Brain, Vol. 125, No. 9, 2125-2133,
September 2002
© 2002 Guarantors of Brain
Transmission of group II heteronymous pathways is enhanced in rigid lower limb of de novo patients with Parkinson’s disease
1 Inserm U455, 2 Centre d’Investigation Clinique, Pavillon Riser, CHU Purpan, Toulouse, 3 Laboratoire de Neurophysiologie Clinique, CHU Pitié Salpêtrière, 4 Service de Neurologie, CHU St Antoine, Paris, France
Correspondence to: Dr M. Simonetta Moreau, Pavillon Riser, CHU Purpan, Place du Dr Baylac, 31059 Toulouse cedex, France E-mail: simonetta.m{at}chu-toulouse.fr
Received February 15, 2002. Accepted March 22, 2002.
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Summary |
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A potent heteronymous excitation of quadriceps motoneurones via common peroneal group II afferents has recently been demonstrated in normal subjects. The aim of this study was to investigate whether this group II excitation contributes to rigidity in Parkinson’s disease. The early and late facilitations of the quadriceps H reflex elicited by a conditioning volley to the common peroneal nerve (CPN) at twice motor threshold, attributed to non-monosynaptic group I and group II excitations, respectively, were investigated. The comparison was drawn between results obtained in 20 ‘de novo’ patients with Parkinson’s disease (hemiparkinsonian, 17; bilateral, three) and 20 age-matched normal subjects. There was no statistically significant effect of ‘group’ (patients/controls), ‘duration’, ‘global severity’ [Unified Parkinson’s Disease Rating Scale (UPDRS)] or ‘side’ (unilaterally versus bilaterally affected) factors on either group I or group II facilitations. To further the analysis, the factors of status (affected or non-affected limb), akinesia (lower limb akinesia score) and rigidity (lower limb rigidity score) were entered in a general linear model to explain the variations of the quadriceps H reflex facilitation. Rigidity was the only factor useful in predicting the value of the group II facilitation of the quadriceps H reflex (P < 0.007). Group I and group II facilitation was then compared between the rigid, non-rigid and control lower limbs [multivariate analysis of variance (MANOVA)]. Results are represented as mean ± SEM (standard error of the mean). Group II facilitation was enhanced in the rigid lower limb of unilaterally affected patients (153.2 ± 7% of control H reflex) compared with non-rigid lower limbs (124 ± 4% of control H reflex; P < 0.007) or control lower limbs (126.1 ± 4.1%; P < 0.01). There was no difference between the non-rigid lower limbs of the unilaterally affected patients and the control lower limbs, but a difference was observed between the rigid lower limbs of unilaterally less affected and bilaterally more affected patients (153.2 ± 7% and 123.8 ± 7.5% of control H reflex, respectively; P < 0.04). These results suggest a facilitation of the transmission in the interneuronal pathway activated by group II afferents in rigid lower limb of de novo hemiparkinsonian patients, probably resulting from a change in their descending monoaminergic inhibitory control.
Keywords: group II afferents; H reflex; Parkinson’s disease; rigidity
Abbreviations: CPN = common peroneal nerve; ISI = interstimulus intervals; LC = locus coeruleus; MT = motor threshold; TA = tibialis anterior
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Introduction |
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Rigidity is a cardinal feature of Parkinson’s disease and is characterized clinically by a sustained increase in resistance to passive movement of a joint thoughout its range. Although it has been studied intensively, the pathophysiology of parkinsonian rigidity is still unclear. While the monosynaptic stretch reflex is not modified in Parkinson’s disease (Mortimer and Webster, 1979
), long latency stretch reflexes have been found to be exaggerated in a variety of upper and lower limb muscles: wrist flexors and extensors (Tatton and Lee, 1975), biceps (Mortimer and Webster, 1979), triceps and flexor pollicis longus (Rothwell et al., 1983), and tibialis anterior and triceps surae (Chan et al., 1979; Berardelli et al., 1983). A causal relationship was proposed between rigidity and these abnormal responses (Tatton and Lee, 1975; Berardelli et al., 1983) but was further discussed (Rothwell et al., 1983; Cody et al., 1986). Among all the hypotheses proposed to explain the origin of long latency stretch reflexes, two main theories have emerged. The first one may involve a trans-cortical long loop. Convincing evidence has accumulated in recent years for such a trans-cortical long loop, fed by Ia afferents-mediated long latency stretch reflexes, in intrinsic muscles of the hand (Marsden et al., 1983; Noth et al., 1991). The second one may involve a segmental spinal cord pathway (Berardelli et al., 1983; Matthews, 1984). In fact, it has been demonstrated recently that the long latency response evoked by stretch in ankle and foot muscles of normal subjects is a spinal segmental reflex mediated by group II muscle afferents (Corna et al., 1995; Schieppati et al., 1995, 1997). A potent heteronymous group II excitation of quadriceps motoneurones has also been demonstrated in normal subjects after stimulation of the common peroneal nerve (CPN) (Marque et al., 1996; Simonetta Moreau et al., 1999). The present research was undertaken to investigate whether this heteronymous group II excitation also contributes to rigidity in Parkinson’s disease. In both animal and human experiments, the excitability of group II pathways can be influenced by monoaminergic drugs (Bras et al., 1990; Noga et al., 1992; Eriksson et al., 1996), therefore the study was performed in patients who had never taken antiparkinsonian medications (‘de novo’ patients). |
Methods |
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Subjects
Twenty de novo patients with Parkinson’s disease [10 men and 10 women aged 42–74 years; mean ± SEM (standard error of the mean) 59.2 ± 2 years] and 20 healthy control subjects (12 men and eight women aged 34–75 years; 56.9 ± 2.5 years) were enrolled in the study. The study was performed before any antiparkinsonian treatment was started. All patients fulfilled the UK Parkinson’s Disease Brain Bank criteria for the diagnosis of idiopathic Parkinson’s disease (except the positive response to L-dopa) (Gibbs and Lees, 1988
), and later had a positive long-lasting response to L-dopa in a 2-year follow-up. Patients gave informed consent to the experimental procedure, which was approved by the local ethics committee (CCPPRB Toulouse II). The diagnosis of Parkinson’s disease was established on the basis of: (i) akineto-rigid symptoms of progressive onset; (ii) absence of clinical evidence of dementia; (iii) absence of signs or symptoms suggesting other degenerative syndromes; (iv) absence of chronic administration of neuroleptic drugs; and (v) normal CT scan or MRI. For technical reasons, patients with predominant lower limb rest tremor had been excluded. Patients were evaluated clinically by two physicians trained in movement disorders (M.V. and M.G.) and a Unified Parkinson’s Disease Rating Score (UPDRS) (Fahn and Elton, 1987) was obtained at the time of the electrophysiological test. Parkinsonian signs were strictly unilateral in most of the patients (17) and bilateral in three. Patients were at Hoehn and Yahr stages I–II and had a UPDRS score (part III) of 11.5 ± 1.1 (mean ± SEM). From the items of the UPDRS score (part III), subscores of rigidity and akinesia were calculated for each lower limb. The lower limb score of rigidity was 0 in 11 unilaterally affected patients, and 
1 in the nine resting patients (hemiparkinsonian, six; bilateral, three). Data for the 20 patients are summarized in Table 1.
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Experimental procedure
General experimental arrangement
The subjects were comfortably seated in an armchair with the limbs supported, the hip semi-flexed (60°), the knee slightly flexed (10–20°) and the ankle at 20° plantar flexion. In this position, complete muscular relaxation of lower limbs was easily achieved and continuously monitored by an audio-visual feedback of background EMG (quadriceps and tibialis anterior muscles).
Recording
EMG was recorded by surface electrodes 2 cm apart, secured to the skin over the muscle belly of the vasto-crureus (15– 20 cm above the patella on the anterior aspect of the thigh) and the tibialis anterior (TA; medial part of the anterior aspect of the leg).
Quadriceps H reflex
The quadriceps H reflex was induced by stimulating percutaneously (single shocks of 1 ms duration, 0.25 Hz) the femoral nerve (FN). The active cathode (half-ball, 2 cm diameter) was in the femoral triangle and the reference electrode under the buttock. The intensity of the stimulation was adjusted so that the size of the unconditioned H reflex was 
50% of its maximal amplitude.
The amplitude of the quadriceps maximum M response (M max) was measured in half of all patients and controls, and the ratio H test/M max was calculated from the mean amplitude of the quadriceps H reflex test during the experiments. The size of the H reflex was >10% of M max in almost all the subjects. In one patient and four controls, reflexes of one or both sides were very small, with sizes <5% of M max.
Conditioning stimulus
Electrical pulses (1 ms duration) were delivered to the CPN at the level of the caput fibulae, through bipolar surface electrodes (1 cm diameter silver plate electrodes, 2 cm apart). The current was measured by a current probe (Tektronix 602, Tektronix Inc., Beaverton, OR, USA) and expressed in multiples of the intensity for motor threshold (MT). The CPN was stimulated at a site where the threshold for the M-response was lower for the TA than for the peroneal muscles. Nevertheless, when intensity was increased at twice TA motor threshold (2x MT) there was also a contraction of the peroneal muscles. It was verified by tendon palpation that stimulating the CPN at 2x MT did not produce any contraction of muscles other than those innervated by the CPN, i.e. it did not encroach upon another nerve.
Experimental protocol
The timing of the conditioning (CPN) stimulation in relation to the test (FN) stimulation was crucial to separate excitation mediated by group I from that mediated by group II afferents. Interstimulus intervals (ISIs) between 8 and 24 ms were investigated. Usually, nine to 10 blocks of 20 reflexes were recorded for each subject. Each block consisted of 10 unconditioned (control quadriceps H reflex) and 10 conditioned reflexes (quadriceps H reflex + CPN stimulation), which were randomly alternated. The amplitude of the reflex responses was measured peak to peak. In a block, mean value of the 10 conditioned responses was expressed as a percentage of the mean value of the 10 control responses. Reflex responses were computer-analysed online and the result stored on disk for further analysis.
Statistics
The dependent variable was the size of the conditioned quadriceps H reflex. To determine in each subject whether the changes evoked in the H reflex amplitude by the conditioning stimulation were significant, a variance analysis using Scheffé’s method was performed.
A multivariate analysis of variance (MANOVA) was used to compare the effects of ‘group’ (patients versus controls), ‘duration’ (short, <10 years of evolution; medium, 10–14 years; long, 15 years), ‘global severity’ (UPDRS score <15 or 15) and ‘side’ (unilaterally and bilaterally affected patients) factors, and their interactions in group I and group II facilitations.
As UPDRS score did not faithfully reflect the clinical status of the tested lower limb, the effects of the rigidity score (rigidity, continuous variable), the akinesia score (akinesia, continuous variable) and the status of the tested limb (affected or non-affected), and their interactions were analysed further with a general linear model using a backwards selection.
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Results |
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Common peroneal nerve-induced effects were assessed at different interstimulus intervals, (ISIs; 8, 10, 12, 14, 16, 18 and 20 ms), on both sides in 18 patients and 18 controls, and on one side for two patients (affected side) and two controls. As described previously in normal subjects (Marque et al., 1996
) and illustrated in Fig. 1 (time course of H reflex facilitation after CPN stimulation in one control subject, black triangles), CPN stimulation at 2x MT evoked a biphasic facilitation of the quadriceps H reflex with an early peak at 10–12 ms ISI and a later peak at 14–20 ms ISI. These facilitations were attributed, respectively, to a non-monosynaptic group I and group II afferents-mediated excitatory effect (see Discussion). When allowance was made for their different afferent conduction times, the conditioning (elicited more distally) and test Ia volleys were expected to arrive simultaneously at the spinal level at the 6 ms ISI, which corresponds to the 0 ms central delay.
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Significant group I- and group II-induced facilitations (P < 0.05; Scheffé’s method) were obtained as frequently in patients as in controls. Group I-induced facilitation was obtained in 80% of right side and 82% of left side in control subjects, and in 75% of patients’ affected or more affected side and 88% of their unaffected or less affected side. Group II-induced facilitation was obtained in 85% of right side and 72% of left side in control subjects, and in 85% of patients’ affected or more affected side and 66% of their unaffected or less affected side.
As the time course of changes in quadriceps H reflex elicited by CPN stimulation at 2x MT can be divided into an early group I facilitation (ISIs 8, 10 and 12 ms) and a later group II facilitation (ISIs 14, 16, 18, 20 ms), statistical analysis was performed averaging the data across ISIs of 8 and 12 ms (group I), and 14 and 20 ms (group II).
There was no statistically significant effect of the group, side, duration and severity factors on either group I or group II facilitations. However, in the patient group a majority of the tested limbs were neither as rigid nor akinetic as the lower limbs of the control group; this could explain the absence of significant differences between the patient and control groups. Indeed, out of the 38 lower limbs of the patients tested, 21 were normal without rigidity or akinesia, five were only rigid, five were only akinetic and seven were akineto-rigid. The question then arises of whether the affected limbs of the patients acted differently or not towards the non-affected limbs regarding the group I and group II facilitations and, if so, what are the respective roles of rigidity and akinesia in the differences observed? To answer these questions we carried out further analysis, taking into account the lower limb rigidity and akinesia scores (see Methods). Akinesia and rigidity scores were put together with the status factor (see Methods) in a general linear model, and their effects on both group I and group II dependent variables were tested using MANOVA. No effect of either akinesia, or rigidity or status factors combined, was observed on the magnitude of the conditioned quadriceps H reflex. The less significant factor (akinesia) was then removed from the model, but rigidity and status factors remained non-significant. Finally, when status factor was also removed from the model, rigidity factor alone became significant and was the only factor useful for predicting the value of group II quadriceps H reflex facilitation (P < 0.007). So the contribution of akinesia in the enhancement of group II facilitation observed in the rigid lower limbs of the patients appeared weak, if it existed, and did not represent a relevant factor.
Figure 1 shows the comparison between the time course of the changes in quadriceps H reflex amplitude elicited by a stimulation of the CPN at 2x MT in the affected side of two hemiparkinsonian patients, one with a lower limb rigidity (thick line, filled circles) and the other without (thin line, open circles), and in the right side of a control subject (thin line, filled triangles). The early facilitation of the H reflex was similar for the three subjects at 10 ms ISI (i.e. 4 ms central delay, 128% of the control value). The late facilitation peaking 4–10 ms later (14–20 ms ISIs) was much greater (P < 0.05; Scheffé’s method) on the affected side of the patient with a lower limb rigidity than on the affected side of the patient without lower limb rigidity or the right side of the control subject. At the 22 ms ISI the late facilitation was over in the control subject and in the non-rigid patient, whereas it was still present, albeit decreased, in the patient with a lower limb rigidity.
Group I and group II facilitations between the rigid (LLR+, n = 12) and non-rigid (n = 26) lower limbs of the patients and the right (n = 19) and left side (n = 19) of the controls were then compared. As there was no difference between the right and left side of the controls, all control limbs were put together. LLR+ hemiparkinsonian (n = 6) and bilaterally affected (n = 3) patients were separated in two subgroups. Results are illustrated in Fig. 2, which shows the comparison between the time course of the mean changes in the quadriceps H reflex amplitude after CPN stimulation in the rigid (hemiparkinson’s LLR+, bilateral Parkinson’s LLR+), non-rigid lower limbs of the patients, and the pooled left and right sides of the controls. Once more the rigidity factor had a highly significant effect on quadriceps H reflex facilitation (MANOVA; P < 0.007). This effect was observed exclusively for group II-induced facilitation (ANOVA; group I facilitation not significant, group II facilitation P < 0.05). Results are expressed as mean ± SEM (standard error of the mean). Group II facilitation was enhanced in the rigid lower limbs of the unilaterally affected patients compared with the non-rigid lower limbs [153.2 ± 7% and 124 ± 4% of the control H reflex, respectively (post hoc P < 0.04); compare filled circles with open circles in Fig. 2] and also compared with the control lower limbs [126.1 ± 4.1% of the control H reflex (post hoc P < 0.01); open triangles in Fig. 2]. There was no difference between the non-rigid lower limbs of the patients and the control lower limbs.
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Although group II facilitation was increased for the 18–20 ms ISIs in the rigid lower limbs (n = 6) of bilaterally affected patients (filled diamonds in Fig. 2), no statistical difference was found when comparing the sum of the late (14–20 ms) ISIs obtained in this subgroup with those obtained in the non-rigid lower limb group or the control group. Surprisingly, for group II facilitation, a significant difference was observed between the LLR+ hemiparkinsonian and bilateral parkinsonian subgroups (153.2 ± 7% and 123.8 ± 7.5% of the control value, respectively; post hoc P < 0.04).
Mean values (±SEM) of quadriceps H reflex group I (sum of 8–12 ms ISIs) and group II (sum of 14–20 ms ISIs) facilitations in the rigid (hemi and bilaterally affected LLR+), non-rigid lower limbs of the patients and in controls are shown in Fig. 3. The mean differences between conditioned and control H reflexes (expressed in as a percentage of control H reflex) are plotted against the sum of the group I (8–12 ms) and group II (14–20 ms) ISIs tested.
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Discussion |
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Whereas the early CP nerve-induced group I facilitation of quadriceps H reflex in de novo patients was not different to that in Parkinson’s disease and control subjects, the amount of late CP-induced group II quadriceps H reflex facilitation was selectively and significantly increased on hemiparkinsonian patients’ rigid compared with non-rigid lower limbs, or compared with controls. Enhancement of group II facilitation was absent in bilaterally more-affected LLR+ patients, and statistical analysis seems to show that this subgroup acted differently to the unilaterally less-affected LLR+ patients.
Origin of the early and late facilitations of the quadriceps H reflex evoked after CPN stimulation at 2x MT
It has been shown previously in normal subjects that stimulation of heteronymous nerve-like CPN at an intensity above the motor threshold evokes two peaks of facilitation in the quadriceps H reflex (Marque et al., 1996; Simonetta Moreau et al., 1999). Similar results have also been obtained in the post-stimulus time histogram of single voluntarily activated quadriceps motor units (Marque et al., 1996; Simonetta Moreau et al., 1999). The early low threshold (0.6x MT) peak is attributable to non-monosynaptic group I excitation (Forget et al., 1989) mediated through an oligo synaptic pathway, the long central delay (3–4 ms) of the effect being explained by the rostral location of the relevant premotor neurones with respect to motor neurones. The characteristics of the second peak (higher threshold, late latency increasing more than that of the early peak when the CPN is cooled) are consistent with a group II effect (Marque et al., 1996; Simonetta Moreau et al., 1999). Pure cutaneous stimulation of the skin, mimicking the sensation elicited by CPN stimulation at two or three times the motor threshold, did not evoke any significant quadriceps H reflex changes (Marque et al., 1996). Some indirect arguments (Chaix et al., 1997; Marchand-Pauvert et al., 1999) suggest that group I and group II excitations might be mediated through common interneurones in humans, as it was described in the cat (Jankowska, 1992). Recent human data have also suggest that these group II interneurones might be implicated in the control of locomotion (Marchand-Pauvert and Nielsen, 2002).
Possible mechanisms underlying the increased CPN-induced facilitation of quadriceps H reflex in patients with lower limb rigidity
Enhanced late CPN-induced facilitation of the quadriceps H reflex may be due to increased excitability of quadriceps alpha motor neurones, CPN-induced decrease of presynaptic inhibition to quadriceps Ia afferents mediating the test volley, or enhanced efficacy of the conditioning volley. Previous studies have failed to demonstrate a significant increase in the excitability of motoneurones in Parkinson’s disease (Angel and Hoffmann, 1963).
The common peroneal afferent volley evokes a presynaptic inhibition of Ia terminals mediating the afferent volley of the quadriceps H reflex (Hultborn et al., 1987; Forget et al., 1989). CPN-induced quadriceps H reflex facilitation is the net result of this presynaptic inhibition and of the postsynaptic excitatory effects mediated through the interneurones fed by group II afferents. Presynaptic inhibition to soleus Ia terminals evoked by heteronymous tibialis anterior or quadriceps Ia afferents has been found to be reduced in Parkinson’s disease (Roberts et al., 1994; Morita et al., 2000). However, in both studies this decrease in presynaptic inhibition did not show a clear relationship with rigidity. A decreased presynaptic inhibition in the rigid lower limb of our patients could therefore be partly responsible for the increased group II facilitation of the quadriceps H reflex. Nevertheless, if hyperexcitability of quadriceps alpha motor neurones or decreased presynaptic inhibition of quadriceps Ia terminals were responsible for the increased common peroneal-induced group II facilitation, the response of quadriceps motor neurones would be expected to be exaggerated to the same extent, whatever the input. The fact that the increase of quadriceps H reflex facilitation was observed only for the late group II peak and not for the early peak suggests that such mechanisms can not be retained. Enhanced late facilitation of quadriceps H reflex observed in lower limb rigid patients seems to be mainly due to a facilitation of transmission in the group II pathways activated by common peroneal afferents.
Origin of the facilitation of transmission in the group II pathways activated by common peroneal afferents
A descending inhibitory monoaminergic control at the level of lumbar premotor neurones in pathways from group II afferents, but not from group I, has been demonstrated and investigated in cats (Bras et al., 1990). This descending monoaminergic pathway comes from locus coeruleus (LC) and medullary raphe nuclei (Noga et al., 1992). Based on the following data it has been proposed that such a monoaminergic descending control to lumbar interneurones fed by group II afferents also exists in humans. First, medium latency response evoked by stretch in ankle and foot muscles is probably a spinal reflex mediated by group II muscle afferents (Matthews, 1984; Dietz, 1992; Siliotto et al., 1996). This response is selectively depressed by monoaminergic drugs such as clonidine or tizanidine, an 
2-agonist (Corna et al., 1995; Schieppati et al., 1995, 1997) known to produce a slowing of LC firing (Foote et al., 1983). Secondly, in spastic patients, exaggerated stretch reflex involves, to a great extent, responses evoked by group II muscle afferents (Eriksson et al., 1996; Marque et al., 2001) and is clearly reduced together with flexion reflexes by tizanidine (Davies, 1982; Skoog, 1996).
Although other mechanisms such as reduction in autogenic Ib inhibition (Delwaide et al., 1991) have been proposed to explain parkinsonian rigidity, we hypothesize that a decrease of the monoaminergic inhibitory descending control, which is specific for group II afferents, could contribute to the selective enhancement of the group II facilitation observed here in the rigid lower limb of de novo parkinsonian patients.
Indeed, the role of the LC in the control of tone and posture via a direct coeruleospinal projection and an indirect projection passing through the dorsal pontine reticular formation has been recently proposed from neurophysiological data by Pompeiano (2001). Neuropathological studies in Parkinson’s disease have shown a significant cell loss (60%) in rostral and caudal portions of the LC (German et al., 1992), even at an early stage of the disease (Hoogendijk, 1995). Cell loss in the LC would be greater in the caudal portion of the nucleus (Chan-Palay and Asan, 1989) than in the rostral one and it has been suggested that only this portion of the nucleus would be related to the main motor symptoms used to characterize the Parkinson’s disease. Comparing tremoring and akineto-rigid subpopulations of patients with Parkinson’s disease, Paulus and Jellinger (1991) disclosed higher neuronal loss in LC and substantia nigra in the latter subpopulation. A disinhibition of noradrenergic coeruleospinal pathway has been proposed in the pathogenesis of drug-induced muscular rigidity in rats (Lui et al., 1990). Moreover, the dramatic depletion (70–80%) of noradrenergic concentrations (contrasting with normal dopamine levels) observed in the lumbar spinal cord of parkinsonian patients (Scatton et al., 1986) is indicative of damage to the descending noradrenergic neurones. These latter results further support the contribution of a spinal noradrenergic depletion to the pathophysiolgy of parkinsonian rigidity.
Difference between unilaterally less-affected and bilaterally more-affected patients
The fact that severely bilaterally affected patients have a less pronounced increase of group II facilitation than unilaterally mildly affected patients is an apparent contradiction. This could be an artefact due to the small number of bilaterally affected patients (n = 3). It could also reflect a differential role of group II afferents in lower limb rigidity, depending on the severity of the disease. Unfortunately the number of bilaterally affected patients who entered this study was too small to answer this question. It is more likely that with disease progression, other dysfunctions may mask the group II effect.
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Acknowledgements |
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The authors wish to thank Christine Brefel-Courbon and Marie Adeline Marques for their contribution to the study. We are indebted to Dr Etienne Hirsch (Inserm I289) for helpful comments and to Pr Alain Mallet and Marie Laure Tanguy (Medical Statistics Department, University Paris VI) for the statistical analysis. This work was supported by grants from INSERM (98/314) and CHU Toulouse (98-02H), and was carried out in the Clinical Investigation Centers of Toulouse (CHU Purpan) and Paris (CHU St Antoine). Dr Sabine Meunier was supported by grants from Assistance Publique (Hôpitaux de Paris), Ministère de la Recherche (UPRES EA 2393) and IRME.
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