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Temporary Remission of Left Hemianesthesia after Vestibular Stimulation. A Sensory Neglect Phenomenon
TEMPORARY REMISSION OF LEFT HEMIANESTHESIA AFTER VESTIBULAR STIMULATION. A SENSORY NEGLECT PHENOMENON Giuseppe Vallar!, Roberto Sterzi2 , Gabriella Bottini!, Stefano Cappa3 and Maria Luisa Rusconil
eIstituto di Clinica Neurologica, Universita di Milano; 2Divisione di Neurologia, Ospedale di Niguarda, Milano; 3Clinica Neurologica, Universita di Brescia)
INTRODUCTION
The symptom-complex of unilateral spatial neglect may be temporarily alleviated by vestibular stimulation (Rubens, 1985; Cappa, Sterzi, Vallar and Bisiach, 1987). The range of positively affected deficits comprises extra-personal visual neglect, as assessed by exploratory tasks, personal neglect and anosognosia for hemiplegia. Neglect patients, in addition to these manifestations of the syndrome, frequently show associated neurological sensory deficits, such as hemianopia and hemianesthesia. In these patients the precise nature of such sensory disorders is, however, unclear. On the one hand, they might be traced back to primary somatosensory or visual co-occurring impairments. This hypothesis is not unlikely since the typical anatomical correlate of neglect is a retrorolandic lesion which, in addition to the crucial posterior-inferior parietal region, frequently involves adjacent cerebral areas, such as the primary somatosensory parietal cortex and the occipital lobe, and may also extend to subcortical regions participating in sensory processing, such as the thalamus and its cortical projections (see Vallar and Perani, 1986). On the other hand, the sensory deficits observed in these patients may be a manifestation of the neglect syndrome, which is usually interpreted in terms of a central cognitive impairment, attentional or representational in nature (see a review in Bisiach and Vallar, 1988). If this is the case, vestibular stimulation could affect not only disorders such as defective exploration of the left half-space, but also apparently «primary» sensory deficits. In this short note we report preliminary evidence from three right braindamaged patients, with a severe neglect syndrome, where vestibular stimulation induced a nearly complete, albeit temporary, remission of left hemianesthesia. MATERIALS AND METHODS
Subjects Three right-handed patients, who suffered a recent ischemic stroke in the right hemisphere were examined. All cases had no history or evidence of previous cerebrovascular attacks or dementia. Case 1 was a 79 year-old woman, case 2 a 47 year-old man, case 3 a 65 year-old man. All three patients had a complete left hemiplegia, hemianesthesia and homonymous hemianopia on a standard neurological examination (Bisiach, Cappa and ValCortex, (1990)26,123-131
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lar, 1983) and a severe conjugate gaze paresis, assessed according to the method of De Renzi, Colombo, Faglioni and Gibertoni (1982). All three patients showed a severe extrapersonal visual neglect on a circle crossing task (Bisiach, Luzzatti and Perani, 1979), failing to cross out not only all the circles in the left half of the sheet, but also some of the circles lying in the left half of the right hemi-sheet. In Case 1 a CT Scan performed in the same day of the stroke onset did not show any focal lesion; it was not possible to repeat the CT assessment since a few days later the patient was transferred to another hospital. In Case 2 a CT Scan performed 10 days after stroke onset revealed a right-sided hypodense lesion in the posterior limb of the internal capsule (see Figure 1), in the vascular territory of the anterior choroidal artery (see, e.g., Savoiardo, 1986). This lesion site may produce a neglect syndrome (Cambier et aI., 1983; Ferro and Kertesz, 1984). Damage of the posterior limb of the internal capsule interrupts a number of cortico-subcortical connections, including the main thalamic (pulvinar nucleus) input to the posterior-inferior parietal region. Damage of this cortical area is the typical neuroanatomical correlate of extrapersonal visual neglect in humans (Vallar and Perani, 1986). A lesion involving the posterior limb ofthe internal capsule may deprive the posterior parietal area of afferent input, producing therefore a functional derangement (diaschisis), which is closely related to the presence/absence of neglect (Perani et aI., 1987). Consistent with this view, a single photon emission computerised tomography (SPECT) study, performed 25 days after stroke onset, showed corticosubcortical hypoperfusion in the right posterior parietal regions (see Figure 2). In Case 3, five days after stroke onset a CT Scan showed a large hypodense lesion in the territory of the right middle cerebral artery (see Figure 3).
Tests Neuropsychological Assessment Extra-personal Neglect. Each patient was required to pick up with his/her right unaffected hand 13 plastic balls (2.5 cm diameter), located in front of him/her on a 50 x 36cm wooden board: one central item, six items in the left hand side of the board, six in the right hand side. The six left-sided and the six right-sided items were arranged in fixed non-symmetrical positions. The center of the board was located on the mid-sagittal plane of the patient's trunk. The patient was free to move his/her head and eyes and, before the task, his/her right Fig. 1 - Case 2: CT Scan showing a right-sided ischemic lesion in the vascular territory of the anterior choroidal artery.
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Fig. 2 - Case 2: SPECT showing hypoperjusion in the posterior parietal regions oj the right hemisphere (the image is inverted, according to neuroradiological conventions).
hand was placed in a baseline position, on the midsagittal plane of the trunk. The patient had received instructions to deliver to the examiner each ball he/she was picking up and to return to the baseline position before searching for another ball. The task ended when the patient stopped his/her search. No further prompting was given by the examiner. The task was given in two conditions, with and without visual control; in this latter case the patient was blind-folded. The two conditions were administered following an ABBA design: Set 1: (1) visual; (2) non-visual; (3) non-visual; (4) visual. Set 2: (1) non-visual; (2) visual; (3) visual; (4) non-visual. Fig. 3 - Case 3: CT Scan showing a massive hypodense cortico-subcorticallesion in the territory oj the right middle cerebral artery.
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After each block the board was rotated 180° anti-clockwise, in order to prevent interblock effects due to memory for the position of the balls. In the two conditions (with and without visual control) the scores were the number of balls gathered up by the patient in the left and in the right halves (max. 24 + 24) and in the center (max 4) of the board. Personal Neglect. The examiner asked the patient, who was lying on his/her back, with the arms extended along the sides ofthe trunk, to touch his/her left hand with the right. A fourpoint scale (Bisiach, Perani, Vallar and Berti, 1986) was used: 0 (target promptly reached); 1 (target reached with hesitation and search); 2 (search interrupted before the target is reached); 3 (no movement towards the target). Personal neglect was assessed with eyes shut. Anosognosia. Awareness of hemiplegia and hemianopia was rated by a four-point scale (Bisiach et aI., 1986): 0 (no defect); 1 (disorder spontaneously reported or mentioned after a general question about the patient's complaints); 2 (disorder acknowledged only after having been demonstrated through routine techniques of neurological examination); 3 (disorder not acknowledged). Somatosensory Deficits. Since the effects of vestibular stimulation are temporary, we confined the experimental assessment to the upper limbs, in order to obtain a number of data adequate for statistical analysis. We used the standard neurological assessment of Bisiach et al. (1983). The examiner, by touching as slightly and shortly as possible the dorsal surface of the patient's hand by his/her fingertips, gave a random sequence of 20 single stimuli, 10 to the left and 10 to the right hand. Before each stimulus the examiner warned the patient by saying "Now". In addition to the actual stimuli, each sequence included 4 catch trials, where the warning was not followed by a stimulus. Throughout the somatosensory assessment the patients were blind-folded.
Vestibular Stimulation Two types of stimulation were used. (1) Cold stimulation: the left external ear canal was irrigated with 20 cc of iced water for 1 min. (2) Warm stimulation: the right external ear canal was irrigated with 20 cc of warm (42°C) water for 1 min. The douching of the left ear with cold water and the douching of the right ear with warm water produce identical manifestations: a horizontal nystagmus (slow phase), and postural and kinetic deviations towards the left side (see De long, 1979, pp. 216-218, for further details). During stimulation the patients lay down in their bed and their head was tilted approximately 30° forward. All patients received cold stimulations, only Case 2 was given both. The time intervals between stroke onset and the beginning of the vestibular stimulation studies were three days (Case 1), 12 days (Case 2) and two days (Case 3). In all patients stimulation evoked a brisk nystagmus to the right. Irrigation seemed to produce discomfort in the patients, who were however unable to explain the nature of their unpleasant sensations and reported neither vertigo nor sense of displacement.
Procedure Extra-personal and personal neglect, and anosognosia were assessed before vestibular stimulation (baseline) and immediately after the treatment. The procedure was repeated twice. In the first stimulation session extra-personal (Set 1) and personal neglect and anosognosia were assessed; in the second only extra-personal neglect (Set 2). The time interval between two successive cold vestibular stimulations was at least 24 hours. The effects of vestibular stimulation upon somatosensory deficits were assessed presenting random sequences of single stimuli in a baseline condition before the stimulation, immediately after the stimulation and after a 30 min delay. The somatosensory effects of vestibular stimulation were investigated in days different from those in which the effects of the treatment upon neglect were assessed. The initial observation which prompted this study was made in Case 1. Case 2 and Case 3 were subsequently studied in more detail.
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Vestibular stimulation and sensory neglect RESULTS
Table I shows the mean percentages of balls picked up by each patient in the two sessions, before and immediately after vestibular stimulation. It is apparent that the treatment induces a temporary remission of extra-personal neglect, both with and without visual control, which is significant in Cases 1 and 2. Two patients (Cases 2 and 3) had severe anosognosia for both hemiplegia and hemianopia and personal neglect (score 3). In Case 2 anosognosia was unaffected by vestibular stimulation, which produced in Case 3 a temporary complete remission. Personal neglect was transiently abolished by the treatment in both cases. The effects of vestibular stimulation on the somatosensory deficits of the three cases are shown in Table II. Case 1 was fully accurate in the case of right-sided stimuli and did not make any error on the catch trials. Cold vestibular stimulation was administered twice, in different days: the treatment induced a temporary remission of hemianesthesia, with a significant difference between the baseline and the post-stimulation levels of accuracy (chF = 16.94; d.f. 1; p<0.001). Case 2 was investigated in more detail by administering a longer sequence of stimuli. An initial cold stimulation was followed, after a 60 min interval, by a warm stimulation session. The patient was very accurate in the case of right-sided stimuli (more than 980/0 correct) and did not make any error on the catch trials. It is apparent from Table II that hemianesthesia was dramatically reduced by both cold (chF = 71.60; d.f. 1; p<0.001) and warm (chF = 10.99; d.f. 1; p<0.001) vestibular stimulation. Cold stimulation had a fairly long-lasting effect: at the 30 min delay assessment the patient was still 80% correct in the first 10 trials. Therefore the sensory assessment was postponed to 30 min later: the level of performance was then comparable to the baseline. In Case 3 only a cold stimulaTABLE [
Effects of Vestibular Stimulation on Extra-personal Visual Neglect: Mean Percentage of Balls Picked up in the Two Sessions before and immediately after Vestibular Stimulation Visual condition Case Assessment Baseline Post-stimulation Difference
.54
.77
.23"
2
3
.25 .58 .33"·
.46 .58 .12
Non-visual condition Case Assessment Baseline Post-stimulation Difference Chi 2 statistics: "p
.44
.86 .42""
2
3
.38 .71 .33""
.65 .79 .14
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Effects of Vestibular Stimulation on Hemianesthesia: Number of Tactile Stimuli Delivered to the Left Hand Correctly Detected before, immediately after Vestibular Stimulation, and after a 30 [and 60 in Case 2 (l)] Min. Delay Assessment Baseline Post-stimulation Delay 30 min 60 min
Case 1 (I)
Case 1 (II)
Case 2 (I)
Case 2 (II) Case 3
6/10
10/10
43/50
1/50
3/50 16/50
40150
2110
1/10
8110
4/50
1120
2110
1/10
3/50
0120
Note. I and II: stimulation sessions. In all cases a left cold-water stimulation was used, with the exception of Case 2 (II), where a right warm-water stimulation was given.
tion test was given. The patient's performance was over 900/0 correct in the case of right-sided stimuli and he made no errors on catch trials. As in the first two cases hemianesthesia in the left hand was temporarily reduced by vestibular stimulation (chP = 37.33; d.f. 1; p < 0.001). In all three patients the severe motor deficit was unaffected by the vestibular stimulation. It is worth noting here that in Case 2 temporary recovery from hemianesthesia was much more complete with left cold-water than with right warm-water stimulation. The percentages of stimuli correctly detected after douching with cold and warm water were 86% and 32%, respectively. In Cases 1 and 3, where only left cold-water stimulations were used, comparable levels of post-stimulation accuracy were observed (Case 1: 60% and 100%; Case 2: 80%). Consistent with these findings Rubens (1985) observed a greater improvement of extrapersonal visual neglect after left cold-water stimulation. This greater effectiveness of the cold stimulus may be traced back to the differences between the body temperature (37°) and the temperatures of the cold (5°) and warm stimuli (42°). In the case of cold stimulation the gradient (32°) was much steeper that when warm water was used (5°).
DISCUSSION
The present findings provide clear evidence that in neglect patients tactile hemianesthesia may be temporarily relieved by vestibular stimulation, a treatment which also affects a number of components of the neglect syndrome, such as extra-personal and personal neglect, and anosognosia. A discussion of the possible (and at present fairly unclear) neural mechanisms whereby vestibular stimulation may ameliorate a number of symptoms of the neglect syndrome is beyond the scope of this short note and may be found in two recent studies which have systematically investigated this phenomenon (Rubens, 1985; Cappa et al., 1987). Here we wish to focus on some implications of these results concerning the nature of the neglect syndrome. (1) The observation that a treatment which produces a temporary alleviation
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of neglect also improves hemianesthesia suggests that this latter deficit may not simply reflect a primary sensory disorder. Tactile hemianesthesia, as other manifestations of the syndrome, should be attributed, at least in some cases, to a more central attentional deficit, which may be influenced by vestibular stimulation. It seems rather unlikely that vestibular stimulation might affect the severity of a primary sensory disorder, but this hypothesis will be specifically investigated by performing a group study on a larger series of right and left brain-damaged patients, with and without manifestations of the neglect syndrome. (2) The temporary remission of hemianesthesia and the improvement of extrapersonal neglect in the condition without visual control rule out the possibility that the effects of vestibular stimulation may be explained simply in terms of a facilitation of ocular movements towards the neglected side. (3) The observation of positive effects on a somatosensory deficit, in a condition where no movements in the extra-personal space were required or needed to be planned, suggests the existence of a sensory component in the manifold manifestations of the neglect syndrome, which cannot be easily accounted for by explanations in terms of a premotor deficit (see Rizzolatti and Camarda, 1987). Borrowing a terminology used in the amnesia literature, the somatosensory disorder of these patients may be described as a defective retrieval of information which has undergone some low-level (sensory) processing, but has not reached the level of conscious awareness required by the task, which, as simple as it is, requires an overt response. The possibility should then be entertained that in neglect patients like the present cases contralesional hemianesthesia represents an instance of defective access to conscious experience (see related data in Marshall and Halligan, 1988; see also Rizzolatti and Gallese, 1988). The present data do not speak directly to the issue of the putative distinction of input and output components in the neglect syndrome, since all three patients had both extra-personal neglect, as assessed by exploratory tasks, and hemianesthesia. It should however be noted that, while in the vast majority of neglect patients somatosensory disorders are also present, double-dissociated cases are on record (Hecaen, 1962; Bisiach et aI., 1986). The existence of patients with extrapersonal neglect without somatosensory disorders suggests a distinction between input attentional components involved in the processing of sensory stimuli delivered to the subject's body and components devoted to the processing of extrapersonal stimuli and the exploration of extrapersonal space. A role of high-level components in the processing of simple somatosensory stimuli and its disorders is also suggested by a number of recent findings in both patients and normal subjects. Two patients with chronic right parietal lesions studied by Tegner (1989), in addition to showing less steep psychophysical curves, failed to detect about 10070 of contralesional tactile stimuli independent of the stimulus strength, a finding which cannot be easily explained in terms of a primary sensory deficit. An intriguing observation by Weiskrantz and Zhang (1987) also indicates a central modulation of the somatosensory deficits produced by right brain-damage. Their patient, a woman with an extensive fronto-temporo-parietal infarct in the right hemisphere, had hemianesthesia in the case of stimuli applied by the experimenter to her left hand. Her level of detection accuracy increased substantially, however, when she touched the left hand with her unaffected right
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hand or with a probe held by that hand. Normal subjects have reduced latencies to unilateral cutaneous stimuli when they fixate a light-emitting diode aligned with the tactile stimulation point, as compared with conditions where the visual target is presented in another point of the same half-space, or in the contralateral half-space (Honore, Bourdeaud'Hui and Sparrow, 1989). These findings indicate that the orientation of attention in the visual space, through eye movements, may positively affect detection in a different sensory domain, suggesting the existence of non-modality-specific effects. The data of Honore et al. do not pertain to the issue of hemispheric asymmetries in the orienting of attention. This, however, is directly addressed by a study by Meador et al. (1988) who have used an experimental situation more comparable to the present study. They found in epileptic patients that a rightsided injection of intracarotid sodium amy tal (the Wada test) produces defective detection of left tactile single stimuli and, with double simultaneous tactile stimulation, extinction of the left stimulus: these contralateral effects are significantly less severe in the case of left-sided injections. This hemispheric asymmetry, like the present study, argues for an attentional component in the somatosensory deficits associated with right brain-damage.
ABSTRACT
In three right-brain damaged patients with contralesional neglect vestibular stimulation induced a temporary remission of left hemianesthesia, in addition to the well-known transient recovery of extrapersonal and personal neglect. These findings indicate that in neglect patients attentional factors may play an important role in producing apparently "primary" sensory deficits, which may be interpreted in terms of defective access to conscious processing.
Acknowledgements. This work was supported in part by a CNR grant. We should like to thank Dr. Milella (Divisione di Medicina Nucleare, Ospedale di Niguarda, Milano), who performed the SPECT assessment in Case 2.
REFERENCES
BISIACH, E., CAPPA, S.F., and VALLAR, G. Guida aWesame neuropsicologico. Milano: Raffaello Cortina Editore, 1983 BISIACH, E., PERANI, D., VALLAR, G., and BERTI, A., Unilateral neglect: personal and extrapersonal. Neuropsychologia, 24: 759-767, 1986. BISIACH, E., LUZZATTI, C., and PERANI, D. Unilateral neglect, representational schema and consciousness. Brain, 102: 609-618, 1979. BISIACH, E., and VALLAR, G. Hemineglect in humans. in F. Boller and J. Grafman (Eds.), Handbook oj Neuropsychology. Vol. 1. Amsterdam: Elsevier Science Publishers, B.V., 1988, pp.195-222. CAMBIER, J., GRAVELEAU, P., DECROIX, J.P., ELGHOZI, D., and MAssoN, M. Le syndrome de l'artere choroidienne anterieure. Etude neuropsychologique de 4 cas. Revue Neurologique, 139: 553-559, 1983. CAPPA, S.F., STERZI, R., VALLAR, G., and BISIACH, E. Remission of hemineglect and anosognosia during vestibular stimulation. Neuropsychologia, 25: 775-782, 1987. DE RENZI, E., COLOMBO, A., FAGLIONI, P., and GIBERTONI, M. Conjugate gaze paresis in stroke patients with unilateral damage. Archives oj Neurology, 39: 482-486, 1982.
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DE JONG. R.A. The Neurologic Examination. Fourth Edition. Philadelphia: Harper and Row, 1979. FERRO, J.M., and KERTESZ, A. Posterior internal capsule infarction associated with neglect. Archives of Neurology, 41: 422-424, 1984. HONORE, J., BOURDEAUD'HUI, M., and SPARROW, L. Reduction of cutaneous reaction time by directing eyes towards the source of stimulation. Neuropsychologia, 27: 367-371, 1989. HECAEN, H. Clinical symptomatology in right and left hemispheric lesions. In V.B. Mountcastle (Ed.), Interhemispheric Relations and Cerebral Dominance. Baltimore: The Johns Hopkins Press, 1962, pp. 215-243. MARsHALL,J.C., and HALLIGAN, P.W. B1indsight and insight in visuospatial neglect. Nature, 336: 766-767, 1988. MEADOR, K.J., LORING, D.W., LEE, G.P., BROOKS, B.S., THOMSON, E.E., THOMSON, W.O., and HEILMAN, K.M. Right cerebral specialization for tactile attention as evidenced by intracarotid sodium amytal. Neurology, 38: 1763-1766, 1988. PERANI, D., VALLAR, G., CAPPA, S.F., MESSA, C., and FAZIO, F. Aphasia and neglect after subcortical stroke. Brain, 110: 1211-1229, 1987. RIZZOLATTI, G., and CAMARDA, R. Neural circuits for spatial attention and unilateral neglect. In M. Jeannerod (Ed.), Neurophysiological and Neuropsychological Aspects of Spatial Neglect. Amsterdam: North Holland, 1987, pp. 289-313. RIZZOLATTI, G., and GALLESE, V. Mechanism and theories of spatial neglect. In F. Boller and J. Grafman (Eds.), Handbook of Neuropsychology, Vol. 1. Amsterdam: Elsevier Science Publishers, B.V., 1988, pp. 223-246. RUBENS, A.B. Caloric stimulation and unilateral visual neglect. Neurology, 35: 1019-1024, 1985. SAVOIARDO, M. The vascular territories of the carotid and vertebrobasilar system. Diagrams based on CT studies of infarcts. The Italian Journal of Neurological Science, 7: 405-409, 1986. TEGNER, R. Tactile sensibility in parietal lesions. Journal of Neurology, Neurosurgery and Psychiatry, 52: 669-670, 1989. VALLAR, G., and PERANI, D. The anatomy of unilateral neglect after right hemisphere stroke lesions. A clinical CT/Scan correlation study in man. Neuropsychologia, 24: 609-622, 1986. WEISKRANTZ, L., and ZHANG, D. Residual tactile sensitivity with self-directed stimulation in hemianaesthesia. Journal of Neurology, Neurosurgery and Psychiatry, 50: 632-634, 1987. Giuseppe Vallar, Istituto di Clinica Neurologica, via F. Sforza 35, 20122 Milano, italy.
eIstituto di Clinica Neurologica, Universita di Milano; 2Divisione di Neurologia, Ospedale di Niguarda, Milano; 3Clinica Neurologica, Universita di Brescia)
INTRODUCTION
The symptom-complex of unilateral spatial neglect may be temporarily alleviated by vestibular stimulation (Rubens, 1985; Cappa, Sterzi, Vallar and Bisiach, 1987). The range of positively affected deficits comprises extra-personal visual neglect, as assessed by exploratory tasks, personal neglect and anosognosia for hemiplegia. Neglect patients, in addition to these manifestations of the syndrome, frequently show associated neurological sensory deficits, such as hemianopia and hemianesthesia. In these patients the precise nature of such sensory disorders is, however, unclear. On the one hand, they might be traced back to primary somatosensory or visual co-occurring impairments. This hypothesis is not unlikely since the typical anatomical correlate of neglect is a retrorolandic lesion which, in addition to the crucial posterior-inferior parietal region, frequently involves adjacent cerebral areas, such as the primary somatosensory parietal cortex and the occipital lobe, and may also extend to subcortical regions participating in sensory processing, such as the thalamus and its cortical projections (see Vallar and Perani, 1986). On the other hand, the sensory deficits observed in these patients may be a manifestation of the neglect syndrome, which is usually interpreted in terms of a central cognitive impairment, attentional or representational in nature (see a review in Bisiach and Vallar, 1988). If this is the case, vestibular stimulation could affect not only disorders such as defective exploration of the left half-space, but also apparently «primary» sensory deficits. In this short note we report preliminary evidence from three right braindamaged patients, with a severe neglect syndrome, where vestibular stimulation induced a nearly complete, albeit temporary, remission of left hemianesthesia. MATERIALS AND METHODS
Subjects Three right-handed patients, who suffered a recent ischemic stroke in the right hemisphere were examined. All cases had no history or evidence of previous cerebrovascular attacks or dementia. Case 1 was a 79 year-old woman, case 2 a 47 year-old man, case 3 a 65 year-old man. All three patients had a complete left hemiplegia, hemianesthesia and homonymous hemianopia on a standard neurological examination (Bisiach, Cappa and ValCortex, (1990)26,123-131
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lar, 1983) and a severe conjugate gaze paresis, assessed according to the method of De Renzi, Colombo, Faglioni and Gibertoni (1982). All three patients showed a severe extrapersonal visual neglect on a circle crossing task (Bisiach, Luzzatti and Perani, 1979), failing to cross out not only all the circles in the left half of the sheet, but also some of the circles lying in the left half of the right hemi-sheet. In Case 1 a CT Scan performed in the same day of the stroke onset did not show any focal lesion; it was not possible to repeat the CT assessment since a few days later the patient was transferred to another hospital. In Case 2 a CT Scan performed 10 days after stroke onset revealed a right-sided hypodense lesion in the posterior limb of the internal capsule (see Figure 1), in the vascular territory of the anterior choroidal artery (see, e.g., Savoiardo, 1986). This lesion site may produce a neglect syndrome (Cambier et aI., 1983; Ferro and Kertesz, 1984). Damage of the posterior limb of the internal capsule interrupts a number of cortico-subcortical connections, including the main thalamic (pulvinar nucleus) input to the posterior-inferior parietal region. Damage of this cortical area is the typical neuroanatomical correlate of extrapersonal visual neglect in humans (Vallar and Perani, 1986). A lesion involving the posterior limb ofthe internal capsule may deprive the posterior parietal area of afferent input, producing therefore a functional derangement (diaschisis), which is closely related to the presence/absence of neglect (Perani et aI., 1987). Consistent with this view, a single photon emission computerised tomography (SPECT) study, performed 25 days after stroke onset, showed corticosubcortical hypoperfusion in the right posterior parietal regions (see Figure 2). In Case 3, five days after stroke onset a CT Scan showed a large hypodense lesion in the territory of the right middle cerebral artery (see Figure 3).
Tests Neuropsychological Assessment Extra-personal Neglect. Each patient was required to pick up with his/her right unaffected hand 13 plastic balls (2.5 cm diameter), located in front of him/her on a 50 x 36cm wooden board: one central item, six items in the left hand side of the board, six in the right hand side. The six left-sided and the six right-sided items were arranged in fixed non-symmetrical positions. The center of the board was located on the mid-sagittal plane of the patient's trunk. The patient was free to move his/her head and eyes and, before the task, his/her right Fig. 1 - Case 2: CT Scan showing a right-sided ischemic lesion in the vascular territory of the anterior choroidal artery.
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Fig. 2 - Case 2: SPECT showing hypoperjusion in the posterior parietal regions oj the right hemisphere (the image is inverted, according to neuroradiological conventions).
hand was placed in a baseline position, on the midsagittal plane of the trunk. The patient had received instructions to deliver to the examiner each ball he/she was picking up and to return to the baseline position before searching for another ball. The task ended when the patient stopped his/her search. No further prompting was given by the examiner. The task was given in two conditions, with and without visual control; in this latter case the patient was blind-folded. The two conditions were administered following an ABBA design: Set 1: (1) visual; (2) non-visual; (3) non-visual; (4) visual. Set 2: (1) non-visual; (2) visual; (3) visual; (4) non-visual. Fig. 3 - Case 3: CT Scan showing a massive hypodense cortico-subcorticallesion in the territory oj the right middle cerebral artery.
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After each block the board was rotated 180° anti-clockwise, in order to prevent interblock effects due to memory for the position of the balls. In the two conditions (with and without visual control) the scores were the number of balls gathered up by the patient in the left and in the right halves (max. 24 + 24) and in the center (max 4) of the board. Personal Neglect. The examiner asked the patient, who was lying on his/her back, with the arms extended along the sides ofthe trunk, to touch his/her left hand with the right. A fourpoint scale (Bisiach, Perani, Vallar and Berti, 1986) was used: 0 (target promptly reached); 1 (target reached with hesitation and search); 2 (search interrupted before the target is reached); 3 (no movement towards the target). Personal neglect was assessed with eyes shut. Anosognosia. Awareness of hemiplegia and hemianopia was rated by a four-point scale (Bisiach et aI., 1986): 0 (no defect); 1 (disorder spontaneously reported or mentioned after a general question about the patient's complaints); 2 (disorder acknowledged only after having been demonstrated through routine techniques of neurological examination); 3 (disorder not acknowledged). Somatosensory Deficits. Since the effects of vestibular stimulation are temporary, we confined the experimental assessment to the upper limbs, in order to obtain a number of data adequate for statistical analysis. We used the standard neurological assessment of Bisiach et al. (1983). The examiner, by touching as slightly and shortly as possible the dorsal surface of the patient's hand by his/her fingertips, gave a random sequence of 20 single stimuli, 10 to the left and 10 to the right hand. Before each stimulus the examiner warned the patient by saying "Now". In addition to the actual stimuli, each sequence included 4 catch trials, where the warning was not followed by a stimulus. Throughout the somatosensory assessment the patients were blind-folded.
Vestibular Stimulation Two types of stimulation were used. (1) Cold stimulation: the left external ear canal was irrigated with 20 cc of iced water for 1 min. (2) Warm stimulation: the right external ear canal was irrigated with 20 cc of warm (42°C) water for 1 min. The douching of the left ear with cold water and the douching of the right ear with warm water produce identical manifestations: a horizontal nystagmus (slow phase), and postural and kinetic deviations towards the left side (see De long, 1979, pp. 216-218, for further details). During stimulation the patients lay down in their bed and their head was tilted approximately 30° forward. All patients received cold stimulations, only Case 2 was given both. The time intervals between stroke onset and the beginning of the vestibular stimulation studies were three days (Case 1), 12 days (Case 2) and two days (Case 3). In all patients stimulation evoked a brisk nystagmus to the right. Irrigation seemed to produce discomfort in the patients, who were however unable to explain the nature of their unpleasant sensations and reported neither vertigo nor sense of displacement.
Procedure Extra-personal and personal neglect, and anosognosia were assessed before vestibular stimulation (baseline) and immediately after the treatment. The procedure was repeated twice. In the first stimulation session extra-personal (Set 1) and personal neglect and anosognosia were assessed; in the second only extra-personal neglect (Set 2). The time interval between two successive cold vestibular stimulations was at least 24 hours. The effects of vestibular stimulation upon somatosensory deficits were assessed presenting random sequences of single stimuli in a baseline condition before the stimulation, immediately after the stimulation and after a 30 min delay. The somatosensory effects of vestibular stimulation were investigated in days different from those in which the effects of the treatment upon neglect were assessed. The initial observation which prompted this study was made in Case 1. Case 2 and Case 3 were subsequently studied in more detail.
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Vestibular stimulation and sensory neglect RESULTS
Table I shows the mean percentages of balls picked up by each patient in the two sessions, before and immediately after vestibular stimulation. It is apparent that the treatment induces a temporary remission of extra-personal neglect, both with and without visual control, which is significant in Cases 1 and 2. Two patients (Cases 2 and 3) had severe anosognosia for both hemiplegia and hemianopia and personal neglect (score 3). In Case 2 anosognosia was unaffected by vestibular stimulation, which produced in Case 3 a temporary complete remission. Personal neglect was transiently abolished by the treatment in both cases. The effects of vestibular stimulation on the somatosensory deficits of the three cases are shown in Table II. Case 1 was fully accurate in the case of right-sided stimuli and did not make any error on the catch trials. Cold vestibular stimulation was administered twice, in different days: the treatment induced a temporary remission of hemianesthesia, with a significant difference between the baseline and the post-stimulation levels of accuracy (chF = 16.94; d.f. 1; p<0.001). Case 2 was investigated in more detail by administering a longer sequence of stimuli. An initial cold stimulation was followed, after a 60 min interval, by a warm stimulation session. The patient was very accurate in the case of right-sided stimuli (more than 980/0 correct) and did not make any error on the catch trials. It is apparent from Table II that hemianesthesia was dramatically reduced by both cold (chF = 71.60; d.f. 1; p<0.001) and warm (chF = 10.99; d.f. 1; p<0.001) vestibular stimulation. Cold stimulation had a fairly long-lasting effect: at the 30 min delay assessment the patient was still 80% correct in the first 10 trials. Therefore the sensory assessment was postponed to 30 min later: the level of performance was then comparable to the baseline. In Case 3 only a cold stimulaTABLE [
Effects of Vestibular Stimulation on Extra-personal Visual Neglect: Mean Percentage of Balls Picked up in the Two Sessions before and immediately after Vestibular Stimulation Visual condition Case Assessment Baseline Post-stimulation Difference
.54
.77
.23"
2
3
.25 .58 .33"·
.46 .58 .12
Non-visual condition Case Assessment Baseline Post-stimulation Difference Chi 2 statistics: "p
.44
.86 .42""
2
3
.38 .71 .33""
.65 .79 .14
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G. Vallar and Others TABLE II
Effects of Vestibular Stimulation on Hemianesthesia: Number of Tactile Stimuli Delivered to the Left Hand Correctly Detected before, immediately after Vestibular Stimulation, and after a 30 [and 60 in Case 2 (l)] Min. Delay Assessment Baseline Post-stimulation Delay 30 min 60 min
Case 1 (I)
Case 1 (II)
Case 2 (I)
Case 2 (II) Case 3
6/10
10/10
43/50
1/50
3/50 16/50
40150
2110
1/10
8110
4/50
1120
2110
1/10
3/50
0120
Note. I and II: stimulation sessions. In all cases a left cold-water stimulation was used, with the exception of Case 2 (II), where a right warm-water stimulation was given.
tion test was given. The patient's performance was over 900/0 correct in the case of right-sided stimuli and he made no errors on catch trials. As in the first two cases hemianesthesia in the left hand was temporarily reduced by vestibular stimulation (chP = 37.33; d.f. 1; p < 0.001). In all three patients the severe motor deficit was unaffected by the vestibular stimulation. It is worth noting here that in Case 2 temporary recovery from hemianesthesia was much more complete with left cold-water than with right warm-water stimulation. The percentages of stimuli correctly detected after douching with cold and warm water were 86% and 32%, respectively. In Cases 1 and 3, where only left cold-water stimulations were used, comparable levels of post-stimulation accuracy were observed (Case 1: 60% and 100%; Case 2: 80%). Consistent with these findings Rubens (1985) observed a greater improvement of extrapersonal visual neglect after left cold-water stimulation. This greater effectiveness of the cold stimulus may be traced back to the differences between the body temperature (37°) and the temperatures of the cold (5°) and warm stimuli (42°). In the case of cold stimulation the gradient (32°) was much steeper that when warm water was used (5°).
DISCUSSION
The present findings provide clear evidence that in neglect patients tactile hemianesthesia may be temporarily relieved by vestibular stimulation, a treatment which also affects a number of components of the neglect syndrome, such as extra-personal and personal neglect, and anosognosia. A discussion of the possible (and at present fairly unclear) neural mechanisms whereby vestibular stimulation may ameliorate a number of symptoms of the neglect syndrome is beyond the scope of this short note and may be found in two recent studies which have systematically investigated this phenomenon (Rubens, 1985; Cappa et al., 1987). Here we wish to focus on some implications of these results concerning the nature of the neglect syndrome. (1) The observation that a treatment which produces a temporary alleviation
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of neglect also improves hemianesthesia suggests that this latter deficit may not simply reflect a primary sensory disorder. Tactile hemianesthesia, as other manifestations of the syndrome, should be attributed, at least in some cases, to a more central attentional deficit, which may be influenced by vestibular stimulation. It seems rather unlikely that vestibular stimulation might affect the severity of a primary sensory disorder, but this hypothesis will be specifically investigated by performing a group study on a larger series of right and left brain-damaged patients, with and without manifestations of the neglect syndrome. (2) The temporary remission of hemianesthesia and the improvement of extrapersonal neglect in the condition without visual control rule out the possibility that the effects of vestibular stimulation may be explained simply in terms of a facilitation of ocular movements towards the neglected side. (3) The observation of positive effects on a somatosensory deficit, in a condition where no movements in the extra-personal space were required or needed to be planned, suggests the existence of a sensory component in the manifold manifestations of the neglect syndrome, which cannot be easily accounted for by explanations in terms of a premotor deficit (see Rizzolatti and Camarda, 1987). Borrowing a terminology used in the amnesia literature, the somatosensory disorder of these patients may be described as a defective retrieval of information which has undergone some low-level (sensory) processing, but has not reached the level of conscious awareness required by the task, which, as simple as it is, requires an overt response. The possibility should then be entertained that in neglect patients like the present cases contralesional hemianesthesia represents an instance of defective access to conscious experience (see related data in Marshall and Halligan, 1988; see also Rizzolatti and Gallese, 1988). The present data do not speak directly to the issue of the putative distinction of input and output components in the neglect syndrome, since all three patients had both extra-personal neglect, as assessed by exploratory tasks, and hemianesthesia. It should however be noted that, while in the vast majority of neglect patients somatosensory disorders are also present, double-dissociated cases are on record (Hecaen, 1962; Bisiach et aI., 1986). The existence of patients with extrapersonal neglect without somatosensory disorders suggests a distinction between input attentional components involved in the processing of sensory stimuli delivered to the subject's body and components devoted to the processing of extrapersonal stimuli and the exploration of extrapersonal space. A role of high-level components in the processing of simple somatosensory stimuli and its disorders is also suggested by a number of recent findings in both patients and normal subjects. Two patients with chronic right parietal lesions studied by Tegner (1989), in addition to showing less steep psychophysical curves, failed to detect about 10070 of contralesional tactile stimuli independent of the stimulus strength, a finding which cannot be easily explained in terms of a primary sensory deficit. An intriguing observation by Weiskrantz and Zhang (1987) also indicates a central modulation of the somatosensory deficits produced by right brain-damage. Their patient, a woman with an extensive fronto-temporo-parietal infarct in the right hemisphere, had hemianesthesia in the case of stimuli applied by the experimenter to her left hand. Her level of detection accuracy increased substantially, however, when she touched the left hand with her unaffected right
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G. Vallar and Others
hand or with a probe held by that hand. Normal subjects have reduced latencies to unilateral cutaneous stimuli when they fixate a light-emitting diode aligned with the tactile stimulation point, as compared with conditions where the visual target is presented in another point of the same half-space, or in the contralateral half-space (Honore, Bourdeaud'Hui and Sparrow, 1989). These findings indicate that the orientation of attention in the visual space, through eye movements, may positively affect detection in a different sensory domain, suggesting the existence of non-modality-specific effects. The data of Honore et al. do not pertain to the issue of hemispheric asymmetries in the orienting of attention. This, however, is directly addressed by a study by Meador et al. (1988) who have used an experimental situation more comparable to the present study. They found in epileptic patients that a rightsided injection of intracarotid sodium amy tal (the Wada test) produces defective detection of left tactile single stimuli and, with double simultaneous tactile stimulation, extinction of the left stimulus: these contralateral effects are significantly less severe in the case of left-sided injections. This hemispheric asymmetry, like the present study, argues for an attentional component in the somatosensory deficits associated with right brain-damage.
ABSTRACT
In three right-brain damaged patients with contralesional neglect vestibular stimulation induced a temporary remission of left hemianesthesia, in addition to the well-known transient recovery of extrapersonal and personal neglect. These findings indicate that in neglect patients attentional factors may play an important role in producing apparently "primary" sensory deficits, which may be interpreted in terms of defective access to conscious processing.
Acknowledgements. This work was supported in part by a CNR grant. We should like to thank Dr. Milella (Divisione di Medicina Nucleare, Ospedale di Niguarda, Milano), who performed the SPECT assessment in Case 2.
REFERENCES
BISIACH, E., CAPPA, S.F., and VALLAR, G. Guida aWesame neuropsicologico. Milano: Raffaello Cortina Editore, 1983 BISIACH, E., PERANI, D., VALLAR, G., and BERTI, A., Unilateral neglect: personal and extrapersonal. Neuropsychologia, 24: 759-767, 1986. BISIACH, E., LUZZATTI, C., and PERANI, D. Unilateral neglect, representational schema and consciousness. Brain, 102: 609-618, 1979. BISIACH, E., and VALLAR, G. Hemineglect in humans. in F. Boller and J. Grafman (Eds.), Handbook oj Neuropsychology. Vol. 1. Amsterdam: Elsevier Science Publishers, B.V., 1988, pp.195-222. CAMBIER, J., GRAVELEAU, P., DECROIX, J.P., ELGHOZI, D., and MAssoN, M. Le syndrome de l'artere choroidienne anterieure. Etude neuropsychologique de 4 cas. Revue Neurologique, 139: 553-559, 1983. CAPPA, S.F., STERZI, R., VALLAR, G., and BISIACH, E. Remission of hemineglect and anosognosia during vestibular stimulation. Neuropsychologia, 25: 775-782, 1987. DE RENZI, E., COLOMBO, A., FAGLIONI, P., and GIBERTONI, M. Conjugate gaze paresis in stroke patients with unilateral damage. Archives oj Neurology, 39: 482-486, 1982.
Vestibular stimulation and sensory neglect
131
DE JONG. R.A. The Neurologic Examination. Fourth Edition. Philadelphia: Harper and Row, 1979. FERRO, J.M., and KERTESZ, A. Posterior internal capsule infarction associated with neglect. Archives of Neurology, 41: 422-424, 1984. HONORE, J., BOURDEAUD'HUI, M., and SPARROW, L. Reduction of cutaneous reaction time by directing eyes towards the source of stimulation. Neuropsychologia, 27: 367-371, 1989. HECAEN, H. Clinical symptomatology in right and left hemispheric lesions. In V.B. Mountcastle (Ed.), Interhemispheric Relations and Cerebral Dominance. Baltimore: The Johns Hopkins Press, 1962, pp. 215-243. MARsHALL,J.C., and HALLIGAN, P.W. B1indsight and insight in visuospatial neglect. Nature, 336: 766-767, 1988. MEADOR, K.J., LORING, D.W., LEE, G.P., BROOKS, B.S., THOMSON, E.E., THOMSON, W.O., and HEILMAN, K.M. Right cerebral specialization for tactile attention as evidenced by intracarotid sodium amytal. Neurology, 38: 1763-1766, 1988. PERANI, D., VALLAR, G., CAPPA, S.F., MESSA, C., and FAZIO, F. Aphasia and neglect after subcortical stroke. Brain, 110: 1211-1229, 1987. RIZZOLATTI, G., and CAMARDA, R. Neural circuits for spatial attention and unilateral neglect. In M. Jeannerod (Ed.), Neurophysiological and Neuropsychological Aspects of Spatial Neglect. Amsterdam: North Holland, 1987, pp. 289-313. RIZZOLATTI, G., and GALLESE, V. Mechanism and theories of spatial neglect. In F. Boller and J. Grafman (Eds.), Handbook of Neuropsychology, Vol. 1. Amsterdam: Elsevier Science Publishers, B.V., 1988, pp. 223-246. RUBENS, A.B. Caloric stimulation and unilateral visual neglect. Neurology, 35: 1019-1024, 1985. SAVOIARDO, M. The vascular territories of the carotid and vertebrobasilar system. Diagrams based on CT studies of infarcts. The Italian Journal of Neurological Science, 7: 405-409, 1986. TEGNER, R. Tactile sensibility in parietal lesions. Journal of Neurology, Neurosurgery and Psychiatry, 52: 669-670, 1989. VALLAR, G., and PERANI, D. The anatomy of unilateral neglect after right hemisphere stroke lesions. A clinical CT/Scan correlation study in man. Neuropsychologia, 24: 609-622, 1986. WEISKRANTZ, L., and ZHANG, D. Residual tactile sensitivity with self-directed stimulation in hemianaesthesia. Journal of Neurology, Neurosurgery and Psychiatry, 50: 632-634, 1987. Giuseppe Vallar, Istituto di Clinica Neurologica, via F. Sforza 35, 20122 Milano, italy.