Transient left-sided alien hand with callosal and unilateral fronto-mesial damage: A case study

Neuropsychologia,Vol. 33, No. 12, pp. 1703--1709,1995 Copyfi'ght© 1995 ElsevierScienceLtd Printed m Great Britain. All fightsrcserv~ 0028-3932/95 $9.50+ 0.00

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0028-3932(95)1111044-5

NOTE TR ANS IE N T LEFT-SIDED ALIEN H A N D WITH CALLOSAL AND U N I L A T E R A L FRONTO-MESIAL DAMAGE: A CASE STUDY C. P A P A G N O * t and C. MARSILE:~ *Clinica Neurologica 11I, Universith di Milano, Milano, Italy and :~Divisione di Neurologia, Ospedale di Melegnano, Vizzolo Predabissi, Italy

(Received 13 December 1994; accepted 17 March 1995) Abstraet--A patientwho showed a transientleftalienhand aftera subarachnoid haemorrhagc, due to a ruptured aneurysm of the anterior communicating artery,is described. N o leftagraphia and leftapraxia could be found. A CT-scan including coronal sectionsshowed a right medial frontal hypodensity and different ischacmic lesions in the anterior part of the corpus callosum. The possible anatomic siteof the lesionresponsiblefor the permanent form of alien hand is discussed. Key Words: alien hand; callosal damage.

INTRODUCTION Alien hand (AH) has been now described in a consistent number of patients who suffered from a lesion of the corpus callosum and frontal lobe (for a review, see e.g. [5] and [7]).It denotes (with some variation in the use of the term) the occurrence of unintended, well-ex~uted, goal-directedcomplex movements of an upper limb, which sometimes interferewith intended actions carried out by the other hand. T w o main matters are discussed:the firstregards the lesionthat causes thissymptom to become chronic and the second the possible clinicaloutcome in relationto differentanatomic sites[5].While there is an almost general agreement that at leasttwo forms of A H exist, a frontal [10] and a caUosal one, the debate has focused on the lesion responsible for the 'chronicity'.Goldberg [8] has proposed that the A H sign would result from an imbalance between the influence of the medial as opposed to the lateral premotor system of the damaged hemisphere: thislastwould be releasedto facilitateaction responsive to the sensory context. It has been suggested [9] that the recovery could be explained by a compensatory process in which the intacthemisphere ipsilateralto the affected hand exerts control over the proximal segments of the limb through ipsilateralprojcctious from promoter regions. Bihcmispberic damage would render thiscompensatory mechanism impossible and A H would become chronic. The same possibilitywas hypothesized by Gasquoine [7] who has concluded, on the basis of a review of 20 published cases,that alienmovements are oRen transient,typicallydisappearing within the firstyear; they persist when the lesion involves bilateral cortical and subcortical structures. However, there are cases o f AH, persistingmany years after surgery, in patientswith unilat~al lesion [5].I~Ua Sala et al. [5] have suggested an alternative hypothesis, i.e. that a callosal lesion is sufficientfor the appearance of A H , but a lesion of the supplementary motor area (SMA), contralatcralto the involved hand, would cause the 'chronic'form. W e report the case of a w o m a n who showed a leftA H without leftidenmotor apraxia and agraphia, who recovered after 4 months, despite ischaemic lesions to the anteriorpart of the corpus callosum and in the right medial frontal lobe. W e discuss the possibilitythat only extensive damage to the corpus r~allosum, involving at least the anterior two-thirds of it,can produce a permanent A H sign.

tAddressfor correspondence: ClinicaNcurolo~ca III,Ospcdale San Paolo aUa Barona, via A. Di Rudini 8, 20142Milano, Italy. 1703

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NOTE CASE REPORT

A.S. is a 40-year-old right-handed woman, with 13 years of education, who, on 26 September 1993, suffered a subarachnoid haemorrhage (SAH) with an intraparenchymal haematoma due to a ruptured aneurysm of the anterior communicating artery. On the same day she was operated on to clip the aneurysm. After she roused from 1 week in coma, she showed disorientation in place (she professed to be in Rome, while she was in a small town near Milano), but no disorientation in time, and she had a mild right hemiparesis. She was slightly disinlaibited and also reported occasional urinary incontinence. From the very first days, A.S. began to show a severe intermanual conflict. For instance, one day while she was trying to undress in the toilet, the AH started to dress her again, so that she had to call for help to take off her pants. In another occasion, she paid for the newspaper with the right hand, while the left was keeping back the money. The left hand also carried out activities hurting the patient: once she was trying to take something out of a drawer, the left hand suddenly closed it and her fight hand was severely hurt. Once discharged, she told us that in a shop she was buying something, while the left hand was stealing an orange. The patient used to speak to her left hand as if it was another person, but never denied that this was hers: she defined it as a 'cheeky' hand that could not be kept under her will; "she is always trying to anticipate my actions" was her major complaint.

Neurological examination When seen on 18 October, A.S. showed only mild balance disturbance with retropulsion. Other motor signs had cleared completely. Cortical disinhibition signs, including grasping, were absent, while there was a mild perseveration of motor acts.

Neuroradiology The first CT-scan performed the same day of the SAH showed a wide intraparenchymal haematoma in the fight frontal lobe, which extended to the interhemispheric fissura, where subarachnoid blood was present. A CTscan performed a month later disclosed a fight frontal hypodensity. Because of the metal clips in the patient's head, an MRI could not be performed, but A.S. underwent a CT-scan exam with coronal sections on 6 December. This showed, beyond the fight fronto-basal lesion, ischaemic lesions of the corpus callosum probably due to occlusion or vasospasm of pericallosal arteries, predominantly in its left part and sparing the splenium (Fig. 1).

RESULTS

Neuropsychological general examination The neuropsychological examination excluded global cognitive deterioration (Table 1). The patient was cooperative, oriented in time, but not in place. There were no verbal memory deficits, both of short- [16] and longterm memory [14], but an impairment in visuo-spatial tests, which was also evident in supra-span learning [1], was present.

Control functions The only 'frontal' signs were a mild perseveration, with inability to reproduce Luria's rhythms, and a low verbal fluency on phonological cue [15], but other tests said to assess frontal functions (such as Weigl Sorting Test, Wisconsin Card Sorting Test and Digit Cancellation Task) were normal (see Table 1) [17].

Callosal signs We checked A.S. performance in a number of tasks devised to show a callosal syndrome, considering that A.S. had multiple ischaemic caUosal lesions and that patients with AH usually show features of the disconnection syndrome. There were almost no 'callosal phenomena': (1) no aphasic errors when writing with the left hand in response to dictation (see Fig. 2); (2) a single error in naming 10 objects manipulated with the left hand without visual control (a gun was called a hammer, perseverating the previous item); (3) 12 gestures executed on verbal command with the left hand and 12 with the left fingers were not performed significantly worse than with the fight; (4) tactile cross-localization of fingertips was errorless; and (5) cross-replication of postures of one arm or hand outside the visual control was very difficult only when the left hand had to replicate fight hand postures, while the patient could perform correctly in the other direction. A.S. reported that she (the AH) refused to execute the task.

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Fig. 1. A.S.'s CT-scan. (a) Right fronto-r~sial hypodensity; Co) and (c) ischaemic lesions of the corpus callosum in coronal sections.

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NOTE Table 1. A.S.'s performance in a formal psychometric battery. All scores have been adjusted for age, education and sex

Memory functions Digit span Paired associate Spatial span Short story Supra-span learning Control functions Weigi Sorting test Wisconsin Card Sorting test Raven Coloured Progressive Matrices Verbal fluency on phonological cue Luria rhythms Digit Cancellation test

28.10

11.11

5.50 9 2.25 14 0.25

5.50 10 3.25 14 3.25

12 6 18.5 18 0/8 34.75

12 6 25.5 20 3/8 38.75

Language Boston Naming Test Token Test

52/60 32/36

Visual perception Street's completion test (0-14) Benton orientation (0-30) Cancellation test (shapes)

4 16 50/50

Normal score >3.75 >6.50 >3.50 >8 >6.75 >4.75 >3 > 18 _>17 >31

>29 5 20

>2.25 >21

Cut-off scores for digit and spatial span are from Orsini et al. (1987); for paired associate and short story from Novelli et al. (1986a); for supra-span learning from Capitani et al. (1991); for verbal fluency from Novelli et al. (1986b). The remaining cut-off from Spinnler and Tognoni (1987). The alien hand

In performing some neuropsychological tests which required manipulation or utilization of objects, a conflict between the two hands became evident, with each of them acting in competition. During the Weigi Sorting Test, for example, the right hand was setting the pieces together, while the left was picking them up, so that the examiner had to retain her left hand in order to have the patient complete the performance. The same phenomenon was present during apraxia test, because the left hand tried to prevent the right's movement. A.S. reported that the left hand was acting as if she wanted to 'arrive first' at what she intended to do, as if she was 'in competition' with the right. Follow-up

The patient was tested again 15 days later: she was now well-oriented in place, and visuo-spatial tests had improved, even if still defective; perseveration in rhythm reproduction was still present. Further examinations were performed 2 and 4 months after the accident. On the last occasion, the patient indicated that AH had almost disappeared from everyday life and during the tearing session the sign was no longer elicitable. All tests now reached normal scores, even visuo-spatial tests and reproduction of rhythms.

DISCUSSION Our patient had an extensive lesion of the right fronto-basal cortex and small multiple ischaemic lesions of the anterior part of the corpus callosum, predomiaanfly on the left. Despite these lesions, A.S. showed no major signs of callosal syndrome and only mild signs of frontal involvement, her malfi symptom being aleft AH. As mentioned in the introduction, Delia Sala et al. [5], after a wide review of the literature, stated that a simultaneous damage to the corpus callosum and unilateral fronto-mesial cortex is necessary for AH to become chronic. In support to this hypothesis, they cited thcir case G.P., Goldstein's case and Trojano et al.'s patient. Nevertheless, if one carefully looks at the 11-montha follow-up in this last case [19], it appears that it does not represent a permanent AH: indeed, the intermanual eonllict is already inconsistent after 2 months and the main dtrangdre has disappeared; at the third month also the lack of bimanual coordination is inconsistent and so is AH

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NOTE

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Fig. 2. Writing to dictation with the right (left side) and the left hand (right side).

at the fifth month. One is inclined to think that the sign is progressively recovering and we can at least wonder whether it will be found if the subject is examined at a still longer interval. In other words, AH seems to be transient, in the sense meant by Gasquoine [7], i.e. slowly disappearing within the first year after stroke. A careful examination of cases of persistent AH (see Table 1 in Ref. [5]) shows that all patients had evident disconnection signs, in relation to massive callosal lesions. An alternative hypothesis to explain a permanent AH could be, therefore, that the extent of the callosal damage is a crucial factor in the recovery of the symptom. In transient (even if persisting for some months, and in this sense 'chronic') cases, such as ours or Trojano et aL's [19], disconnection signs are constantly absent. A small (or multiple) lesion of the anterior part of the corpus callosum is not sul~cient to produce a persistent AH, which appears to be a callosal disconnection sign. Della Sala et aL [4] had already proposed a specular hypothesis: they suggested that a callosal lesion is necessary for the appearance of AH, but that to continue there must be a fronto-mesial lesion encroaching upon the SMA contralateral to the AH. By contrast, we suggest an opposite possibility: first of all, given that most of the AH cases with fronto-mesial lesion are usually described after anterior communicating artery aneurysm, we think that a lesion of the anterior part of the corpus callosum cannot be excluded for certain; secondly, even if a frontomesial lesion could be sufficient to produce an AH, the presence of disconnection signs suggests that only extensive involvement of the corpus callosum would be responsible for the permanent form. In line with the hypothesis that the extent of the callosal lesion is crucial, there are the data of partial caUosotomy (see for example, Ref. [11]), which show that circumscribed sections of the corpus callosum preserving at least portions of the genu and posterior splenium (for example to remove tumours of the third ventricle) produce only transient (if any at all) disconnection signs. Of course, this does not necessarily refute the hypothesis that patients with bihemispheric involvement of frontal-mesial cortex are less fikely to recover from AH sign, but it would suggest that, in the presence of significant unilateral damage, residual function of the corpus caHosum is required to permit the recovery process to ensue. We think that two more points are worth underlining: first, as has been observed for example in subcortical apraxia [3], minimal variations in the site of a lesion can produce different patterns, and this could be applied to cases of transient vs persistent AH. Second, as already underlined for thalamic aphasia [2], no studies are devoted to the analysis of negative cases; in other words, case reports have consistently focused on positive cases and it is

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not known how many callosal and/or SMA lesions did not produce either transient or permanent AH. There are for example a large number of group studies on anterior communicating artery aneurysms, where there is no mention of AH (see e.g. [6], [12], [13], [18]). An evaluation of a series of all relevant cases would be a first rate contribution to the understanding of the anatomy of this syndrome. Acknowledgements--The authors wish to thank S. Della Sala and Clelia Marchetti for helpful suggestions and H. Spinnler for reading a first draft of the paper.

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