Journal of Neurology, Neurosurgery, and Psychiatry 1988;51:218-222 "Alien hand" and loss of bimanual coordination after dominant anterior cerebral artery territory infarction A W McNABB, W M CARROLL, F L MASTAGLIA From the Department of Neurology and University Department of Medicine, Queen Elizabeth II Medical Centre and Royal Perth Rehabilitation Hospital, Perth, Western Australia SUMMARY Three patients with dominant anterior cerebral artery territory infarction demonstrated a severe disturbance of upper limb motor control with impaired bimanual coordination, the "alien hand" sign, and intermanual conflict, in addition to signs of callosal interruption and a transcortical motor aphasia. Recordings of movement-related potentials in one patient showed an attenuated Bereitschaftspotential and a greater asymmetry of the NS' component of the premotor negativity with left finger than with right finger movement. The impairment of bimanual motor control and associated abnormal motor behaviour of the right hand in these cases are postulated to be due to involvement of the supplementary motor area and related areas of the medial frontal cortex. The anterior cerebral artery supplies the rostral sensorimotor cortex and the anterior two-thirds of the corpus callosum by way of its calloso-marginal and pericallosal branches. Proximal occlusion of the anterior cerebral artery may not only damage the motor cortex, resulting in weakness of the contralateral limbs, but may also produce a number of other abnormal motor phenomena. These include compulsive movements of a reflex nature, described as forced grasping and groping, and a grasp reflex.1 Abnormal motor behaviour of a more complex and semipurposive nature may also occur in the contralateral upper limb and has been described as the alien hand sign. 2 3 In extreme cases, where one hand acts at cross-purposes to the other, the term intermanual conflict has been used to describe this behaviour. Anterior cerebral artery occlusion may also disrupt interhemispheric connections. If the dominant artery is occluded the non-dominant hemisphere is disconnected from centres concerned with the organisation of speech and skilled motor activity in the dominant hemisphere resulting in agraphia and apraxia in the ipsilateral upper limb.4" The combination of these effects produces a unique and disabling disturbance of upper limb motor control. Address for reprint requests: Professor F L Mastaglia, University Department of Medicine, Queen Elizabeth 1I Medical Centre, Nedlands WA 6009, Australia. Received 24 April 1987 and in revised form 19 August 1987. Accepted 29 August 1987 218 We describe three patients with infarction in the dominant anterior cerebral artery territory who demonstrated the alien hand sign and intermanual conflict as well as marked impairment of bimanual coordination as part of their neurological syndrome. It is postulated that these abnormalities of motor behaviour resulted from damage to the supplementary motor area and related areas in the medial frontal cortex. Case reports Case I A 75 year old dextral woman was admitted to a rehabilitation hospital 6 weeks after the sudden onset of a dense right hemiplegia and mutism. Her initial illness had been complicated by urinary and bowel frequency, urgency and incontinence. A past history of treated hypertension of 10 years, and a transient episode of right hand paraesthesiae 12 months prior to presentation was elicited. On examination she was found to have a blood pressure of 150/85 mm Hg and signs of aortic valve sclerosis. She was alert but disinhibited, laughing readily and inappropriately, and cursing in a jocular fashion. There was a minimal right upper motor neuron facial paresis, mild right upper limb weakness (MRC grade 4/5), particularly evident proximally, and severe weakness of the right leg (grade 1-2/5), particularly distally. Right sided hyperreflexia was present. Vision and somatic sensation were normal. Although initially mute, her speech subsequently was soft and dysfluent with abnormal prosody but normal comprehension, repetition and reading. Object naming to visual and tactile presentation in either hand was intact. She had a left dyspraxic agraphia and "Alien hand" and loss of bimanual coordination after dominant anterior cerebral artery territory infarctionz 219 a mild left ideomotor dyspraxia was also evident with more complex tasks. Bimanual coordination was markedly I I I impaired; for example she was unable to use simultaneously a knife and fork when eating, or to do up buttons when NS dressing. A number of other abnormal motor phenomena were also noted. On the left side, semi-coordinated moveC4 4;Cz ments of the hand or arm would occur whilst speaking or if C3 she was distracted by other tasks. On the right side, a tonic Left hand palmar grasp reflex was present, and initially this hand I I showed an uncontrollable tendency to reach out and take hold of objects and then be unable to release them. The patient would repeatedly express astonishment at these C4 actions. At times the right hand interfered with tasks being performed by the left hand, and she attempted to restrain it 5pV L by wedging it between her legs or by holding or slapping it 100 ms with the left hand. Attempts to execute regular repetitive Fig 2 Movement-related potentials associated with right self-paced flexion-extension movements of individual fingers and leftfinger extension. Note the wider (bilateral) of the right hand resulted in errors of timing and sequencing distribution of the NS' component of the premotor negativity which were not seen in the left hand. with right-sided movements than with left-sided movement, A cranial CT scan showed extensive infarction of the left and the attenuation of the preceding Bereitschaftspotential superior and medial frontal and parietal cortex and of the (BP) for both right and left-sided movement. The arrows genu and body of the corpus callosum (fig 1). indicate movement onset which was detected using an Movement-related potentials Potentials (fig 2) were infra-red system.6 recorded by averaging lS s epochs of EEG preceding 100 extension movements of the index finger of each hand from electrodes at C3, Cz and C4 (10-20 system) referenced to motor potential of Deecke et al8 9 and Lee et al,'0 which is linked-ears.6 With movement of the left index finger the thought to represent activity in pyramidal tract neurons in negativity preceding movement onset by 150-250 ms, corre- pre- and post-Rolandic areas,"0 was localised to the (consponding to the NS' component of Shibasaki et al7 and the tralateral) C4 electrode site. By contrast, with movement of C3hA-AMW-Y'ACZ Fig 1 Transverse (a and b) and semi-coronal (c and d) CT scans of Case 1, 2 months after left anterior cerebral artery occlusion showing extensive destruction of the left medial frontal and parietal cortex andcorpus calosum. 220 the right index finger, this potential was present at each electrode site, although of maximal amplitude contralaterally at C3. The earlier negativity preceding NS' (the Bereitschaftspotential), was poorly developed at all electrode sites for both right and left finger movement. Subcomponents of this earlier negativity as described by Barrett et al" could not be identified. Case 2 (P.A.) A 58 year old obese dextral woman was first seen 6 weeks after the sudden onset of right hemiparesis and abnormal speech. There was a past history of endogenous depression, hypertension and a recent myocardial infarction. On examination there was mild right facial and upper limb weakness with a tonic palmar grasp reflex, profound weakness of the right leg, right-sided hyperreflexia, ankle clonus and a Babinski response. Spontaneous speech was hesitant, with word-finding difficulties but normal comprehension, repetition and naming of visually-presented objects. Tactile naming of objects was normal with the right hand (10/10) but was severely impaired with the left hand (0/10) although in most instances the object could be retrieved from a collection of unrelated items indicating a tactile anomia. Writing was normal with the right hand while the left hand produced only stereotyped doodling. The left hand was severely dyspraxic making stereotyped waving movements in the air when she was instructed to perform simple or complex movement sequences or to use objects. There was also a constructional apraxia with perseveration when using the right hand. Tasks involving the coordinated use of both hands, such as eating or dressing, were severely impaired, the two hands appearing to act quite independently of each other. At times the right hand would be raised toward the head or would interfere with tasks being performed by the left hand. Case 3 (R.S.) A 68 year old dextral woman was examined some weeks after the acute onset of a right hemiparesis, speech difficulty and urinary incontinence. Examination showed residual right sided weakness which was more severe in the leg, with mild spasticity in the arm and a strong palmar grasp reflex. Her speech was hesitant with occasional paraphasic errors and echolalia but normal comprehension, repetition and visual naming of objects presented in either hemifield. Tactile naming of objects was normal with the right hand (5/5) while there was a mild tactile anomia with the left hand (6/8 correct). Writing was normal with the right hand but was impaired with the left hand which was also mildly dyspraxic when attempting to use common objects or to perform motor sequences. Construction of simple geometric shapes was normal with the right hand but markedly impaired with the left hand. When the patient was attempting to write with her left hand the right hand would frequently be raised and would reach over and attempt to take the pencil from the left hand. The left hand would respond by grasping the right hand to restrain it. The performance of bimanual tasks such as eating or manipulating buttons was severely impaired. During conversation the right hand would frequently drift upwards or make other purposeless movements. McNabb, Carroll, Mastaglia Discussion The present cases each displayed the characteristic pattern of limb weakness and associated sphincteric disturbance found after infarction in the territory of the anterior cerebral artery."2 In the most recent case (Case 1) the anatomical location of the lesions was confirmed by computed tomography which showed infarction of the medial frontal cortex and corpus callosum. In addition, each patient showed features of a transcortical motor aphasia (table) with reduced, non-fluent spontaneous speech (one patient was mute initially), normal auditory comprehension, reading and repetition, and in one case echolalia (Case 3). This type of aphasia, which has been reported only infrequently in patients with anterior cerebral artery occlusion, 13 -'5 has previously been ascribed to lesions involving the supplementary motor area (SMA) or its connections with Broca's area. 15 - 17 The lesions responsible for the alien hand and other abnormal motor phenomena have not been well localised. Brion and Jedynak2 introduced the concept of the alien hand (la main etrangere) to draw attention to the uncooperative behaviour of the left hand in three patients with tumours of the corpus callosum. Similar phenomena have been described in patients with other lesions of the corpus callosum and for the first few weeks after commissurotomy in epileptic patients.3 18 In contrast to patients with callosal lesions in whom the alien hand and conflicting hand in bimanual tasks was the left hand, in the present cases and in the two cases described by Goldberg et all9 with left medial frontal cortex infarction, the right hand displayed these abnormalities. We believe, as did Goldberg et al,'9 that these abnormal forms of motor behaviour are the result of damage to the medial frontal cortex, which includes the SMA, rather than to callosal interruption which is the basis for the apraxia of the left hand and agraphia.4 5 There is now considerable evidence implicating the SMA, which lies upstream from the primary motor cortex, in the planning and programming of coordinated motor tasks.202' Penfield and Jasper22 showed that stimulation of the SMA in man evoked complex Table Summary of neurologicalfindings in the present cases Case I Contralateral hemiparesis (leg > arm) Transcortical motor aphasia Grasp reflex Forced grasping Alien hand Intermanual conflict Ipsilateral apraxia Ipsilateral agraphia Ipsilateral tactile anomia + + + + + + + + - Case 2 + + + + + + + + Case 3 + + + + + + + + "Alien hand" and loss of bimanual coordination after dominant anterior cerebral artery territory infarction 221 movements of the contralateral upper limb and at vation of motor centres in both hemispheres because times arrest or slowing of movement, as well as vocal- of the difficulty the patient had in making individual isation or speech arrest. Stimulation of the anterior finger movements with the right hand without simulcingulate cortex, which is reciprocally interconnected taneously activating the left hand. with the SMA, has also been shown to produce highly integrated forms of motor behaviour.23 Regional The authors are grateful to Mr GW Thickbroom who cerebral blood flow studies in normal subjects per- performed the motor potential recordings and to Mrs forming a sequence of finger movements with one P McBryde for secretarial assistance. hand showed an increase in blood flow in the SMA References bilaterally, even when the subject imagined the unilateral movement sequence without actually making 1 Walton J. Brain's Diseases of the Nervous System, 8th ed. Oxford University Press, 1977. any movement.24 Single cell recordings in primates interhemispherique a have also shown a relationship between bilateral 2 Brion S, Jedynak CP. Trouble du detransfert tumeurs du corps calleux; propos de trois observations SMA unit activity and the performance of unilateral Le signe de la main etrangere. Rev Neurol (Paris) learned motor tasks.25 1972;126:257-66. Lesions of the dominant SMA in man have been 3 Bogen JE. The Callosal Syndrome. In: Heilman KM, Valenstein E, eds. Clinical Neuropsychology. New York: Oxford Univerreported to cause mutism, transcortical motor aphasity Press, 1985:295-338. sia, forced grasping, groping and a grasp reflex, 4 Liepman H, Maas 0. Fall von linksseitiger Agraphie und Apraxie reduced spontaneous motor activity and impaired bie rechtsseitiger Lahmung. J Psychol Neurol 1907;10:214-27. bimanual coordination.'5 1626-28 Unilateral SMA 5 Geschwind N. Disconnexion syndromes in animals and man. Brain 1965;88:237-94,585-644. ablation in monkeys results in a long-lasting deficit in GW, Mastaglia FL, Carroll WM, Davies HD. the execution of precision movements of the two 6 Thickbroom Cerebral potentials accompanying visually triggered finger use cooperative of the hands and marked impairment movement in man. Electroencephalogr Clin Neurophysiol of the hands in bimanual tasks,29 deficits which are 1985;62:209-18. E, Halliday AM. Components remarkably similar to those observed in the present 7 Shibasaki H, Barrett G, Halliday of the movement-related cortical potential and their scalp cases. The alien hand sign and associated abnormal topography. Electroencephalogr Clin Neurophysiol 1980;49: motor behaviour, and the speech disturbance in these 213-26. cases, may therefore be an expression of impaired 8 Deecke L, Scheid P, Kornhuber HH. Distribution of readiness potential, pre-motor positivity and motor potential of the programming, execution or inhibition of normal human cerebral cortex preceding voluntary finger movements. motor subroutines as a result of damage to the SMA Exp Brain Res 1969;7:158-68. or interconnected areas of the dominant medial fron9 Deecke L, Grozinger B, Kornhuber HH. Voluntary finger movement in man: Cerebral potentials and theory. Biol Cybernetics tal cortex. 1976;23:99-1 19. The virtual absence of the Bereitschaftspotential BI, Luders H, Lesser RP, Dinner DS, Morris HH. Cortical before finger movement in Case 1 is of interest, in 10 Leepotentials related to voluntary and passive finger movements view of the postulated origin of this potential from the recorded from subdural electrodes in humans. Ann Neurol 1986;20:32-7. SMA by some workers.30 31 If the BereitH, Neshige R. 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