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Improvement of The Motor Deficit of Neglect Patients Through Vestibular Stimulation: Evidence for A Motor Neglect Component
IMPROVEMENT OF THE MOTOR DEFICIT OF NEGLECT PATIENTS THROUGH VESTIBULAR STIMULATION: EVIDENCE FOR A MOTOR NEGLECT COMPONENT G. Rode1,2, M.T. Perenin2, J. Honoré3 and D. Boisson1 (1Hôpital Henry Gabrielle, Université Claude Bernard, St Genis-Laval, France; 2Vision et Motricité, Inserm U94, Bron, France; 3Laboratoire de Neurosciences du Comportement, Université de Lille I, Villeneuve d’Ascq, France)
ABSTRACT The effect of vestibular stimulation on motor performance has been studied comparatively in 2 groups of hemiplegic patients, one including 9 right brain-damaged patients (RBD) with neglect, the other 9 left brain-damaged patients (LBD) without neglect. In the RBD group, a transient but significant improvement of motor performance was observed following stimulation, although motor scores remained unchanged in two cases. Moreover, a temporary remission of personal neglect and anosognosia was obtained in 8 out of 9 patients. In contrast to the RBD group, the motor performance of the LBD group was not improved through vestibular stimulation, although a moderate improvement of force was noticed in one ambidextrous patient who had shown transient signs of neglect at the acute stage. These results suggest the participation of a motor neglect component in the motor deficit of neglect patients. The motor neglect component may be considered as one of the many manifestations of the neglect syndrome and, as such, can be improved by the sensory manipulations which presumably restore a conscious representation of the left side of space. Key words: neglect, hemiplegia, anosognosia, vestibular stimulation
INTRODUCTION Most manifestations of unilateral neglect may be temporarily reduced by vestibular stimulation. Improvement not only concerns extrapersonal and personal neglect, but also neglect of imaginal space, anosognosia, somatoparaphrenic delusions and the somatosensory deficits often seen in association with the syndrome (Rubens, l985; Cappa, Sterzi, Vallar et al., 1987; Bisiach, Rusconi and Vallar, 1991; Rode, Charles, Perenin et al., 1992; Vallar, Bottini, Rusconi et al., 1993; Rode and Perenin, 1994). In a previous report on a single case of a long-lasting and severe neglect, we have shown that vestibular stimulation could also improve the hemiplegic deficit, as well as extrapersonal and personal neglect, anosognosia and somatoparaphrenia (Rode et al., 1992). While the patient did not move her left limbs spontaneously, she was able to flex and stretch her left leg following the stimulation, suggesting the participation of a motor neglect component in the motor deficit. Cortex, (1998) 34, 253-261
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The aim of the present study was to confirm this finding in a group of nine right brain-damaged (RBD) patients with neglect and, by comparison with a group of nine left brain-damaged (LBD) control patients, to further support the idea of a specific effect of the vestibular activation on neglect-related symptoms. Although they typically occur in association, neglect-related symptoms may also be seen separately. Various examples of dissociations have been observed (e.g. Bisiach, Perani, Vallar et al., 1986; Bisiach, Vallar, Perani et al., 1986; Barbieri and De Renzi, 1989, Guariglia, Padovani, Pantano et al., 1993). Laplane et Degos (1983) reported cases of ‘motor neglect’ described as an underutilization of the contralesional limbs in the absence of hemiplegia and visuospatial neglect. Differences and similarities between this isolated ‘motor neglect’ and the ‘motor neglect component’ we have investigated will be discussed. MATERIALS
AND
METHODS
Patients Nine right brain-damaged hemiplegic patients with unilateral neglect and nine left braindamaged hemiplegic patients without unilateral neglect participated in the study. Demographic features are described on Table I. Apart from one ambidextrous patient (case 17), all were right-handed. All the patients showed a rather extensive unilateral brain lesion, which was documented by CT-scan. Aethiology was always vascular, ischaemic in nine and haemorrhagic in the other nine cases. None of them suffered from impaired vigilance, confusion, mental deterioration or psychiatric disorders. Hemiplegia was always associated TABLE I
Demographic Features and CT Assessed Lesion Sites of the Two Groups of Patients Lesion Patient
Age/Sex
Neglect
Aetiology
Side
Site
1
69/F
+
I
R
2
63/M
+
H
R
3 4 5 6 7 8 9
52/F 61/F 71/F 63/M 68/F 67/M 69/F
+ + + + + + +
I H H H I I H
R R R R R R R
10 11 12 13 14
40/F 66/M 69/M 63/F 73/M
– – – – –
I H I I I
L L L L L
15 16 17 18
48/M 65/M 60/F 46/F
– – – –
I I I I
L L L L
Parietal temporal (occipital), basal ganglia Paraventricular subcortical white matter (parietal) basal ganglia Parietal (frontal) temporal Parietal Frontal temporal parietal Parietal occipital (frontal) Basal ganglia Parietal temporal (frontal) Paraventricular subcortical white matter, thalamus Frontal (parietal) Basal ganglia Temporal parietal (frontal) Basal ganglia Paraventricular subcortical white matter Frontal parietal (temporal) (Frontal) basal ganglia Parietal (basal ganglia) Frontal, parietal (basal, ganglia)
Neglect: +/– = presence/absence. Lesion: R = right, L = left. Aetiology: I = ischaemic, H = haemorrhagic. Site: brackets indicate a minimal involvement.
Vestibular stimulation and neglect syndrome
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with pyramidal signs in both groups. All RBD patients showed a severe neglect affecting both extrapersonal and personal spaces in all cases and imaginal space in most cases too. Neglect was assessed using a battery of 15 tasks, including a cancellation task (Albert, 1973), a line crossing task (Schenkenberg, Bradford and Ajax, 1980), a task of mental representation of a map (see Rode, Perenin and Boisson, 1995, for a detailed description of the different tasks). The patients were examined after a mean delay of 2 months 1/2 after stroke onset. All were severely impaired in at least half of the tasks. Procedure Assessment of the Motor Deficit Motor performance was assessed using a standard procedure with the patient lying on his bed, in dorsal or lateral decubitus position. The following movements were tested: (1) For the lower limb: flexion, extension, adduction and abduction at the hip joint; flexion and extension at the knee; flexion and extension at the ankle; flexion and extension of the toes; for the upper limb: shoulder raising, adduction and abduction, flexion and extension at the shoulder joint; flexion and extension at the elbow; flexion and extension at the wrist; finger flexion and extension; finger spreading; thumb flexion, extension, opposition and thumb-index grip. A score from the following scale (Held, Pierrot-Desseilligny, Bussel et al., 1975) was ascribed to each movement: score 0 = no movement; score 1 = palpable contraction; score 2 = movement not involving gravity; score 3 = movement against gravity; score 4 = movement against resistance; score 5 = normal movement. By adding scores obtained for each single movement, a ‘total motor score’ (maximum: 5 × 26 = 130 points) was then defined for each patient, as well as ‘arm’ and ‘leg scores’ (maximum 80 and 50 respectively). Normalized limb scores were also computed for each patient (raw limb score divided by maximal limb score). Assessment of Personal Neglect Personal neglect was evaluated following the procedure proposed by Bisiach et al. (1986a): the patient lies with his left upper limb positioned at the side of his trunk; the examiner, clearly pointing to the patient’s righ hand, orders: ‘with this hand, touch your other hand’. Score 0 = the patient promptly reaches for the target; score 1 = the target is reached with hesitation and searching; score 2 = the search is interrupted before the target is reached; score 3 = no movement towards the target is performed. Assessment of Anosognosia Anosognosia was assessed using the standard procedure proposed by Bisiach et al. (1986b), based on the patient’s report: score 0 = the deficit was spontaneously reported or mentioned by the patient following a general discussion about his complaints; score 1 = the disorder was reported only after a specific question was put about the strength of the patient’s left limbs; score 2 = the disorder was acknowledged only after its demonstration through routine techniques of neurological examination and score 3 = no acknowledgment of the disorder could be obtained from the patient. Vestibular Stimulation Vestibular stimulation was performed by using a cold caloric stimulation of the left ear in RBD patients and of the right ear in LBD patients. The external ear canal was irrigated for 30 sec with 60 cc of cold (20°) water. During stimulation the room lighting was turned down; the patient lay on his bed and his head was tilted approximately 30° forward. He was blindfolded. In normal subjects such a vestibular activation produces a horizontal nystagmus with a leftward slow phase lasting about 3 mn and a marked sensation of vertigo. An oculomotor response could be observed in all the patients. Subjective manifestations were reported by most of the LBD patients but, strikingly, none of the RBD experienced any effect of self-motion or vegetative sensation.
256
G. Rode and Others 60 50 total motor score
RBD 40 30 20 10
3
8
9
4
2
7
1
5
– X
6
cases
60
total motor score
50 40
LBD
30 20 10
3
8
9
4
2
7
1
5
6
– X
cases
Fig. 1 – Individual and mean total motor scores in the two groups of patients before (white bars) and after (black bars) vestibular stimulation. RBD: right brain-damaged patients with neglect; LBD: left brain-damaged patients without neglect.
RESULTS Motricity In the RBD group, the contralesional limb motricity improved markedly through vestibular stimulation. The mean of the total motor scores was raised from 8.2 (sd 10) before stimulation to 20 (sd 16.4) after stimulation. In contrast, the right limb motricity of the LBD patients remained virtually unchanged. The
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mean of the total motor scores in this group was 14.6 (sd 18.5) before stimulation and 15.5 (sd 18) after stimulation (Figure 1). A three-way ANOVA with one between- and two within-group factors was performed using normalized scores. Two main effects were found to be significant, ‘stimulation’ [F (1, 16) = 15.17, p < 0.0013] and ‘limb’ [F (1, 16) = 16.51, p < 0.0009], as well as the ‘group × stimulation’ interaction [F (1, 16) = 11.31, p < 0.0039]. Thus, vestibular stimulation only improves motor capacities in the RBD group. 40
RBD
leg score
arm score
30 20 10
10 20 30
3
8
9
4
2
7
1
5
– X
6
cases 40
LBD
leg score
arm score
30 20 10
10 20 30 10
11
12
13
14
15
16
17
18
– X
cases
Fig. 2 – Individual and mean arm and leg scores in the two groups of patients before (white bars) and after (black bars) vestibular stimulation. RBD and LBD: same as Figure 1.
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Moreover, although both the upper and lower limbs appeared affected (Figure 2a), improvement only reached significance in the lower limb, as shown by post hoc Scheffé comparison (p < 0.0024). Despite the significant overall effect of the stimulation on the RBD group, two patients (cases 5 and 6) from this group were not improved. In the other patients, the motor improvement consisted either in increased strength of movements or in recovery of movements which were completely absent before stimulation. These changes were observed on the lower limb in seven patients and on both limbs in five of them (Figure 2). They were more marked at proximal level: adduction and abduction of the leg, flexion and extension of the hip and knee recovered more often than ankle or toes flexion and extension. Similarly, adduction and abduction of the arm, flexion and extension of the elbow reappeared more often than wrist and fingers flexion and extension. The effects of the vestibular stimulation on motor performance were only transitory. Even movements that recovered best were no more improved after 15 to 20 mn. We were able to repeat the experimental procedure in 3 patients and a similar motor improvement could be obtained. Increase of motor scores was observed after a second stimulation in case 2, and after three and five stimulations in cases 3 and 9 respectively. In the control group, only one subject (case 17) showed an improvement of strength following vestibular stimulation, affecting the shoulder adduction and the knee extension (Figure 1 and 2 LBD). This subject was ambidextrous and had had initially a transient right unilateral neglect. At the time of the present investigation he only showed a right auditory extinction. In contrast with the motor improvement observed under vestibular stimulation in the RBD group, none of the patients showed any similar effect, when urged verbally to move their contralesional arm or leg. Personal Neglect Before vestibular stimulation, personal neglect was noted in all RBD patients, with a maximal score in 6 out of 9 cases (Table II). This disappeared completely in 8 patients after vestibular stimulation. In one case (4), personal neglect was TABLE II
Effects of Vestibular Stimulation on Motor, Personal Neglect and Anosognosia Scores of RBD Patients Patient
Delay post-onset
1 2 3 4 5 6 7 8 9
6 months 1 month 3 weeks 1 month 1 month 3 months 1 month 5 months 2 months
Motricity score
Personal neglect
Anosognosia
b.v.s.
a.v.s.
b.v.s.
a.v.s.
b.v.s.
a.v.s.
0 0 33 12 4 4 8 5 8
12 15 56 18 4 4 12 33 26
3 3 2 3 3 3 3 2 1
0 0 0 2 0 0 0 0 0
3 3 0 3 2 3 3 0 0
0 0 0 0 0 3 0 0 0
b.v.s. = before vestibular stimulation; a.v.s. = after vestibular stimulation.
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only slightly improved by the stimulation; the patient searched for her arm without reaching it (Bisiach’s score = 2). As illustrated in Table II motor recovery in our RBD sample (i.e. the difference between scores obtained after and before stimulation) was not correlated with the degree of personal neglect nor with the degree of personal neglect remission through vestibular stimulation (r = – 0.05 and 0.03 respectively, using normalized scores). Anosognosia All RBD patients had displayed anosognosia for hemiplegia at the acute stage. In 6 cases, anosognosia was severe (Bisiach’s score = 3 in most of them) associated with somatoparaphrenic delusions in 2 cases (1 and 2). Case 1 showed an exceptionally long-lasting anosognosia and somatoparaphrenia (for more details see Rode et al., 1992). Case 2 had a particular affective behavior with his left upper arm, which he caressed and talked to as it were a person. In 3 cases anosognosia was no longer present at the time of vestibular stimulation, i.e. 3 weeks, 2 and 5 months post-onset for cases 9, 3 and 8 respectively. Anosognosia disappeared completely following stimulation in 5 cases but remained unchanged in case 6 (Table II). As is the case of personal neglect motor recovery (as defined above) did not appear related to the degree of anosognosia nor to the degree of its remission after stimulation (r = – 0.4 and 0.3 respectively). DISCUSSION The main finding of the present study lies in the partial recovery of the motor deficit in neglect patients following vestibular stimulation, thus confirming our previous single-case report (Rode et al., 1992). Only 2 patients did not benefit from the stimulation, which may have been due to more extensive damage of their motor pathways. In the other 7 cases, a significant improvement was observed, consisting in both recovery of movements previously absent and increased strength in the lower and/or upper limbs. In contrast to the positive effects in the RBD group, the right hemiplegic deficit of the LBD control patients was not improved, with the exception of the sole ambidextrous patient (case 17), who had exhibited a transient right-sided neglect Our study also confirms, in a larger series of patients, previous findings (Cappa et al., 1987) on the remission of personal neglect and anosognosia through vestibular stimulation. The better recovery observed in the lower limb was unlikely related to the fact that this was tested first in all the patients. Due to the severity of hemiplegia this could be performed in less than 2 mn in all of them. Therefore the vestibular activation was still present at the time the upper limb motricity was tested, as evidenced by the marked remission of personal neglect and anosognosia which were assessed lastly. In fact, the pattern of motor recovery under vestibular stimulation appeared similar to spontaneous recovery of motor deficits from cortical origin, predominating at axial and proximal levels. The
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sensory manipulation would act by unmasking latent motor capacities. Our results can be compared to those reported by Vallar et al. (l993) on the remission of somatosensory deficits in patients with unilateral neglect. These authors proposed that an important non-sensory or ‘perceptual’ component could worsen a primary sensory deficit in this type of patient. We believe that, likewise, improvement of the motor deficit through vestibular stimulation in our neglect patients may be due to the remission of a ‘motor neglect component’, which was associated with and worsened the pyramidal deficit. The higher incidence of motor deficits in RHD compared to LHD patients has received a similar interpretation (Sterzi, Bottini, Celani et al., 1993). Whether this ‘motor neglect component’ has any relationship with the condition of ‘motor neglect’ described by Laplane and Degos (1983) is questionable. In our patients, the ‘motor neglect component’ was associated with other neglect symptoms. It was not improved by verbal command. In contrast, patients with ‘motor neglect’ fail to perform spontaneous movements, while showing nearly normal movements and strength when actively encouraged to use the affected limbs. Moreover, in the series of 21 patients reported by the authors, 12 had right-sided and 8 left-sided lesions. Finally, none of them showed any sign of associated sensory neglect. An additional discrepancy would be the unresponsiveness to vestibular stimulation that we observed in 2 patients with ‘motor neglect’ (unpublished data). In the present study, the existence of a ‘motor neglect component’ in neglect patients was revealed by the vestibular stimulation. The way this manipulation works is still a matter of debate. The fact that motor improvement was found in only one group of patients, despite similar motor deficits, makes any interpretation in terms of general hemispheric activation quite unlikely. Our results argue instead for a specific effect of the vestibular stimulation which transiently reduces the motor deficits of neglect patients as well as personal neglect and anosognosia in the same patients. Vestibular informations as well as proprioceptive and visual informations participate in the building and updating high-order egocentric representations, a process presumably disrupted in unilateral neglect (e.g. Karnath, Schenkel and Fischer, 1991; Vallar et al., 1993; Perenin, 1997). As already argued (Rode and Perenin, 1994), vestibular stimulation would activate undamaged parts of a distributed system underlying multisensory integration and conscious representation of space (corporeal and/or extracorporeal). The motor neglect component shown by our patients may be considered as one of the many manifestations of the unilateral neglect syndrome and similarly related to a disturbed awareness of one side of space. Acknowledgments. We would like to thank Mrs Roisin Vidal for her language assistance. REFERENCES ALBERT, M.L. A simple test of visual neglect. Neurology, 23: 658-664, 1973. BARBIERI, C., and DE RENZI, E. Patterns of neglect dissociation. Behavioral Neurology, 2: 13-24, 1989. BISIACH, E., PERANI, D., VALLAR, G., and BERTI, A. Unilateral neglect: personal and extra-personal. Neuropsychologia, 24: 759-767, 1986a.
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BISIACH, E., VALLAR, G., PERANI, D., PAPAGNO, C., and BERTI, A. Unawarenesss of disease following lesions of the right hemisphere: anosognosia for hemiplegia and anosognosia for hemianopia. Neuropsychologia, 24: 686-694, 1986b. BISIACH, E., RUSCONI, M.L., and VALLAR, G. Remission of somatoparaphrenic delusion through vestibular stimulation. Neuropsychologia, 29: 1029-1031, 1991. CAPPA, S., STERZI, R., VALLAR, G., and BISIACH, E. Remission of hemineglect and anosognosia during vestibular stimulation. Neuropsychologia, 25: 775-782, 1987. GUARIGLIA, G., PADOVANI, A., PANTANO, P., and PIZZAMIGLIO, L. Unilateral neglect restricted to visual imagery. Nature, 364: 235-237, 1993. HELD, J.P., PIERROT-DESSELLIGNY, E., BUSSEL, B., PERRIGOT, M., and MAHLER, M. Devenir des hémiplégies vasculaires par atteinte sylvienne en fonction du côté de la lésion. Annales de Médecine Physique, 18: 592-604, 1975. KARNATH, H.O., SCHENKEL, P., and FISCHER, B. Trunk orientation as the determining factor of the ‘contralateral’ deficit in the neglect syndrome and as the physical anchor of the internal representation of body orientation in space. Brain, 114: 1997-2014, 1991. LAPLANE, D., and DEGOS, J.D. Motor neglect. Journal of Neurology, Neurosurgery and Psychiatry, 46: 152-158, 1983. PERENIN, M.T. Optic ataxia and unilateral neglect: clinical evidence for dissociable spatial functions in posterior parietal cortex. In P. Thier and H.O. Karnath (Eds.), Parietal Lobe Contribution to Orientation in 3D Space. Heidelberg: Springer Verlag, 1997, pp. 289-308. RODE, G., CHARLES, N., PERENIN, M.T., VIGHETTO, A., TRILLET, M., and AIMARD, G. Partial remission of hemiplegia and somatoparaphrenia through vestibular stimulation in a case of unilateral neglect. Cortex, 28: 203-208, 1992. RODE, G., and PERENIN, M.T. Temporary remission of representational hemineglect through vestibular stimulation. Neuroreport, 5: 869-872, 1994. RODE, G., PERENIN, M.T., and BOISSON, D. Négligence de l’espace représenté: mise en évidence par l’évocation mentale de la carte de France. Revue Neurologique, 151: 161-164, 1995. RUBENS, A.B. Caloric stimulation and unilateral visual neglect. Neurology, 35: 1019-1024, 1985. SCHENKENBERG , T., BRADFORD, D.C., and AJAX, E.T. Line bisection with neurologic impairment. Neurology, 30: 509-517, 1980. STERZI, R., BOTTINI, G., CELANI, M.G., RIGHETTI, E., LAMASSA, S., RICCI, S., and VALLAR, F. Hemianopia, hemianesthesia, and hemiplegia after right and left hemispheric damage. A hemispheric difference. Journal of Neurology, Neurosurgery and Psychiatry, 56: 308-310, 1993. VALLAR, G., BOTTINI, G., RUSCONI, M.L., and STERZI, R. Exploring somatosensory hemineglect by vestibular stimulation. Brain, 116: 71-86, 1993. Marie-Thérèse Perenin, Vision et Motricité, INSERM Unité 94, 16 Avenue du Doyen Lépine, 69500 Bron, France.
(Received 26 February 1997; accepted 17 July 1997)
ABSTRACT The effect of vestibular stimulation on motor performance has been studied comparatively in 2 groups of hemiplegic patients, one including 9 right brain-damaged patients (RBD) with neglect, the other 9 left brain-damaged patients (LBD) without neglect. In the RBD group, a transient but significant improvement of motor performance was observed following stimulation, although motor scores remained unchanged in two cases. Moreover, a temporary remission of personal neglect and anosognosia was obtained in 8 out of 9 patients. In contrast to the RBD group, the motor performance of the LBD group was not improved through vestibular stimulation, although a moderate improvement of force was noticed in one ambidextrous patient who had shown transient signs of neglect at the acute stage. These results suggest the participation of a motor neglect component in the motor deficit of neglect patients. The motor neglect component may be considered as one of the many manifestations of the neglect syndrome and, as such, can be improved by the sensory manipulations which presumably restore a conscious representation of the left side of space. Key words: neglect, hemiplegia, anosognosia, vestibular stimulation
INTRODUCTION Most manifestations of unilateral neglect may be temporarily reduced by vestibular stimulation. Improvement not only concerns extrapersonal and personal neglect, but also neglect of imaginal space, anosognosia, somatoparaphrenic delusions and the somatosensory deficits often seen in association with the syndrome (Rubens, l985; Cappa, Sterzi, Vallar et al., 1987; Bisiach, Rusconi and Vallar, 1991; Rode, Charles, Perenin et al., 1992; Vallar, Bottini, Rusconi et al., 1993; Rode and Perenin, 1994). In a previous report on a single case of a long-lasting and severe neglect, we have shown that vestibular stimulation could also improve the hemiplegic deficit, as well as extrapersonal and personal neglect, anosognosia and somatoparaphrenia (Rode et al., 1992). While the patient did not move her left limbs spontaneously, she was able to flex and stretch her left leg following the stimulation, suggesting the participation of a motor neglect component in the motor deficit. Cortex, (1998) 34, 253-261
254
G. Rode and Others
The aim of the present study was to confirm this finding in a group of nine right brain-damaged (RBD) patients with neglect and, by comparison with a group of nine left brain-damaged (LBD) control patients, to further support the idea of a specific effect of the vestibular activation on neglect-related symptoms. Although they typically occur in association, neglect-related symptoms may also be seen separately. Various examples of dissociations have been observed (e.g. Bisiach, Perani, Vallar et al., 1986; Bisiach, Vallar, Perani et al., 1986; Barbieri and De Renzi, 1989, Guariglia, Padovani, Pantano et al., 1993). Laplane et Degos (1983) reported cases of ‘motor neglect’ described as an underutilization of the contralesional limbs in the absence of hemiplegia and visuospatial neglect. Differences and similarities between this isolated ‘motor neglect’ and the ‘motor neglect component’ we have investigated will be discussed. MATERIALS
AND
METHODS
Patients Nine right brain-damaged hemiplegic patients with unilateral neglect and nine left braindamaged hemiplegic patients without unilateral neglect participated in the study. Demographic features are described on Table I. Apart from one ambidextrous patient (case 17), all were right-handed. All the patients showed a rather extensive unilateral brain lesion, which was documented by CT-scan. Aethiology was always vascular, ischaemic in nine and haemorrhagic in the other nine cases. None of them suffered from impaired vigilance, confusion, mental deterioration or psychiatric disorders. Hemiplegia was always associated TABLE I
Demographic Features and CT Assessed Lesion Sites of the Two Groups of Patients Lesion Patient
Age/Sex
Neglect
Aetiology
Side
Site
1
69/F
+
I
R
2
63/M
+
H
R
3 4 5 6 7 8 9
52/F 61/F 71/F 63/M 68/F 67/M 69/F
+ + + + + + +
I H H H I I H
R R R R R R R
10 11 12 13 14
40/F 66/M 69/M 63/F 73/M
– – – – –
I H I I I
L L L L L
15 16 17 18
48/M 65/M 60/F 46/F
– – – –
I I I I
L L L L
Parietal temporal (occipital), basal ganglia Paraventricular subcortical white matter (parietal) basal ganglia Parietal (frontal) temporal Parietal Frontal temporal parietal Parietal occipital (frontal) Basal ganglia Parietal temporal (frontal) Paraventricular subcortical white matter, thalamus Frontal (parietal) Basal ganglia Temporal parietal (frontal) Basal ganglia Paraventricular subcortical white matter Frontal parietal (temporal) (Frontal) basal ganglia Parietal (basal ganglia) Frontal, parietal (basal, ganglia)
Neglect: +/– = presence/absence. Lesion: R = right, L = left. Aetiology: I = ischaemic, H = haemorrhagic. Site: brackets indicate a minimal involvement.
Vestibular stimulation and neglect syndrome
255
with pyramidal signs in both groups. All RBD patients showed a severe neglect affecting both extrapersonal and personal spaces in all cases and imaginal space in most cases too. Neglect was assessed using a battery of 15 tasks, including a cancellation task (Albert, 1973), a line crossing task (Schenkenberg, Bradford and Ajax, 1980), a task of mental representation of a map (see Rode, Perenin and Boisson, 1995, for a detailed description of the different tasks). The patients were examined after a mean delay of 2 months 1/2 after stroke onset. All were severely impaired in at least half of the tasks. Procedure Assessment of the Motor Deficit Motor performance was assessed using a standard procedure with the patient lying on his bed, in dorsal or lateral decubitus position. The following movements were tested: (1) For the lower limb: flexion, extension, adduction and abduction at the hip joint; flexion and extension at the knee; flexion and extension at the ankle; flexion and extension of the toes; for the upper limb: shoulder raising, adduction and abduction, flexion and extension at the shoulder joint; flexion and extension at the elbow; flexion and extension at the wrist; finger flexion and extension; finger spreading; thumb flexion, extension, opposition and thumb-index grip. A score from the following scale (Held, Pierrot-Desseilligny, Bussel et al., 1975) was ascribed to each movement: score 0 = no movement; score 1 = palpable contraction; score 2 = movement not involving gravity; score 3 = movement against gravity; score 4 = movement against resistance; score 5 = normal movement. By adding scores obtained for each single movement, a ‘total motor score’ (maximum: 5 × 26 = 130 points) was then defined for each patient, as well as ‘arm’ and ‘leg scores’ (maximum 80 and 50 respectively). Normalized limb scores were also computed for each patient (raw limb score divided by maximal limb score). Assessment of Personal Neglect Personal neglect was evaluated following the procedure proposed by Bisiach et al. (1986a): the patient lies with his left upper limb positioned at the side of his trunk; the examiner, clearly pointing to the patient’s righ hand, orders: ‘with this hand, touch your other hand’. Score 0 = the patient promptly reaches for the target; score 1 = the target is reached with hesitation and searching; score 2 = the search is interrupted before the target is reached; score 3 = no movement towards the target is performed. Assessment of Anosognosia Anosognosia was assessed using the standard procedure proposed by Bisiach et al. (1986b), based on the patient’s report: score 0 = the deficit was spontaneously reported or mentioned by the patient following a general discussion about his complaints; score 1 = the disorder was reported only after a specific question was put about the strength of the patient’s left limbs; score 2 = the disorder was acknowledged only after its demonstration through routine techniques of neurological examination and score 3 = no acknowledgment of the disorder could be obtained from the patient. Vestibular Stimulation Vestibular stimulation was performed by using a cold caloric stimulation of the left ear in RBD patients and of the right ear in LBD patients. The external ear canal was irrigated for 30 sec with 60 cc of cold (20°) water. During stimulation the room lighting was turned down; the patient lay on his bed and his head was tilted approximately 30° forward. He was blindfolded. In normal subjects such a vestibular activation produces a horizontal nystagmus with a leftward slow phase lasting about 3 mn and a marked sensation of vertigo. An oculomotor response could be observed in all the patients. Subjective manifestations were reported by most of the LBD patients but, strikingly, none of the RBD experienced any effect of self-motion or vegetative sensation.
256
G. Rode and Others 60 50 total motor score
RBD 40 30 20 10
3
8
9
4
2
7
1
5
– X
6
cases
60
total motor score
50 40
LBD
30 20 10
3
8
9
4
2
7
1
5
6
– X
cases
Fig. 1 – Individual and mean total motor scores in the two groups of patients before (white bars) and after (black bars) vestibular stimulation. RBD: right brain-damaged patients with neglect; LBD: left brain-damaged patients without neglect.
RESULTS Motricity In the RBD group, the contralesional limb motricity improved markedly through vestibular stimulation. The mean of the total motor scores was raised from 8.2 (sd 10) before stimulation to 20 (sd 16.4) after stimulation. In contrast, the right limb motricity of the LBD patients remained virtually unchanged. The
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mean of the total motor scores in this group was 14.6 (sd 18.5) before stimulation and 15.5 (sd 18) after stimulation (Figure 1). A three-way ANOVA with one between- and two within-group factors was performed using normalized scores. Two main effects were found to be significant, ‘stimulation’ [F (1, 16) = 15.17, p < 0.0013] and ‘limb’ [F (1, 16) = 16.51, p < 0.0009], as well as the ‘group × stimulation’ interaction [F (1, 16) = 11.31, p < 0.0039]. Thus, vestibular stimulation only improves motor capacities in the RBD group. 40
RBD
leg score
arm score
30 20 10
10 20 30
3
8
9
4
2
7
1
5
– X
6
cases 40
LBD
leg score
arm score
30 20 10
10 20 30 10
11
12
13
14
15
16
17
18
– X
cases
Fig. 2 – Individual and mean arm and leg scores in the two groups of patients before (white bars) and after (black bars) vestibular stimulation. RBD and LBD: same as Figure 1.
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Moreover, although both the upper and lower limbs appeared affected (Figure 2a), improvement only reached significance in the lower limb, as shown by post hoc Scheffé comparison (p < 0.0024). Despite the significant overall effect of the stimulation on the RBD group, two patients (cases 5 and 6) from this group were not improved. In the other patients, the motor improvement consisted either in increased strength of movements or in recovery of movements which were completely absent before stimulation. These changes were observed on the lower limb in seven patients and on both limbs in five of them (Figure 2). They were more marked at proximal level: adduction and abduction of the leg, flexion and extension of the hip and knee recovered more often than ankle or toes flexion and extension. Similarly, adduction and abduction of the arm, flexion and extension of the elbow reappeared more often than wrist and fingers flexion and extension. The effects of the vestibular stimulation on motor performance were only transitory. Even movements that recovered best were no more improved after 15 to 20 mn. We were able to repeat the experimental procedure in 3 patients and a similar motor improvement could be obtained. Increase of motor scores was observed after a second stimulation in case 2, and after three and five stimulations in cases 3 and 9 respectively. In the control group, only one subject (case 17) showed an improvement of strength following vestibular stimulation, affecting the shoulder adduction and the knee extension (Figure 1 and 2 LBD). This subject was ambidextrous and had had initially a transient right unilateral neglect. At the time of the present investigation he only showed a right auditory extinction. In contrast with the motor improvement observed under vestibular stimulation in the RBD group, none of the patients showed any similar effect, when urged verbally to move their contralesional arm or leg. Personal Neglect Before vestibular stimulation, personal neglect was noted in all RBD patients, with a maximal score in 6 out of 9 cases (Table II). This disappeared completely in 8 patients after vestibular stimulation. In one case (4), personal neglect was TABLE II
Effects of Vestibular Stimulation on Motor, Personal Neglect and Anosognosia Scores of RBD Patients Patient
Delay post-onset
1 2 3 4 5 6 7 8 9
6 months 1 month 3 weeks 1 month 1 month 3 months 1 month 5 months 2 months
Motricity score
Personal neglect
Anosognosia
b.v.s.
a.v.s.
b.v.s.
a.v.s.
b.v.s.
a.v.s.
0 0 33 12 4 4 8 5 8
12 15 56 18 4 4 12 33 26
3 3 2 3 3 3 3 2 1
0 0 0 2 0 0 0 0 0
3 3 0 3 2 3 3 0 0
0 0 0 0 0 3 0 0 0
b.v.s. = before vestibular stimulation; a.v.s. = after vestibular stimulation.
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only slightly improved by the stimulation; the patient searched for her arm without reaching it (Bisiach’s score = 2). As illustrated in Table II motor recovery in our RBD sample (i.e. the difference between scores obtained after and before stimulation) was not correlated with the degree of personal neglect nor with the degree of personal neglect remission through vestibular stimulation (r = – 0.05 and 0.03 respectively, using normalized scores). Anosognosia All RBD patients had displayed anosognosia for hemiplegia at the acute stage. In 6 cases, anosognosia was severe (Bisiach’s score = 3 in most of them) associated with somatoparaphrenic delusions in 2 cases (1 and 2). Case 1 showed an exceptionally long-lasting anosognosia and somatoparaphrenia (for more details see Rode et al., 1992). Case 2 had a particular affective behavior with his left upper arm, which he caressed and talked to as it were a person. In 3 cases anosognosia was no longer present at the time of vestibular stimulation, i.e. 3 weeks, 2 and 5 months post-onset for cases 9, 3 and 8 respectively. Anosognosia disappeared completely following stimulation in 5 cases but remained unchanged in case 6 (Table II). As is the case of personal neglect motor recovery (as defined above) did not appear related to the degree of anosognosia nor to the degree of its remission after stimulation (r = – 0.4 and 0.3 respectively). DISCUSSION The main finding of the present study lies in the partial recovery of the motor deficit in neglect patients following vestibular stimulation, thus confirming our previous single-case report (Rode et al., 1992). Only 2 patients did not benefit from the stimulation, which may have been due to more extensive damage of their motor pathways. In the other 7 cases, a significant improvement was observed, consisting in both recovery of movements previously absent and increased strength in the lower and/or upper limbs. In contrast to the positive effects in the RBD group, the right hemiplegic deficit of the LBD control patients was not improved, with the exception of the sole ambidextrous patient (case 17), who had exhibited a transient right-sided neglect Our study also confirms, in a larger series of patients, previous findings (Cappa et al., 1987) on the remission of personal neglect and anosognosia through vestibular stimulation. The better recovery observed in the lower limb was unlikely related to the fact that this was tested first in all the patients. Due to the severity of hemiplegia this could be performed in less than 2 mn in all of them. Therefore the vestibular activation was still present at the time the upper limb motricity was tested, as evidenced by the marked remission of personal neglect and anosognosia which were assessed lastly. In fact, the pattern of motor recovery under vestibular stimulation appeared similar to spontaneous recovery of motor deficits from cortical origin, predominating at axial and proximal levels. The
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sensory manipulation would act by unmasking latent motor capacities. Our results can be compared to those reported by Vallar et al. (l993) on the remission of somatosensory deficits in patients with unilateral neglect. These authors proposed that an important non-sensory or ‘perceptual’ component could worsen a primary sensory deficit in this type of patient. We believe that, likewise, improvement of the motor deficit through vestibular stimulation in our neglect patients may be due to the remission of a ‘motor neglect component’, which was associated with and worsened the pyramidal deficit. The higher incidence of motor deficits in RHD compared to LHD patients has received a similar interpretation (Sterzi, Bottini, Celani et al., 1993). Whether this ‘motor neglect component’ has any relationship with the condition of ‘motor neglect’ described by Laplane and Degos (1983) is questionable. In our patients, the ‘motor neglect component’ was associated with other neglect symptoms. It was not improved by verbal command. In contrast, patients with ‘motor neglect’ fail to perform spontaneous movements, while showing nearly normal movements and strength when actively encouraged to use the affected limbs. Moreover, in the series of 21 patients reported by the authors, 12 had right-sided and 8 left-sided lesions. Finally, none of them showed any sign of associated sensory neglect. An additional discrepancy would be the unresponsiveness to vestibular stimulation that we observed in 2 patients with ‘motor neglect’ (unpublished data). In the present study, the existence of a ‘motor neglect component’ in neglect patients was revealed by the vestibular stimulation. The way this manipulation works is still a matter of debate. The fact that motor improvement was found in only one group of patients, despite similar motor deficits, makes any interpretation in terms of general hemispheric activation quite unlikely. Our results argue instead for a specific effect of the vestibular stimulation which transiently reduces the motor deficits of neglect patients as well as personal neglect and anosognosia in the same patients. Vestibular informations as well as proprioceptive and visual informations participate in the building and updating high-order egocentric representations, a process presumably disrupted in unilateral neglect (e.g. Karnath, Schenkel and Fischer, 1991; Vallar et al., 1993; Perenin, 1997). As already argued (Rode and Perenin, 1994), vestibular stimulation would activate undamaged parts of a distributed system underlying multisensory integration and conscious representation of space (corporeal and/or extracorporeal). The motor neglect component shown by our patients may be considered as one of the many manifestations of the unilateral neglect syndrome and similarly related to a disturbed awareness of one side of space. Acknowledgments. We would like to thank Mrs Roisin Vidal for her language assistance. REFERENCES ALBERT, M.L. A simple test of visual neglect. Neurology, 23: 658-664, 1973. BARBIERI, C., and DE RENZI, E. Patterns of neglect dissociation. Behavioral Neurology, 2: 13-24, 1989. BISIACH, E., PERANI, D., VALLAR, G., and BERTI, A. Unilateral neglect: personal and extra-personal. Neuropsychologia, 24: 759-767, 1986a.
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(Received 26 February 1997; accepted 17 July 1997)