Neuropsychologia 39 (2001) 1250– 1254 www.elsevier.com/locate/neuropsychologia
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Prism adaptation improves representational neglect Gilles Rode a,b,c,*, Yves Rossetti a,b,c, Dominique Boisson a,b,c a
Ser6ice de Re´e´ducation Neurologique, Hoˆpital Henry Gabrielle, Hospices Ci6ils de Lyon and Uni6ersite´ Claude Bernard, Lyon Cedex, France b Espace et Action, Institut National de la Sante´ et de la Recherche Me´dicale, Unite´ 534, 16 A6enue Le´pine, Case 13, 69676 Bron, France c Institut Fe´de´ratif des Neurosciences Lyon, Hoˆpital Neuro-cardiologique, 59 Boule6ard Pinel, 69394 Lyon Cedex 03, France Received 25 November 1998; received in revised form 22 February 2001; accepted 15 March 2001
Abstract Previous work has shown that various symptoms of unilateral neglect, including the pathological shift of the subjective midline to the right, may be improved by a short adaptation period to a prismatic shift of the visual field to the right. We report here, in two neglect patients the improvement of imagery neglect after prism exposure. Despite a strong neglect observed for mental images, as well as for conventional tests, the mental evocation of left-sided information from an internal image of the map of France was fully recovered following prism adaptation to the right. This improvement could not be explained by the alteration of visuomotor responses induced by the prism adaptation. Therefore, prism adaptation may act not only on sensory– motor levels but also on a higher cognitive level of mental space representation and/or exploration. © 2001 Elsevier Science Ltd. All rights reserved. Keywords: Unilateral neglect; Mental representation; Prism adaptation; Cognitive neuropsychology
1. Introduction Using a short adaptation period to a prismatic shift of the visual field to the right, Rossetti et al. [7] recently reported an improvement of various symptoms of hemispatial neglect in a group of right-brain damaged neglect patients. A reduction of the subjective body midline shift toward the ipsilesional side, shown by these patients, was also noted following the prism adaptation. These findings suggested that the effect of prism adaptation may be thought to stimulate active processes involved in brain plasticity related to multisensory integration and space representation. However, the tasks used in this experiment involved a visuomanual response (e.g., line canceling, drawing), that is a system involved in the adaptation procedure. * Corresponding author. Present address: Service de Re´e´ducation Neurologique, Hoˆpital Henry Gabrielle, Hospices Civils de Lyon, Route de Vourles, BP 57, F-69565 Saint-Genis Laval, France. Tel.: +33-4-78865024; fax: +33-4-78865030. E-mail address:
[email protected] (G. Rode).
An interesting question is whether the improvement observed after prism adaptation would also affect aspects of hemispatial neglect which are free from manual responses. In two patients, we thus tested the effects of prism adaptation on neglect at three different levels: a sensory –motor level using a simple manual pointing task, an intermediate level via the free drawing of a daisy from memory and a cognitive level using a mental imagery task.
2. Methods
2.1. Subjects Four right-handed subjects participated in this study. Two patients (a female MCC aged 62 and a male JCG aged 46) who showed a left-unilateral neglect following a damage of the right hemisphere and two control subjects (two males aged 56 and 67, respectively). The two patients had been admitted to a neurological reha-
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G. Rode et al. / Neuropsychologia 39 (2001) 1250–1254
bilitation unit for treatment of left hemiplegia. Clinical features and CT-scan data are described in Table 1. At the time of examination, 1-month post-onset, patients were quite alert, well oriented in time and co-operative. They were not anosognosic for the motor deficit.
2.2. Procedure For JCG and MCC, the effectiveness of prism adaptation was tested on neglect at three different levels.
2.2.1. Simple manual pointing task The patient was seated blindfolded in front of a horizontal box that permitted measurement of the finger movement endpoints with an accuracy of 1°. He was required to point straight-ahead while his head was kept aligned with the body’s sagittal axis. Ten pointing trials were performed in the pre-test (without prisms) and in the post-test (immediately upon the prism removal), in order to check that prism adaptation had been efficient. The cover of the experimental box allowed the patient to perform free pointing movements either without vision of the arm, or with a partial sight of the arm trajectory (exposure condition). 2.2.2. Free drawing The patient was asked to draw a daisy from memory. The drawing was repeated in three sessions: prior to prism exposure (pre-test), on prism removal (post-test) and 24 h later (late-test). 2.2.3. Mental imagery Subjects were asked to mentally evoke the map of France and to name as many towns as possible on the map that they could ‘see’ within 2 min (see details in Ref. [4]). The patient was tested before adaptation (pre-test), immediately after (post-test) and 24 h after (late-test) prism exposition.
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Performance was rated by a global score corresponding to the total number of towns named within 2 min (total score). In addition, two scores were computed according to the geographical position of each named town, either on the right of the map central axis (Perpignan-Lille; right score), or on the left of this axis (left score). Results were analyzed by a comparison of the right and left scores with a 2 analysis. For the control subjects, only the mental imagery task was performed before and after adaptation.
2.3. Prism adaptation Subjects were exposed to a shift of the visual field to the right produced by prismatic lenses. The goggles were fitted with wide-field, wedge lenses creating an optical shift of 10°. The exposure period consisted in 50 pointing responses to visual targets presented 10° to the right or to the left of the objective body midline. During the prism exposure, subjects were asked to point at a fast but comfortable speed; they could see the target, the second half of their pointing trajectory and their terminal error. Their head was kept aligned with the body’s sagittal axis by a chin-rest and controlled by an investigator. The total duration of this exposure was about 3 min. This experimental procedure was applied 1 month post-onset of their stroke.
3. Results
3.1. Pointing to straight-ahead In the pre-test, in patients, the straight-ahead was initially shifted from the midline in either direction (respectively, mean: − 5°; standard error of the mean
Table 1 Clinical features and CT-scan dataa
Left hemiparesis Left hemianesthesia Left hemianopia Head and gaze deviation Extrapersonal neglect Personal neglect Neglect of imagined space Constructive apraxia Etiology Site lesion
a
JCG
MCC
Severe Severe Present Present Present Present Present Present Ischemic Parietal, temporal, frontal periventricular white matter
Moderate Moderate Present Present Present Absent Present Present Ischemic Temporal, occipital periventricular white matter thalamus
Extrapersonal neglect was assessed by a line cancellation test, a line bisection test, drawings from memory and in copying, reading and writing. Personal neglect was evaluated by clinical examination. Neglect of imagined space was assessed, asking the patient to evoke mentally a street or a place of his town. Constructive apraxia was evidenced from drawing of 3D-objects.
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G. Rode et al. / Neuropsychologia 39 (2001) 1250–1254 Table 2 Left, right and total scores of towns evoked by JCG and MCC from mental evocation of the map of France, within 2 min, prior to prism exposure (pre-test), immediately after prism adaptation (post-test) and after a delay of about 24 h following prism exposure (late-test)
Fig. 1. Effect of prism adaptation on free drawing of object (daisy) in two neglect patients (JCG and MCC) prior to prism exposure (pretest), immediately after prism adaptation (post-test), and after a delay of about 24 h following prism exposure (late-test).
(SEM): 1.26 for JCG and mean: +5.4°; SEM: 1.2 for MCC). In the post-test, patients demonstrated a larger straight-ahead shift to the left (mean: −14°; SEM: 0.52 for JCG and mean: 0.4°; SEM: 0.6 for MCC). Comparison by t-test of mean deviation observed before and following the adaptation revealed a highly significant difference (t(9)= 7.73; P B0.0001 for JCG and (t(10)= 11; PB 0.0001 for MCC) indicating that the two patients could adapt to a lateral shift of the visual field to the right.
3.2. Free drawing of object In the pre-test, both JCG and MCC neglected the left half of a daisy drawn from memory. In the post-test, patients draw an entire daisy with a surprising larger left half than the right in JCG and in the late-test, an incomplete daisy with a smaller left half than the right (Fig. 1).
3.3. Mental imagery task For the two control subjects, the mean total score of named towns given prior to prism exposure (pre-test) was 47.5 (respectively, 22.5 for the right and 25 for the left). In the post-test, the value was 44.5 (respectively, 23 for the right and 21.5 for the left). Moreover, the comparison of the difference between the right and left scores showed no difference prior to prism exposure ( − 2.5) and after (1.5). For the two control subjects, the mental evocation of the map of France thus was not modified by the prism adaptation. For JCG and MCC, immediately after prism adaptation, the total number of towns named by the two patients within 2 min was increased, suggesting that the prism adaptation facilitated the mental evocation of the map (Table 2). This increase concerned mainly the evocation of towns located on the left half of map,
Left scores
Right scores
Total score
Patient JCG Pre-test Post-test Late-test
3 22 6
18 17 28
21 39 34
Patient MCC Pre-test Post-test Late-test
3 10 4
13 14 19
16 24 23
suggesting a regression of left-representational neglect (Tables 3 and 4). After a delay of about 24 h following the prism exposure, the previous modifications of mental evocation had disappeared and the patients again showed a left neglect of representational space, comparable with performance prior to adaptation (Fig. 2). 4. Discussion Before prism exposure, both patients showed a leftvisual hemineglect on free drawing of daisy and a left neglect of imagined space on a task requiring the patients to report from an imagined representation of the map of France. In two patients the same side of space (left) was affected by representational and visuospatial neglect. But the shift of the subjective midline was in the opposite direction in JCG and the same in MCC, further supporting that this particular manifestation can be dissociated from other symptoms of neglect [4]. The neglect of imaginal space shown by JCG and MCC in the mental evocation of the map of France is similar to that reported previously in 14 neglect patients [6]. It suggests a distorted representation of the geographic map [1,2]. Table 3 Statistical dataa 2 test
JCG
MCC
Both
Pre–post–late
15.63 (PB0.001) 11.83 (PB0.01) 0.11 (P\0.5)
4.25 (P =0.11)
20.29 (P =0.0001) 11.83 (P= 0.001) 0.02 (P= 0.87)
Pre–post Pre–late
2.3 (P= 0.13) 0.01 (P\0.5)
a For JCG, a 2 test performed on the left–right scores obtained showed a significant effect in the three sessions, a significant difference between the pre- and the post-tests but no difference between the pre- and the late-tests. For MCC, the differences observed are close to significance. For both patients, 2 test revealed an increase of significance.
G. Rode et al. / Neuropsychologia 39 (2001) 1250–1254 Table 4 Left, right and total scores of town evoked by the two control subjects from mental evocation of the map of France.
Controls a Pre-test Post-test
Left scores
Right scores
Total score
25 21.5
22.5 23
47.5 44.5
a
For the two control subjects, the comparison of the difference between the right and left scores showed no difference prior to prism exposure (−2.5) and after (1.5). For the two control subjects, the mental evocation of the map of France thus was not modified by the prism adaptation.
In two patients, immediately after prism adaptation, modifications of the mental evocation were evidenced: (i) the total number of towns named by the two patients within 2 min was increased, suggesting that the prism adaptation facilitated the mental evocation of the map; (ii) this increase concerned mainly the evocation of towns located on the left half of map, suggesting a reduction of left-representational neglect; and (iii) no town is evoked on the east-most part of map, in JCG, suggesting a significant shift of mental evocation toward the left side of the image and a paradoxical ‘neglect’ of the right side.
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Morever, following adaptation, both patients showed improved drawing with reduced asymmetry of the daisy. This improvement was also paralleled by the significant increase of the straight-ahead shift toward the left side, which again suggests that these two symptoms can be dissociated. The reversal effect observed after prism adaptation strongly supports the idea that the effect of this manipulation on neglect is attributable to a specific directional mechanism, and not just to a general improvement of cognitive functions. After a delay of about 24 h, following the prism exposure, the previous modifications of mental evocation had disappeared and the patients again showed left neglect of imaginal space, comparable with performance prior to adaptation. However, the total number of towns named remained larger than before prism exposure, probably reflecting learning of the mental task. On the other hand, the improvement in daisy drawing was partially maintained. This difference may be explained by the involvement of a manual response in drawing task. In this case, a novel effect of prism adaptation is reported in a task of mental imagery. In this task, the subject had to generate an inner image of a map from long-term memory and explore it. It should be noticed
Fig. 2. Maps of France described from mental evocation in three conditions: prior to prism exposure (pre-test), immediately after prism adaptation (post-test) and after a delay of about 24 h following prism exposure (late-test) in two neglect patients (JCG and MCC). The filled circles indicate the geographical loci of the different responses and the bold number indicates the total number of responses.
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that this level of space representation clearly differs from the sensory–motor level, directly stimulated by prism adaptation. The reduction of imaginal neglect shown by JCG and MCC after the prism adaptation suggests that the stimulation of active processes involved in the plasticity of sensory– motor correspondences can also influence cognitive processes at the level of mental representation. This result further supports the idea [7] that the process of prism adaptation may activate brain functions related to multisensory integration and higher spatial representations. The recent observations of neglect-like behavior in line bisection test in normals following a short (rTMS) repetitive magnetic stimulation of the parietal cortex [5] and prism adaptation to a leftward visual shift [3] suggest that prism adaptation is likely to alter the function of the parietal cortex.
Acknowledgements This work was supported by the Re´ gion Rhoˆ neAlpes, by the Hospices Civils de Lyon (PHRC no.
95.035). We thank J. Danckert for his comment on the manuscript and J.L. Borach for his technical help. References [1] Bisiach E, Luzzatti C. Unilateral neglect of representational space. Cortex 1978;14:129 – 33. [2] Bisiach E, Berti A. Dyschiria. An attempt at its systemic explanation. In: Jeannerod M, editor. Neurophysiological and neuropsychological aspects of spatial neglect. Amsterdam: North Holland, 1987:183 – 201. [3] Colent C, Pisella L, Bernieri C, Rode G, Rossetti Y. Cognitive bias induced by visuo-motor adaptation to prisms: a simulation of unilateral neglect in normal individuals? Neuroreport 2000;9:1899 – 902. [4] Farne´ A, Ponti F, Ladavas E. In search of biased egocentric reference frames in neglect. Neuropsychologia 1998;36:611 –23. [5] Fierro B, Brighina F, Olivieri M, Piazza A, La Bua V, Buffa D, et al. Contralateral neglect induced by right posterior parietal rTMS in healthy subjects. Neuroreport 2000;11:1519 – 21. [6] Rode G, Perenin MT. Temporary remission of representational hemineglect through vestibular stimulation. Neuroreport 1994;5:869 – 72. [7] Rossetti Y, Rode G, Pisella L, Farne´ A, Li L, Boisson D, et al. Prism adaptation to a rightward optical deviation rehabilitates left hemispatial neglect. Nature 1998;395:166 – 9.
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