should enhance both the accuracy in predicting functional outcome of epilepsy surgery and our ability to relate cognitive deficits to dysfunction in discrete brain areas. Acknowledgments We are grateful to the Wellcome Trust for its support and to the patients, their families, and the control subjects for giving their time and effort to this study. We also wish to thank Elizabeth Isaacs for carrying out a substantial part of the testing. References 1. Milner B. Psychological aspects of focal epilepsy and its neurosurgical management. Adv Neurol 1975;8:299-321. 2. Blakemore CB, Falconer MA. Long-term effects of anterior temporal lobectomy on certain cognitive functions. J Neurol Neurosurg Psychiatry 1967;30:364-367, 3. Milner B. Memory and the medial temporal regions of the brain. In: Pribram KH, Broadbent DE, eds. Biology of memory. New York: Academic Press, 1970:29-50. 4. Rausch R. Effects of temporal lobe surgery on behavior. Adv Neurol 1991;55:279-292. 5. Milner B, Penfield W. The effects of hippocampal lesions on recent memory. Trans Am Neurol Assoc 1955;80:42-48. 6. Dimsdale H, Logue V, Piercy M. A case of persisting impairment of recent memory following right temporal lobectomy. Neuropsychologia 1964;1:287-298. 7. Penfield W, Milner B. Memory deficit produced by bilateral lesions in t h e hippocampal zone. Arch Neurol Psychiat 1958;79:457-497. 8. Penfield W, Mathieson G. An autopsy and a discussion of the role of the hippocampus in experiential recall. Arch Neurol 1974;31: 145-154. 9. Connelly A, Jackson GD, Duncan JS, King MD. Gadian DG. Magnetic resonance spectroscopy in temporal lobe epilepsy. Neurology 1994;44:14 11-1417. 10. Jackson GD, Connelly A, Duncan JS, Griinewald RA. Ondian DG. Detection of hippocampal pathology in intractable partial epilepsy: increased sensitivity with quantitative magnetic r e s o n a n c e T, r e l a x o m e t r y . Neurology 199:1; 43: 1793-1799. 11. Engel J J r , Van Ness PC, Rasinussen TB, Ojemann LM. Outcome with respect to epileptic seizures. In: Engel J, cxl. Surgical t r e a t m e n t of t h e epilepsies. New York: Raven Press, 1993:609-621. 12. Nose U. In vivo proton spectroscopy in presence of‘ eddy currents. Magn Reson Med 1990;14:26-30. Alien hand syndrome: Interhemispheric motor disconnection due to a lesion in the midbody of the corpus callosum D.H. Geschwind, MD, PhD; M. Iacoboni, MD, PhD; M.S. Mega, MD; D.W. Zaidel, PhD; T. Cloughesy, MD; and E. Zaidel, PhD Article abstract-The neuroanatomic substrate of the alien hand syndrome has remained controversial due to the noncircumscribed nature of cerebral injuries present in most cases. There have been few cases studied in which damage was restricted to portions of the body of the callosum, and most of those involved surgical callosotomy fior tumors o r epilepsy. We report the case of a woman with a transient alien hand syndrome caused by a stroke limited to the middle and posterior portions of the body of the corpus callosum. This case provides supportive evidence for damage to the midbody of the corpus callosum as the anatomic basis of nondominant alien hand syndrome and conforms to a model of‘ interhemispheric motor disconnection as the essential component of this unusual behavioral syndrome. Thus disconncction can occur with injuries involving interhemispheric premotor and motor fibers traveling in the midportion of the callosum in individuals with left hemisphere dominance for motor activities. NEUROLOGY 1995;45:802-808 Alien hand syndrome remains as striking and controversial a clinical entity as when first, described as a type of apraxia by Go1dstein.l Although Brion and Jedynak” coined the vivid term “main etrangere,” or “alien hand,” in describing patients with callosal lesions and neglect or alienation from their hand, the term is commonly used to describe a predominantly motor phen ~ m e n o nThe . ~ hallmark of alien hand syndrome is the patient’s perception of alienation from and loss of control over one or both upper extremities coincident From the Department of Neurology (Drs. Geschwind, Iacoboni, Mega, and Cloughesy) and the Division of Brain Mapping tDr. Iacoboni), LJCIA School ol‘ Mrdicine, and the Departnient of Psychology (Drs. Iacoboni, D.W. Zaidel, and E. Zaidel), University of California, Los Angeles, CA. Supported by NIH grant N S 20187 (to M.I. and E.Z.) and by NIMH RSA MH 00179 (to E.Z.). Kcct,ived July 11, 1994. Accepted in final form October 3, 1994 Address correspondence and reprint requests to Dr. Daniel H. Geschwind, Department of Neurology, Reed Neurological Research Center, 710 Westwood PI:iza, I m Angeles, CA 90095. 802 NEUROILEY 45 April 1996 with the left hand, she did this concurrently with mirror with observable complex involuntary movement^.^-^ movements of her right hand. If these mirror movements The alien hand acts at odds with the patient’s will, crewere suppressed, her praxis deteriorated. She exhibited no ating a sense of intermanual conflict. The ipsilateral grasp, snout, or palmomental reflexes and performed well lower extremity is oRen subtly involved as well. The on alternating motor programs and in reproducing rhythms observed behavior is so odd that often the patient’s that were tapped by the examiner. She did not perseverate complaint is initially dismissed as functional. on verbal commands or on copying alternating sequences. To clarify previous clinical-anatomic observations, Motor examination revealed a mild left-sided facial droop Feinberg et a15 classified alien hand syndrome into and a left-sided pronator drift, but strength was full and two separate syndromes. One, comparable to a frontal symmetric throughout. Rapid alternating movements were release syndrome involving the dominant limb, is slowed on the left in both upper and lower extremities. She could not accomplish fine motor tasks with her left fingers characterized by grasping, groping, and other positive or hands without mirroring them with her right. She was exploratory behaviors and is associated with domiunaware of this until it was brought to her attention, and nant medial frontal lesion^.^^^ The second corresponds she had trouble suppressing the mirror movements when to the archetypal alien hand syndrome and is characasked. During the examination, her left hand was observed terized by nondominant limb apraxia and oppositugging a t her shirt, trying to undo her buttons. When tional intermanual conflict, with an absence of frontal asked to pick up the phone, she tried to do so with her left sign^.^,^,^ Lesions in the second type involve the antehand but had to wrestle it away with the right hand. She rior corpus callosum but often extend into adjacent would crush cups given to her to hold in both hands but was areas such as the supplementary motor cortex or the able to feed herself with utensils held in her right hand. She body of the corpus callosum. The lesion typically is had neither sensory neglect, tactile anomia, nor a deficit in tactile recognition in either hand. She performed cross-taccaused by vascular lesions, and the damage is not tile matching equally well with both hands. Her deep tenwell circum~cribed.~J~ In cases of surgical callosotomy, don reflexes were normal and symmetric throughout, and large areas of the callosum are transected, oRen sparplantar responses were flexor. She was initially unable to ing only the ~ p l e n i u mSeveral .~ reports of patients stand unassisted because she fell to the left, but she had no with more circumscribed callosal sections have not decerebellar ataxia or dysmetria. scribed alien hand phenomena,11J2although one of On reexamination 8 hours later, she had regained most the first descriptions of alien hand involved a patient of the control over her left hand and had less asymmetry in with a midposterior callosal tumor.13 Thus, there repraxis; she could carry out commands with both hands, but mains debate over the extent of damage necessary to she demonstrated body part substitution for objects in her produce the archetypal alien hand syndrome and left hand and inappropriate proximity with her right. Handwriting was good with her right hand and grammatically what the syndrome represents from a neurobehavintact but poorly legible with her left hand. Her walking ioral per~pective.~,~ was back to her premorbid baseline. Here we report the case of a 68-year-old woman Imaging. An MRI done on postoperative day 11revealed with an archetypal transient alien hand syndrome an area of increased signal on T,-weighted images, confined secondary to an embolic stroke confined to the postelargely to the posterior body of the callosum and sparing the rior two-thirds of the body of the corpus callosum, genu and splenium, with some extension into the right pensparing the splenium and most of the anterior half of callosal region (figure 1). The most rostral area of high T, the corpus callosum. This patient did not manifest the signal extended a few millimeters into the anterior half of profound callosal apraxia or deficits in intermanual the callosum. An incidental left dorsolateral frontal meninsomatosensory transfer previously reported with legioma that has remained asymptomatic was also noted. Resions in the body of the corpus ~ a l l o s u m . ~ JIn~ J ~ Jpeat ~ ~ ~postacute MRI obtained during postoperative week 8 revealed an area of infarction involving the posterior half of stead, she showed a delay in visuomotor transfer, evithe callosal body, sparing the splenium and the anterior dent only on detailed laboratory testing. Case report. A 68-year-old right-handed Hispanic woman was admitted for coronary artery bypass grafting. On postoperative day 11, she was noted by nursing staff to have left-sided weakness and difficulty walking. According to her family, she had complained of loss of control of her left hand for the previous 3 days, as if the hand were performing on its own. She awoke several times with her left hand choking her, and while she was awake her left hand would unbutton her gown, crush cups on her tray, and fight with the right hand while she was answering the phone. To keep her left hand from doing mischief, she would subdue it with the right hand. She described this unpleasant sensation as if someone “from the moon” were controlling her hand. She also felt some degree of clumsiness in her left arm and leg. Neurologic consultation was called on postoperative day 11, and examination revealed her to be alert and oriented as well as pleasant and cooperative. Her speech in Spanish was fluent, without dysarthria, and her comprehension and reading were intact. She had significant ideomotor apraxia with the left hand and left leg. Although she could mimic half of the corpus callosum, with slight extension into the white matter underlying the right cingulate cortex (figure 2). Clinical follow-up, This patient has been followed for 6 months. She has had no further events but continues to complain of left hand clumsiness, manifested by occasional dropping of cups or other objects she is holding. She reports a similar sensation of clumsiness in her left leg but has had no falls. At times her two hands will collide if she is not watching them. She also complains that her right hand feels larger than her left. Neurologic examinations a t 8 weeks and a t 5 months postinfarct revealed no pronator drift and normal simple fine motor movements bilaterally. But she exhibited an intermittent, effort-dependent decrease in finger and hand strength on the left. Fine motor movements during tactile exploration of objects with the left hand were also diminished. However, stereognosis and graphesthesia were intact bilaterally. No mirror movements or unusual oppositional movements of her hands were noted. Her writing was grammatically intact and intelligible with both the left and right hands. April 1995 NEUROLOGY 45 803 Laboratory neuropsychological testing. This patient's restricted callosal lesion is unique. To our knowledge, only eight cases with lesions restricted to portions of the callosal body (sparing the genu and splenium) are discussed in the 804 NEUROLOGY 45 April 1996 l i t e r a t ~ r e . ~ ~ ' "Each ' ~ ~ ' ~of those cases demonstrates significant signs of callosal disconnection. While oRen most pronounced acutely, the signs lasted 5 to 6 months in several patients. Thus, we undertook formal laboratory testing at 8 RT that was greater than 3 SD from its respective condition mean was removed from the analysis. The highest number of outliers (13.1%) was observed in the left hand-right visual field condition, suggesting high variability of RTs for this condition. A reliable advantage of 40 msec (F[1, 2891 = 12.02, p < 0.001) was observed for the uncrossed right hand-right hemifield condition (420 msec) compared with the crossed right hand-left hemifield condition (460 msec). There was no statistical difference between the uncrossed left hand-left hemifield (496 msec) and crossed left hand-right hemifield (478 msec) conditions. The difference between the crossed and uncrossed conditions (crossed-uncrossed difference; CUD) for the right hand was of the same order as in split-brain patients. l8 Figure 1. Acute proton-density and T,-weighted sagittal and coronal MRIs. Sagittal proton-density and T, views close to the midline reveal the rostral-caudal extent of the infarction, which extends approximately 3 cm. The rostra1 border is approximately 3 mm anterior to the midline of the callosum, and the stroke extends caudally to encompass the entire posterior half o f the callosal body (arrows). Both the genu and splenium are spared, as is most of the anterior half of the callosal body. The coronal views confirm that the stroke is confined to the callosum, with slight extension into the adjacent white matter, seen in the second coronal image. A n incidental, heavily calcified left frontal meningioma is seen in the first coronal image. On the coronal images, the distance from the level of the mamillary bodies is marked in millimeters (A = anterior, P = posterior). I weeks and at 5 months after the infarction to uncover the presence of apraxia, agraphia, or auditory, sensory, motor, or visual di~connection.~ On initial bedside testing, in addition to the acute alien hand, our patient exhibited ideomotor apraxia, apraxic agraphia, and mirror movements but not aphasic agraphia, tactile anomia, or deficits in intramanual tactile transfer or localization. None of the deficits present acutely were observed during the 8-week and 5-month testing sessions. Additionally, dichotic listening ( 8 weeks) and several additional tests of proprioceptive and stereognostic transfer (8 weeks and 5 months), which were not done in the acute setting, demonstrated the absence of auditory or somatosensory disconnection. However, formal testing of interhemispheric visuomotor transfer at 8 weeks and at 5 months revealed a deficit in transcallosal visuomotor integration as described below. Interhemispheric transfer of visuomotor information. Unimanual simple reaction times (RTs) to lateralized flashes are used to measure interhemispheric transfer time (ITT) of visuomotor information through the corpus callosum. The difference in RTs between the crossed condition (motor response contralateral to the visual stimulus) and the uncrossed condition (motor response ipsilateral to the visual stimulus) reflects the ITT, which is 3 to 4 msec in normal subjects.18Marked increases in the I n , seen in patients with agenesis of the corpus callosum and commisurotomy patients,'* support the hypothesis that the transfer occurs via the corpus callosum. The most efficient channel for interhemispheric transfer of visuomotor information is likely via callosal motor Our patient's lesion interrupted these callosal motor fibers. Thus, we measured the I l T in our patient to further the understanding of the disconnection phenomena caused by the callosal lesion. The experimental design was similar to that in a previously reported study.I9 The visual stimulus was presented on a high-resolution RGB monitor of a Macintosh IIsi computer. Stimuli were presented for 50 msec. A response panel placed at the midline was used for manual responses, which were carried out by the patient's pressing a key on the panel with her index finger. Sixteen blocks of 40 trials in two separate testing sessions (8 weeks and 5 months after the lesion) were performed, and the order of response hand was counterbalanced in the two testing sessions. Results. Since the two testing sessions did not show any significant difference, data were collapsed. Any Discussion. Alien hand syndrome and motor disconnection. This case demonstrates that alien hand syndrome can occur with an injury restricted to the middle and posterior portions of the body of the corpus callosum, supporting the anatomic model proposed by Brion and Jedynak.13 We propose that this lesion implicates interhemispheric motor disconnection in the pathogenesis of archetypal alien hand. Furthermore, it presents an intriguing example of visuomotor disconnection in the dominant hand of a patient with damage to the midbody of the corpus callosum, sparing the splenium. Our patient had a transient alien hand syndrome that was coincident with acute edema in the most rostral extent of the posterior half of the corpus callosum with slight extension anteriorly and into the adjacent subcortical white matter (figure 1). Her postacute lesion involved an infarcted area slightly smaller than the posterior half of the body of the corpus callosum (figure 2). Thus, her transient alien hand and mild nondominant limb apraxia were correlated acutely with damage to the middle of the body of the corpus callosum. Previous reports(5J0~'1~22 have emphasized damage to the anterior portion of the corpus callosum and neighboring frontal cortex as the basis for alien hand syndrome. The lesions involved were large, often secondary to anterior communicating or anterior cerebral aneurysmal rupture or stroke, and affected anterior regions primarily. The inclusion of frontal groping and impulsive exploratory behaviors in alien hand cases has biased clinical-anatomic interpretations toward implicating frontal lesions in alien hands pathogenesis. All but five of the 20 patients reviewed by Feinberg et al" had significant involvement of cingulate or frontal cortex. Two of the five, who had damage limited to the callosum, had lesions reportedly confined to the genu, but these cases were not based on MRI data and involved aneurysmal rupture, which likely resulted in an area of damage larger than that seen on CT.23,24 Two of the remaining cases had documented large lesions involving the genu as well as the body of the callosum,16and the patient of Watson and Heilman8 had a lesion involving the entire body of the callosum. April 1995 NEUROLOGY 45 805 Figure 2. Postacu sagittal and coronal MRIs. Scans were done 8 weeks after those shown i n figun? 1 and reveal the postacute extent of the stroke (TI-weighted; sagittal proton-densi ty). The area of damage is seoeral millimeters smaller at the rostra1 and caudal borders and is confined to the posterior half of the body of the callosum (arrows:). The coronal T2-weighted images demonstrate that the damage is confined to the callosal white matter and that the medial-to-lateral extent of the lesion hlzs not changed significantly. The present case is unique in the circumscribed nature of the lesion documented by acute and postacute MRI and is the only MRI-documented case with a le806 NEUROLOGY 45 April 1996 sion confined to the middle and posterior blody of the corpus callosum resulting in alien hand syndrome. Case number 4 of Brion and Jedynak':' had a tran- sient alien hand, with damage confined to a small Preliminary data from a studyz8with a large sample portion of the posterior body of the callosum. Howof patients seem to support this model. However, why ever, their patient’s symptoms were more akin to does callosal alien hand syndrome predominantly inhemineglect, and the dependence on autopsy for localvolve the nondominant hand? ization (remote from the event) made precise clinicalData from lesion studies in humans suggest that anatomic correlation difficult. Our patient’s concurthe left hemisphere is dominant for complex or fine rent intermanual conflict, alienation from the nonmotor movements in right-handed individual~.8.~,’7.27,2~ dominant hand, and ideomotor apraxia, in the abRecent data from functional MRI and PET support sence of groping, grasping, or frontal system dysfuncthis proposition by showing a clear asymmetry of tion, are analogous to those observed in other cases of motor cortex activation during volitional fine motor archetypal callosal alien hand s y n d r ~ m e and ~ ~ ~sup~ ~ * movements of the hand.30331Fine motor movements of the nondominant (leR) hand in right-handed individuport the distinction between callosal and frontal alien hand syndrome advanced by Feinberg et aL5 Addials involve activation of bilateral motor areas, while tionally, the present case, with a limited callosal body right hand movements involve primarily the domiinfarction, supports the observed association between nant (left) motor areas. Thus, nondominant hand ideomotor apraxia and callosal alien hand movement requires transfer and coordination of information between the PMA, SMA, and primary motor and suggests that the relevant callosal fibers travel in close proximity. areas of both hemispheres. Dominant hand moveOur case also suggests that, when seen in conjuncment does not require this transcallosal information tion with alien hand syndrome, the signs of tactile transfer. The left hand’s dependence during fine anomia, aphasic agraphia, and ideational apraxia motor movements on bilateral primary motor, PMA, likely reflect the more widespread damage to adjacent and SMA activation explains why the archetypal calanterior callosal or cortical areas oRen seen with anlosal alien hand syndrome predominantly involves terior cerebral artery infarction or aneurysmal rupthe left hand in left hemisphere-dominant individuture.10J6~21~22 Tactile anomia has been previously assoals. This is further supported by the absence of alien ciated with splenial damage as well as medial frontal hand symptoms and ideomotor apraxia in a n amand callosal damage6~10~13~16~21~~z and is not observed in bidextrous individual with a callosal lesion similar to cases of limited callosal body damage in the acute15or that of our patient.16 Most of the cases of right-handed postacuteHJ setting. Aphasic agraphia has similarly alien hand syndrome involve damage to left frontal shown variable localization, occurring with damage to areas, including the SMA, and are more akin to the frontal release ~ h e n o m e n o n . ~ * ~ the anterior callosum or genu as well as to anterior Our patient’s lesion acutely disrupted interhemisplenium and posterior body.8.’7.z1’.22 The singular vasspheric motor, PMA, and SMA connections coincident cular event in our patient suggests that many of these with her alien hand syndrome and ideomotor apraxia. accompanying signs of anterior or posterior callosal disconnection can be dissociated from the alien hand She also was unable to carry out any fine movements with her left hand without unconsciously mirroring phenomenon. them with her right. The observation of mirror moveAnatomic data on the gross topography of interhemispheric connections in the human corpus calloments in the right hand during the acute phase of our patient’s lesion further demonstrates the importance sumz5suggest that the supplementary motor cortex of transcallosal SMA-to-SMAcommunication for indeand much of the primary motor (precentral) cortex send interhemispheric connections via a region that pendent, purposeful fine movements i n t h e left hand.22,273 When our patient’s alien hand complaint overlaps with the anterior portion of our patient’s lesubsided, so did her apraxia and right-hand mirror sion. The work of Pandya et alZ6in nonhuman primovements, as has been reported by others.8,9J6,27,32 mates maps the interhemispheric fibers of primary Parallel evidence supporting a deficit in preparatory motor, premotor (PMA),and supplementary motor motor activity a n d implicating interhemispheric areas (SMAj to the same callosal regon. The more anSMA-to-SMA disconnection is the attenuation of the terior extent of our patient’s lesion acutely encomBereitschaftspotential coincident with alien hand synpasses this area, whereas the more posterior extent d r ~ m e . ~ ~ ~ ~ overlaps with regons carrying postcentral parietal, insular, and posterior temporal interhemispheric conOther signs of callosal disconnection. Visuomotor n e c t i o n ~ .The ~ ~ ,SMA ~ ~ and PMA were not involved, disconnection in our patient is supported by the large CUD favoring the ipsilateral condition in the but it is likely that interhemispheric pathways conright hand’s RTs to lateralized flashes. In normal necting these areas were acutely disturbed. subjects, the ITT averages 3 to 4 msec. In our paThus, we propose that the disruption of volitional tient’s right hand, the ITT was 40 msec, consistent motor control and the presence of the alien hand synwith observations in split-brain patients.18J9 drome in the nondominant hand in our patient is due Based on the proposal that motor disconnection to the interhemispheric disconnection of the motor underlies alien hand syndrome, one might expect difand supplementary motor areas.g The loss of interficulty in measuring interhemispheric visuomotor hemispheric motor integration caused by this discontransfer in the left hand, since this would require innection can cause a sense of alienation from the nontact interhemispheric motor integration. Indeed, our dominant limb and the resulting intermanual conflict patient demonstrated large variance in response that are the hallmarks of alien hand April 1996 NEUROLOGY 45 807 times with the left hand compared with the right, and no positive CUD was demonstrated. A fundamental motor disconnection in our patient led to the disruption of fine motor control of the left hand and confounded the reliable measurement of any concomitant visuomotor disconnection. This suggests that, even months after the disappearance of the alien hand sign, a subclinical deficiency in nondominant hand motor control was evident in a laboratory setting. Our patient had no deficit in intermanual somesthetic transfer or dichotic listening. This is in contrast to several other published r e p o r t ~ ~that ~ J described ~<~~ profound deficits in interhemispheric somatosensory transfer in patients with lesions affecting the body of the corpus callosum. However, others3~Lg~3z-34 did not observe such deficits as long as the splenium was spared, suggesting that the splenium provides an additional pathway for the interhemispheric transfer of somatosensory information. 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Neurology 1995;45;802-808 DOI 10.1212/WNL.45.4.802 This information is current as of April 1, 1995 Updated Information & Services including high resolution figures, can be found at: http://www.neurology.org/content/45/4/802.full.html References This article cites 27 articles, 5 of which you can access for free at: http://www.neurology.org/content/45/4/802.full.html##ref-list-1 Citations This article has been cited by 7 HighWire-hosted articles: http://www.neurology.org/content/45/4/802.full.html##otherarticles 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. Published continuously since 1951, it is now a weekly with 48 issues per year. 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