Neuroscience Letters 240 (1998) 131–134 Three hands: fragmentation of human bodily awareness Riitta Hari a , c ,*, Ritva Hänninen b, Timo Mäkinen b, Veikko Jousmäki a, Nina Forss a, Mika Seppä a, Oili Salonen d a Brain Research Unit, Low Temperature Laboratory, Helsinki University of Technology, P.O. Box 2200, FIN-02015 HUT, Espoo, Finland b Department of Neurology, Central Hospital of Central Finland, Keskussairaalantie 19, FIN-40620 Jyväskylä, Finland c Department of Clinical Neurosciences, Helsinki University Central Hospital, FIN-00290 Helsinki, Finland d Department of Radiology, Helsinki University Central Hospital, FIN-00290 Helsinki, Finland Received 5 September 1997; received in revised form 5 December 1997; accepted 5 December 1997 Abstract We describe patient E.P. who occasionally perceives a ‘ghost’ hand which copies the previous positions of the left hand with a 0.5–1 min time lag, but follows the movement patterns of the right hand. The symptoms started after an operation of a ruptured aneurysm, followed by an infarction of the right frontal lobe; E.P. also has a previously lesioned corpus callosum. Neuromagnetic recordings revealed that activity of the left secondary somatosensory cortex was strongly suppressed during the ghost arm percept, thereby providing an objective correlate for E.P.’s sensations. We conclude that simultaneous mental contents about body scheme may be based on neural information extracted at considerably different times, resulting in fragmentation of bodily awareness.  1998 Elsevier Science Ireland Ltd. Keywords: Body image; Bodily awareness; Anterior supplementary motor area; Corpus callosum; Secondary somatosensory cortex; Magnetoencephalography A healthy human’s unitary bodily awareness relies on a stable body scheme, which may be in part genetically determined and which may change after brain lesion. We report here on a patient whose bodily awareness became fragmented after operation of a ruptured aneurysm of the left pericallosal artery, resulting in a frontal lobe lesion. E.P., a previously healthy 37-year-old right-handed female suffered from subarachnoidal hemorrhage in January 1994. She had no psychiatric history and had worked successfully before her illness in a paper product factory. The ruptured aneurysm of the left pericallosal artery was operated on but the recovery was slow, in part because of an infarction in the right dorsomedial frontal lobe (Fig. 1). The MRI also showed an apparently prenatal lesion of the body of corpus callosum. According to postoperative tests, E.P. had average intelligence and a very good memory. Her left hand was slightly clumsy, easily started to follow the right hand, and was * Corresponding author. Fax: +358 9 4512969; e-mail: hari@neuro.hut.fi disturbed during rhythmical movements. E.P. had slight tactile anomia in the left hand and left-hand dominant constructional apraxia, but she was able to write and draw with both hands. As a sign of motor perseveration she had difficulties stopping some rhythmical movements. When attempting to greet with the right hand she sometimes raised both hands. Position sense was normal. E.P.’s facial expression was often rigid when she was been spoken to or when she did not talk herself. She was not able to change her mind, plans, or order of actions quickly, and she often had competing thoughts (e.g. ‘to go in or to continue walking outside’) which paralyzed her. After the operation E.P. had suffered from intermanual conflict and alien hand syndrome, in agreement with her partial callosal disconnection and the infarction of the mesial frontal cortex [2,3]. For example, while E.P. was reading a newspaper and turning the page with the right hand, the left hand turned back the same page. While eating, the left hand tried to put more food into the mouth than what E.P. was able to swallow. During swimming, E.P. was afraid that the left hand wanted to drown her. 0304-3940/98/$19.00  1998 Elsevier Science Ireland Ltd. All rights reserved PII S0304- 3940(97) 00945- 2 132 R. Hari et al. / Neuroscience Letters 240 (1998) 131–134 Fig. 1. Top: surface reconstruction of E.P.’s brain based on magnetic resonance images (Siemens 1.5-T Magnetomy) recorded 3 years after the operation. For clarity, the infarcted right frontal region has been removed by the computer. Bottom: the arrows point to lesions of the right mesial frontal lobe, the anterior corpus callosum, and the evidently perinatal lesion of the body of corpus callosum. E.P. also developed other disturbances in her body image [9]. Several times a day she sensed a third arm and, less frequently, a third leg. Fig. 2 illustrates her own drawing of such a situation (the left/right mistake in the drawing was frequent for her). E.P. was fully conscious of the abnormality of her percepts and was able to observe analytically her symptoms. The ghost limbs were always on the left side of the body and often felt so real that E.P. had difficulties in distinguishing them from the real limbs. Seeing the real limb removed the ghost, as did strong tactile stimulation. Interestingly, the position of the ghost hand copied, in a perseverative manner, the previous position of the left real hand: for example, if the left hand had previously been on the arm rest of a chair but was now on a table, the (proprioceptically) appearing ghost hand was on the arm rest. When the left hand was moved back to the arm rest, the ghost limb disappeared but reappeared soon, this time to the table. The time delay from the new position of the left arm to the appearance of the ghost limb was measured several times and was typically 0.5–1 min. If E.P. stayed immobile, the ghost percept could last for tens of minutes. The ghost limbs were not under voluntary control but frequently followed movements of the right limbs. For example, when E.P. moved one finger of the right hand, she felt like the corresponding finger would have moved in the ghost hand at the same time. However, the general position of the ghost was determined by the previous position of the left hand. E.P. occasionally experienced splitting of her body: when she was rising from a bench, she felt that only the right half started walking, whereas the left side remained on the bench. Repetitive and monotonical movements triggered this percept whereas dancing, for example, prevented its appearance. E.P.’s neuromagnetic [8] cortical activity was recorded with a 122-channel whole-scalp neuromagnetometer [1]. The left and right median nerves were stimulated at the wrists with 0.3-ms constant-current pulses once every 3 s, with stimulus intensities exceeding the motor threshold. About 70 artefact-free single responses were averaged selectively during periods when E.P. perceived or did not perceive the extra limb. EP was able to provoke the ghost hand percept with certain positions of the left extremity and she reported verbally when the ghost appeared/disappeared. Fig. 3 shows activation strengths of the left primary and secondary (SI and SII) cortices after right median nerve stimuli. Both responses occurred at normal latencies. However, responses of the SII cortex [6], strongest about 80 ms after the stimulus onset, were dampened by 50% during the ghost hand percept; the finding was well replicable during successive measurements, and practically identical results were obtained five months later. The SI cortex showed a trend to enhanced responses at 115 ms during the ghost percept whereas the earlier responses were identical in both conditions. The responses of the right SII (ipsilateral to the stimuli) were very small and showed no consistent differences between the conditions. The right-hemisphere SI and SII responses were normal to left median nerve stimuli but it was not possible to study the ghost limb effect on them since the stimuli immediately abolished the ghost. We consider the modification of the SII responses during the ghost hand percept as an objective correlate of E.P.’s sensations, especially since the effect is markedly stronger than the previously described attentional effects on the SII activity [5]. SII is considered to be related to e.g. haptic processing, tactile learning and retention, motor intent, and also to autotopognostic body scheme [4,7,13]. The SII cortices of both hemispheres are activated after unilateral limb stimulation and thus SII may have a role in combining R. Hari et al. / Neuroscience Letters 240 (1998) 131–134 somatosensory information from the two body sides to allow interhemispheric unification which was apparently distorted in E.P due to callosal lesion. Area 5 in the parietal lobe contains representations of current limb postures [10], which are constantly updated on the basis of proprioceptive information, visual input, and probably also by ‘efferent copies’ from the motionrelated brain areas as the limb is deliberately moved. We cannot exclude the possibility that the 115-ms response from the SI cortex, stronger during the presence than the absence of the ghost, would in fact have received contribution form the nearby area 5. The anterior supplementary motor area, so-called preSMA (area 6ab), is essential for updating motor plans [12,14–16] and thus a probable source of efferent copies. Probably due to pre-SMA lesion, signals about intended movements of E.P.’s left hand fail to update her limb position representation(s); this deficit is certainly accentuated by the distorted callosal transfer. As a result, E.P. seems to have Fig. 2. E.P.’s drawing of herself when she has the ghost limb percept. The upper ghost limb typically originated in the upper left part of the torso, and the lower ghost limb at the same place as the left lower limb. Some objects in one real hand (either left or right) were perceived in all three hands and generated embarassing situations: while shopping E.P. suddenly felt like having three bags, instead of one, and was anxious of having accidentally taken bags from other people. E.P.’s description of this figure (translated from Finnish): ‘this is the feeling I have when I go with a bag or something in my hand. I have even had three dogs on a lead, although in reality there was only one’. 133 Fig. 3. Time courses of activation of the left SI and SII cortices after right median nerve stimulation when E.P. did not perceive the ghost limb (solid lines) and when the ghost limb was present (dashed lines). The coordinate systems of the magnetic resonance images and neuromagnetic data were aligned by means of a 3-D digitizer and a head position indicator system, and the sources of evoked signals were modelled as current dipoles [8]. The same measurements were repeated once, shown with the superimposed traces. The circles on the MRI slice illustrate the dipole locations in the left SI and SII cortices. at least two representations of the left arm (leg), which do not always coincide and lead to the percept of the additional limb at the previous position of the real left limb. Somatosensory and visual signals still correctly update the representation and cause the ghost to disappear. Signals about the intended right hand movements seem to incorrectly update (one of) the left hand representation(s), thereby giving rise to a moving ghost. The necessity of the efferent copy for proper updating of the position representation is supported by the finding that the ghost hand imitates only active, not passive movements of the right hand. We hypothesize that due to pre-SMA lesion, E.P.’s representations of limb postures are not properly updated and, due to callosal disconnection, her hemispheres support different body images. Consequently E.P.’s bodily awareness is fragmented so that one part relies on current proprioceptive information and another on the previous data which were relevant tens of seconds earlier. A very similar phenomenon is palinopsia (‘seeing again’) which refers to a visual perseveration with persistence or reappearance of a visual image when the original stimulus is no longer present [11]. Palinopsia has been reported mainly after right-hemisphere lesions. Both palinopsia and the ghost hand percept of E.P. could be explained by a lack of active suppression of neural activity. It thus seems evident that simultaneous mental contents of body scheme may be based on neural activity which has emerged at considerably different times and that conscious body image may be based on competing activity of more than one brain region. These results are in line with modularity of human bodily awareness. The modules act in concert during normal circumstances but may become independent, and result in fragmentation of bodily awareness, after distorted updating of cerebral representations. 134 R. Hari et al. / Neuroscience Letters 240 (1998) 131–134 This study was supported by the Academy of Finland. We thank C. Frith, S. Salenius, G. Curio, O.V. Lounasmaa, R. Paetau, S. Vanni, and V. Virsu for discussions and comments, and M. Illman for help with MEG measurements. 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