h’eumprychol~ia, Vol. 29, No. 1, pp. 47-58,1991. Printed in Great Britain.

00%3932/91 53.00+0.@l 0 1991 Pcrgamon Pm8 plc

CONTRIBUTION OF THE RIGHT FRONTAL LOBE TO THE ENCODING AND RECALL OF KINESTHETIC DISTANCE

INFORMATION

GABRIEL LEONARD* and BRENDA MILNEZR

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

(Received 2 March 1990: accepted 20 August 1990)

AIrstract-Sixty-two patients with unilateral temporal- or frontal-lobe excisions and 16 normal control subjects were tested on a kinesthetic task, which required the monitoring of peripheral feedback in order to duplicate the distance of examiner-defined arm movements. Temporal lobectomy did not interfere with performance. Patients with left frontal-lobe or small right frontal- lobe excisions also performed normally, whereas those with large right frontal-lobe removals were impaired, the deficit being equal for the two arms. The results point to an important role played by the right frontal lobe in the monitoring of kinesthetic feedback both during the presentation of the movements and during the recall attempt.

INTRODUCTION

KONOR~KI [ 161 has suggested that the prefrontal cortex is of critical importance in processing movement-produced feedback from muscle receptors. Following Konorski’s suggestion, several attempts have been made to ascribe delayed-response and delayed-alternation deficits to a difficulty in monitoring feedback from proprioceptors. Although these attempts failed [7,21], some evidence in support of an important contribution of the frontal lobes to the processing of kinesthetic cues evolved. In particular, a study by MISHKIN et al. [23] raised the question of whether spatial delayed-response impairments, seen after dorsal prefrontal lesions, might be attributable to a more general deficit in kinesthetic discrimination. These authors found that combined bilateral removal of the dorsal prefrontal and dorsal premotor areas resulted in chance-level performance on the relearning of a go/no-go kinesthetic discrimination task, which was uncontaminated by spatially directed responses. The animals had been trained to discriminate between small (20”) and large (40”) angular displacements of a lever. To prevent location cues from being used, the starting-point of the lever was varied randomly between two positions. Deficits were not found following lesions of either the dorsolateral prefrontal cortex or the dorsal premotor area alone, but were contingent upon the removal of both areas. These results suggest that both the dorsolateral prefrontal and the dorsal premotor cortices play a role in the processing of kinesthetic information.

The systematic experimental investigation of short-term kinesthetic memory in human

*Address for correspondence: Gabriel Leonard, Department of Neuropsychology, Montreal Neurological Institute, 3801 University Street, Montreal, P.Q., Canada H3A 2B4.

47

48 G. LFZONARD AND B. MILNER

subjects began with the experiments of ADAMS and DIJKSTRA [ 11, who looked for a possible similarity between short-term verbal memory (STVM) and short-term motor memory (STMM). Adams and Dijkstra proposed that STMM follows the same laws as STVM, because they found that error in the reproduction of linear arm movements also increased rapidly as a function of retention interval, and that the number of repetitions of the criterion movement before the recall interval was a factor in improving performance, although more repetitions were required to produce an effect than for STVM. Adams and Dijkstra were led to conclude that the movement cues were not coded in terms of verbal labels, on the grounds that such labels could not have been finely scaled enough to identify movements that differed from each other to the extent of only 4 cm. Kinesthetic memory for discrete movements has not been studied in patients with focal brain lesions.

The main goal of the present study was to examine the effects of frontal-lobe lesions on the encoding and reproduction of distance information derived from kinesthetic cues. It was hypothesized that, if the frontal lobes are critically involved in monitoring information related to movement, then subjects with frontal-lobe lesions should perform poorly on a task that depends on feedback from muscles in order to develop an internal representation of the distance traversed.

A second goal of this study was to examine the ability of patients with temporal-lobe lesions to reproduce arm movements when an intratrial delay was imposed and vision was excluded. In view of the important contribution of the right hippocampal region to the recall of visual location [S, 281, and of the left hippocampal region to the recall of simple verbal material after a distraction [S], the contributions of the right and left hippocampal systems to the retention of information supplied kinesthetically was a question of interest.

METHOD Subjects

Each patient who participated had undergone a unilateral cortical excision at the Montreal Neurological Hospital. The operations were carried out for the relief of focal cerebral seizures. In most instances, the epileptogenic lesion dated from birth or early life and was static in nature; however, the sample also includes 18 cases of indolent tumours. Patients who had independent electrographic abnormalities arising from both hemispheres, or who had evidence of fast-growing tumours or diffuse cerebral damage were excluded, as were those known to have right- sided, or bilateral, speech representation, as demonstrated by preoperative intracarotid Amytal tests [Z]. Only patients between the ages of 16 and 60 with Full-Scale Wechsler IQs above 80 were tested.

The hand preference of each subject was assessed by means of a modified version of the questionnaire developed by CROVITZ and ZENER [6]. On this scale, a score of 29 or less signifies a strong preference for the right hand [22]; all subjects accepted had a score below this cut-off point.

In order to ensure that subjects had no motor or sensory deficits that could have interfered with their test performance, the strength and the somatosensory status of the hands were established beforehand. Grip-strength was measured by having the subjects pull on a wooden handle connected to a Dillon Tensile-Force Gauge, graduated in pounds [30]. Three readings were taken for each hand in a balanced order, beginning with the hand ipsilateral to the lesion. For men, scores below 75 lb for the right hand, and 74 lb for the left hand, resulted in exclusion from the study. The corresponding scores for women were 50 lb for the right hand and 49 lb for the left hand. These cut-off scores had been established for a normal control group matched to the patients in the present investigation with respect to age, education and socio-economic status [19]. The sensory status of the hands was determined by quantitative testing [4]; the measures used included two-point discrimination on the palm and sense of passive movement of the fingers. All patients obtained normal scores for both hands on these tests and on a test of tactual object recognition [4].

Subjects were assigned to eight groups as shown in Table 1; the sex distribution, mean age and mean education for all the groups and the mean Wechsler Full-Scale IQ and time of testing for the patient groups are also given. Separate one-way analyses of variance failed to reveal any significant differences between the groups with respect to age (F=0.76, d.f. = 7, 70, P=O.62) or education (F= 1.06, d.f. = 7, 70, P=O.39), and the patients groups did not

KINESTHETIC INFORMATION

Table 1. Kinesthetic distance: main subject groups

49

Time of testing

Group &2X Age (yr) Education (yr) Wechsler IQ Post- Follow-

M F Mean Range Mean Range Mean Range operative up

Left temporal small hip- pocampal removal

Left temporal large hip- pocampal removal

Left frontal Right temporal small

hippocampal removal Right temporal large hip-

pocampal removal Right frontal small remo-

val Right frontal large remo-

val Normal control

4 4 31.8

4 4 32.4

I 1 30.8 2040 13.0 8 5 21.1 17-45 11.7

4 3 28.6 17-37 10.1

6 4 31.4 16-57 10.8

5 3 30.6 2045 11.6

IO 6 26.8 1555 12.4 8-16

1745

2145 11.6

10.7 612

3-16

7-18 8-15

l&11

7-19

l&14

111.5 89127 3 5

111.1 94-129 1 7

98.0 8&113 7 1 112.8 84129 6 7

100.8 85123 2 5

108.7 94132 3 7

100.1 8&119 1 7

not assessed -

Temporal-lobe groups. The patients within the temporal-lobe groups were subdivided according to the extent of removal from the hippocampal region. This method of classification resulted in four groups: two left temporal-lobe groups (one [LTh] with small, and one [LTH] with large removals from the hippocampal region), and two right temporal-lobe groups (one [RTh] with small, and one [RTH] with large hippocampal excisions). The hippocampal removals were classified as small or large on the basis of the surgeon’s drawing and report at the time of operation. The removal was considered to be small if no more than the pes of the hippocampus was excised, and large if the excision encroached further upon the body of the hippocampus or the parahippocampal gyrus. The removals in all cases included the anterior temporal neocortex and the amygdala.

Frontal-lobe groups. For the patients with frontal-lobe resection, the extent of the removal was considered important, because, in an initial study of kinesthetic memory using the same paradigm [18], only patients with large frontal-lobe lesions had sufIered a deficit. Since the left hemisphere was dominant for speech in all cases, the removals from the left frontal lobe tended to be more conservative than those from the right and only two patients had large removals. Therefore, the subjects who had left frontal-lobe lesions were assigned to one group (LF) for all analyses. The patients with right frontal-lobe excisions had approximately equal numbers of subjects with small (RFS) and large (RFL) resections of the frontal cortex. Hence, for all experiments, these patients were maintained in two separate groups. The classification of lesions into small and large was carried out by an independent judge.

Lefttfrontal-lobe group

The resected area for the patients who underwent left frontal lohectomies is illustrated in Fig. 1. Only two patients in this group had large removals (Dw. Mi., No. Sa.). Two patients (An. Co., Wi. Wh.) had limited removals from the dorsolateral cortex and three had dorsolateral removals, which extended forward to include the frontal pole (Ke. Ke., Ra. Ja., Sy. Ra.). In one patient (Ho. Sp.), the removal was confined to the orbital frontal cortex. The LF group contained four cases of low-grade astrocytoma (An. Co., Dw. Mi., Ho. Sp., and Wi. Wh.) and one case of arteriovenous malformation (Ke. Ke.).

Right frontal-lobe group with small removals

Figure 2 shows the cortical excisions for the 10 patients in this group. Three patients (Da. Co., Br. Fo., Ja. Ne.) had excisions from the orbital and inferior lateral cortex, and the remaining six had lesions which partially encroached on the dorsolateral and medial surfaces. Five patients had low-grade astrocytomas (Ro. Bo., Br. Fe., Br. Fo., GI. Ji., El. Sa.).

Rightfrontal-lobe group with large removals

Figure 3 shows the cortical excisions for the eight patients in the RFL group. All patients had removals which encroached extensively upon both the medial and dorsolateral surfaces; and except in the case of Bo. Gr., the removals also included the orbital cortex.

Normal control subjects. A normal control group (NC) of 16 was selected to match the patient groups as far as possible with respect to sex, age and level of education (see Table 1).

50 G. LFDNARD AND B. MILNER

An

Ho. Sp.

Q2J

Ke. Ke.

c3

Sy. Ra.

c3

/

Wi. Wh. __

No. Sa. -

c3

Dw. Mi.

49

Fig. 1. Diagrams based on the surgeon’s drawings at the time of operation, showing the estimated extent of the cortical excisions for subjects in the left frontal-lobe group. For all figures illustrating frontal-lobe resections, the medial view (above) and the inferior view (below) will be included

whenever available, together with the lateral view.

Apparatus and procedure

The apparatus used was a slightly modified version of the Manual Lever D, described by SULZER [31]. The top drawing in Fig. 4 shows the examiner’s view of the apparatus, which consisted of a movable lever (0.9 cm in diameter) mounted on a flat board. The radius of the lever was 30 cm, as measured from the centre of the shaft to the top of the grip. The total possible range of movement was 140” (73.3 cm of the arc) and the scale, which was attached to the examiner’s side of the instrument, was marked in one-degree steps. A metal plate, mounted on the same side as the scale, had holes drilled at each degree of the arc, thus enabling the examiner to insert a metal rod to stop the lever at any predetermined position.

The subject was seated on an adjustable chair, the head being supported by a chin rest which was mounted on the testing table. An opaque screen was attached to the chin rest which prevented the subject from seeing his hand or arm (see Fig. 4).

At the beginning of the first testing session, the subject was informed that the experiment would involve movements of the arm and hand. It was explained that the test would be run with vision excluded, and that the body and head position would be kept constant by the use of the chin rest.

The subject began the test by placing the hands, palms down, on the table. The position of the apparatus was then adjusted so that no movements ofeither hand would cross the midline of the subject’s body. The examiner guided the subject’s hand to the lever, with the instruction that it be grasped with a full grip (see Fig. 4). The subject was then allowed to move the lever until the full range of possible movements had been explored. It was required that movements be made smoothly and at a constant speed, as demonstrated by the examiner. The movements were always to be made away from the subject’s body, as shown for the right hand in Fig. 4.

KIN&WHEllC INFORMATION 51

Da. co. m Ja. Ne. a \

El. Sa.

m

Ja. Ro. , _

Do. co. a

Ro. Bo. -

CD GI. Ji.

Fig. 2. Diagrams showing the estimated extent of cortical excision for the patients in the right frontal- lobe group with small removals.

Six practice trials were then given, three with each hand, preceded by the following instructions:

I am now going to place your hand on the lever. Move the lever until it comes to a stop; remember the distance moved, and replace your hand on the table.

The lever was then moved to a new starting position and the subject’s hand was replaced on the lever with the instruction to move it through the same distance as before. After completion of the practice trials, the examiner said:

From now on, you will be asked to reproduce the movement either immediately after you have made it, or following a &lay, during which you will sometimes have to count backwards by threes from a number that I will read to you. (An example of a three-digit number was then given.)

On the rare occasion when a subject had difficulty in understanding the instructions, additional practice trials were given until the correct procedure was established. No subjects had to be excluded because of failure to follow instructions.

It was explained to all participants that trying to remember the location of the finishing point would not be

52 G. bDNARD AND B. MILNJZR

Mi. To.

m

Da. Br.

I-l’r

Jo. Ed.

m

Ka. Wh. __

R

Fig. 3. Diagrams showing the estimated extent of cortical excision for the patients in the right frontal- lobe group with large removals.

beneficial, because the starting position for the recall movement would always be different from that used for the criterion trial (i.e. the standard given by the examiner). Starting and finishing points were selected such that as much of the scale as possible was sampled over the entire range of movements. In addition, some recall movements were performed in a part of the scale not utilized for the standard movement. Each subject received 120 trials, divided equally between the hands; 30 trials with each hand were administered in two 60-nin sessions on consecutive days.

The 120 trials encompassed 30 different angle sizes, repeated four times. The angles ranged from 4” to 90”, and were designated as small (4”-20”), medium (24”48”) or large (56”-90”) on the basis of previous studies [12, 18). These three angle-size categories each contained 10 unique angles. In order to randomize the order of presentation of the angles, two blocks of trials (each consisting of 15 angles, with an equal number of small, medium and large) were constructed. Angles in the same category were not allowed to follow one another more than once within each block. Blocks of angles were presented to the patients either in the order ABBA (starting with the hand ipsilateral to the lesion), or BAAB (starting with the hand contralateral to the lesion). These orders were alternated within groups (including the normal control group) for successive subjects.

For the reproduction of the angles, four different recall conditions were employed: less than 5 set (termed immediate); 30 set unfilled interval; 15 set with an interpolated counting task; and 30 set also with an interpolated counting task. These four recall conditions were distributed over the two testing sessions in such a way that, within each of the three categories of angle size (small, medium and large), the four recall conditions each recurred 10 times.

KINESTHETIC INFORMATION 53

Fig. 4. Modified version of the Manual Lever D (SULZER [31]). Above: examiner’s view. Below: subject’s position with respect to the apparatus. The arrow indicates the direction of movement for the

right hand.

RESULTS

The data from this experiment were analyzed in terms of absolute error, the difference between the criterion movement and the subject’s actual response score, without respect to sign. The Newman-Keuls multiple-comparisons method, with the corresponding pooled error term and Satterthwaite degrees of freedom where appropriate, were used for all a posteriori testing [ 13, 331.

The analyses of variance contained four factors; thus the experimental design employed was an 8 x4x 3 x2 (GroupxRecall Conditionx Angle SizexHand) with repeated measures over the last three factors. The Greenhouse and Geisser correction was applied to all factors with repeated measures [8].

54 G. LEONARDANDB.MILNER

Absolute error

Main effect of recall condition. Recall condition did not interact with group but there was a significant main effect (F= 64.95, d.f. = 3,210, P-C O.OOl), which is illustrated in Fig. 5. Post hoc analyses revealed that performance was most accurate in the immediate

Wkhout Counting With Counting

OS 30s 1%

Recall Condition

30s

Fig. 5. Absolute error: main effect of recall condition. Increased error is associated with delay, and the interpolated counting task further interferes with accuracy.

recall condition (q> 10.0, PcO.01 vs all other conditions). Recall accuracy deteriorated significantly over 30 set by approximately the same amount as over 15 set with interpolated activity, the difference between these two conditions being non-significant. Both 30 set without, and 15 set with interference were associated with significantly better performance than 30 set with distraction (q > 7.0, P < 0.01 for both conditions vs 30 set with distraction). The difference between 30 set without distraction and 30 set with distraction although small is consistent, and indicative that distance information is, to some extent, codable [9, 11, 12, 17, 24, 321.

Group x Angle Size x Hand interaction. The absolute-error analysis yielded a three-way interaction between group, angle size and hand (F=2.31, d.f. = 14, 140, PcO.01). Post hoc examination of this interaction, with respect to between-group differences, revealed no significant findings for small- or medium-sized movements, irrespective of the hand used. In contrast, for the large angles (see Fig. 6), the performance of the RFL group was significantly impaired with both hands. When using the left hand, this group of subjects was impaired relative to the NC subjects and they also differed significantly from the LTh, RTh and LF groups (q=6.15, PcO.01; q=5.67, PcO.01; q=4.65, P~0.05; and q=4.63, P~0.05, respectively). With the right hand (i.e. the hand ipsilateral to the lesion), the RFL group was again impaired with respect to the NC group, and also to the patients in the LTH group (q=4.28, P~0.05; and q= 5.16, PcO.01, respectively). There were no other between-group

KINESTHETIC INFORMATION 55

10-

15 -

9-

8-

L

Group

N

q Left Hand

w Right Hand

LTh LTH

8 8

LF

8

T

RTH

7

RFL

8

Fig. 6. Absolute error (large angular displacements): Group x Angle Size x Hand interaction. The RFL group is impaired with both hands relative to the NC group. In addition, when using the left hand, the RFL group differs significantly from the LTh, RTh and LF groups. When using the right

hand, the RFL group performs worse than the LTH group.

differences. Patients who had small removals from the right frontal lobe and those who had left frontal-lobe excisions performed equally well with both hands.

The Group x Angle Size x Hand Interaction was then examined in terms of within-group differences, and the following pattern of results emerged. The NC subjects performed similarly with both hands for small- and medium-sized angles. However, they were significantly more accurate with the left hand (see Fig. 6) for the large angles (q= 3.63, PcO.05). Subjects in the RFS, RFL, RTh, RTH and LF groups had no significant difference between the hands for small, medium or large movements. The LTh group performed better when using the right hand, for both small- and medium-sized movements (q = 3.15, PcO.05; q=6.75, P~0.01, respectively). However, for the large angles they showed a left-hand advantage similar to that shown by the NC subjects (q = 3.88, PcO.05). The patients with LTH removals had a right-hand superiority for medium- and large-sized movements (q=3.46, PcO.05; q=6.51, PcO.01, respectively).

DISCUSSION

A general finding in this kinesthetic recall task was that accuracy was greatest in immediate recall and became less over time. The presence of an interpolated task in the recall interval had a deleterious effect on recall accuracy, and in this regard the 30 set recall condition with interpolated counting activity was associated with the largest error scores. The observation that accuracy decreases following a delay is consistent with SCRIPTURE’S [26] statement that the memory trace for kinesthetic information decays spontaneously over time. The fact that performance was negatively affected when subjects had to perform an

56 G. LEQNARD AND B. MILNFR

interpolated task during the recall interval suggests that the kinesthetic cue employed in the present study was, at least partially, coded centrally.

Although POSNER and KONICK'S [25] finding for kinesthetic short-term memory, that there is spontaneous decay over time, was subsequently replicated by WILLIAMS et al. [32], the latter authors demonstrated that a kinesthetic interpolated task (unlike a verbal one) produced increased forgetting over a 30 set interval. They interpreted their finding to mean that kinesthetic distance cues were in fact being coded, and therefore susceptibility to interference was an important aspect of STMM. Williams et al. also concluded that the neurobehavioural mechanisms for verbal and kinesthetic short-term memory are indepen- dent processes.

In the present study, left or right temporal lobectomy (irrespective of the extent of the hippocampal excision) did not impair performance. It is particularly interesting that patients who underwent extensive removals from the right hippocampal region performed well, a finding that is in contrast to the deficit that such patients display for recall of visual location, whether for the position of objects in a complex array [28], or simply for the position of a spot on a line [S]. The finding of no deficit on the present task may be related to the difference between the kinesthetic and visual modes, or to the different cognitive demands made by location and distance cues. For location, topographical relationships are preeminent, whereas in remembering distance traversed (with location cues made unreliable) the subject must code the extent of the movement without regard to the position in space where it was initially performed.

Patients with large right frontal-lobe lesions were impaired in reproducing the extent of the large angular displacements, and there was no interaction with recall condition. Therefore, the deficit could be interpreted as a failure of this group to monitor feedback from the periphery in the encoding and/or reproduction of large movements. In contrast to the deficit on the present task, patients with large right frontal-lobe lesions had been indistinguishable from normal control subjects when recalling visually the location of objects in an array, even after 24 hr [29]. The findings are consistent with the idea that kinesthetic and visual cues are processed differently [ 17,24,32-J, and demonstrate a double dissociation between the effects of a frontal- and a temporal-lobe removal on the recall of kinesthetic distance and visual location. This dissociation is particularly convincing, because seven of the eight patients with large right frontal-lobe lesions in the present study had also participated in Smith and Milner’s object-location experiment.

The overall analyses revealed no hand differences, and this finding rules out the possibility that the deficits were consequent to awkwardness or to a slight reduction in strength in the hand contralateral to the removal. The finding of bilateral deficits following unilateral frontal-lobe lesions is consistent with the results of other movement-related studies [ 10, 15, 20, 343.

None of the patients examined in this investigation demonstrated contralateral neglect, either of external space or of their own bodies. Even had they done so, the fact that the hand- movements never crossed the midline of the body would counter the suggestion that the impairment ensued because the subjects with right frontal-lobe lesions neglected the contralateral half of space [27].

Although patients with extensive right frontal-lobe removals were impaired when reproducing large movements, the fact that they were able to reproduce small- and medium- sized movements normally, within the same block of trials, argues against the deficit being a consequence of proactive interference from one trial to another. The impairment was not

KP4BTHETlCINFORMATlON 51

dependent on recall condition, being evident irrespective of delay, thus strengthening the notion that the deficit was primarily one of encoding. The fact that the impairment only emerged for the large movements may be related to an inability of the right frontal-lobe group to monitor the additional kinesthetic feedback provided by these large angular displacements. It is possible that the difficulty may also be related to a similar inability to monitor the kinesthetic feedback from the reproduction movements.

The side of frontal-lobe resection also appears to be of critical importance since the patients in the left frontal-lobe group were efficient at recalling the extent of their arm movements, regardless of the distance covered, and despite the fact that the group contained patients with lesions as large as those of the subjects in the group with extensive right frontal- lobe resections (see Fig. 2, No. Sa., Dw. Mi.). It is interesting that the patients with left frontal-lobe lesions, whether small or large, obtained normal scores, despite the fact that the majority of them were tested from 2 to 3 weeks following the surgical intervention, whereas the patients with large right frontal-lobe lesions were practically all tested in long term follow-up. The finding of normal performance for the subjects with left frontal-lobe excisions is in sharp contrast to the severe impairment of the same patients on a bimanual tapping task [20]. Failure on the tapping task might have been related to difficulty in performing the required sequence of movements [14]; the task used in the present investigation involved single movements and therefore ordering was unnecessary.

In conclusion, an important role for the right frontal lobe in the encoding and the recall of examiner-defined movements has been demonstrated. The results are in accordance with the earlier findings of CARMoN [3], who had shown that patients with extensive right-hemisphere damage were impaired in their ability to monitor kinesthetic-tension information. Although it was not possible to identify a region within the frontal lobe that is critical for kinesthesis, it is worth noting that the large lesions included parts of the prefrontal, premotor and supplementary motor cortices, and that lesions confined to any one of these regions were not sufficient to produce a deficit. This latter observation is similar to the finding of MISHKIN et al. [23] that monkeys with lesions restricted to the dorsolateral or premotor region performed normally on a movement task, whereas those animals that had combined lesions of these two areas had impressive deficits. In the present study, the laterality of the lesion was an important factor contributing to the observed deficit, suggesting some right-hemispheric specialization for the encoding and subsequent recall of kinesthetic distance information.

Acknowledgements-This study is based on a thesis submitted by Gabriel Leonard in September 1987 to McGill University in partial fulfilment of the requirements for the Ph.D. degree. The research was supported by Grant MT 2624 to Brenda Milner. We are grateful to Drs T. Rasmussen, W. Feindel, A. Olivier and J. G. Villemure of the Montreal Neurological Hospital for the opportunity to study their patients, and for providing detailed descriptions of the surgical removals.

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