Brain, Vol. 124, No. 6, 1131-1137,
June 2001
© 2001 Oxford University Press
Examination of motor output pathways in patients with corticobasal ganglionic degeneration using transcranial magnetic stimulation
Unitat d'EMG and Unitat de Parkinson i Trastorns del Moviment, Neurology Service, Hospital Clínic, Villarroel, 170, Facultad de Medicina, Universitat de Barcelona, Institut d'Investigació Biomèdica August Pi i Sunyer (IDIBAPS), Barcelona, Spain
Correspondence to:
Josep Valls-Solé, Unitat d'EMG, Servei de Neurologia, Hospital Clinic, Villarroel, 170 Barcelona 08036, Spain E-mail: jvalls{at}clinic.ub.es
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Abstract |
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The alien hand sign (AHS) is often encountered in patients with corticobasal ganglionic degeneration (CBGD), revealing a unilateral dysfunction of the motor system of unknown pathophysiology. We examined the possibility of an abnormal cortical representation of hand muscles in 10 patients with probable CBGD and a prominent AHS. Cortical maps were obtained from the responses to magnetic stimuli applied with a figure of eight coil at an intensity of 110% above motor threshold. For comparison, the same study was carried out in 10 normal volunteers, eight patients with Parkinson's disease and eight patients with Alzheimer's disease. AHS patients had a larger extension of the cortical map to stimulation of the hemisphere contralateral to the AHS in comparison with the ipsilateral hemisphere. Furthermore, in six patients, focal stimulation of the hemisphere ipsilateral to the AHS gave rise to ipsilateral responses, delayed by a mean of 7.7 ± 2.2 ms with respect to those recorded in the same muscle to contralateral stimulation. None of the other patients or control subjects had ipsilateral responses. Our results indicate an enhanced excitability, or reduced inhibition, of the motor area of the hemisphere contralateral to the AHS. The delay of the ipsilateral responses is compatible with a disinhibited transcallosal input.
transcranial magnetic stimulation; corticobasal ganglionic degeneration; ipsilateral motor evoked potentials; alien hand; cortical map
AHS = alien hand sign; CBGD = corticobasal ganglionic degeneration; MEP = motor evoked potential; TMS = transcranial cortical magnetic stimulation
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Introduction |
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The alien hand sign (AHS) is usually described as an autonomous behaviour of the patient's hand, perceived as involuntary, and is different from other identifiable movement disorders (Doody and Jankovic, 1992
). It may manifest as simple arm levitation or as involuntary bizarre and complex arm movements, even with a purposeful behaviour (Grimes et al., 1999). The AHS is a clinical feature commonly seen in patients with corticobasal ganglionic degeneration (CBGD) syndrome, even when their post-mortem histopathological examination indicates other diagnoses (Ball et al., 1993; Boeve et al., 1999; Grimes et al., 1999). The pathophysiology of AHS remains obscure. We hypothesized that involuntary arm movements may be related to cortical motor or premotor dysfunction and, specifically, to an abnormal intracortical connectivity. Therefore, we considered the possibility that transcranial cortical magnetic stimulation (TMS) studies of the extension of cortical representation of hand muscles will be helpful in revealing some pathophysiological aspects of the cortical dysfunction underlying AHS. |
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The study was done in 10 patients with AHS in the context of a CBGD syndrome, whose clinical features are summarized in Table 1
. We also studied eight patients with idiopathic Parkinson's disease, aged 48–71 years, and eight patients with Alzheimer's disease, aged 54–69 years. Diagnosis was made according to the established clinical criteria for each disease. Patients with idiopathic Parkinson's disease responded to L-dopa therapy for more than 2 years and exhibited no symptoms or signs of other neurological disease (Koller, 1992; Gelb et al., 1999). Four of them (50%) had an asymmetric syndrome, with predominantly unilateral rigidity and tremor. Patients with Alzheimer's disease were diagnosed according to the NINCDS/ADRDA (National Institute of Neurological and Communicative Disorders and Stroke/Alzheimer's Disease and Related Disorders) report (McKhann et al., 1984; Lopez et al., 1999). We also studied 10 healthy subjects, aged 38–83 years, who served as a control group. All control subjects and patients gave their informed consent for the studies, which were approved by the ethical committee of our Institution, Faculty of Medicine, University of Barcelona.
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Methods |
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Neurophysiological study
TMS was performed with a focal, figure of eight, magnetic coil (MagStim), with two joint circular windings of 7 cm diameter each. This coil induces a biphasic current pulse of equal magnitude in both phases and is suitable for mapping studies (Cohen et al., 1991a
; Brasil-Neto et al., 1992b). Patients were sitting relaxed in a chair with armrests. Surface recording electrodes were attached over each thenar eminence at the best position to record the supramaximal compound muscle action potential elicited by median nerve stimulation at the wrist. A commercially available swimming cap was used to cover the scalp and draw a 1 cm width graticule, centred in Cz. We then applied single TMS to look for the best coil position to obtain a motor evoked potential (MEP) in the contralateral hand, and determined the motor threshold for that position, for each hemisphere. Motor threshold was considered as the intensity in which single stimuli elicited an MEP of an amplitude of at least 50 µV in 50% of a series of six stimuli.
We applied three single TMS at an intensity 110% of motor threshold at each marked scalp position, and recorded the MEPs simultaneously in both thenar muscles. We constantly monitored the EMG signal from the thenar muscles to make sure that they were relaxed before delivering the stimuli. All traces were printed on photosensitive paper, for off-line analysis. All stimuli were applied by the same experimenter, who held the coil flat over the scalp with the handle facing backwards. We introduced several periods of rest during the experiment and the temperature of the coil was reduced during these rest periods by placing it among bags of dry ice.
The inhibition induced by TMS in the ongoing EMG activity during voluntary contraction of the thenar muscles was examined in six patients with CBGD, four patients with Parkinson's disease and one patient with Alzheimer's disease. These patients were selected on the basis of their availability to come for a second examination. They had no clinical features different from those of their whole group. A sustained unilateral voluntary contraction of the thenar muscles was obtained by asking the patient to hold a sheet of paper between the thumb and the index finger. With this manoeuvre, the level of background EMG activity of the thenar muscles was ~30% of that obtained during maximum contraction. TMS was applied to the contralateral hemisphere at the best coil position for eliciting the MEP, and the same intensity was used for the whole procedure.
Data analysis
We measured the MEP latency and amplitude in responses larger than 50 µV obtained from the three stimuli applied at each scalp position. Absent responses were assigned 0 for amplitude calculation and no data for latency evaluation. Data were grouped separately for right and left hemispheres in control subjects and patients and also for ipsilateral and contralateral hemispheres with respect to the most affected limb in patients with CBGD and Parkinson'disease. We determined the mean latency and amplitude of the MEPs, considering 0 as the amplitude of missing responses, and absent data for their latency. Cortical maps of scalp positions of representation of thenar muscles were plotted in an x–y graticule. Data for statistical comparison of the extension of the cortical representation of thenar muscles between hemispheres in the same group of patients and between patients of different groups (ANOVA) were obtained by counting the scalp sites from which MEPs larger than 50 µV were obtained in the contralateral thenar muscles, and calculating the mean MEP amplitude for those stimulation sites.
In the 11 patients in whom we analysed the TMS-induced silent period, data were collected simultaneously from both hands. Silent period latency was measured as the time in which the EMG activity decreased consistently to <80% of the background level. Silent period duration was measured as the time interval between the stimulus and the point at which the EMG activity reached an amplitude similar to, or higher than, that of the background.
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Results |
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Unilateral focal TMS induced MEPs in the contralateral hand in all control subjects and patients, except for two patients with CBGD (Patients 8 and 9 in Table 1
), and one patient with Alzheimer's disease. Patients in whom no responses could be elicited in either hand at the maximum intensity of the magnetic stimulator (100%) were not included in the analysis of the MEP or of the cortical maps. Focal unilateral TMS induced strictly contralateral MEPs in all scalp positions stimulated in control subjects, patients with Parkinson's disease and patients with Alzheimer's disease. Strikingly, however, in six out of the eight patients with CBGD in whom TMS induced the expected MEP in the contralateral hand, focal TMS applied to many points of the hemisphere ipsilateral to the AHS also elicited a well-defined response in the ipsilateral hand (Fig. 1). The ipsilateral MEP was a mean of 7.7 ± 1.2 ms delayed with respect to the responses elicited in the same hand by contralateral stimuli. Ipsilateral responses were not elicited by stimuli applied to the hemisphere contralateral to the AHS in any CBGD patient, except one (Patient 10) who had bilateral responses elicited by stimulation of either side.
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Table 2
shows all parametric data obtained in control subjects and patients. No statistically significant differences were observed between control subjects and any group of patients, nor between right and left hemispheres, with respect to motor threshold, scalp position at which the maximum amplitude MEP was elicited and the MEP latency. However, patients with CBGD had a statistically significantly larger extension of the cortical map in the hemisphere contralateral to the more symptomatic limb than in the opposite hemisphere (Fig. 2). Differences between hemispheric maps of cortical representation of thenar muscles were not observed in any other group of patients, nor by comparing right with left or the side clinically more affected with the contralateral side in the four idiopathic Parkinson's disease patients with predominantly unilateral symptoms.
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Silent periods were analysed in the patients in whom TMS elicited no MEPs (two patients with CBGD and one patient with Alzheimer's disease), as well as in four other patients with CBGD and four patients with Parkinson's disease. In the patient with Alzheimer's disease and in the four patients with Parkinson's disease, TMS induced contralateral silent periods of 62–110 ms duration, with no significant differences between sides (0–13 ms). In the two patients with CBGD and no MEPs, TMS induced a silent period whose duration in the more affected hand was significantly reduced in comparison with the contralateral hand (34 ± 31 ms versus 74 ± 38 ms; t test; P = 0.002). In one patient (Patient 9, Table 1
), silent periods were absent in the more affected hand during unilateral or bilateral contraction, with stimulation of the ipsilateral or contralateral hemispheres (Fig. 3). In contrast, in two patients with CBGD and bilateral MEPs, TMS applied over the motor cortex ipsilateral to the more symptomatic limb induced silent periods in both the contralateral and ipsilateral thenar muscles.
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Discussion |
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Mapping studies using TMS are considered reliable and reproducible when they are obtained by complying with due technical requirements (Cohen et al., 1991a
; Brasil-Neto et al., 1992b; Wilson et al., 1993; Mortifee et al., 1994; Kaneko et al., 1996). In a study correlating the results of brain mapping of the motor cortex with the magnetic resonance of the brain, the site of maximal response always coincided with the anterior bank of the central sulcus (Wassermann et al., 1996) and there was a good correlation between the sites of maximal response to focal TMS and the site of activation of hand muscles determined with functional MRI (Krings et al., 1997). Therefore, we think that our results reliably indicate differences between sides in the area of cortical representation of hand muscles, defined as the number of sites in the scalp from which an MEP can be obtained in the monitored hand muscle, in a number of patients with CBGD and AHS.
TMS has been used previously in the characterization of the motor cortical dysfunction of patients with CBGD (Kujirai et al., 1993; Yokota et al., 1995; Hanajima et al., 1996; Lu et al., 1998). Yokota and colleagues reported unilateral hyperexcitability of the motor cortex to inputs from peripheral nerves in the more affected side of 10 patients with L-dopa-non-responsive hemiparkinsonism, assumed to have CBGD (Yokota et al., 1995). Hanajima and colleagues (Hanajima et al., 1996) used the paired shock TMS technique (Kujirai et al., 1993) in patients with various CNS disorders, and found reduced corticocortical inhibition in those with suspected CBGD. Lu and colleagues found a significant shortening of the post-MEP silent period duration in muscles of the more affected hand of two patients with probable CBGD (Lu et al., 1998), as was the case in six of our patients. A reduced inhibitory effect of cortical stimulation on the contralateral voluntary EMG activity was also reported by other authors (Ashby et al., 1996; Kato, 1997). The purpose of our study was to look for signs of asymmetric abnormalities that could be underlying the pathophysiology of AHS. We hypothesized that the AHS can be the result of an increased or unwanted motor cortical activity, and that this can show up as an increased extension of the cortical map. The extension of the motor cortical representation of hand muscles is an indirect measure of the corticocortical connectivity network and, therefore, could reveal the extent of motor plasticity changes occurring in health and in certain disease conditions (Brasil-Neto et al., 1992a; Pascual-Leone et al., 1993, 1996; Hallett, 1996; Oliveri et al., 1999).
We found a larger extension of the contralateral cortical representation of muscles involved with AHS and well defined MEPs to ipsilateral cortical stimulation in muscles in a substantial percentage of patients with CBGD. This observation, which has not been reported previously in any healthy subject nor in patients with movement disorders, was characteristic of patients with CBGD. It was not present in patients with other neurodegenerative disorders even if they featured a predominantly unilateral involvement, as was the case in some of our patients with Parkinson's disease.
The asymmetric enlargement of the cortical map of representation of hand muscles is compatible with a unilateral enhancement of excitability in the motor cortex contralateral to the AHS. This can be due to an abnormal increase of facilitatory inputs, or to an abnormal decrease of the inhibitory inputs. There are many observations in favour of the latter: SPECT (single positron emission computerized tomography) usually shows reduced frontal lobe perfusion (Caselli et al., 1992), and PET shows depressed oxygen metabolism in many cortical areas, including the posterior part of the frontal lobe (Sawle et al., 1991). The coincidence of regional hypometabolism and enhanced cortical excitability is compatible with functional or structural loss of cortico-cortical inhibitory neurones.
TMS elicitation of ipsilateral MEPs occurred selectively in patients with AHS. Ipsilateral responses to focal TMS have not been reported before in normal controls at rest, nor in any group of patients with parkinsonism. However, they can be obtained in normal subjects during voluntary contraction (Wassermann et al., 1991; Ziemann et al., 1999), or using averaging techniques and relatively sophisticated statistical analyses (Wassermann et al., 1994). Ipsilateral MEPs are obtained in patients with congenital mirror movements after stimulation of both hemispheres (Farmer et al., 1990; Cohen et al., 1991b). They are also found after stimulation of the spared hemisphere in patients who underwent hemispherectomy or had severe unilateral hemispheric damage (Benecke et al., 1991), and may occur after a stroke (Turton et al., 1996). We think that responses to stimulation of the ipsilateral hemisphere may actually be the consequence of a dysfunction in the contralateral motor cortex. We suggest that functional or structural reduction of inhibitory connections can generate both an extended area of cortical representation of contralateral MEPs and a reduced inhibitory action on TMS-induced transcallosal inputs. In experimental animals, focal stimulation of the motor cortex induced excitatory responses in a very small area of the contralateral motor cortex (Asanuma and Okuda, 1962). The cortical field of this excitatory response is surrounded by a larger inhibitory field. In humans, Cracco and colleagues showed that the latency of interhemispheric corticocortical excitatory connections was around 8 ms (Cracco et al., 1989), and Ferbert and colleagues observed interhemispheric inhibition between 5 and 9 ms (Ferbert et al., 1992). The mean delay of 7.7 ms that was observed in our patients between the ipsilateral and contralateral MEPs is compatible with an interhemispheric transit of impulses. Further support for the possible implication of the corpus callosum in the generation of the ipsilateral responses in our patients comes from the observations of Meyer and colleagues in 10 patients with abnormalities of the corpus callosum. In these patients, ipsilateral silent periods were absent or reduced, indicating reduced transcallosal inhibition (Meyer et al., 1995). It is possible that in some CBGD patients, reduced neuronal metabolism also involves excitatory neurones of the frontal lobe and hence preclude the elicitation of MEPs, as was the case in two of our patients.
Cortical sensorimotor dysfunction and parkinsonism are essential features of CBGD (Gibb et al., 1989). However, recognition of cortical dysfunction may sometimes be difficult if the akinetic–rigid syndrome is the dominant clinical feature (Riley et al., 1990). Variants from the most classical clinical presentation have been recognized (Bergeron et al., 1996). The spectrum of diseases that manifest like CBGD is rapidly widening, including cases with progressive aphasia (Arima et al., 1994), progressive supranuclear palsy (Bergeron et al., 1996), Alzheimer's disease (Ball et al., 1993) and dementia with frontotemporal atrophy (Grimes et al., 1999). Neurophysiological examination may introduce another variable to the diagnostic assessment of these patients. However, the pathophysiological correlate of some clinical signs might help in further characterization of the disease. Our finding of asymmetrically enhanced cortical excitability is consistent with the asymmetric motor dysfunction shown by patients with AHS.
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Received July 10, 2000. Revised October 30, 2000. Accepted February 6, 2001.
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