale of impairment in daily life; HCG: grade of chorea (Lange et al., 1983) (1 = mild; 2 = moderate; 3 =severe chorea); AtC: percentage of caudate atrophy (normal =8–12%; mild atrophy =12–16%; moderate atrophy = 16–20%; severe atrophy: \20%); AtF: measure of frontal cortical atrophy (0 = normal (B2 mm); 1=mild (2–4 mm); 2 = moderate atrophy (4–6 mm); 3 =severe atrophy (\6 mm)); AtP: measure of posterior atrophy (scale as before: degrees 0–3); Med: medication (0 = no medication; 1 = Tiaprid; 2 =Haloperidol).

up to 14 are accepted as normal, between 14 and 16 as suspicious, between 16 and 20 as mild atrophy, between 20 and 24 as moderate atrophy, and higher than 24 as severe caudate atrophy. Cortical atrophy was estimated by measuring the width of the sulci in the frontal and occipito-parietotemporal cortices. The values obtained were set on a scale from 0 to 3: degree 0 includes values lower than 2 mm (no atrophy); degree 1, values between 2 and 4 mm (mild atrophy); degree 2, values between 4 and 6 mm (moderate atrophy); and degree 3 comprised values higher than 6 mm (severe atrophy). For patient number HD9 the results of the CT scans were not available (see Table 1 for a synopsis of the clinical data). The HD patients were recruited from the Huntington support group of the University of Du¨sseldorf and were tested in the Neurological Therapy Centre (NTC) of

Du¨sseldorf University. individually.

All

patients

were

tested

2.2. Patients with PD 12 PD patients, six males and six females, with an average age of 67.0 years (S.D., 10.3; range, 46–82) took part in the experiment. Their average formal education was 9.8 years (S.D., 2.1; range, 8–13). Mean verbal IQ was 103.4 (S.D., 13.1; range, 86–124) and mean APM-Set I score was 6.2 (S.D., 1.2; range, 4–8). Patient number PD3 could not be tested with the MWT-B because he was not fluent enough in German, but could understand and follow the instructions for the other tests without difficulty, and patient number PD1 missed out on the testing with the APM. The duration of the disease since diagnosis ranged from 1 to

Table 2 Description of the Parkinson’s disease (PD) patient samplea Patient

Age

Gen

Edu

IQ

APM

Dur

H&Y

Med

PD1 PD2 PD3 PD4 PD5 PD6 PD7 PD8 PD9 PD10 PD11

56 74 46 82 70 54 75 67 65 68 73

F M M M F F M F M F F

13 10 13 8 8 8 13 8 8 8 10

120 112 – 94 86 101 124 92 95 95 100

– 5 6 6 4 8 6 8 6 7 6

9 2 6 4 6 14 12 5 1 7 2

I I III II III I II I II II II

1, 4 0 0 1, 1, 1, 1 1, 1, 1,

5

3, 9 4, 9 3, 4 6, 7 2, 4 9

a Gen: gender (M, male; F, female); Edu: years of formal education; IQ: verbal IQ; APM: advanced progressive matrices (scores: B6, ‘dull’; between 6 and 10, ‘average’; \10, ‘bright’); Dur: number of years since diagnosis; H&Y: Hoehn & Yahr scale; Med: medication (1= L-dopamine; 2= bromocriptine; 3 = amantadine; 4 = anticholinergic; 5 = deprenyl; 6 = alprazolam (tranquiliser); 7 =amitriptyline (antidepressant); 8 =selegilin (MAO-inhibitor Type B); 9 =coronary medication).

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14 years (mean, 6.0; S.D., 4.0). Medication and stage of severity, according to the Hoehn and Yahr scale [16], are shown in Table 2. Patient number PD3 had had no medication since 21 days before the experiment and patient number PD4 since 14 days before. The PD patients were recruited from the Parkinson self-help group of Wuppertal and from the NTC in Du¨sseldorf. The PD patients were tested at the NTC of Du¨sseldorf University and in the Barmen Klinikum of Wuppertal. The patients were tested individually. Due to the fact that PD has a later onset than HD, it was not possible to match the two patient groups exactly for age, thus the PD patients were significantly older than the HD patients (t =4.52, d.f. = 21, PB 0.001). Therefore, to control for possible age effects, age was always entered as a covariate in the analyses of variance (MANOVAs).

2.3. Procedure and task In order to screen for dementia and to establish that the intelligence level of the patients was sufficient to understand and follow correctly the instructions of the experiment, two intelligence tests were administered to all of the patients prior to the experiment: Mehrfachwahlwortschatztest (MWT-B), measuring verbal IQ, and Set I of the Raven’s advanced progressive matrices (APM-Set I). The apparatus, test material and task employed in this experiment were the same as previously described [42]. Thus, the procedure will be outlined only briefly. Once the cognitive level of the patients was established, each patient filled out (in German translation) a short form of the ‘Individual Differences Questionnaire’ (IDQ) [26] in order to assess the percentage of visual and verbal thinking habits, skills and preferences of the patients. Additionally, an Imagery and Background Test Battery was administered, which consisted of the following tests. Alphabet Imagery Test (based on [4]) in which the subjects had to imagine the alphabet and first name all of the letters that rhymed with the German word ‘Tee’ as quickly as possible (‘verbal imagery task’), and afterwards they were required to imagine the alphabet as capital letters and name all those which contained a curve (e.g. B, C, D, etc.) as quickly as possible (‘visual imagery task’). In the Line Crossing task [42], the subjects had to draw a line mentally, without using the fingers, connecting in counting order encircled numbers, which were placed randomly on a sheet of paper, and at the same time to count how many times the imaginary lines crossed one another. The Tower of Du¨sseldorf task [42] was designed following the logic of the ‘Tower of Hanoi Test’. The task consisted in finding out the minimum number of

movements necessary to ‘transport’ mentally numbered boxes from a left tower to the positions indicated on a right tower adhering to specific rules. Finally, verbal and visuospatial working memory were measured with the Digit Span sub-test of the WAIS-R, and with the Corsi Block Tapping Test. The graphomotor task consisted of copying two ideograms (as described in Ref. [42]) twice each for each of the five sizes (1, 2, 4, 6 and 8 cm) within the boundaries provided (see Fig. 1). The subjects were instructed to copy the ideograms as accurately as possible and with one stroke, without taking the pen off the paper. They were to work at a speed that allowed them to keep accuracy. The stimulus material was fixed on a digitiser tablet (Terminal Display Systems, Blackburn, UK; recording surface, 45 cm×33 cm) connected to a Compaq PC Deskpro 386/20e, monitoring all movements made by the stylus (which had the form and size of a common pen) on and just above the tablet from the point of first contact until the sheet was completed. The software used [41] allowed the collection of trajectorial data, registering the stylus co-ordinates on the digitiser board at a sampling rate of 100 Hz. Off-line interactive analy-

Fig. 1. Working sheet with the two ideogram types for the graphomotor task.

L. Ya´gu¨ez et al. / Beha6ioural Brain Research 102 (1999) 115–127 Table 3 Motor imagery training instructions Look at the ideograms printed on the sheet thoughtfully. Close your eyes and try to picture them in your mind. Open your eyes, look at the printed ideograms and compare if they were as you had imagined them. Imagine how your hand movements would look if you were drawing the ideograms twice in each of the different sizes. Imagine now how the movements of the pen would look. Imagine them on each of the lines. Try now to concentrate upon which muscles would be activated while drawing the ideograms. Try to imagine how the movements would feel, and how much effort would be needed with each part of each ideogram at each size. Now imagine drawing the ideograms at each size. Try to imagine and feel the hand movements. Imagine also the lines that the pen produces while you are drawing the ideograms in your mind.

119

patients and the motor improvements after imagery was carried out.

3. Results

3.1. Trajectorial learning: shape 6ariables

2.4. Statistical analysis

The movement kinematics of one PD patient in the post-practice occasion could not be analysed due to a data storage failure. The results of the repeated-measures MANOVAs for the two shape variables showed, for the width of the ideograms (F(1, 20)=8.74, P= 0.008) as well as for height (F(1, 20)=10.76, P= 0.004), significant group effects, as well as significant interaction effects group× size of ideograms for the width (F(1, 20)= 5.15, P= 0.034) and the height (F(1, 20)= 7.80, P= 0.011) of the ideograms. As be seen in Fig. 2, the HD patients produced somewhat wider ideograms than the PD patients, both for the small sizes (baseline, t= 2.74, d.f. 21, P=0.012; post-imagery occasion, t= 2.65, d.f. 21, P=0.015, post-practice occasion, t= 2.10, d.f. 20, P= 0.048) as well as for the large sizes (baseline, t=2.97, d.f. 21, P= 0.007 and post-imagery occasion, t=2.71, d.f. 21, P=0.013), with the exception of the post-practice occasion, in which the large ideograms of the two patients groups did not differ significantly. The same relation was confirmed for the height of the ideograms. Hence, the HD patients produced systematically higher ideograms than the PD patients on all measurement occasions (small sizes: baseline, t =2.52, d.f. 21, P= 0.020; post-imagery occasion, t= 3.27, d.f. 21, P= 0.004; post-practice occasion, t= 2.42, d.f. 20, P=0.024; large sizes: baseline, t= 2.77, d.f. 21, P=

Regions of Interest (ROIs) were defined by cursor movements on the stored trajectories to capture individual ideograms. The first four smallest ideograms (1 cm high) and the last four largest ideograms (8 cm high) from the sheet before training (baseline), from the first sheet after imagery training (post-imagery) and the fifth sheet after motor practice (post-practice) were defined as individual ROIs for each subject and entered into automatic parameter analysis. In every case, the values for the four ideograms of the same size were averaged within subjects. All parameters were analysed in a two groups (HD patients vs PD patients)×two sizes (small vs large ideograms) × three occasions (baseline, post-imagery, post-practice) repeated-measures MANOVA design with age as the covariate, and post hoc independent and paired t-tests where appropriate. Additionally, a correlational analysis between the results of the imagery tests, the basic cognitive tests, the clinical data of the

Fig. 2. Control variables for accuracy of performance: width =the horizontal size of the ideogram; height = ideogram size in the vertical plane; post-i. = post-imagery occasion, after the imagery training; post-p. =post-practice occasion.

sis of the data provided information concerning movement kinematics, which were used to assess trajectorial learning. For assessing the accuracy of performance, the heights and widths of the drawn ideograms were registered. The first 20 drawn ideograms served as the baseline, and afterwards the patients received 10 min of guided imagery (see Table 3 for the instructions). At the end of the imagery training, the patients drew again the same two ideograms 20 times (post-imagery measurement occasion). This was followed by a physical practice phase, in which the patients completed four full sheets of the same ideograms. The last 20 ideograms (on the sixth sheet) served as the post-practice measurement occasion.

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Fig. 3. Mean tangential velocity. A = Small ideogram. B = Large ideogram. HD = Huntington’s group; PD = Parkinson’s group; post-i. = postimagery occasion, after the imagery training; post-p. = post-practice occasion.

0.011; post-imagery occasion, t = 2.73, d.f. 21, P= 0.013; post-practice occasion, t =2.87, d.f. 20, P= 0.009). The significant occasion main effect (F(2, 40)= 4.31, P=0.020) for ideogram width was due to a significant increase in the width of the small ideograms after the practice phase. This increase was proportional for the two patient groups (post-imagery vs post-practice: PD patients, t =2.92, d.f. 10, P= 0.014; HD patients, t = 2.69, d.f. 10, P = 0.023). There was, however, no significant change in ideogram width and height comparing baseline and post-imagery occasions. Age did not turn out to be a significant covariant either for the width (F(1, 19)= 0.03, P =0.866) or for the height (F(1, 19) =0.00, P = 0.987).

3.2. Trajectorial learning: mo6ement kinematics Age was not a significant covariant for any of the analysed variables (tangential velocity, F(1, 19) =0.79, P=0.386; movement duration, F(1, 19) =0.01, P= 0.906). Thus, the results of the repeated-measures MANOVAs were not affected by the differences in age between the two patient groups. The repeated-measures MANOVA for the mean tangential velocity showed a significant group main effect (F(1, 20)= 6.62, P = 0.018) and a significant occasions main effect (F(2, 40) = 8.72, P =0.001). There were no significant two-way interaction effects. There was, however, a significant three-way group× occasion ×movement amplitude interaction effect (F(2, 40) = 3.44, P= 0.042).

As can be seen in Fig. 3, the HD patients achieved significantly faster tangential velocities than the PD patients on all occasions for the small movement amplitudes (baseline, t= 3.05, d.f. 21, P= 0.006; post-imagery, t= 3.12, d.f. 21, P= 0.005; post-practice, t=2.90, d.f. 20, P= 0.009) and for the large movement amplitudes (post-imagery, t=2.13, d.f. 21, P= 0.046; post-practice, t= 2.26, d.f. 20, P= 0.034) with the exception of the baseline, in which the differences between the two patient groups did not reach significance level. The post-hoc t-test (see Table 4) confirmed that the HD patients showed no significant velocity increase for the small movement amplitudes after the imagery training, but they increased it significantly for the large amplitudes (Fig. 3). After the practice phase, the tangential velocity showed a significant increase for the small movement amplitudes, whereas the velocity of the large movement amplitudes did not change further. Nevertheless, the final tangential velocity was significantly increased for the two movement amplitudes in relation to the initial tangential velocity in the baseline. The PD patients showed, as can be seen in Fig. 3, a different pattern: Here the tangential velocity increased significantly after the imagery training only for the small movement amplitudes, and not for the large amplitudes. Furthermore, while the tangential velocity of the small movement amplitudes increased significantly after the practice phase, the velocity of the larger amplitudes showed no significant change between any measurement occasion (see Table 4).

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Table 4 t-Test results for the changes between the measurement occasions Baseline vs post-imagery

Small ideograms HD PATIENTS Movement duration Tangential velocity PD PATIENTS Movement duration Tangential velocity Large ideograms HD Patients Movement duration Tangential velocity PD Patients Movement duration Tangential velocity

Post-imagery vs post-practice

Baseline vs post-practice

t

d.f.

P

t

d.f.

P

t

d.f.

P

3.09 1.08

10 10

0.011 n.s.

1.58 2.27

10 10

n.s. 0.047

3.49 3.30

10 10

0.006 0.008

1.78 2.60

11 11

n.s. 0.025

2.51 3.31

10 10

0.031 0.008

2.98 3.49

10 10

0.014 0.006

2.43 2.53

10 10

0.036 0.030

0.66 0.27

10 10

n.s. n.s.

1.22 2.23

10 10

n.s. 0.050

0.61 0.60

11 11

n.s. n.s.

1.91 1.36

10 10

n.s. n.s.

1.88 1.28

10 10

n.s. n.s.

Thus, the three-way interaction effect reflected the fact that the HD patients increased the mean tangential velocity significantly more for the large movement amplitudes than for the small amplitudes and that this patient group showed this effect already after the imagery training, reflecting a scaling velocity effect in relation to movement amplitude, whereas the PD patients did not show this effect. This effect was further evident in the results of the repeated-measures MANOVA for movement duration

(see Fig. 4), showing a significant occasion main effect (F(2, 40)= 13.96, P = 0.000). Subsequent post-hoc ttests (see Table 4) confirmed that the HD patients reduced significantly the movement duration of the two movement amplitudes after the imagery training. In contrast, the movement duration of the PD patients remained unaffected for the two movement amplitudes after the imagery training. However, after the practice phase, the movement duration did not change significantly further in the HD patients, either for the small

Fig. 4. Mean movement duration. A, Small ideogram. B, Large ideogram. HD, Huntington’s group; PD, Parkinson’s group; post-i., post-imagery occasion, after the imagery training; post-p., post-practice occasion.

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122

or large movement amplitudes, whereas the PD patients showed a significant decrease in movement duration only for the small movement amplitudes, but not for the large amplitudes.

The descriptive statistics of the results obtained with the Imagery Battery for the HD patients and PD patients are summarised in Table 5 together with results obtained by Ya´gu¨ez et al. [42], with healthy subjects as a reference index. Statistical group comparisons between the HD patients and the PD patients, due to the limited number of PD patients able to perform the imagery tests, could be carried out only for the memory span tests and IDQ, which showed no significant differences between the two groups. Comparing the results of the patients with those of the healthy subjects reported in Ref. [42], it is evident that the two patient groups, in general, needed more time to solve the imagery tasks, with the exception of the verbal part of the Alphabet Imagery Test. On this test, the solving time of the seven PD patients did not differ from the solving time of the healthy subjects. In relation to the number of correct answers on the Crossing Lines task, both the HD and five PD patients achieved, on average, similar results to the healthy subjects. In contrast, the average number of correct answers on the Tower of Du¨sseldorf task was clearly lower in the HD patients than in the healthy subjects. In the Alphabet Imagery Test, although less PD patients than HD patients attempted to solve the task, proportionally more PD patients (42.9%) than HD patients (27.3%) solved correctly the verbal part, as well as the visual part of the Alphabet Imagery Test (28.6% of the PD patients in contrast to only 18.2% of the HD patients).

3.3. Results of the Imagery and Background Test Battery Since the age differences between the two patient groups were significant, a correlational analysis between age and the test variables was carried out. There were, however, no significant age correlations. Most of the PD patients, although not demented clinically or on IQ testing, had very marked difficulties in performing the background and imagery tests. Only five PD patients were able to solve the Crossing Lines task and only one PD patient was able to solve the Tower of Du¨sseldorf task. The patients who were not able to solve these tasks, after a long period of unsuccessful trying with the first item, refused to continue with the task. The same happened with the Alphabet Imagery Test. In this case, only seven PD patients were able to perform the task. Furthermore, in three PD patients, memory span could not be assessed due to fatigue and concentration problems. Finally, the IDQ could not be administered to one PD patient due to time restrictions. In contrast, in only one HD patient was it not possible to administer the Crossing Lines and Tower of Du¨sseldorf tasks and to measure the memory span, due to fatigue problems.

Table 5 Scores obtained on the imagery test batterya HD patients

Crossing lines Crossing time Tower of Du¨sseldorf Tower time IDQ-visual IDQ-verbal Alphabet visual time Alphabet verbal time Digit forwards Digit backwards Corsi forwards Corsi backwards

PD patients

Controls

M

S.D.

N

M

S.D.

N

M

S.D.

N

3.9 246.7 4.4 279.4 67.0 52.0 87.2 66.0 4.6 3.5 4.1 4.4

1.8 168.6 1.43 202.9 21.1 32.6 91.9 61.7 0.8 0.5 0.7 1.0

10 10 10 10 11 11 11 11 10 10 10 10

4.0 209.6 8.0 260.0 60.9 54.1 54.7 32.3 4.6 3.9 4.7 4.4

1.6 110.7 – – 19.6 21.8 34.5 6.42 0.9 0.9 0.9 0.7

5 5 1 1 11 11 7 7 9 9 9 9

4.4 106.0 7.5 199.1 73.0 66.0 34.9 31.4 6.7 5.6 6.3 5.5

1.5 67.5 2.2 122.0 0.2 0.2 11.9 10.6 1.0 1.1 0.8 1.0

31 31 31 31 31 31 31 31 31 31 31 31

a M, mean; S.D., standard deviation; N, number of subjects; crossing lines, number of correct answers (maximal 10); crossing time, time needed to solve the Crossing Lines task (in s); Tower of Du¨sseldorf, number of correct answers (maximal 10); Tower time, time needed to solve the Tower of Du¨sseldorf task (in s); IDQ-visual, percentage visual score on the IDQ; IDQ-verbal, percentage verbal score on the IDQ; alphabet visual time, time needed to solve the Alphabet Imagery Test visual part (in s); alphabet verbal time, time needed to solve the Alphabet Imagery Test, verbal part (in s); digit forwards, digit span forwards; digit backwards, digit span backwards; Corsi forwards, Corsi Block Tapping Test forwards; Corsi backwards, Corsi Block Tapping Test backwards.

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Table 6 Significant correlation coefficients between the imagery variables, the neuropsychological test results and the clinical data in the HD patientsa

Cross lines Cross lines sec. Tower Du¨. Tower Du¨. sec. AlphVisSec AlphVisEr. AlphVerEr. IDQ-vis T.F. T.B. D.B. MWT-B APM

MWT-B

APM

D.F.

0.80**

0.79**

0.68*

0.65*

0.68*

D.B.

T.F

T.B.

0.73*

Educ.

S&F

AtC

0.63* 0.64* −0.70** 0.93***

−0.57* −0.60*

−0.60* −0.60*

−0.66*

0.58* 0.82** 0.81**

−0.73** −0.71**

0.55* 0.66* 0.62* 0.67**

0.79**

−0.60* −0.54* −0.72**

a Educ., years of school education; S&F, functional ratings (Shoulson and Fahn scale) for the abilities of the patients in daily tasks; AtC, percentage of Caudate atrophy; cross lines, number of correct answers on Crossing Lines task; cross lines sec, time needed to solve the Crossing Lines task in s; Tower Du¨., number of correct answers on the Tower of Du¨sseldorf task; Tower Du¨. Sec, time needed to solve the Tower of Du¨sseldorf task in s; AlphVisSec, time needed to solve the visual part of the Alphabet Imagery Test in s; AlphVisEr, number of errors on the visual part of the Alphabet Imagery Test; AlphVerEr., number of errors on the verbal part of the Alphabet Imagery Test; IDQ-vis, visual factor of the IDQ; T.F., Corsi Block Tapping Test span forwards; T.B., Corsi Block Tapping Test span backwards; D.F., digit span forwards; D.B., digit span backwards; MWT-B, verbal IQ; APM, Raven’s advanced progressive matrices, Set I. * PB0.05; ** PB0.01; *** PB0.001.

3.4. Correlational analysis The correlational analysis between the results of the imagery tests and the basic cognitive tests as well as clinical data of the PD patients showed only a significant positive correlation between verbal IQ (MWT-B) and the years of school education (r= 0.88, P B 0.001). The remaining correlations did not achieve significant values. However, in the HD patients significant correlations were present (see Table 6). The two tests that measured the general cognitive level of the patients, i.e. verbal IQ (MWT-B) and reasoning (APM-Set I), were significantly correlated with the number of correct answers on the Crossing Lines task and with the digit and visuo-spatial background memory spans. These two IQ tests and the number of correct answers on the Crossing Lines task also showed a positive correlation with the years of formal education. Additionally, the results on the APM-Set I showed a positive relationship to the number of correct answers on the Tower of Du¨sseldorf task. Furthermore, the memory spans showed significant correlations with the imagery tasks: the memory span for digits (forwards condition) was positively correlated with the number of correct answers on the Crossing Lines and Tower of Du¨sseldorf tasks, and the memory span for visuo-spatial sequences was negatively correlated with the number of errors on the verbal part of the Alphabet Imagery Test. The backwards digit span was positively correlated with the number of correct answers on the Crossing Lines task and negatively with the number of errors as well as with the solving time for the visual part of the Alphabet Imagery Test. The

visuo-spatial backwards span was negatively related to the number of errors on the verbal part of the Alphabet Imagery Test, as well as to the solving time for the visual part. Finally, the percentage of visual factor on the IDQ was positively related to the backwards digit span, whereas the verbal factor showed no significant relationship to any of the employed tests. Concerning the relationships between the clinical data of the patients and the results of the tests, the only two variables that showed significant correlations were the functional ratings on the Shoulson and Fahn scale, and the percentage of caudate atrophy: The two IQ tests and the number of correct answers on the Tower of Du¨sseldorf tasks were negatively correlated to the percentage of caudate atrophy, whereas the solving time for these two tasks was positively correlated to the percentage of atrophy. Finally, the results of the two conditions of the Corsi Block Tapping Test and the functional ratings on the Shoulson and Fahn scale were negatively correlated, which probably reflected their impairments in the motor components of this task. Additionally, a correlational analysis between the results of the imagery tests and the kinematic parameters as well as between the size effect of the imagery training on the motor performance was carried out. However, none of the analysed correlations achieved substantial values.

4. Discussion In the present experiment, the effects of motor imagery training upon the acquisition of spatio-temporal

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features of graphomotor trajectories in PD and HD patients were investigated. The motor trajectories consisted of novel ideograms, which had to be drawn in different sizes. This kind of task can be considered a procedural skill with minimal cognitive or declarative reasoning. Furthermore, the extent of achieved isochrony, which can be assumed to reflect a process in which the motor programme becomes generalised, was analysed as a criterion for motor learning. Moreover, since the ideograms were new for all subjects, but nevertheless all patients had previous experience in writing, it can be assumed that the skill level of the subjects was similar. Additionally, the effects of the combination of imagery training and physical practice were also analysed. Although the PD patient group was, on average, older than the HD patients, age did not turn out to be a significant covariant. Hence, it can be concluded that differences in age did not influence the pattern of results. Furthermore, since the two patient samples performed the same number of trajectories, fatigue effects, if there were any, were held constant. Moreover, the performance of the two patient groups showed no significant deterioration over the course of the experiment. Therefore, it is improbable that the differences between the two groups can be explained by fatigue factors. The main concern in analysing the shape of the produced movement trajectories was in establishing that increases in velocity were not accompanied by changes in the shapes of the movements. The results confirmed that the two patient groups maintained the amplitude of the trajectories over the course of the experiment and only after repeated motor practice did the width of the small ideograms increase, albeit proportionally in the two patient groups. It can, however, be concluded that the two patient groups were able to maintain the gross movement shape over the entire experiment. Looking at the effects of the imagery training upon movement kinematics, the results show a marked contrast between the two patient groups: The HD patients displayed a clear benefit of imagery in terms of movement duration for both the small and large movement amplitudes. Moreover, in the HD patients, the velocity increase for the large movement amplitudes was significantly greater than the increase of velocity for the small movement amplitudes, and was accompanied by a proportional decrease in movement duration. Hence, in the HD patients there was evidence of a velocity scaling effect in relation to movement amplitude, reflecting that in the HD patients motor imagery training alone had a similar effect on the movement kinematics as previously reported by Ya´gu¨ez et al. [42] for healthy subjects, namely an approach to movement isochrony. This approach to isochrony through motor imagery was not

found in the PD patients: The PD patient group showed no effects whatsoever in their movement performance of the large amplitudes, neither in terms of velocity increase nor in decrease of movement duration. These patients showed an increase only in velocity after imagery for the small amplitudes which, however, was not sufficient to alter the overall movement duration. Thus, the PD patients were not able, through motor imagery, to adjust the spatio-temporal pattern of this particular movement towards isochrony. These results suggest that the dopaminergic input to the basal ganglia, especially the striatum, plays an important role in the translation of motor imagery into motor performance. In contrast, the pathology of HD, with predominant loss of intrinsic neurones in the caudate, does not appear to have an influence on the acquisition of the spatio-temporal characteristics of a graphomotor pattern by motor imagery. The next issue addressed in the experiment was concerned with the effects of the combination of previous imagery training with actual practice. In this phase of the experiment, the HD patients showed no further increase in velocity or decrease in movement duration, with the exception of the velocity for the small amplitudes, which indeed showed a further increase. These results suggest that the improvement achieved by the HD patients after imagery reflected their maximal possible performance, and further practice, at least over the limited number of repetitions studied, did not have additional influences. On the other hand, PD patients showed benefits from subsequent practice which, however, were restricted to the small amplitude movements. For the small amplitudes, the velocity increased and the movement duration diminished compared with the performance after the imagery training as well as in comparison with the initial performance in the baseline. The performance of the large amplitude movements remained nevertheless unaffected either by motor imagery or by motor practice. In this context, it has been already reported that small amplitude movements are performed better in PD patients than large ones [15]. This might be related to the different firing characteristics of substantia nigra pars compacta neurones for small and large movement amplitudes; DeLong and Georgopoulos [9] as well as Schultz et al. [32] found that in monkeys, the substantia nigra pars compacta neurones did not show changes in firing rates during the execution of small amplitude movements, whereas they showed a clear increase in firing rates during the execution of large amplitude movements. Hence, deficits in dopamine release appear to be more relevant for large amplitude movements than for small amplitude ones, which probably reflects the difficulty of PD patients in scaling velocity in relation to movement amplitude and thus approaching movement isochrony.

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In the earlier stages of HD, the pathology is usually more pronounced in the basal ganglia [21,22], whereas in the later stages there is increasing cortical involvement. Thus, the early stages of HD (as in this study) can be regarded as a model for basal ganglia function disruption, clearly distinct from the deficit of dopaminergic modulation, as in PD. The present experiment was also concerned with cognitive factors involved in visual imagery and the relationships between visual imagery abilities and motor learning through motor imagery. Since it is supposed that motor plans and motor programmes are stored in memory in terms of their spatial and temporal features rather than as specific motor actions [35], it may be reasonable to assume that motor imagery also involves some aspects of visual imagery. First, it can be concluded that all of the imagery tasks employed in this experiment were rather difficult to solve by the two patient groups studied. These difficulties were, however, considerably more accentuated in the PD patients. These patients reported almost unanimously that although they knew exactly what was required from them, they nevertheless were unable to keep the images long enough mentally to solve the tasks. In particular, on the Tower of Du¨sseldorf task, this handicap was very marked. Similar difficulties in solving imagery tasks in PD patients have also been reported by Annett and Smith [1]. Second, impairments in similar problem solving tasks have been reported, e.g. for the Tower of Toronto task [31]. In relation to the Alphabet Imagery Test, although the PD patients reported more difficulties than the HD patients, the PD patients committed proportionately less errors than the HD patients in the two sub-tests. These results suggest that basal ganglia impairments may have effects on the generation of mental images, specifically in their maintenance. However, it could also be possible that the impairments found in these two patient groups are more related to their difficulties in the performance of more complex or simultaneous tasks, similar to their difficulties in performing simultaneous movements (for example, [2,14,39]). In all these four tasks, the subjects are required, first, to form visual images, to inspect them and at the same time to manipulate the images mentally and remember the generated manipulations. On the Tower of Du¨sseldorf task, they had additionally to plan the movements and apply problem-solving strategies. Therefore, these deficits could be also explained by the increasing demands in attentional resources, since the two patient groups did not differ either in their cognitive level or memory spans. Thus, with increasing resource demands, the PD patients showed poorer performance. In the PD patients, it was not possible to establish any substantial correlations between the neuropsychological tests and the imagery test, due to the limited

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sample size of PD patients able to complete the imagery tests. However, in the HD patients there were significant correlations. In this patient group, general intelligence, in particular the level of reasoning ability (APM), showed a positive relation to the number of correct answers on the two imagery tasks. Interesting in this context is also that the degree of caudate atrophy showed a significant relationship to the results on the Tower of Du¨sseldorf task, the backwards verbal and visuo-spatial spans, and to the solving times; i.e. a higher degree of atrophy appears to be correlated with a poorer performance on these tests and with a prolonged solving time. Conversely, higher verbal and visuo-spatial spans were also related to a better performance on the imagery tests, pointing to some working memory influence on these tasks. The associations in the HD patients between the imagery tasks and basic cognitive functions, on one hand, and between those and the degree of caudate atrophy on the other, indicate that the specific basal ganglia damage of the HD patients not only affects their other cognitive performances, but that it may also have important contributions in generating and transforming mental visual images. The degree of cortical atrophy in this sample of mildly affected HD patients showed no significant correlations to any of the variables studied. Also in this sample of HD patients there was no substantial correlation between the performance on the visual imagery tasks and the improvement of motor performance through motor imagery. This is similar to the reported lack of correlations between visual imagery abilities and motor improvements through motor imagery in healthy subjects [42], and suggests that visual imagery and motor imagery do not share the same processes. It can be concluded that motor imagery facilitates the acquisition of the invariant spatio-temporal features of graphomotor trajectories in HD patients. PD patients, on the other hand, show no marked improvements either with motor imagery or physical practice in the performance of graphomotor trajectories. While HD patients seem able to compensate their impairments using motor imagery, this is not the case for the PD patients. Beside the impaired dopaminergic balance in the basal ganglia versus the loss of GABAergic neurones in the caudate nucleus, another reason for this disparity between the two patient groups could reside in the limited attentional resources of the PD patients. Thus, although PD patients might be able to generate conscious motor representations [10], they have, nevertheless, difficulties in maintaining the motor representations and at the same time translating these into motor actions or in maintaining visual images and simultaneously manipulating them mentally. These findings also correspond to the often observed inability of PD

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patients to use predictive motor strategies (for example, [3,5,11]) in the sense that lack of prediction entails lack of putting forward a mental representation of a movement sequence. The results of this study show that this deficit in mental motor manipulations is already present at the stage of non-repetitive isolated movements and is not a problem appearing only with motor sequences. In the case of the HD patients, the subcortical atrophy in the caudate nucleus has rather more repercussions in higher cognitive processes and probably visual imagery than in the generation and translation of motor representations into motor actions.

Acknowledgements We thank Prof. Jo¨rg for his kind help in recruiting the PD patients and for his generosity in providing the lab at the Klinikum Barmen. We are in debt to Dr A. Ulich, of the Department of Neurology, Institute of Diagnostic Radiology from the University of Du¨sseldorf, for providing the measurements of CT scans of the HD patients. This work was supported by a grant from the DFG (SFB 194, A3) to VH.

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