Paroxysmal alien limb phenomena due to epileptic seizures and electrical cortical stimulation Frank Boesebeck, MD; and Alois Ebner, MD Abstract—Alien limb phenomena (ALPs) are characterized by limb movements, which are subjectively experienced as involuntary or alien induced. ALPs regularly remain unchanged and occur as a consequence of frontal, callosal, or posterior cerebral lesions. The authors present two patients with paroxysmal ALP proved to be focal seizures by using video-EEG monitoring. In another two patients, ALP could experimentally be induced by electrical cortical stimulation. Based on the stimulation results, the authors suspect a functional disconnection of 1) sensory cortical areas providing information about the extrapersonal space; and 2) areas of the frontal and/or limbic cortex that are regularly involved in the processing and executing of intentional motor activity as a pathophysiologic substrate for ictal ALP. NEUROLOGY 2004;63:1725–1727 Alien limb phenomena (ALPs) describe a variety of abnormal motor and sensory symptoms of the arms and legs resulting in seemingly purposeful and oftenwayward limb movements that were subjectively experienced as involuntary or alien induced.1 ALP in the dominant extremities may occur after contralateral frontal lesions affecting the anterior cingulate gyrus and the anterior corpus callosum. ALP in the nondominant limbs may follow lesions restricted to the anterior part of the corpus callosum or more rarely after right frontal or bilateral frontal lesions. In the posterior or sensory type, ALPs occur after nondominant posterior or bilateral parietal lesions.2 Most ALPs remain unchanged or improve gradually during varying periods. Here we present two patients who had paroxysmal ALPs that could unequivocally be proved to be epileptic seizures by using video-EEG monitoring. In another two patients, nonhabitual ALPs could be elicited by cortical electrical stimulation. Case reports. Case 1. This 44-year-old woman had temporal lobe epilepsy resulting from left-sided mesial temporal sclerosis. She reported seizures with a feeling in her right arm of it not belonging to her body and her arm performing involuntary movements like stretching and grabbing. She tried to resist the movements by pulling back her right arm with her unaffected left hand. Neurologic and psychiatric examination yielded regular findings. The amobarbital test revealed left hemispheric speech dominance. During video-EEG monitoring, two seizures with involuntary rotating and abduction movements of the right arm were registered. Each time these movements were initiated by intended motor activities. In the postictal interview, she reported an alien arm performing funny movements (“that arm does not belong to me”). The ictal EEG showed a focal seizure pattern over the left posterior temporal area (figure 1). A left-sided anterior temporal resection led to a complete cessation of the seizures associated with the alien hand sensations. Case 2. This 16-year-old boy with frontal lobe epilepsy caused by a pilocytic astrocytoma in the right cingulate gyrus reported episodes with spontaneous involuntary movements of his left leg associated with the perception of estrangement of his leg. On neurologic examination, he had a movement-related dystonia of his left leg. Functional MRI showed the primary motor cortex for the leg closely located posterior to the lesion and left hemispheric speech dominance. During the video-EEG monitoring, two seizures with paroxysmal involuntary anteversion and rotating movements of his left leg were documented while the patient reported the sensation that his moving left leg did not belong to him and that the movement was alien induced (“I am not doing that, somebody else is doing it, . . . I don’t want it [the leg] to do it.”). The involuntary movements could repetitively be elicited by attempting to lift the left leg during the ictal test procedure. The ictal EEG showed a seizure pattern over Cz (see figure 1B). In the following two patients with partial epilepsy, invasive EEG monitoring using subdural electrode grids was performed to assess the regions of seizure onset more precisely. To delineate the area to be resected, a topographic mapping of the functional eloquent cortex was performed by electrical stimulation of the subsequent subdural electrodes. Case 3. This 16-year-old patient had partial epilepsy caused by a left temporoparietal oligodendroglioma. The cortical stimulation of two electrodes above the upper part of the postcentral gyrus (figure 2) induced involuntary abduction and rotating maneuvers of his right arm accompanied by the perception of the moving arm not belonging to his body. Stimulation of the more posterior localized electrodes elicited pure sensory responses, whereas the more anterior localized electrodes induced solely motor responses, proving those two electrodes are located above the anterior border of the primary sensory cortex. ALPs were also elicited by stimulating another three electrodes above the planum infraparietale of the operculum. The patient was somewhat astonished to have made those movements but could do nothing to prevent them. Case 4. This 14-year-old patient had parietal lobe epilepsy as a consequence of a malformation of cortical development in the left postcentral cortex. Neurologic examination revealed a postictal paresis of his right leg but otherwise regular findings. The electrical stimulation of two electrodes above the border between the precentral and the postcentral gyrus and one electrode above From the Department of Presurgical Evaluation, Epilepsy Center Bethel, Bielefeld, Germany. Received February 16, 2004. Accepted in final form June 21, 2004. Address correspondence and reprint requests to Dr. Alois Ebner, Mara Krankenhaus, Maraweg 21, Bielefeld, 33617 Germany; e-mail: ae@mara.de Copyright © 2004 by AAN Enterprises, Inc. 1725 Figure 1. Ictal EEG of both patients with spontaneous seizure-related alien limb phenomena (ALP). The arrows indicate the EEG-seizure onset. (A) Seizure pattern of Patient 1 above the left temporal lobe, maximal at electrode P7. (B) Seizure pattern of Patient 2 above the mid-central traces (CZ). Both seizure patterns were time locked to the clinical manifestation of the ALP. the frontal operculum (figure 3) induced episodes of involuntary grabbing maneuvers of the right arm accompanied by the perception of alienness (“someone else is playing with that arm”). Those involuntary movements markedly terrified the patient. The ALPs were reproducible and persisted even under visual fixation of the right arm. Discussion. From the phenomenologic point of view, all our patients fulfilled the clinical criteria of perception of foreignness and unintended motor activity in one limb, both of which have been shown to be major and common features of alien limb syndromes.1 Furthermore, Patients 1, 2, and 3 denied ownership of the affected limb (verbal asomatogno- Figure 2. Results of the cortical electrical stimulation of the subsequent subdural implanted grid electrodes in Patient 3. Alien limb phenomena (ALPs) were induced by stimulation of electrodes A17 and A18 and A44, A45, and A46. The electrodes located posterior to A17 and A18 elicited numbness (A1 and A2) and pure asomatognosia (A9). A25 and A26 induced clonic contractions of the right arm, which proved A17 and A18 to be located above the anterior border of the primary sensory cortex of the arm. 1726 NEUROLOGY 63 November (1 of 2) 2004 Figure 3. Stimulation results in Patient 4. Alien limb phenomena (ALPs) were induced by electrical stimulation of the electrodes A2 against A3, A3 against A4, and A2 against reference electrode B1. The latter electrode pair induced symptoms lasting for another 10 seconds after the end of stimulation, which was accompanied by an EEG seizure pattern over the electrodes adjacent to A2. A2 and A3 were shown to be located above the border between the precentral and the postcentral gyrus by stimulating the adjacent electrodes. Furthermore, the stimulation of electrode B4 against B5 and against the reference B1 also induced ALP. In a widespread cortical area located anterior to the lesion (*), the stimulation induced either somatosensory (tingling) or unclassified auras (indescribable wholebody perception), indicating the irritative zone. sia), which has been published for some but not all patients with ALP.3,4 Interictally, none of the patients showed any neuropsychological deficits regularly found in patients with stationary ALP. Focusing on our Patients 1 and 2, our data confirm the assumption of two other research groups who suspected focal epileptic seizures to be the pathophysiologic substrate for paroxysmal ALPs in some of their patients because of 1) concomitant generalized tonicclonic seizures;5 2) improvement of ALP under antiepileptic drug administration;5,6 or 3) repetitive spikes in the right frontotemporal traces recorded simultaneously to the clinical manifestation.6 Pathophysiologically, the motor activity may be interpreted as limb automatisms— otherwise neglected in complex partial seizures— but now realized under preserved consciousness. It may be speculated that the simultaneous appearance of motor automatisms and ictal asomatognosia7 in the same limb reflects a time-locked activation/inhibition of two or more distinct cortical areas. This could explain the relative rarity of ictal ALP because semiologies in partial epileptic seizures normally follow a topic and temporal propagation and, in the case of complex motor automatisms, are regularly accompa- nied by an impaired awareness of the ictal symptoms. The eliciting of ALP by previous ipsilateral movements may be attributed to the rare condition of simple partial reflex seizures induced by voluntary movements of the affected limb8 but has also been noticed in nonepileptic posterior ALP.9,10 Eliciting ALP by contralateral volitional movements (diagnostic dyspraxia) has been reported in stationary ALP5 but in none of our epileptic patients. In our Patients 3 and 4, ALPs were elicited by the stimulation of two distant cortical areas in the left hemisphere. One cortical area is located in the crossing between the primary sensory cortex (S1) and the primary motor cortex (M1)— both representing the affected limb. The second area is located in the supplementary sensory area (S2) of the planum infraparietale. In Patient 3, the stimulation of one electrode posterior to the two parietal electrodes, which elicited ALPs, induced isolated asomatognosia of the contralateral arm. It may be speculated that stimulation of electrodes above the rolandic fissure may have led to a bidirectional propagation of electrical current in our patients, which may have led to a simultaneous inhibition of primary sensory areas (asomatognosia) and activation of primary motor areas (involuntary movements) that were subjectively experienced as alien movements. Another possible mechanism may be a functional disconnection of association fibers between the primary (S1) and supplementary sensory areas (S2). The latter assumption is supported by our results in both patients in whom the stimulation of S2 also elicited ALP. References 1. Smith-Doody R, Jankovic J. The alien hand and related signs. 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Ay H, Buonanno FS, Price BH, Le DA, Koroshetz WJ. Sensory alien hand syndrome: case report and review of the literature. J Neurol Neurosurg Psychiatry 1998;65:366 –369. 10. Levine DN, Rinn WE. Opticosensory ataxia and alien hand syndrome after posterior cerebral artery territory infarction. Neurology 1986;36: 1094 –1097. November (1 of 2) 2004 NEUROLOGY 63 1727 Paroxysmal alien limb phenomena due to epileptic seizures and electrical cortical stimulation Frank Boesebeck and Alois Ebner Neurology 2004;63;1725-1727 DOI 10.1212/01.WNL.0000143064.81746.E9 This information is current as of November 8, 2004 Updated Information & Services including high resolution figures, can be found at: http://www.neurology.org/content/63/9/1725.full.html References This article cites 10 articles, 6 of which you can access for free at: http://www.neurology.org/content/63/9/1725.full.html##ref-list-1 Citations This article has been cited by 3 HighWire-hosted articles: http://www.neurology.org/content/63/9/1725.full.html##otherarticles Subspecialty Collections This article, along with others on similar topics, appears in the following collection(s): All Epilepsy/Seizures http://www.neurology.org//cgi/collection/all_epilepsy_seizures All Neuropsychology/Behavior http://www.neurology.org//cgi/collection/all_neuropsychology_behavio r Cortical localization http://www.neurology.org//cgi/collection/cortical_localization Epilepsy monitoring http://www.neurology.org//cgi/collection/epilepsy_monitoring_ Permissions & Licensing Information about reproducing this article in parts (figures,tables) or in its entirety can be found online at: http://www.neurology.org/misc/about.xhtml#permissions Reprints Information about ordering reprints can be found online: http://www.neurology.org/misc/addir.xhtml#reprintsus Neurology ® is the official journal of the American Academy of Neurology. 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