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Nwopsycholug~o. Vol. 26. No. 1. pp. 79-91, 1988 Pnnted in Great Bnfain. 002X-3932:88 $3.00+0.00 Pergamon Journals Ltd. PERFORMANCE ON UNIMANUAL AND BIMANUAL TAPPING TASKS BY PATIENTS WITH LESIONS OF THE FRONTAL OR TEMPORAL LOBE GABRIEL LEONARD,* BRENDA MILNER and LYNETTE JONES Montreal Neurological Institute, and Department of Neurology and Neurosurgery, McGill University, 3801 University Street, Montreal, Quebec, Canada H3A 2B4 (Received 16 July 1986: accepted 7 April 1987) Abstract-The performance of 151 patientswith unilateral excisions from either the frontal or the temporal cortex and 60 normal subjects was examined on three motor tasks: (1) simple unimanual tapping; (2) spatially ordered unimanual tapping; and (3) bimanual tapping in which the movements of the two hands were out-of-phase. All patient groups were impaired with both hands on spatially ordered unimanual tapping. In contrast, only those patients with either left or right frontal-lobe lesions performed poorly on the bimanual tapping task. Our findings demonstrate that the frontal cortex plays a critical role in the co-ordination of arm and hand movements, particularly when different movements have to be performed simultaneously. INTRODUCTION STUDIES of motor function in both human and non-human primates indicate that lesions involving the frontal cortex impair the performance of complex motor acts, even though the precentral gyrus is spared [lo, 18, 24, 26, 31-331. In the monkey, unilateral lesions of the supplementary motor cortex give rise to deficits on bimanual co-ordination tasks in which the two hands must perform different actions simultaneously [l , 21. In human subjects, unilateral lesions of either frontal lobe produce bilateral impairments in the copying of complex arm and hand movements, whereas subjects with temporal-lobe lesions of either hemisphere perform such tasks normally [24]. In addition, bilateral deficits after large unilateral brain lesions have been observed on other complex motor tasks (e.g., pursuit tracking [17,48]), these impairments being noted more frequently after damage to the left cerebral hemisphere than after damage to the right [9,20,47]. In contrast to the deficits seen in these complex motor activities, the impairment on simpler motor tests (such as finger tapping) has usually been restricted to the hand contralateral to the cerebral lesion [ 15, 161. Simple finger-tapping tasks have been used in studies of motor performance in human subjects as tests of motor speed and co-ordination [4, 11, 15,22,23,37]. Two main findings to have emerged from this research are that men tap faster than women [ 11,22,23] and that in right-handed subjects the right hand is consistently faster than the left [4,22,34,35]. This superiority of the right hand is also evident when subjects use a stylus to tap a board repetitively [S, 471. *Author to whom correspondence should be addressed at: Montreal Neurological Institute, 3801 University Street, Montreal, P.Q., Canada H3A 2B4. 79
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Page 1: Performance on unimanual and bimanual tapping tasks by patients with lesions of the frontal or temporal lobe

Nwopsycholug~o. Vol. 26. No. 1. pp. 79-91, 1988 Pnnted in Great Bnfain.

002X-3932:88 $3.00+0.00 Pergamon Journals Ltd.

PERFORMANCE ON UNIMANUAL AND BIMANUAL TAPPING TASKS BY PATIENTS WITH LESIONS OF THE FRONTAL OR

TEMPORAL LOBE

GABRIEL LEONARD,* BRENDA MILNER and LYNETTE JONES

Montreal Neurological Institute, and Department of Neurology and Neurosurgery, McGill University, 3801 University Street, Montreal, Quebec, Canada H3A 2B4

(Received 16 July 1986: accepted 7 April 1987)

Abstract-The performance of 151 patients with unilateral excisions from either the frontal or the temporal cortex and 60 normal subjects was examined on three motor tasks: (1) simple unimanual tapping; (2) spatially ordered unimanual tapping; and (3) bimanual tapping in which the movements of the two hands were out-of-phase. All patient groups were impaired with both hands on spatially ordered unimanual tapping. In contrast, only those patients with either left or right frontal-lobe lesions performed poorly on the bimanual tapping task. Our findings demonstrate that the frontal cortex plays a critical role in the co-ordination of arm and hand movements, particularly when different movements have to be performed simultaneously.

INTRODUCTION

STUDIES of motor function in both human and non-human primates indicate that lesions involving the frontal cortex impair the performance of complex motor acts, even though the precentral gyrus is spared [lo, 18, 24, 26, 31-331. In the monkey, unilateral lesions of the supplementary motor cortex give rise to deficits on bimanual co-ordination tasks in which the two hands must perform different actions simultaneously [l , 21. In human subjects, unilateral lesions of either frontal lobe produce bilateral impairments in the copying of complex arm and hand movements, whereas subjects with temporal-lobe lesions of either hemisphere perform such tasks normally [24]. In addition, bilateral deficits after large unilateral brain lesions have been observed on other complex motor tasks (e.g., pursuit tracking [17,48]), these impairments being noted more frequently after damage to the left cerebral hemisphere than after damage to the right [9,20,47]. In contrast to the deficits seen in these complex motor activities, the impairment on simpler motor tests (such as finger tapping) has usually been restricted to the hand contralateral to the cerebral lesion [ 15, 161.

Simple finger-tapping tasks have been used in studies of motor performance in human subjects as tests of motor speed and co-ordination [4, 11, 15,22,23,37]. Two main findings to have emerged from this research are that men tap faster than women [ 11,22,23] and that in right-handed subjects the right hand is consistently faster than the left [4,22,34,35]. This superiority of the right hand is also evident when subjects use a stylus to tap a board repetitively [S, 471.

*Author to whom correspondence should be addressed at: Montreal Neurological Institute, 3801 University Street, Montreal, P.Q., Canada H3A 2B4.

79

Page 2: Performance on unimanual and bimanual tapping tasks by patients with lesions of the frontal or temporal lobe

80 GABKIEL LEONARD, BRENDA MILNER and LYNETTE JONES

The difficulty of a tapping task can be increased by requiring subjects to tap in a specific temporal pattern [27,45] or in a spatially ordered sequence [12,43, 471. THURSTONE [43] devised a unimanual and a bimanual task in which subjects used a stylus to tap in a prescribed sequence on a board. On the bimanual task, the movements made by the two hands were out-of-phase, and the tapping rates achieved were thus considerably slower than the speeds determined for each hand individually. These two tasks were used in the present investigation in conjunction with a simple tapping test to study the effects of circumscribed lesions of the frontal cortex on motor speed and co-ordination. Patients with temporal-lobe lesions were included in the study as a control for the frontal-lobe groups.

On the basis of KOLB and MILNER’S [24] findings and JASON’S [19] demonstration that right or left frontal-lobe lesions impair the rapid reproduction ofa series of hand movements, we predicted that lesions involving either frontal lobe would give rise to a bilateral impairment on the unimanual sequential tapping task. The above findings, together with BRINKMAN’S [l] observations in the monkey, led us to expect that patients with frontal-lobe lesions would also perform poorly on the task demanding bimanual co-ordination.

SUBJECTS One hundred and fifty-one patients at the Montreal Neurological Hospital. each of whom had undergone a

unilateral brain operation for the relief of focal cerebral seizures, were tested. Except where stated in the description of the individual patient groups, the cpileptogcnic lesions had been static and atrophic, dating from birth or early life. Excluded from the patient population were those subjects with Full-Scale Wechsler IQ ratings below 80, and those known to have atypical speech representation as demonstrated by preoperative intracarotid Amytal tests 130. 441. The hand preference ofexch patient was assessed using a handedness questionnaire adapted from CROVITZ and ZI NI K [ 71. A score above 30 on this questionnaire is taken to mean that the subject is not completely right-handed 1291, and any patient with a xorc greater than 30 was excluded from the study.

The patients ranged in age from 12 to 58 yr. All had normal sensory status of the hands, aa determined by quantitative tests that included two-point discrimination on the palm [h. 39.411, and the detection ofthc direction ofpassive movement of the lingers 16.411. Fifty-eight patients were seen in the early postoperative permd (from 2 3 weeks after surgery), and the remaining 93 patients were seen from 1 to 27 yr after the operation.

Sixty normal control (NC) suhjccts were chosen to match the patient population as closely as possible with rcspcct to age. education, and occupational status. These subjects did not report any history of neurological illness or phyxal injury that might have alrectcd their tapping ability. All the control subjects also had a score of30 or less on the handedness questionnaire. Table I shows the sex. age and educational level for all subject groups, and the

Full-Scale IQ data for the patient groups.

Table I. Subjects

Group

Left frontal Right frontal Left temporal Right tcmpornl Normal control

sex Age (yr) Education (yr) Wechsler tQ

F M Mean Range Mean Range Mean Range

4 9 26.6 14~ 38 11.x 5 18 97.9 80 Ill IO 12 32.7 15 58 Il.9 7 I9 105.9 X0 I36 2x 38 2X.6 I4 -50 12.6 3 18 107.3 84 I35 20 30 29.0 I2 54 11.2 6 IX 110.0 84 134 30 30 76.X IS 55 12.4 8 I6 Not asscased

f.c/f /r~~n/rr/-/&c, c,roup (L/;). The extent of removal for each ofthese I3 patlents IS illustrated in Fig. 1. The lateral aspect of the frontal I&c w;~s always invaded hut in all cases Broca’s area was spared. The LF group included two huhjccth (An.Be., Ra.Ja) with \axular lesions and two (Ch.Kn.. Hu.Ma) with indolent turnours. Six patients w’crc tc\tcd in the cnrly postoperative period, and the other seven patients were tested one or more years following their opcratlon.

Page 3: Performance on unimanual and bimanual tapping tasks by patients with lesions of the frontal or temporal lobe

PERFORMANCE ON UNIMANUAL AND BIMANUAL TAPPING TASKS 81

Bo. Ba.

An. Co

WI. Wh

An. Be.

f’

17 /’ i -f

JO. De

sy. FIa.

C-J 16 / ,_--

Ke. Ha.

17

Mi. MI.

, _.,_!a. Ja.

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W . .

23

17

MO. Au

FIG. 1. Diagrams based on the surgeon’s drawings at the time of operation, showing the estimated extent of cortical excision for the patients in the left frontal-lobe group. For Figs 1 and 2, the medial view (above) and the inferior view (below) have been included whenever available, together with the lateral view. The score obtained by each patient on the bimanual tapping test is shown beside the

corresponding brain map.

Riyhtfrontal-lobe group (RF). Figure 2 shows the extent of cortical removal for 20 of the 22 patients who had had right frontal-lobe removals. Drawings were not available for the other two patients in this group. All removals involved the lateral frontal cortex and many encroached upon the medial cortex as well. The RF group included three patients (Do.Co., BoGr., La.Ha) with vascular lesions, four (Er.Bu., Br.Fo., Ra.Mi., MaSi) with indolent tumours, two (Su.He., Je.Bi) with porencephalic cysts and one case of tuberous sclerosis (Ja.Ro). Six patients were seen in the early postoperative period and 16 in follow-up testing.

Temporal-lobe groups

The cortical removals in the 116 patients with temporal-lobe excisions ranged from 3.5 to 6.5 cm along the Sylvian fissure and from 3.5 to 7.5 cm along the base of the brain. The temporal-lobe resections always included the amygdala but varied with respect to the extent of removal from the hippocampus and/or parahippocampal gyrus. The 116 patients were subdivided according to the hemispheric side of the lesion. On average, the left temporal-lobe removals were smaller than those from the right temporal lobe.

Lefi temporal-lobe group (LT). The 66 patients in this group included 2 with vascular lesions, and 10 with slow- growing tumours. All excisions were well anterior to the temporal speech zone. Twenty-nine patients were tested from 2-3 weeks after their operation, and the remaining 37 patients were seen one or more years postoperatively.

Right temporal-/obe group (RT). In this group there were 50 patients, including 3 cases of indolent tumour. Seventeen patients were seen in the early postoperative period and the remaining 33 patients in follow-up.

APPARATUS The apparatus, shown in Fig. 3, consisted of two circular brass plates, each with a diameter of 130 mm; the plates

were mounted 130 mm apart on a wooden board, which measured 267 mm by 457 mm. Each plate was divided into four distinct pie-shaped sectors, which were numbered 1, 2, 3, and 4, respectively (as indicated in Fig. 3.). For the sequential and the simple tapping tasks, the board was wired so that any contact made with a stylus on one of the four sectors would complete an electrical circuit that activated a mechanical counter. For the bimanual condition the circuit was changed, so that both similarly numbered plates had to be touched simultaneously for the counter to function. The same apparatus was used for all three tapping tasks.

Page 4: Performance on unimanual and bimanual tapping tasks by patients with lesions of the frontal or temporal lobe

GAHKIEL LEOSARI), BRENDA M~LNER and LYNETE JOKES 82

La Ho.

Ma Ja

Da co !

? ,34 Ja Ne

Ka Wh

Ra. MI

I;rc;. 2. Diagrams showing the estimated extent ofcortical excision for the patients in the right frontal- lobe group.

FIG 3. Tapping apparatus, (Thurstone. 1944).

PROCEDURE

The subject stood fxxng the apparatus with feet together and with the resting hand held behind the back.

In this unimanual condition, subjects were asked to tap as quickly as possible with a stylus on each of the four sectors of the plate, in ascending numerical order. The subject tapped the plate on the left side of the board with the left hand and the plate on the right side with the right hand. The total number oftaps made in 30 set was recorded on the counter. and any errors made were noted down independently by the experimenter. Three types of error were pc’siblc: (I) squrutid. which occurred when the subject tapped in an incorrect order (e.g., 1, 2. 4, 3): (2)

Page 5: Performance on unimanual and bimanual tapping tasks by patients with lesions of the frontal or temporal lobe

PERFORMAXCE ON UNIMANUAL AND BIMANUAL TAPPING TASKS 83

persewratiue, when the subject tapped the same sector twice (e.g., 1 , ?,2,3,4), and (3) misses. which occurred when the tap did not make contact with the circular plate. Because the counter was activated by the first two types of error, the number of such errors was subtracted from the total score. It has been shown previously on other motor tasks (e.g., copying hand and arm movements [24]) that patients with either left or right frontal-lobe lesions make significantly more errors than other subject groups.

Thurstone bimanual tapping

This test was administered after completion of the first two sequential tapping trials. The experimenter first demonstrated the nature of this spatially asymmetric bimanual task. and then subjects were given one practice trial to ensure that they had understood the task. Holding a stylus in each hand, subjects had to tap on corresponding sectors of the two plates in ascending numerical order, as rapidly and as accurately as possible. The score was the total number of simultaneous contacts achieved in 30 sec. Errors were recorded by the experimenter and were of the same types as described for sequential tapping.

Smple tapping

In this unimanual test, subjects tapped as quickly as possible with the stylus on one sector only (Sector 4 with the left hand or Sector 2 with the right hand [see Fig. 31). The scores recorded were the total number of taps in I5 set for each hand.

Order of trials

The sequential tapping test was performed twice, and the simple tapping and bimanual tasks once each. yielding a total of seven test conditions administered in the following order: (1) sequential tapping with the hand ipsilateral to the cortical lesion; (2) sequential tapping with the hand contralateral to the cortical lesion; (3) bimanual tapping; (4) repetition of sequential tapping with the contralateral hand; (5) repetition of sequential tapping with the ipsilateral hand; (6) simple tapping with the ipsilateral hand; (7) simple tapping with the contralateral hand. For the NC subjects the hand used first on the unimanual tapping tasks was counterbalanced across subjects.

RESULTS

A one-way analysis of variance indicated no significant difference between the groups with respect to age, and no difference between the patient groups with respect to Full Scale IQ. Although there was a significant group difference with respect to education (F=2.62, P<O.O4), post hoc examination of this effect (using Tukey’s test) did not identify any one group as being significantly different from the other groups. Because the correlation between education and the bimanual tapping score was only 0.14, it did not seem appropriate to treat education as a covariate in the analyses. In addition it should be pointed out that the patient group with the least education (RT) was not the most impaired group on the tapping tests.

The scores on the three tapping tasks were analysed separately and the initial analyses were performed with sex as a factor, in view of the demonstrated male superiority in tapping speed [22]. Because there were no significant differences between the scores of patients seen in the early postoperative period and those seen during follow-up testing, the results from postoperative and follow-up patients were combined for each group. The findings from the three tapping tests are presented below in order of increasing task difficulty, beginning with the simple tapping test.

Simple tapping. A three-way analysis of variance on the simple-tapping scores yielded a significant main effect of group (F=7.08, P<O.OOl), of sex (F=26.16, P<O.OOl), and of hand (F= 95.70, P < 0.001). None of the interactions was significant. Because of the effect of sex on tapping speed, two-way analyses were performed separately on the scores from men and women.

The mean tapping scores for each group of male subjects are shown in Fig. 4. The results from the two-way analysis indicated a main effect of hand (F=48.44, P-cO.001 ), but not of

Page 6: Performance on unimanual and bimanual tapping tasks by patients with lesions of the frontal or temporal lobe

84 GABKIEL LEONARD, BREKDA MILNER and LYNETTE JONES

115

EI Left hand

110 q Right hand

105 T

Group Left Rtght Left Rtghl Normal

Frontal Frontal Temporal Temporal Gontrol

N 9 12 38 30 30

FS~(;. 4. Simple tapping: Histograms showing the mean (+ S.E.M.) scores for the left and right hands, respectively, for each group of male subjects.

group (F=2.20, PcO.07); the interaction was not significant. The right hand was consistently faster than the left for all male groups, but there was no significant difference between the groups in tapping speed.

Figure 5 shows the mean tapping scores for each group of female subjects. A two-way analysis of variance yielded a significant main effect of group (F= 5.35, P<O.OOl) and of hand (F= 52.61, P<O.OOOl); the interaction was not significant. Post hoc examination of the group effect showed that both the LF and the RF groups were impaired relative to the NC subjects (LF: Q=5.61, PcO.01; RF: Q=3.86, P-cO.05). The right hand was consistently faster than the left for all female subject groups, as had been the case for the men.

7hurstonr sequential tupping

In contrast to the simple-tapping condition, there was clearly no significant difference between the performance ofmen and women on this task (F=O.OOl, P=O.97), and hence the results from each group of subjects were collapsed across sex. For each hand, the analyses were performed on the mean scores for the two trials, because all groups had obtained higher mean scores with each hand on the second trial than on the first and there was no significant interaction between group and trial (P= 0.56).

Figure 6 shows the mean tapping scores for the left and right hand, respectively, for each group of subjects. A two-way analysis of variance yielded a significant main effect of group (F=9.72, P<O.OOl), and of hand (F= 107.78, P<O.OOl), but no significant interaction. Tukey’s post lm analysis showed all patient groups to be impaired with both hands relative to the normal control group (LF: Q-6.75, P<O.Ol; RF: Q=6.13, PcO.01; LT: Q=3.93,

Page 7: Performance on unimanual and bimanual tapping tasks by patients with lesions of the frontal or temporal lobe

PERFORMANCE ON UNIMANUAL AND BIMANUAL TAPPING TASKS 85

IlOr

105 -

100 -

z In t 95-

E 0 $j go-

c” .-

8 85-

F

60 -

75 -

T

q Left hand

n Right hand

0

Group Left Right Left Right Normal

FrOlltal Frontal Temporal Temporal Control

N 4 10 27 20 30

FIG. 5. Simple tapping: Histograms showing the mean (+ S.E.M.) scores for the left and right hands, respectively, for each group of female subjects.

135

130

125

12c

3 0

z 11:

s!

8 co IlC

c” ‘h

% 10: t-

%

9 1oc

9:

9c

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EA Left Hand

n Right Hand

Len ^. ._ Rtght R\ght Normal Gruup

Frontal Frontal Temporal Temporal Controt

N 13 22 66 50 60

FIG. 6. Sequential tapping: Histograms showing the mean (+ S.E.M.) scores for the left and right hands. respectively, for each group of subjects. The subject’s score was the mean of the two trials.

Page 8: Performance on unimanual and bimanual tapping tasks by patients with lesions of the frontal or temporal lobe

86 GAEXI~L LLOVAIW, BRENDA MILSLK and LVNETTL JCKES

P<O.O5; RT: Q =4.78, P<O.O5). The patient groups did not differ from one another. All groups of subjects tapped faster with the right hand than with the left.

Thurstone himanual tuppiq

There was no difference between the tapping scores obtained by men and women on the bimanual tapping task (F=0.74, P=O.39), and so their results have been combined to calculate the group means shown in Fig. 7. A one-way analysis of variance performed on these data demonstrated a significant main effect of group (F=5.11, P<O.OOl); post hoc examination of this effect indicated that the LF group was impaired relative to both the NC and LT groups (Q = 6.08, Q = 4.70, P < 0.01) and that the RF group was impaired relative to the NC group (Q = 4.08, P-c 0.05). The score obtained on this test by each patient with either a left or right frontal-lobe lesion is shown beside the corresponding brain map in Figs 1 and 2, respectively. No consistent relation could be discerned between either the size or site of the excision from the frontal lobe and the score obtained on the bimanual task. It should also be noted that the impaired performance of patients with frontal-lobe lesions cannot be attributed to the size of the cortical excisions as such, since many of these lesions are considerably smaller (e.g., Bo.Ba., An.Co., Wi.Wh., La.Ho., Ma.Ja., Da.Co.) than those in the temporal lobe. Furthermore, patients with left frontal-lobe lesions generally have lower scores on both the sequential and bimanual tapping tasks (Figs 6 and 7) than patients with right frontal-lobe lesions, even though the extent of the excisions from the left frontal lobe is on average smaller than that from the right frontal lobe.

33-

31 -

27 -

7

N 13 22 66 50 60

I tapping: Histograms showing the mean (f S.E.M.) scores for subjectb.

each g, ‘“UP of

Page 9: Performance on unimanual and bimanual tapping tasks by patients with lesions of the frontal or temporal lobe

PERFORMANCE ON UNIMANUAL AND BIMANUAL TAPPING TASKS 87

Thurstone ratio-score

In order to examine the relation between the tapping speeds achieved on the unimanual sequential task and those obtained on the bimanual test (in which the two hands were moving out-of-phase), a ratio-score devised by THURSTONE [43] was calculated. The score was defined as

S= NRLINR+ NL

where NR is the number of taps made by the right hand on the first trial of sequential tapping, NL is the number for the left hand on the first trial, and NRL is the number of simultaneous taps achieved with both hands together. A subject who does as well with both hands as with each hand separately will get the maximum score of 0.5. The mean ratio for the normal control subjects was 0.12, indicating that subjects were considerably slower on the bimanual than on the unimanual condition. A one-way analysis of variance performed on these ratio- scores revealed no significant difference between the groups (P=O.lO).

Errors

Subjects made few errors and most of these were errors of sequence rather than perseverations or misses. Because more errors were made on the first trial of the sequential tapping test than on the second, separate analyses were performed on the total number of errors made on each trial of sequential tapping, and on the bimanual tapping test. There were no significant differences between the groups in the errors made in any of the tasks.

The number of errors made on each tapping test was then examined in relation to the number of correct responses. A proportional error score was calculated, which was the ratio between the number oferrors made and the score on each tapping test. A one-way analysis of variance performed on these relative scores indicated a significant main effect of group only on the bimanual tapping test (F= 4.0, P < 0.01); post hoc examination of this effect showed that the RF group made proportionately more errors than the NC group (Q = 4.44, P < 0.05).

DISCUSSION

The mean scores obtained by the normal control subjects on the simple tapping test are higher than the scores that have been reported elsewhere for finger tapping [ 1 I, 341, a difference that presumably reflects the greater speed with which repetitive movements involving the wrist, elbow and shoulder can be executed as compared to movements of the metacarpophalangeal joint. The superior tapping performance of the preferred right hand, and the faster tapping speed of men confirm similar findings from other studies with normal subjects 113, 22, 34, 461. On our simple tapping test there were no significant differences between the mean scores obtained by any of the male subject groups. Deficits that emerge as the task becomes more complex cannot therefore be attributed to a general slowness in responding, such as has been reported for some groups of patients with cerebral lesions [g].

Contrary to our expectations, there were significant group differences for the female subjects in simple tapping speed; women with either left or right frontal-lobe lesions obtained lower scores with both hands than the normal control subjects. This difference in the simple tapping results obtained from men and women with frontal-lobe lesions was unexpected but appears to be consistent with KIMURA'S [21] hypothesis that manual praxic functions in women are more dependent on the anterior part of the left cerebral hemisphere than on the posterior part, and that in men these two regions contribute equally to manual functions.

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88 GAUKIEL LEONAKD. BKENDA MILNEK and LYNETTE JONES

The results for the Thurstone sequential tapping test differed in two ways from those obtained on the simple tapping test. First, there were no differences between the tapping speeds of men and women, suggesting that performance differences between the sexes may diminish as the complexity of the motor task increases. LOMAS and KIMURA [25] also noted that there was no difference between the scores obtained by men and women on another manual sequential-tapping task.

Second, patients with unilateral excisions from either the temporal or frontal lobe were impaired on the sequential tapping task, the deficit being manifested on both hands. This result was unexpected and suggests that there is a general slowing ofmotor output in patients with cortical lesions, but only when the motor activity reaches a certain level of complexity. JASON 1191 also found that patients with unilateral excisions from either the frontal or temporal lobes performed poorly on a speeded motor task. Rapid and accurate execution of the movements involved in sequential tapping depends on both visual and kinesthetic cues, and on attending to four different spatial locations. Auditory feedback from the sound of the stylus hitting the board might also contribute to the regulation of the movement sequence [3, 421.

The superior performance of the right hand over the left in both the simple and sequential tapping tasks was evident in all patient groups, irrespective of the laterality of the cerebral lesion (see Figs 4 6). This finding is in contrast to the results from a recent unpublished study of handgrip strength in a similar group of patients, where we found that the normal pattern of preferred-hand dominance for strength [38] was reversed in patients with left-hemisphere lesions. On motor tasks requiring skill rather than strength, a consistent superiority of the right hand over the left has been noted in right-handed patients with unilateral cerebral

lesions [ 17, 47, 511. All subjects were slower on bimanual than on unimanual sequential tapping, a finding

reported previously for other bimanual motor tasks [49%51]. Whereas patients with unilateral excisions from the temporal lobes were unimpaired on the bimanual task (in contrast to their impaired performance on unimanual sequential tapping), patients with lesions of either the left or right frontal lobe were again deficient. On this task there was a differentiation between the efTects of frontal and temporal-lobe lesions within the left cerebral hemisphcrc, with patients who had excisions from the left frontal lobe being significantly slower than those with lesions in the left temporal lobe.

The difference in the pattern of results obtained from patients with temporal-lobe lesions on the two sequential tapping tests suggests that the requirements of the two tasks are dissimilar. Although the unimanual condition involved execution of a complex movement sequence, speed was a primary requirement of this task. In contrast, the normal performance of patients with temporal-lobe lesions on bimanual tapping suggests that speed is less

important in this situation, and that the ability to co-ordinate out-of-phase movements of the two arms may bc the critical factor. The striking deficits observed in patients with frontal- lobe lesions on the bimanual tapping task presumably result from an impairment in the co- ordination of simultaneous arm movements. This interpretation is consistent with BIIIVKMAN’S [I. ?] finding that deficits in bimanual co-ordination occur in monkeys with unilateral excisions from the supplementary motor area, and that these impairments arc most apparent when the monkeys have to perform different movements with the two hands at the same time.

In the initial stages of learning a motor skill, performance is usually characterized by slow,

jerky movcmcnts. This awkwardness is a reflection of the organism’s reliance on visual and

Page 11: Performance on unimanual and bimanual tapping tasks by patients with lesions of the frontal or temporal lobe

PERFORMANCE ON UNIMANUAL AND BIMANUAL TAPPING TASKS 89

kinesthetic feedback for the guidance of each movement [14, 28, 403. With practice, the sequencing and timing of movements shifts from direct visual control to a form of internal control that still utilizes visual and kinesthetic information [36], but that no longer requires constant reference to feedback. The impaired performance of patients with frontal-lobe excisions on bimanual tapping could be attributed to difficulties in switching from an external to an internal form of control, and in particular in developing an internal representation of the complex movement sequence. Support for this notion of an increased dependence on sensory feedback comes from the finding that the low scores of patients with frontal-lobe lesions on the unimanual tapping test result from slow and not inaccurate performance. Although patients with right frontal-lobe lesions did make significantly more errors than the normal control subjects on the bimanual tapping test, most of their errors were sequential, which fits with the hypothesis that there is a failure in translating the requirements of the task into an internal motor plan.

A further requirement of bimanual tapping is that subjects distribute their attention over the eight positions with which the stylus must make contact. It could therefore be hypothesized that the combined effect ofdifficulties in switching attention between a number of different spatial locations and an increased reliance on visual and kinesthetic feedback resulted in the impaired tapping performance of patients with frontal-lobe lesions.

Acknowledyements-This research was supported by the Medical Research Council of Canada through a grant (MT2624) and a Career Investigatorship to Brenda Milner and through a Fellowship to Lynette Jones. We thank Dr Gilles Bertrand, Dr William Feindel, Dr Andrt: Olivier, Dr Theodore Rasmussen, Dr Jean-Guy Villemure and their associates at the Montreal Neurological Hospital for the opportunity to study their patients, and for providing detailed descriptions of the surgical removals.

REFERENCES 1. BRINKMAN, C. Lesions in supplementary motor area interfere with a monkey’s performance of a bimanual

coordination task. Neurosci. Lett. 27, 267.-270, 1981. 2. BRINKMAN, C. Supplementary motor area of the monkey’s cerebral cortex: short- and long-term deficits after

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PERFORMANCE ON IJNIMANUAL AND RIMANUAL TAPPING TASKS 91

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