Article Text
Abstract
Alien hand syndrome (AHS) is rare, but important due to its disabling impact on everyday life. The determining characteristic of AHS is intermanual conflict, a type of inhibitory motor behaviour that occurs against willed action. Its components have previously been described as single case reports, but not as a systematic study. This review includes eight chronic cases, all of which are due to infarcts of the anterior cerebral artery. Clinical investigation included testing of motor behaviour related to everyday activities, such as tying shoelaces, lighting a candle and other bimanual tasks. Video-analysis showed that conflicting behaviour occurs in two distinct forms. One consists of interfering, rudimentary, hesitant and repetitive movements of the (alien) hand, often initiated by movements of the other hand. In some instances, disturbance of ongoing action is seen as spacious, ballistic-like extensions of the whole arm. This was most prevalent in three of the eight cases. In one patient, it was also seen as conflict with both feet (eg, when putting on slippers) or as a conflict of intentions (eg, when planning to enter a room). The other form consisted of massive groping and grasping behaviour as the most dominant features, such as a “tug of war between hands”, and was seen in five patients. Avoidance behaviour included sitting on the affected arm, holding it under the table or keeping objects out of reach. Enforcement of such strategies was used for rehabilitation and—although beneficial in the training sessions—carried over very little to everyday life. All cases had two distinct brain lesions, one in the genu or anterior rostrum of the corpus callosum and one in the contralateral frontomedial cortical and subcortical region.
Chronic AHS is the only clinical syndrome that shows complex inhibitory motor behaviour in a more or less pure form because it has become detached from the control of motor planning and execution. It can best be understood as sequences of complex inhibitory motor programmes that have become isolated from normal motor planning, which usually suppresses them via the contralateral cortico-subcortical prefrontal circuits and the corpus callosum. Thus, the mirror world of complex motor inhibition becomes clinically visible in such patients.
- hemispheric disconnection
- limb apraxia
- ideomotor apraxia, alien hand syndrome
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The alien hand syndrome (AHS) refers to apparently purposeful upper-extremity movements that the patient reports are beyond his/her control. It is rarely an isolated occurrence, as there is a high occurrence of associated motor phenomena such as loss of motor spontaneity, including hesitation of speech, limb dyspraxia, tactile dysnomia and a palette of frontal behaviour patterns. Almost all reports, including recent ones, are single case studies that have descriptions of varying detail.1–4 For the purpose of this review, we agree with Fisher5 who pointed out that the term “alien hand” originally had a restricted connotation: “Its scope has been expanded to apply, not always in consistent fashion, to several types of abnormal behaviour, such as movements of a limb which the patient regards as foreign, involuntary (unwilled), strange, uncooperative or interfering, the limb seeming to act on its own, outside the patient’s control”.
AHS was first described by Kurt Goldstein in 19086 who reported a case of a 57-year-old woman with paresis of the left hand. After the paresis improved, the patient reported that the left hand did not obey but rather did whatever it wanted by itself. Once, the left hand even strangled her neck and could only be loosened by force. In addition, he reported a notable slowing of spontaneous movements, but other non-volitional movements, such as stroking the hair or rubbing the nose, were performed with ease and without difficulties. Importantly, he stated that this was neither a paresis nor ataxia.
Brion and Jedynak7 coined the term “le signe de la main étrangère” in their report on three patients, denoting the experience of the hand as belonging to someone else or at least not to one’s own body. Zaidel et al8 described this syndrome in their study of epileptic patients who had been callosotomised. In these patients, two dissociated psychomotor phenomena had been described as a consequence of this operation: the alien hand and/or the intermanual conflict, the difference between these two not being consistently clear in the literature. It is well noted, however, that the French term denotes a misidentification resulting from failure of interhemispheric sensory transfer and has been misread as being synonymous with anything that gives the patient a strange feeling about his hand or limb.8
Goldberg et al9 described two such patients with additional vascular lesions in the medial frontal cortex and conclude from their observations that the underlying cause is a “faulty initiation, execution, and inhibition of preexisting essentially intact motor subroutines”.
Since these first descriptions, two seminal papers have been published on AHS, by Della Salla et al10 and by Feinberg et al.11
Della Salla and co-workers analysed 35 cases from the literature, including one personal case.10 They analysed all cases according to the lesion described, as well as the timing of investigations. They listed all cases according to preferred hand, grasp reflex, spontaneous grasping, mirror movements, callosal signs, alien hand, intermanual conflict, autocriticism, main étrangère, motor perseverations and transcortical motor aphasia. The authors conclude that that there is an acute, transient form that occurs in isolated lesions of the corpus callosum and a second, chronic form that additionally shows a frontomedial lesion. Della Salla et al stress that “we are not dealing with two wills, that of the right hemisphere and that of the left hemisphere,…but with an erroneous control of actions, in one hemisphere the internal/external balance being normal and the other imbalanced because the internal is virtually absent”.10 They come close to the interpretation given by Goldberg et al9 who postulated that the inner control of motor inhibition, which is guided via the arcuate premotor area to the motor cortex, is defective; it thus responds with defective inhibition, resulting in exploratory behaviour that is mediated via the frontal and prefrontal cortex. Della Salla et al. thus conclude that AHS represents a fragment of the frontal syndrome.10
Feinberg and co-workers11 review the clinical characteristics and neuroanatomy of 20 reported cases of AHS, add one personal case and come to the conclusion that there exist two distinct forms of AHS. One form is a frontal AHS that occurs in the dominant hand and is associated with reflexive grasping, groping and compulsive manipulation of tools. This syndrome results from damage to the supplementary motor area, anterior cingulated gyrus, and medial prefrontal cortex of the dominant hemisphere and the anterior corpus callosum. The other distinct type, callosal AHS, is characterised primarily by intermanual conflict and requires only an anterior callosal lesion. The authors explain the frontal type by the exploratory behaviour that is controlled via the dominant hemisphere being in conflict with asymmetrical inhibition within the non-dominant hemisphere.
More recently, a third type of AHS has been described and is referred to as posterior or sensory AHS and involves posterior cortical and subcortical areas.12 These cases have multiple disorders of sensation and sensory processing, with feelings of estrangement from the non-dominant upper limb. In addition, sensory, optic and cerebellar ataxia (triple ataxia) of the left arm has been noted.13
Despite the many acronyms and hypotheses involving AHS, all available evidence to date rests on single case descriptions and reviews of previously published cases. In these descriptions, the authors reported varying types of behaviour that seemed most remarkable, strange or perplexing either to the patients, their relatives or the author. Many observations, especially in the early surgical cases, were not made directly by the authors but were based on spouses’ reports and anecdotes. To our knowledge, no systematic study has been performed to date, especially one based on a prospective, video-documented protocol of standard motor tasks with relevance to everyday life. As most motor activities that are required in everyday life are more or less bimanual, special consideration was given to include such activities in our protocol.
PATIENTS AND METHODS
The authors have encountered eight cases that were due to a stroke in the frontal and/or callosal region, the details of which are described in the Supplementary Appendix. The patients were identified in the subacute stage of the brain infarct either on the basis of a behavioural description given by the nurses or therapists at the weekly staff conferences, or at the daily neuroimaging conferences, which depicted lesions that were suggestive of an AHS. One patient (TT) was referred from a neurosurgical department due to his behaviour being suggestive of AHS and the known authors’ interest in this field. All others were depicted from a stroke unit, including the adjacent stroke neuro-rehabilitation ward.
Six of the eight cases had been video-documented on repeated occasions, including training sessions during rehabilitation, and two cases were only documented by serial photography. Assessment for all cases included a neurological investigation, serial CT and/or MRI, standard laboratory examinations, colour-coded Duplex sonography, 12-lead ECG, echocardiography when indicated, as well as EEG, and other examinations when indicated. In addition, routine behavioural assessment included neuropsychological investigations, such as tests for visual or motor neglect, attention, orientation, memory, and speech production and comprehension.
Testing was performed with a protocol that focused on serial testing under standard conditions in the same room. Behavioural examinations included testing the ability for bimanual transfer. For this, an object (eg, hammer) was given to the patient and he/she was asked to give to the other hand and then back again. Usually, this was repeated several times. In most of the cases, this already showed prolonged grasping or groping behaviour. Utilisation behaviour was tested by spreading objects with everyday relevance on the table within reach for the patient, while engaging him/her into a conversation. If the patient did not spontaneously reach for these objects, one or the other was touched by the examiner to make sure that the patient took notice of these objects. Apraxia was tested for by standard tests14 and included testing with real objects.
For evaluation, a detailed review of the cases was undertaken and semi-quantitative ratings were given at the weekly staff conferences according to the clinical findings and the video-documentations, which showed the patients at the initial evaluation and at various stages of their training sessions in occupational therapy. Ratings were consensual among the weekly staff conferences and were given on a four-scale basis for grasping, groping behaviour, “Gegenarbeiten” ( = counteracting or working against; a definition chosen in analogy to “Gegenhalten” as seen and previously described in frontal lobe disease but with a phenomenological working aspect), main ètrangère , utilisation behaviour, ideomotor apraxia, autocriticism, avoidance behaviour, and sensory deficit (tactile anomia) with one cross delineating less pronounced behaviour and three crosses severely pronounced behaviour. If there were conflicting ratings among the therapeutic team members, the video sequences were reviewed repeatedly and consensus was achieved (see tables 1 and 2). Illustrative examples of patients 1 and 2 are given in figures 1–6.
For the purpose of this review, a literature search was undertaken, but due to the variations of published descriptions and their varying causes, a systematic search was difficult. In PubMed, there is no single MeSH heading for either “alien hand sign”, “main ètrangère” or “intermanual conflict”, but only for “apraxia” or “apraxia, ideomotor” (which clearly denote different signs). When using the text version of PubMed, we have found 28 single case descriptions, but most papers were identified through citations from other articles, reviews and discussion with colleagues who shared with us a longstanding interest in this disorder.
DISCUSSION
These cases show a spectrum of behavioural disturbances that have, to some extent, been previously described in such patients. Our cases vividly demonstrate that the significant symptoms of AHS represent a continuum rather than a clearly defined deficit behaviour. They represent a sample of systematically evaluated patients with chronic AHS that had been caused by strokes. Correspondingly, all eight patients had vascular lesions, including patient 2 who was operated for an epidermoid in the frontal interhemispheric cleft but had intraoperatively suffered an infarct of the left pericallosal artery, which included the callosomarginal branch. All lesions were located in the anterior portion of the corpus callosum, with an additional, second lesion encroaching on the upper medial frontal lobe. No case with a complete or isolated callosal lesion, or a posterior callosal syndrome, was included. Our patients were examined for up to 2 years (median: 3 months, range: 2–24 months). AHS was present on the right hand in three patients and on the left hand in five patients. All patients were right-handed. The sequence of the patient listings in tables 1 and 2 is, according to the severity of “Gegenarbeiten”, the first two patients showing a severe manifestation and the third a moderate form. Interestingly, three out of four patients with prominent “Gegenarbeiten” showed a left-sided lesion; all others were right-sided.
In some of our patients, the frontal symptomatology was overwhelmingly present. Forced tonic grasping resulted in the inability to let go with the symptomatic hand, which overshadowed most other symptoms, as was most impressively the case in patient 4 who became unable to perform most simple bimanual tasks (such as any kind of adaptive or correcting movement with both hands). On questioning, she clearly stated that the one hand “wants to give”, whereas the affected hand “wants to hold”, thus implying a typical intermanual conflict. But this patient showed almost no counteracting (“Gegenarbeiten”) with the affected hand. In this respect, she resembled the first description by Goldstein6 of a patient who was unable to let go once she had seized some objects or parts of her body.
Feinberg et al.11 argue that previous descriptions for grasping, groping and related behaviour occurring after frontal lesions have been provided by Denny-Brown who coined the term “magnetic apraxia”, denoting a type of behaviour of compulsive tactile exploration seen in both monkeys and humans. Lhermitte offered a similar explanation for bilateral utilisation behaviour due to frontal lobe lesions in humans.15 A detailed analysis of grasping behaviour in a frontal-brain-damaged patient was performed by de Renzi and Barbieri.16 They found that grasping was most significantly associated with lesions in the cingulate gyrus, the supplementary motor cortex being less often affected and that no hemispheric preponderance for this behaviour was apparent. Although de Renzi and Barbieri found such behaviour frequent in patients with damage to the frontal lobes, the pathological behaviour that they described was less pronounced and less distressing than the type we have seen in our series. For example, our observations also included the inability to let go of body parts, such as the contralateral hand, once it had been firmly seized. We saw this extremely impressive and disabling “tug of war between hands” in two of our cases. The severity of this is unusual for patients with frontal lobe damage, except with those with damage to the corpus callosum.
The supplementary motor area (SMA), in contrast, has far more competence for motor planning and motor control than the cingulate gyrus or any other structure that is frequently associated with AHS. Anatomically, widespread connections exist from the medial component of the SMA to the primary motor cortex, to the prefrontal motor cortex and to subcortical motor areas, as well as reciprocal connections to the contralateral SMA. Already, Goldberg et al9 stated that, in addition to damage to the anterior corpus callosum, the critical lesion for the development of an AHS is the SMA. He conjectured that a unilateral lesion in the SMA and anterior corpus callosum could release ipsilateral primary motor cortex activity from inhibitory control, resulting in a type of behaviour that is consistent with AHS. Thus, he described the essential features as “apparently purposeful (ie, goal-directed) movements that appeared to be occurring independent of conscious volitional control [were noted in the right arm]”. Both his patients tried to control this unwanted activity “by restraining the right arm physically with the left arm”.
A broad spectrum of pathological behaviour disrupting everyday activities has been described in the acute disconnection syndromes seen in the well-publicised “split-brain” patients.8 These patients have been callosotomised due to intractable seizures and, apart from a reduction of seizure frequency, some of these patients have demonstrated a type of behaviour that has also been described as the callosal type of AHS.17 In this type of syndrome, a distinct pattern of behaviour has been recorded that shows less frontal release signs or frontal motor behaviour patterns but intermanual conflict, alien hand signs, as well as a series of reactions that are summarised as autocriticism.
Autocriticism refers to the patient’s expression of astonishment and frustration when conflicting behaviour occurs. We have also seen this behaviour in the frontal type of AHS; in some cases, we have also seen this result with severe chronic depression. In other cases, the autocritical component was less pronounced, probably due to widespread frontal damage, which decreases the capacity for critical behaviour altogether. One patient (No. 1), who was also moderately aphasic, desperately cried out “mama” several times when she failed to tie a shoe lace. This autocritical reaction is often a response to failure in a seemingly simple procedural motor task that is related to everyday life or to a formal test situation. The distress caused refers to the self-conscious feeling of awkwardness towards the onlookers. As a consequence, the patient sometimes tries to hide the faulty hand by sitting on it or somehow mechanically blocking it from participating in any motor action that might be necessary. Such evasive procedures can be quite elaborate and strenuous for the patient. But only patients with marked autocritical reactions showed signs of avoidance behaviour, thus making an autocritical reaction a probable prerequisite for the development of avoidance strategies.
The main symptom of AHS is the intermanual conflict. As can be seen from table 2, there was a marked difference in the elements that constitute AHS. In cases 5, 6, 7 and 8, marked grasping and groping behaviour were the main elements, whereas in cases 1 and 2 it was counteracting (“Gegenarbeiten”), and in cases 3 and 4 both types were equally expressed.
One patient (KK) tried to eat a “Wiener Schnitzel” by sitting on her right hand and trying to cut the Schnitzel with the fork she was holding in her left hand. Eventually, the right hand came up and grabbed the knife, but instead of cutting little pieces it shoved away the schnitzel and tried to keep it away from the motor reach of the left hand, which was holding the fork and was held useless above the plate. As in other examples, there is an element that is reminiscent of mischief. In addition, we have never seen such counteracting movements without a touch of clumsiness. Identical motor behaviour came up when the same patient was asked to hold a candle in her right (alien) hand and light it with a lighter held in the left hand. Without recognisable preparatory action, the right hand grabbed the candle and held it out of reach of the left hand (figs 1 and 2). When the task was reversed and she was asked to light it with her right hand, she had obvious difficulties to bring the lighter to the candle wick and she gave the impression that some kind of motor force was preventing her from bringing her hand towards the object. She even tried to lean her whole body towards the candle, thus reducing the space between her right hand and the candle. A similar intermanual conflict was seen when tying a shoelace (fig 3). In patient 2 (TT), the task of lighting a candle was prevented by the left hand snatching away the lighter from the right hand (figs 4 and 5).
Another example (fig 6) refers to patient 2 who was asked to hit a nail with a hammer. The nail had already been stuck into a wooden block that was lying on the table. When the right hand holding a hammer was just about to come down to hit the nail, the left hand shoved away the wooden block. Thus, the hammer landed on the table instead of the nail. This was repeated in several trials to the same effect, which gave the impression that the initiation of the hammer movement triggered this mischievous action from the left hand.
Thus, intermanual conflict can be caused by various types of behaviour, one being forced grasping (“not letting go”), the other being counteracting by incomplete and rudimentary inhibitory movements. To us, it seems important to understand at which levels of motor planning and execution the disturbances are taking place. Clinical observation shows that such movements appear incomplete or clumsy and therefore do not reflect high-level sequential motor programming. Often, these movements are small, repetitive, hesitant and as hidden as possible, but can also be exaggerated, forceful and even ballistic-like. Therefore, we conclude that motor responses constituting AHS reflect motor elements that become visibly detached and isolated inhibitory motor patterns. This hypothesis is strengthened by experimental evidence showing that transcallosal inhibition can be triggered by purposeful motor action in chronic stroke patients.18 Other studies show differences in task-related motor activation following a stroke, such as those that have a poorer prognosis and result in a larger cortical activation pattern when compared with strokes with a more favourable outcome.19 It is therefore understandable that cerebral implementation of action includes the activation of inhibitory patterns that are usually either not activated or that are effectively suppressed. One case report interprets the motor behaviour as mirror-like and compares it with the early stages of motor learning.20
This type of inhibitory motor behaviour is always coordinated in the sense that there is a clear relationship with the task; it never resembles nonsense movements or a geste antagoniste. These movements can be most distressing and lead to severe and lasting impairment of everyday activities. They are often accompanied by an extreme sense of annoyance, surprise or emotional distress. Anguish, outspoken anger or severe depression can result. An autocritical component, which is often fundamentally a feeling of embarrassment, can become noticeable. As a result, compensatory actions are undertaken to prevent these failures. These are important to notice because they can be used as a therapeutic lead. For instance, leaning towards the object occurs, as well as putting the object on the table into the working space of the unobtruded hand before taking hold of it, thus avoiding a conflict of both hands.
Detailed analysis of counteracting versus groping and grasping in AHS has only been studied in detail in one previous report, by Tanaka and co-workers.21 They describe three of their own cases of AHS that occurs on the left hand, and give a description of their lesion topology and motor behaviour. They draw attention to an observation made by Fisher22 that AHS performs the task before the healthy right hand can—for example, snatching the object with the left hand before proper reaching occurs with the right hand. They call this type of behaviour “abnormal motor behaviour of the left hand elicited by voluntary movements of the right hand”. We confirm this observation and have also seen this behaviour in our cases as well as others.23
Furthermore, Tanaka et al21 hold that the intermanual conflict is elicited by lesions in the anterior third of the rostrum. They conclude this from their three cases, as well as from other published cases, in contrast to typical frontal lesions with groping and grasping that showed that their lesion was situated more in the genu and the adjoining anterior rostrum. We can confirm this observation only to some extent. In our cases with counteracting (“Gegenarbeiten”), MRI showed involvement of the rostrum up to its anterior third, but this was not always the case.
Nishikawa et al24 report three patients with conflicting wills that result in “freezing” and despair. We have also seen “conflict of intentions” in our patients outside the testing or therapeutic settings—for example, when patient No. 2 stood in front of the door to his room and was unable to enter it, because as he said, he had the feeling of wanting to enter but also the feeling that he should go out at the same time. We have no reason to regard this conflict of intentions as an additional symptom because, in our view, this only shows that the preparatory act of a motor action can trigger conflicting action.
The disability resulting from a chronic intermanual conflict is considerable if the large number of daily activities that are based on bimanual motor coordination is imagined. All the patients that we have seen also remained dependent on help from other individuals for very simple tasks of their everyday life, including most procedures of self-care. In addition, extended daily-activities, including daily routines in the preparation of food or house-keeping, were essentially not possible without constant help. Although some improvement resulted within therapy sessions that aimed at improving bimanual performance (eg, by using rhythmic behaviour such as switching objects between hands before using for the intended bimanual task, or training while viewing oneself in a monitor or in a mirror), such training effects were rarely carried over to the “real” world. To a varying degree, social seclusion, despair and chronic depression were seen in all cases.
The intermanual conflict seen in chronic AHS patients can therefore be best understood as a spectrum of manifestations caused by uncontrolled inhibitory motor programmes that have become detached from normal motor planning and execution. Thus, in AHS, the mirror world of motor inhibition becomes visible as a clinical phenomenon.
REFERENCES
Supplementary materials
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Footnotes
Competing interests: None.
Patient consent: Patient consent was obtained for publication of the case details and figures in this paper.