Prism adaptation improves spatial dysgraphia following right brain damage

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Neuropsychologia 44 (2006) 2487–2493 Prism adaptation improves spatial dysgraphia following right brain damage G. Rode a,b,c,d,, L. Pisella b,d , L. Marsal a , S. Mercier a , Y. Rossetti a,b,c,d , D. Boisson a,b,c,d a Service de R´ education Neurologique, Hospices Civils de Lyon, Hˆ opital Henry Gabrielle, 20 Route de Vourles, 69230 St. Genis Laval, France b Espace et Action, UMR-S 534, Institut National de la Sant´ e Et de la Recherche M´ edicale, and Universit´ e Claude Bernard, 16 Avenue L´ epine, Case 13, 69676 Bron, France c ‘Mouvement et Handicap’, IFNL et Hospices Civils de Lyon, France d IFR 19, Institut F´ ed´ eratif des Neurosciences de Lyon, Hˆ opital Neurologique, Bˆ at B13, 59 Bd Pinel, 69394 Lyon Cedex, France Received 7 September 2005; received in revised form 27 March 2006; accepted 2 April 2006 Available online 18 May 2006 Abstract Visuo-manual adaptation to prisms produces a long-lasting improvement of visuo-spatial neglect. Improvement is also observed in tasks that do not involve visuo-manual component and that can all be consider to rely on a rightward (ipsilesional) orienting bias. Here, we report positive effects of prism adaptation on spatial dysgraphia, in a neglect patient following right brain damage. A long-lasting improvement concerned the right-page preference reflecting the ipsilesional bias but also the sloping lines and the broken lines reflecting visuo-constructive disorders in handwriting. Moreover, a transient improvement was also evidenced for the graphic errors. These results reinforce the idea that the process of prism adaptation may activate brain functions related to multisensory integration and higher spatial representations and show a generalization at a functional level. Prism adaptation therefore appears as useful tool in the theoretical attempt to identify the underlying ‘core’ mechanisms of the neglect syndrome. © 2006 Elsevier Ltd. All rights reserved. Keywords: Neglect; Spatial dysgraphia; Prism adaptation; Visuo-constructive disorder; Right hemisphere; Rehabilitation 1. Introduction Hemispatial neglect may be considered as a failure to gener- ate or maintain a normal representation of the left side of space (Bisiach, Luzzatti, & Perani, 1979) that expresses as a failure to report, respond to, or orient toward novel and/or meaningful stimuli of this space (Heilman, Watson, & Valenstein, 1985). Far from being a unitary condition, hemispatial neglect is a protean disorder whose symptoms can selectively affect differ- ent sensory modalities, cognitive processes, spatial domains and coordinates systems (Halligan, Fink, Marshall, & Vallar, 2003). Interestingly many of these different manifestations may be alleviated following visuo-motor adaptation to right-deviating prisms (Rossetti et al., 1998); the improvement concerns not only the visuo-spatial domain and egocentric reference frame (Frassinetti, Angeli, Meneghello, Avanzi, & Ladavas, 2002; Correspondence to: Service de R´ eeducation Neurologique, Hospices Civils de Lyon, Hˆ opital Henry Gabrielle, Route de Vourles, F-69230 St. Genis-Laval, France. Tel.: +33 4 78 86 50 66; fax: +33 4 78 86 51 86. E-mail address: [email protected] (G. Rode). Rossetti et al., 1998) but also the representational space (Rode, Rossetti, & Boisson, 2001; Rossetti et al., 2004) and other sen- sory modalities like audition or touch (Dijkerman et al., 2003; Maravita et al., 2003; McIntosh, Rossetti, & Milner, 2002). Therefore, these effects cannot be explained by a simple sensori- motor post-effect and rather suggest a cognitive post-effect induced by prism adaptation. Functionally, prism adaptation has been shown to improve disabiliting deficits of everyday life activities like postural bal- ance (Tilikete et al., 2001), reading (Farn` e, Rossetti, Toniolo, & L` adavas, 2002) and wheel-chair driving (Courtois-Jacquin et al., 2006). Another disabiliting deficit observed in right- brain damaged patients with hemineglect concerns the hand- writing (Rode, Perenin, & Boisson, 1996). In their more severe expression, handwriting difficulties have been qualified as spa- tial dysgraphia (Ardila & Rosselli, 1993; Cubelli, Guiducci, & Consolmagno, 2000; ecaen, Angelergues, & Douzenis, 1963; Hecaen & Marcie, 1974; Lebrun, 1985). Spatial dysgraphia has been defined as “a disturbance of graphic expression due to an impairment of visuo-spatial perception resulting from a lesion in the nonlanguage-dominant hemisphere” (ecaen & Albert, 1978, p. 66). According to these authors, four main features 0028-3932/$ – see front matter © 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2006.04.002

Transcript of Prism adaptation improves spatial dysgraphia following right brain damage

Neuropsychologia 44 (2006) 2487–2493

Prism adaptation improves spatial dysgraphia following right brain damage

G. Rode a,b,c,d,∗, L. Pisella b,d, L. Marsal a, S. Mercier a, Y. Rossetti a,b,c,d, D. Boisson a,b,c,d

a Service de Reeducation Neurologique, Hospices Civils de Lyon, Hopital Henry Gabrielle, 20 Route de Vourles, 69230 St. Genis Laval, Franceb Espace et Action, UMR-S 534, Institut National de la Sante Et de la Recherche Medicale, and Universite Claude Bernard,

16 Avenue Lepine, Case 13, 69676 Bron, Francec ‘Mouvement et Handicap’, IFNL et Hospices Civils de Lyon, France

d IFR 19, Institut Federatif des Neurosciences de Lyon, Hopital Neurologique, Bat B13, 59 Bd Pinel, 69394 Lyon Cedex, France

Received 7 September 2005; received in revised form 27 March 2006; accepted 2 April 2006Available online 18 May 2006

Abstract

Visuo-manual adaptation to prisms produces a long-lasting improvement of visuo-spatial neglect. Improvement is also observed in tasks that donot involve visuo-manual component and that can all be consider to rely on a rightward (ipsilesional) orienting bias. Here, we report positive effectsof prism adaptation on spatial dysgraphia, in a neglect patient following right brain damage. A long-lasting improvement concerned the right-pagepMmP©

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reference reflecting the ipsilesional bias but also the sloping lines and the broken lines reflecting visuo-constructive disorders in handwriting.oreover, a transient improvement was also evidenced for the graphic errors. These results reinforce the idea that the process of prism adaptationay activate brain functions related to multisensory integration and higher spatial representations and show a generalization at a functional level.rism adaptation therefore appears as useful tool in the theoretical attempt to identify the underlying ‘core’ mechanisms of the neglect syndrome.2006 Elsevier Ltd. All rights reserved.

eywords: Neglect; Spatial dysgraphia; Prism adaptation; Visuo-constructive disorder; Right hemisphere; Rehabilitation

. Introduction

Hemispatial neglect may be considered as a failure to gener-te or maintain a normal representation of the left side of spaceBisiach, Luzzatti, & Perani, 1979) that expresses as a failureo report, respond to, or orient toward novel and/or meaningfultimuli of this space (Heilman, Watson, & Valenstein, 1985).ar from being a unitary condition, hemispatial neglect is arotean disorder whose symptoms can selectively affect differ-nt sensory modalities, cognitive processes, spatial domains andoordinates systems (Halligan, Fink, Marshall, & Vallar, 2003).nterestingly many of these different manifestations may belleviated following visuo-motor adaptation to right-deviatingrisms (Rossetti et al., 1998); the improvement concerns notnly the visuo-spatial domain and egocentric reference frameFrassinetti, Angeli, Meneghello, Avanzi, & Ladavas, 2002;

∗ Correspondence to: Service de Reeducation Neurologique, Hospices Civilse Lyon, Hopital Henry Gabrielle, Route de Vourles, F-69230 St. Genis-Laval,rance. Tel.: +33 4 78 86 50 66; fax: +33 4 78 86 51 86.

Rossetti et al., 1998) but also the representational space (Rode,Rossetti, & Boisson, 2001; Rossetti et al., 2004) and other sen-sory modalities like audition or touch (Dijkerman et al., 2003;Maravita et al., 2003; McIntosh, Rossetti, & Milner, 2002).Therefore, these effects cannot be explained by a simple sensori-motor post-effect and rather suggest a cognitive post-effectinduced by prism adaptation.

Functionally, prism adaptation has been shown to improvedisabiliting deficits of everyday life activities like postural bal-ance (Tilikete et al., 2001), reading (Farne, Rossetti, Toniolo,& Ladavas, 2002) and wheel-chair driving (Courtois-Jacquinet al., 2006). Another disabiliting deficit observed in right-brain damaged patients with hemineglect concerns the hand-writing (Rode, Perenin, & Boisson, 1996). In their more severeexpression, handwriting difficulties have been qualified as spa-tial dysgraphia (Ardila & Rosselli, 1993; Cubelli, Guiducci, &Consolmagno, 2000; Hecaen, Angelergues, & Douzenis, 1963;Hecaen & Marcie, 1974; Lebrun, 1985). Spatial dysgraphia hasbeen defined as “a disturbance of graphic expression due to animpairment of visuo-spatial perception resulting from a lesionin the nonlanguage-dominant hemisphere” (Hecaen & Albert,

E-mail address: [email protected] (G. Rode). 1978, p. 66). According to these authors, four main features

028-3932/$ – see front matter © 2006 Elsevier Ltd. All rights reserved.oi:10.1016/j.neuropsychologia.2006.04.002

2488 G. Rode et al. / Neuropsychologia 44 (2006) 2487–2493

define spatial dysgraphia—(i) “right-page’ preference: writingis crowded onto the right side of the page leaving an excessivelywide “margin” on the left side; (ii) sloping lines (inclination):patients fail to write horizontally and produce oblique or wavylines; (iii) broken lines: patients leave abnormally large spacebetween words, thus leading to the fragmentation of the lineinto small segments; (iv) graphic errors: production of an uncor-rect number of strokes for a given letter or of letters for a givenword. The present article reports the first investigation of theeffect of prism adaptation on spatial dysgraphia.

The heterogeneous manifestations of left hemispatial neglectmay be classified in two categories: those that can be explainedby a right-oriented behavioural disorder and the others, dynamicand visuo-constructive disorders in nature, that cannot (Pisella& Mattingley, 2004). The question of the effect of prism adapta-tion on the second category of disorders is still open. Clinically,these two categories of disorder are frequently associated, in par-ticular in spatial dysgraphia. Indeed, the “right-page” preferencereflects the right-oriented bias while the inclination of lines, thegaps and the graphic errors may be considered different in nature,perhaps as visuo-constructive errors. Prism adaptation clearlyinduces a reduction of the right orienting bias that has beenmeasured in straight-ahead pointing (e.g. Pisella, Rode, Farne,Boisson, & Rossetti, 2002; Rossetti et al., 1998) and can be advo-cated for the improvement of space-based neglect as measuredby postural balance and wheel-chair driving (Courtois-Jacquinele(hiFFofpod

2. Methods

2.1. Case description

A 69-year-old, right-handed man (R.C.) was admitted to hospital in october2001 for acute left hemiplegia secondary to a vascular infarct in the territory ofthe right middle cerebral artery (Fig. 1). A CT-scan performed one month post-onset showed a temporo-parietal infarct including internal capsule, putamen andcorona radiata.

The patient initially had a severe left upper and lower limbs paresis with atactile sensory deficit and an asterognosis. Speech was midly dysarthric due toa left central facial paresis. On Goldmann’s perimetry there was a left superiorquadranopia. Neuropsychological examination at one month post-onset revealeda head and gaze deviation toward the right side and a marked left-sided neglect.The patient omitted most of the left-sided items and exhibited visuo-constructiveerrors when asked to draw from memory or copy a daisy, a house or a bicycle.On a line-crossing task (Albert, 1973), the patient omitted all the segmentsof the leftmost column (25/40). When required to bisect horizontal lines, hesignificantly transected to the right of the centre. When asked to touch his lefthand with the right, he reached the target with hesitation and search, (i.e. he gota score of 1 on the four-point scale of Bisiach, Perani, Vallar, & Berti, 1986, forpersonal neglect). He omitted to shave the left half of his face and sometimesalso forgot to slip on the left side of his clothes. The patient had no aphasicdeficit, was well oriented in time and exhibited no mental deterioration.

The patient also displayed a marked spatial dysgraphia. When asked to writeon an A4 placed in front of him under dictation or by copy, the leftmost partof the sheet was neglected. Others disturbances were noted: an inclination oflines with an attraction of written text to the right and superior coin of thesheet, some lines broken with an inability of the patient to follow a horizontalline. Lastly, analysis of writing revealed several errors as omissions or repeti-tor

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t al., 2006; Tilikete et al., 2001), visuo-graphic tasks like cancel-ation or copy (Rossetti et al., 1998) and mental imagery (Rodet al., 2001; Rossetti et al., 2004). In addition, the symmetryobject-based neglect) and the spatial organisation of drawingas already been reported to improve following prism adaptationn individuals e.g. in the Gainotti test (Rode, Pisella, Rossetti,arne, & Boisson, 2003, Fig. 6, p. 284; Rossetti et al., 1998;ig. 6 p. 284), suggesting a possible effect of prism adaptationn visuo-constructive disorders. An improvement of the foureatures of spatial dysgraphia described above could thus beredicted. The aim of this study was to test the potential effectf prism adaptation on each of the four parameters of spatialysgraphia.

Fig. 1. Right hemispheric lesion

ions. By contrast, the patient exhibited a minor spatial dyslexia with only fewmissions in the left space of the page during a task of single word or texteading.

At the time of examination, the patient did not show personal neglect andnosognosia had disappeared, the patient was quite alert, well oriented in timend cooperative. The experimental procedure was applied one month post-nset.

.2. Prism adaptation

.2.1. ApparatusThe apparatus used in this experiment is similar to that employed by Redding

nd Wallace (1996). Specifically, this structure consisted of a two-layer rectan-ular black wooden box-like frame (30 cm high, 80 cm wide and 80 cm deep)laced on a table and opened on the side facing the subject. Throughout thexperiment, the patient was seated in front of the structure and placed his arms

tient R.C. See details in the text.

G. Rode et al. / Neuropsychologia 44 (2006) 2487–2493 2489

within the structure. Their head was kept aligned with the body sagittal axisusing a chin-rest situated on the top of the box. A piece of foam placed on thelower layer of the box near the sternum of the patient indicated the hand start-ing position. Sight of the starting hand position and of the first approximately15 cm of the pointing surface was not permitted by the structure. The last partof their pointing trajectory remained visible throughout the adaptation proce-dure. Throughout the experiment, the patient was required to point on the lowersurface of the box and return to the starting position after each trial. The lowerhorizontal surface of the box was covered by electrosensitive paper that allowedthe movement endpoints to be recorded via a metallic thimble attached to thetip of a subject’s index finger. This apparatus produced measurements with anaccuracy of 0.1◦.

2.2.2. Adaptation procedureThe patient was exposed to a shift of the visual field to the right produced by

prismatic lenses. The goggles were fitted with wide-field, wedge lenses creatingan optical shift of 10◦. The exposure period consisted in 50 pointing responsesto visual targets presented 10◦ to the right or to the left of the objective bodymidline. During the prism exposure, the patient was asked to point at a fast butcomfortable speed; they could see the target, the second half of their pointingtrajectory and their terminal error. Their head was kept aligned with the body’ssagittal axis by a chin-rest and controlled by an investigator. The total durationof this exposure was about 3 min (see details in Rossetti et al., 1998).

2.2.3. Straight-ahead pointing testThe patient was seated blindfolded in front of the horizontal box. He was

required to point straight-ahead while his head was kept aligned with the body’ssagittal 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 checkthat prism adaptation had been efficient. Mean deviations observed before andi

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Fig. 2. Effects of prism adaptation on writing under dictation and free drawingfrom memory (daisy and o’clock) in a neglect patient with a neglect dysgraphia.Before adaptation, writing showed a neglect of the left part of the sheet, a right-ward shift of beginning of line and oblique slope of lines. These abnormalitiesare reduced after prism adaptation. The patient used the entirety of sheet space;the lines are horizontal and the legibility of text was improved; this improve-ment persisted 48 h later. A comparable improvement was observed in the freedrawing from memory.

‘Stella’ by Hugo on an A4 paper sheet. In this task, the model was placed abovethe paper sheet and in the midsaggital plane.

The four following parameters of spatial dysgraphia were measured (seeFig. 2):

- Right-page preference: The surface of the sheet neglected by the patient (thearea of the page not used to write) was measured in mm2 and then expressedin percentage of the surface of the sheet.

- Broken lines: The number of abnormal spaces inserted between words wascounted. These spaces often resulted in “steps” in the written line.

- Sloping lines: The angle of inclination of the lines of writing (to the topor bottom of the page) was measured comparatively to the horizontal (indegrees). A positive value indicates a top inclination and a negative value adown inclination.

- Graphic errors: The number of omissions, of duplications of strokes, lettersor words and of abnormal spaces between letters was added.

Given the differential variation ranges between parameters and betweenformat (A4/name-card), statistics have been realised on data expressed in per-

mmediately after prism adaptation were compared by t-test.

.3. Neuropsychological assessment

.3.1. ProcedureThe performance of the patient on line bisection, free drawing and writing

as repeatedly evaluated over six sessions within a time period of four consec-tive days. These three tasks were administered one day before (−24 h), justefore (−2 h), just after the short prism adaptation session (0 h), 2 h after, thengain 24 h and 48 h after.

.3.2. Assessment of neglectUnilateral spatial neglect was assessed free drawing and line bisection. The

atient was asked to draw a daisy and a clock from memory and to mark theidline of 20 horizontal lines presented in the right, centre and left part of the

ame testing sheet (Schenkenberg, Bradford, & Ajax, 1980). This sensitive testllowed us to compute a score reflecting the bias in line bisection as proposedy Schenkenberg et al. (1980). It expresses the mean percentage of horizontaleviation in line bisections, towards the right (signed positive) or towards theeft (signed negative).

A one-way factorial ANOVA was performed with the three periods of testingPre-adaptation, Immediately Post-adaptation and Late after adaptation (2 h, 24 hnd 48 h)) only for the line bisection test. Then planned comparisons have beensed to evaluate the presence of a short-term effect (Pre- versus Post-Immediate)nd/or a long-term effect (Pre versus Late) of prismatic adaptation.

.3.3. Assessment of handwritingWriting performance was assessed under two different conditions: writing

rom dictation or direct copy. In the writing-from-dictation task, the patient wassked to write firstly eight sentences (68 words, ranging from 2 to 9 letters)rom a poem entitled ‘Le chemin creux’ by Richepin on an A4 paper sheet andecondly four sentences (28 words, ranging from 2 to 10 letters) from a ‘poemeaturnien’ by Verlaine on a visiting card (7.9 cm × 11.2 cm). The two texts wereead aloud by the examiner.

In the copying task, four printed sentences (33 words, ranging from 2 to5 letters) were presented to the patient in cursive style from a poem entitled

2490 G. Rode et al. / Neuropsychologia 44 (2006) 2487–2493

centage of deviation with respect to the mean of the two pre-tests (dependentvariables). For each of the four parameters evaluating the writing deficits, afactorial ANOVA was performed with two factors: (1) the three periods of test-ing (Pre-adaptation, Immediately Post-adaptation and Late after adaptation (2 h,24 h and 48 h)) and (2) the three conditions of testing (Copy on A4 sheet, Dic-tation on A4 sheet, Dictation on visiting card). Then planned comparisons havebeen used to evaluate the presence of a short-term effect (Pre- versus Post-Immediate) and/or a long-term effect (Pre versus Late) of prismatic adaptationon each parameter of writing deficit.

3. Results

3.1. Straight-ahead demonstration

In the pre-test, the straight-ahead pointing was initiallyshifted from the midline toward the ipsilesional side (mean:16.2◦; standard error of the mean (S.E.M.): 2.6). In the post-test,R.C. demonstrated a reduction of straight-ahead shift (mean:1.4◦; S.E.M.: 3.6). Comparison by t-test of mean deviationobserved before and following the adaptation revealed a highlysignificant difference (t(1,9) = 7.9; p < 0.0001) indicating that

the patient showed adaptive after-effects to a lateral shift of thevisual field to the right.

3.2. Line bisection test

For the line bisection test, in the two pre-tests, the devia-tion scores of R.C. were, respectively, 37.5% and 31.8%. In thepost-tests the deviation scores were, respectively, 25.7% in theimmediate post-test, 29.4% at 2 h, 24.6% at 24 h and 20.2% at48 h. Performance of R.C. was significantly improved after adap-tation (F(1,137) = 5.15; p < 0.05 between pre and post-values).However, note that this same test has been performed again oneweek later on occasion of routine clinical assessment with aperformance similar to the pre-test (deviation score of 41.1%,F(1,137) = 1.23; p < 0.3).

3.3. Free drawing from memory

For the free drawing of object, in the pre-test, R.C. neglectedthe left half of a daisy or a clock drawn from memory. In the post-

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ig. 3. Temporal evolution of mean values of the four different parameters of spatialaper sheet, on a visiting card and writing by copy on an A4 paper sheet. These three fhis factor condition). The shadowed area represents the “Pre” period gathering the twhe “Post Imm” period corresponds to the test performed immediately after prism adh, 24 h and 48 h after prism adaptation.

dysgraphia (measured in three writing tasks: writing-from-dictation on an A4ormats have been collapsed because of the absence of significant main effect ofo sessions realised by the patient before the single prism adaptation procedure.aptation. The “Late” period gathers the three sessions performed by the patient

G. Rode et al. / Neuropsychologia 44 (2006) 2487–2493 2491

tests, the patient drew an entire daisy with symmetrical numberof petals and a symmetrical clock (see Fig. 2).

3.4. Handwriting

For each of the four parameters measured to evaluate thewriting deficits, the factorial ANOVA did show a significantmain effect of the period of testing (Pre, Immediately Post andLate after prismatic adaptation) on the writing performance (allF(2,9) > 4; p < 0.05). By contrast, no main effect of the condi-tions of testing (Copy on A4, Dictation on A4 and Dictation ona name-card) was revealed by the statistical analysis, for noneof the four parameters (all F(2,9) < 1.7; p > 0.05). No significantinteraction was revealed between the two factors. Evolution ofeach parameter of writing deficit is thus illustrated in Fig. 3 as amean measure of the three conditions of testing with respect oftesting time (in hours). Periods of testing are mentioned on thegraphs.

For the right-page preference: planned comparisonsshow a significant short-term (Pre- versus Post-Immediate:F(1,9) = 8.16; p < 0.05) and long-term effect (Pre versus Late:F(1,9) = 13.62; p < 0.05) of prism adaptation on the neglectedsurface area.

For the broken lines: planned comparisons show a signif-icant short-term (Pre- versus Post-Immediate: F(1,9) = 26.08;p < 0.05) and long-term effect (Pre versus Late: F(1,9) = 24.30;p

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secondly revealed the reduction of the lines inclination and ofthe number of broken lines, maintained 48 h later, as well as thetransient decrease of graphic errors after prism adaptation. Thisrehabilitation technique is therefore able to induce a significantimprovement of handwriting in neglect patients. The ability toplace and orient correctly the words in the page and relatively toeach others was durably improved; the decrease of the graphicerrors observed within words was only observed immediatelyafter the prism removal. The improvement of these features ofspatial dysgraphia is hardly explained by the leftward-orientedsensori-motor after-effect of prism adaptation. The positiveeffect of prism adaptation on visuo-constructive disorders sug-gests that prism adaptation does not act specifically on theipsilesional bias characteristic of hemineglect but rehabilitatesmore generally the visuo-spatial functions attributed to the rightcortical hemisphere. Prism adaptation may enlarge or shift thepart of space represented in the spared cortical hemisphere (seeRedding & Wallace, 2006). This different distribution of therepresentation of space between hemispheres could explain theimprovement of both the right-oriented behavioural disordersand the visuo-constructive disorders.

The short-term effect of prism adaptation on the graphicerrors can lead to rather distinguish this latter parameter from theother parameters which were still improved after 48 h. Accord-ingly, the graphic errors of spatial dysgraphia have been oftenclaimed in the literature to result from a disorder distinct fromtdcdaw

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< 0.05) of prism adaptation on the number of broken lines.For the sloping lines: planned comparisons show a

arginally significant short-term (Pre- versus Post-Immediate:(1,9) = 4.98; p = 0.05) effect but a long-term effect (Pre versusate: F(1,9) = 12.63; p < 0.05) of prism adaptation on the line

nclination.Lastly for the graphic errors: planned comparisons

how a significant short-term (Pre- versus Post-Immediate:(1,9) = 8.05; p < 0.05) effect but no long-term effect (Pre versusate: F(1,9) = 0.4; p > 0.05) of prism adaptation on the numberf graphic errors.

. Discussion

The aim of this study was to assess the effects of prismdaptation on spatial dysgraphia, a disabiliting deficit frequentlyssociated to neglect following right brain damage. Moreover,his constituted a mean to test whether prism adaptation couldeduce the visuo-constructive disorders related to the right hemi-phere function, as it had been shown already for the leftwardrienting behavioural biases of the neglect syndrome.

First, the results did confirm the positive effect of prismdaptation on the oriented behavioural disorder, as previouslyeported (e.g. Pisella et al., 2002; Rode et al., 2003; Rossetti etl., 1998). In the present paper, it is clearly demonstrated by theeduction of the ipsilesional shift in the straight-ahead pointingn darkness and in the line bisection task and by the decrease ofhe neglected surface. The reduction of the neglected area alsoersisted in the late test (48 h), confirming the potential long-asting improvement of this category of disorder (Farne et al.,002; McIntosh et al., 2002; Pisella et al., 2002). The results

he oriented behavioural bias and the visuo-constructive disor-er. The definition of graphic error has however not always beenonsistent in these papers. In the present paper, graphic errorsid include iterations (duplications of strokes, letters or words)s well as omissions and abnormal spaces between letters andords (Hecaen & Albert, 1978).Ardila and Rosselli (1993) have comparatively studied hand-

riting deficits in retro-rolandic and pre-rolandic right hemi-phere damaged patients. In a group of 21 patients, about halff pre-rolandic and three-quarters of retro-rolandic presentedith writing errors and spatial dysgraphia of variable degrees.or further investigations of handwriting performance, rightemisphere damaged patients were selected on the presencef spatial dysgraphia but exhibited associated disorders includ-ng left hemiparesis, visual field defects, spatial hemineglect,onstructional apraxia, spatial alexia or spatial acalculia. Itera-ions have been considered the most distinctive type of writingrror in right hemisphere damage patients (Hecaen & Marcie,974) and neglect has been considered partially responsible forterations of strokes and letters: once the stroke and letter isritten, the patient neglects it, since it moves to the left visualeld (Simerniskaya, 1974). However, Ardila and Rosselli (1993)stablished that neglect did not correlate with iterations andhat iterations, when produced during writing, are also observedhen drawing figures and the information remains in the same

bsolute position in the visual field. On the other hand, featuredditions did significantly correlate with left hemiparesis andence pre-rolandic damage. Altogether, the correlation studyuggested that writing deficits in right hemisphere damagedatients can be associated to and depending on four components:1) left hemi-neglect, reflected in increased and unsteady mar-

2492 G. Rode et al. / Neuropsychologia 44 (2006) 2487–2493

gins; (2) constructional deficits, reflected in changes in the typeof handwriting and misgroupings of elements; (3) general spa-tial defects, reflected in the inability to use correctly the spacesbetween words, difficulty in keeping the written line in a hori-zontal position, disrespect to spaces and spatial disorganizationof the written material; (4) a tendency to perseverate, reflectedin iterative errors. Although all types of errors were produced inboth groups of patients and were more numerous in patients withretro-rolandic damage (not only in writing words and sentences,but also in writing letters and syllables), the authors put for-ward that iterative errors (feature additions and letter additions)represented the most evident type of writing defect in the rightpre-rolandic patients, whereas misgrouping of elements and let-ter omissions represented the two most evident types of writingerrors in right retro-rolandic patients.

Lebrun and Rubio (1972) have argued that errors as dupli-cations and omissions of strokes and letters correspond to“afferent-type” errors because these errors are similar to thosemade by normal subjects when requested to write with theireyes closed or with delayed visual feedback. The patients pro-ducing these afferent-type errors may add a fourth down stroketo the letter ‘m’ or omit the second downstroke of the letter‘n’ (Lebrun, 1976). These errors occur mainly in writing wordswith double letters or in writing letters with repeated strokes(Hecaen & Marcie, 1974; Margolin, 1984). However, unlike nor-mals, dysgraphic patients are reported not to be more defectivewgionbMmwedmftaswa

nttotmapaRmc

authors explained that in right brain damaged patients a remap-ping impairment would result in an overwriting from visual con-scious representation of the visual space opposite to the visualorientation, which is usually rightward due to the ipsilesionalbias. The overwritten left visual space is defined with respectto the previous eye position, i.e. before the saccade occurred.The visual integration of successive retinal images appears par-ticularly important during handwriting, which involves multipleeye movements and a constant monitoring and on-line integra-tion of which part of the sentences, words and letters has beenalready written and which part remains to be written, in what way(inclination) and where (gaps). With an impairment of remap-ping mechanisms, the successive rightward saccades involvedduring handwriting would lead to progressive overwriting of theleft space, corresponding to the part of the sentence that hasalready been produced. This would therefore affect the on-linevisual monitoring of handwriting and lead to errors like dupli-cations of words, letters or strokes, incorrect inclinations, gapsbetween words and broken lines, as if the handwriting was donewith eyes closed. Consistent with this hypothesis, there wouldbe no reason to distinguish errors due to this “visual” monitor-ing defect occurring within words (graphic errors) or betweenwords (inclinations and gaps/broken lines). However, in case offrontal dysfunction (that the infarct, which included the internalcapsule, putamen and corona radiate, suggests may be presentin the patient reported in this paper), handwriting errors of apRwtrwcnhtcwcAfacetc

aphaarlagv

hen vision is prevented (Lebrun, 1976), the term ‘afferent dys-raphia’ was thus used to refer to the inability to use afferentnformation in monitoring writing movements. Some pure formsf afferent dysgraphia with no evidence of left visuo-spatialeglect following a focal damage of the right hemisphere haveeen reported (Croisile & Hibert, 1998; Cubelli & Lupi, 1999).oreover, Cubelli et al. (2000) have studied the writing perfor-ances of a series of nine right hemisphere damaged patientsith a written production disorder and shown that afferent-type

rrors may be clearly dissociated from neglect-related writingeficits and spatial errors. For these authors afferent dysgraphiaay be even considered as an autonomous syndrome, distinct

rom the spatial dysgraphia picture. The neglect-related and spa-ial writing errors should reflect an oriented behavioural disordernd/or a visuo-constructive disorder although the afferent-errorshould reflect rather a disorder in monitoring the actual hand-riting movements in order to compare what is written with the

bstract representation of letters (Cubelli et al., 2000).More recently, Pisella and Mattingley (2004) have listed a

umber of manifestations that cannot be explained by currentheories of neglect, and especially by the dominant attentionalheory that solely postulates an orienting bias toward the sidef lesion (ipsilesional bias), a local bias and impaired sus-ained attention. They have postulated that these manifestations,

ostly visuo-constructive in nature, can be accounted for byn additional underlying disorder of spatial remapping due toarietal dysfunction. In primary visual areas, retinotopic mapsre renewed and thus overwritten at each new ocular fixation.emapping processes operating in higher-level oculocentricaps of the parietal cortex ensure visual integration of these suc-

essive retinal images over time and space. More specifically, the

erseverative nature can be exhibited (Ardila & Rosselli, 1993;usconi, Maravita, Bottini, & Vallar, 2002), especially withinords, probably due to impaired “motor” monitoring between

he actual handwriting movements produced and the abstractepresentation of letters (Cubelli et al., 2000). The present resultsould suggest that the former, spatial visuo-constructive errors,

an be durably improved by prism adaptation, whereas this isot true of the latter, perseverative graphic errors. Our patientas both a parietal and a frontal lesion. The absence of long-erm improvement of graphic errors suggests that these can beonsidered as a frontal perseverative dysfunction in our patient,hereas the other dysfunctions can be considered as visuo-

onstructive in nature and caused by the parietal dysfunction.lthough spatial dysgraphia that possesses all of the four main

eatures of right-page preference, line inclination, broken linesnd graphic errors, as indicated by Hecaen et al. (1963), is a rarelinical condition, it is never clear to what extent one can gen-ralize from single case studies. For this reason, it is importanto note that further studies of similar cases will be necessary toonfirm whether the interpretation offered here is correct.

Since the spatial deficits consecutive to right brain damagere still weakly defined and have almost all been shown to beossibly dissociated, the symptoms of spatial dysgraphia andemispatial neglect have been classified in multiple mannersnd divided into more or less numerous components. Thesettempts of classifications are interesting because of their theo-etical and/or experimental work in order to identify the under-ying ‘core’ mechanisms of these multiple manifestations, ifny. Although discrepancy in the duration of the amelioration ofiven tests has already been observed within and between indi-idual patients in the literature (e.g. Pisella et al., 2002; review

G. Rode et al. / Neuropsychologia 44 (2006) 2487–2493 2493

in Rode et al., 2003), the potential modification of the postu-lated components by prismatic adaptation appears as an usefuladditional test of the various classifications.

Acknowledgments

The authors wish to thank J.L. Borach for his work on thefigures. This work was supported by ACI Neurosciences (Plas-ticite), Leverhulme Trust and INSERM PROGRES.

Parts of this study were presented to the European Congressof Neuropsychology, 18–20 avril 2004, Modena, Italy.

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