Verbal commands help the execution of endogenous movements in anarchic hand

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Verbal commands help the execution of endogenous movements inanarchic handAnna Cantagalloa; Lucia Spinazzolabc; Marco Rabuffettid; Sergio Della Salae

a Modulo di Neuropsicologia Riabilitativa, UOMR, Dipartimento di Neuroscienze/Riabilitazione, AUOdi Ferrara, Italy b Department of Psychology, University of Turin, Italy c Department of Rehabilitation,Ospedale A. Bellini, Somma Lombardo, Italy d Polo Tecnologico, Fondazione Don Carlo GnocchiIRCCS, Milano, Italy e Human Cognitive Neuroscience and Centre for Cognitive Ageing and CognitiveEpidemiology, Psychology, University of Edinburgh, UK

First published on: 14 April 2010

To cite this Article Cantagallo, Anna , Spinazzola, Lucia , Rabuffetti, Marco and Della Sala, Sergio(2010) 'Verbalcommands help the execution of endogenous movements in anarchic hand', Neuropsychological Rehabilitation, 20: 3,406 — 422, First published on: 14 April 2010 (iFirst)To link to this Article: DOI: 10.1080/09602010903345298URL: http://dx.doi.org/10.1080/09602010903345298

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Verbal commands help the execution of endogenous

movements in anarchic hand

Anna Cantagallo1, Lucia Spinazzola2,3, Marco Rabuffetti4, andSergio Della Sala5

1Modulo di Neuropsicologia Riabilitativa, UOMR, Dipartimento di

Neuroscienze/Riabilitazione, AUO di Ferrara, Italy; 2Department of

Psychology, University of Turin, Italy; 3Department of Rehabilitation, Ospedale

A. Bellini, Somma Lombardo, Italy; 4Polo Tecnologico, Fondazione Don Carlo

Gnocchi IRCCS, Milano, Italy; 5Human Cognitive Neuroscience and Centre for

Cognitive Ageing and Cognitive Epidemiology, Psychology, University of

Edinburgh, UK

Patients with anarchic hand (AH) syndrome exhibit involuntary but seeminglypurposeful controlesional upper limb movements. Here we report on the case ofa patient (AC) presenting with a right AH following a left medial frontal lesion.Previous literature indicated that endogenous movements, particularly in thepresence of distractors, are impaired in AH, whereas exogenous movementsare spared. In this study we examined exogenous and endogenous (or sequen-tial) movements using a new experimental procedure. Our main aim was toinvestigate whether the ability to perform sequential movements improvesunder verbal command as anecdotally observed in patients with AH. Resultsshowed that the performance of AC’s right AH was impaired in sequentialtasks and that this impairment was improved by verbal command. The observedreduction in errors in sequential tasks under external verbal command wascoupled with a compensatory increase in response times.

Keywords: Anarchic hand (AH); Rehabilitation; Verbal command.

Correspondence should be sent to Lucia Spinazzola, Department of Rehabilitation Ospedale

A. Bellini, Via Bellini n82, 21019 Somma Lombardo (VA), Italy. E-mail: [email protected]

NEUROPSYCHOLOGICAL REHABILITATION

2010, 20 (3), 406–422

# 2010 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business

http://www.psypress.com/neurorehab DOI:10.1080/09602010903345298

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INTRODUCTION

Anarchic hand (AH) syndrome (Della Sala, 2009a) is a rare condition(Marchetti & Della Sala, 1998; see review by Fisher, 2000) defined as “theoccurrence of complex movements of an upper limb which are clearly goal-directed and well performed but totally unintended” (Della Sala, Marchetti,& Spinnler, 1994). Patients with AH are always aware of having problemswith intentional control of their hand; they are dismayed by the defiantactions of their rebellious hand and often spontaneously report this bizarremotor behaviour to the examiner (Della Sala & Marchetti, 2005). When thewayward hand manifests its unruly behaviour there is an evident contrastbetween what the AH is doing and the patient’s own explicit will (Blakemore,Wolpert, & Frith, 2002; Frith, Blakemore, & Wolpert, 2000; Goldberg, Mayer,& Toglia, 1981). In spite of their feeling that their hand has a will of its own(Della Sala, 2005), AH patients never deny that their hand is part of theirbody (Marchetti & Della Sala, 1998). The sight of an object at reaching distanceis often sufficient to elicit a grasping and utilisation action, even though thisdoes not fit with the patient’s declared current goals (Goldberg & Bloom,1990). It appears that the AH is driven by environmental distractors (Boccardi,Della Sala, Motto, & Spinnler, 2002; Giovannetti, Buxbaum, Biran, & Chatter-jee, 2005). The outcome is a serious impediment that affects both unimanualand bimanual actions (Fisher, 2000), often resulting in a conflict between thetwo hands (Akelaitis, 1944; Tanaka, Iwasa, & Yoshida, 1990) whereby theunaffected hand attempts to restrain the affected hand (Della Sala, Marchetti,& Spinnler, 1991). Relevant to the experiment that we are reporting here, it isworth noting that even if AH patients are aware of these unwelcome actionsthey often fail to inhibit them (Della Sala & Marchetti, 2005). Indeed, AHhas been nicknamed “Dr. Strangelove syndrome” (Della Sala, 2005, 2009b).

Several anatomo-functional hypotheses have been put forward to accountfor AH (Bogen, 1985; Feinberg, 1997; Goldberg & Bloom, 1990; see for adiscussion Marchetti & Della Sala, 1998), but all converge in agreeing thata lesion to the supplementary motor area (SMA) plays a major role in elicitingAH (Blakemore et al., 2002; Boccardi et al., 2002; Della Sala et al., 1991)leaving the AH at the mercy of the exogenously driven movements ruledby the undamaged premotor cortex (PMC) sitting on the lateral side of theanterior frontal lobes (Boccardi et al., 2002; Goldberg, 1985).

Studies on monkeys have provided support for this hypothesis whichaccounts for AH as resulting from the imbalance between a damaged contro-lateral SMA and a spared PMC by showing that premotor neurons are moreactive during the pre-movement and movement periods in a visually triggeredtask (Graziano, Yap, & Gross 1994), whilst the majority of SMA neurons aremore active during the pre-movement and movement periods in the internallyguided task (Mushiake, Inase, & Tanji, 1991).

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The presence of AH in brain damaged patients affects the proper executionof many activities of daily life. Anecdotal observations suggested the possi-bility of using verbal command to control AH behaviours. In the first knownobservation of AH, Goldstein (1908, 1909) reported on patient HM whotried to inhibit the unwanted actions of her left hand by hitting it or bytalking to it in a falsetto voice. HM used verbal commands spontaneouslywith the aim of controlling her hand: “I hit it and told my little hand tobehave itself”. Recently, Kritikos, Breen, and Mattingley (2005) described apatient (MA) with left AH following an ischaemic lesion encroaching uponthe apex of the right sided precentral gyrus. The authors reported severalepisodes in which external verbal commands were employed to block orunblock the action of the AH. For example, the patient opened a door andstarted to walk through only to find himself unable to release the doorknob.He remained “glued” to the door in this way until a nurse passed by andtold him to let the knob go. In this case the verbal command came fromoutside, i.e., from the nurse. These anecdotal observations indicate the possi-bility of using a verbal aid to minimise the pathological behaviour of the AH.

In the neuropsychological literature external verbal incitation has also beenemployed to improve motor performance in cases of unilateral motor neglect(Laplane & Degos, 1983); in these patients the brain lesion frequentlyinvolved the frontal lobe.

In the current study we investigated the possibility that these pathologicalendogenous movements could be ameliorated by the use of external prompts.To this end we examined the performance of a patient (AC) affected by rightAH following anterior lesions of the corpus callosum and the left SMA. Theaims of the experiment were: (1) to confirm the different performancebetween endogenous and exogenous movements in a patient with AHsyndrome; (2) to demonstrate the effect of verbal command (either externalor personal) in improving the performance of endogenous movements inpatients affected by AH syndrome; and (3) to investigate the influence ofverbal commands on the timing of movement (response time) in endogenousconditions.

PARTICIPANTS

Patient AC

AC was 34 years old at the time of testing. He is a right-handed male with 8years of formal education. He suffered a spontaneous haemorrhage whichdamaged his left frontal lobe. Brain magnetic resonance imaging (MRI)(see Figure 1) demonstrated cortical-subcortical hypodensity foci in thefronto-basal area bilaterally, in the left fronto-opercolar area and in the left

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frontal superior area. The latter lesion was the largest and extended mediallyencroaching upon the anterior third of the cingulated gyrus and the mesialsurface of the left frontal lobe (SMA). In the acute phase AC presentedwith a right upper limb paresis which was no longer detectable at the timeof the assessment, three months post-onset. However, he was still affectedby a right homonymous lateral haemianopia.

Before the stroke

Before his stroke, AC worked as a police officer and was in good health. Hewas a blood donor and had never been admitted to hospital or taken any medi-cation. He was a keen cyclist and enjoyed taking care of his family’s vineyard.AC is married and has two children.

At work, he was considered a perfectionist by his colleagues and had asimilar attitude towards his family life. He was described as demandingand severe by his sons and wife. He was very concerned with tidiness andtook special care of both his physical appearance and the quality of hisdiet. He was an introverted person who was not very sociable.

After the stroke

AC’s character and behaviour changed after the stroke. Although he was stillintroverted and tended to perfectionism, he has became softer and more easy-going; he is now more prone to follow what other people suggest and hasstarted taking other people’s advice. He has put on some weight.

Neuropsychological assessment

Three months post-onset, AC was attentive, oriented and cooperative. Hissimple and choice reaction times were fast and accurate (with visual stimuli:Simple Reaction Times average 360 msec, SD 120; Choice Reaction Timesaverage 441 msec, SD 132). No evidence of neglect was found. However, hescored below cut-off in tests assessing visuo-spatial short-term memory(Corsi blocks), immediate and delayed verbal learning (Rey’s 15 words test;Carlesimo, Caltagirone, & Fadda, 1995) and prose memory (Spinnler &Tognoni, 1987) (Table 1). A standard language examination (ENPA;

Figure 1. Reconstruction of patient’s lesion from MRI scan (11 months from onset).

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Capasso & Miceli, 2001) showed a mild motor aphasia with some difficulty inoral comprehension. He reported some errors in writing with his right hand.Some trouble with spontaneous speech was also noted, he spoke with slow

TABLE 1General neuropsychological assessment

Range Cut-off

AC’s performance

3 month post-onset

Attention

Simple reaction times1 – .287 360�

Multiple choice reaction times1 – .601 441

Visual scanning2 0–60 ,31 25.25�

Memory

Verbal span2 0–10 ,3.0 3.5

Visuospatial span2 0–10 ,3.7 3.5�

15 Rey’s words3

Immediate 0–15 ,28.53 17.1�

Delayed (15 min) 0–75 ,4.69 22.1�

Memory’s prose2 0–16 ,4.75 0.06�

Language

ENPA4

Oral word comprehension 0–20 ,18.4 18.4

Visual word comprehension 0–20 ,17 16.6�

Oral phrase comprehension 0–14 ,11.6 8.8�

Visual phrase comprehension 0–14 ,11.3 12.9

Oral name denomination 0–10 ,8.2 10

Written name denomination 0–5 ,2.7 3.8

Oral verbs denomination 0–10 ,6.1 6.9

Written verbs denomination 0–5 ,3.0 2.8�

Token Test2 0–36 ,26.50 18.75�

Executive function

Raven’s Coloured Progressive Matrices 473 0–36 ,18.96 27.9

Frontal Assessment Behaviour 5 0–18 ,14.4 9.5�

Behavioural Assessment Dysexecutive Syndrome6

Rule’s change – ,70 28.85�

Action’s programme – ,70 84.9

Key’s search – ,70 67.46�

Temporal opinion – ,70 71.59

Zoo’s map – ,70 0�

Six elements – ,70 46.6�

Wisconsin Card Sorting Test (WCST)7

Global score 0–128 .90.5 110�

Perseverative errors (right hand) – .42.6 62.2�

Non perseverative errors (right hand) – .29.9 48.6�

� Pathological score, i.e., below the 5th centile of the normal distribution.1Zimmermann and Fimm (1993); 2Spinnler and Tognoni (1987); 3Carlesimo et al. (1995);

4Capasso and Miceli (2001); 5Appollonio et al. (2005); 6 Wilson et al. (1996); 7 Caffarra et al. (2004)

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and limited word production. His nonverbal intelligence performance wasnormal (Raven Progressive Matrices; Carlesimo et al., 1995). However,signs of a dysexecutive syndrome emerged from the Frontal AssessmentBehaviour (FAB; Appollonio et al., 2005), from the Behavioural AssessmentDysexecutive Syndrome (BADS; Wilson, Aderman, Burgess, Emslie, &Evans, 1996; Italian version by Antonucci, Spitoni, Orsini, Di Olimpio, &Cantagallo, 2001) and from the Wisconsin Card Sorting Test (WCST; Italiannorms in Caffarra, Vezzadini, Dieci, Zonato, & Venneri, 2004).

AC also showed signs of callosal disconnection, including ideo-motorapraxia (left hand only); impaired somesthetic transfer in reproducing pos-tures of one hand with the other hand; tactile anomia of the left hand; andcomplete agraphia with the left hand. He took notice of his writing deficit,was surprised by it, but failed to correct his errors.

Right anarchic hand

AC presented with the typical AH-related behaviour. For example, when heshaved he was able to complete the task correctly, but then started all overagain. In another instance, with his right hand he was able to open thewindow but closed it immediately afterwards. In a grocery shop AC’s righthand tried to steal an apple against his will, and while walking his right

TABLE 2Transcallosal disconnection signs

Range Cut-off 3 month

Ideomotor apraxia

Monolateral1

Imitation

Right hand 0–72 ,62 65

Left hand 0–72 ,62 58�

Bilateral2

Pantomime to verbal command 0–18 – 11�

Tactile anomia

Right hand 0–30 – 30

3�Left hand 0–30

Writing

Right hand 0–10 – 10

0�Left hand 0–10 –

Cross-replication of hand posture

Right hand 0–3 – 0�

1�Left hand 0–3 –

�Pathological score, i.e., below the 5th centile of the normal distribution.1De Renzi et al. (1980); 2Goldenberg et al. (2001). The other tasks do not

have norms.

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hand tried to lift the skirt of a passing girl. During AH episodes the patientappeared aghast and worried, but these feelings faded quickly. AH episodeswere more frequent when the patient was involved in various motor actionsoccurring simultaneously, but were not clearly evoked solely by distractinginternal events. Distracting external events influenced the clinical picturemuch less at the time of formal assessment than they did just immediatelyfollowing the brain lesion. AH episodes occurred only when the patientwas alert and were never observed during sleep.

Motor perseverations in the right hand

We observed numerous motor perseverations with AC’s right hand duringwriting, copying drawing and reproducing building models, in rhythm repro-duction, in rapid and alternate movement reproduction, in WCST and in amodified Tower of London (Allamanno, Della Sala, Laiacona, Pasetti, &Spinnler, 1987), as well as in more ecological situations such as when thepatient tried to unnecessarily use a fork repeatedly with his right hand.Furthermore, there were almost continuous rhythmic movements affectinghis right hand.

Functional autonomy in activities of daily living

The patient obtained a low global score (172 out of 210) in the FunctionalAssessment Measure (FAM; Hall, Hamilton, Gordon, & Zasler, 1993), ascale assessing the autonomy in primary and secondary daily activities. Thisreveals a reduction in self-care activities (i.e., the injury risk in shaving washigh, so much so as to require the assistance of an occupational therapist)and in instrumental activities (i.e., using public transport or driving a car).These problems were particularly evident in potentially hazardous activities.

Controls

AC’s performance was compared to that of two neurologically intact right-handed males (30 and 35 years old, with 16 and 8 years of formal education,respectively).

MATERIALS AND METHODS

Apparatus

The experimental hardware apparatus, which allowed us to present stimuliand measure the participant’s response, consisted of a standard personal com-puter equipped with a touch-screen monitor (Clear Tek 1000, MicroTouch,USA) and loudspeakers. The test software (developed in Microsoft Visual

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Basic) fulfilled two main functions: to control and administer arrays ofstimuli, both visual and auditory; and to detect and record the participant’sresponse, both qualitatively (which stimulus was chosen) and quantitatively(timing of response).

Experimental procedures

Participants were seated in front of the computer screen which was at handreach. All trials started with the participants’ index finger in the startingposition (a 70 mm black square positioned centrally, in the lower third ofthe white screen). After a half second delay, a single stimulus (in condition1) or a set of three stimuli (in all other conditions) were shown in the upperthird of the screen, about 100 mm above the starting position, horizontallyaligned and equally spaced. Participants were required to choose, reach andtouch a visual target (X-crosses, squares and triangles about 70 mm inheight), with their index finger. Participants were asked to respond immedi-ately after the appearance of the visual stimuli. The apparatus recorded theparticipants’ responses (detecting which stimulus was chosen and touchedby the finger) and the response time (from stimulus onset to finger tip takeoff from the starting position).

For the purpose of the experiment we defined endogenous movements asactions internally generated (see e.g., Lau, Rogers, Ramnani, & Passingham,2004) whereas exogenous movements were conceived as externally generatedmovements. Hence, exogenous movements were movements towards a visualtarget whereas endogenous movements were predefined sequentialmovements. The experimental test was composed of four tasks (exogenousmovements; endogenous movements without aid; endogenous movementswith external command; endogenous movements with self-command). Eachtask encompassed two conditions (no distractors and distractors). The firsttwo conditions examined exogenous movements while the others assessedendogenous movements. Therefore the experimental conditions, in detail, were:

Task A - Exogenous movements

. Condition 1 (stimulus: X): The participant was asked to make unimanualmovements towards the target stimulus X, which always appeared alonein one out of three different spatial positions in the upper third of thescreen.

. Condition 2 (stimuli: square, triangle and X): In each trial, three differ-ent stimuli were presented in a different order, so that each stimulusoccupied each position in five trials, and the participant was asked tomake unimanual movements toward the target X.

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Task B - Endogenous movements without aid

. Condition 3 (stimuli: Xs): Three X stimuli were presented, in each trial,on the screen, the participant was asked to choose and reach the targetaccording a predefined iterative “left to centre to right” sequence.

. Condition 4 (stimuli: square, triangle and X): Three different stimuliwere presented on the screen. The participant was asked to reach andtouch a visual target according to the predefined sequence (left-centre-right); note that the X never corresponded to a target in the sequence.

Task C - Endogenous movements with external command

. Condition 5 (stimuli: Xs): Three Xs were presented similarly toCondition 3, but, before stimulus onset, a recorded voice indicated atwhich location the subject had to reach the screen, according to a prede-fined sequence.

. Condition 6 (stimuli: square, triangle and X): Three different stimuliwere presented similarly to Condition 4, but, before stimulus onset, arecorded voice indicated at which location the subject had to touchthe screen, according to a predefined sequence.

Task D - Endogenous movements with self-command

. Condition 7 (stimuli: Xs): Three Xs were presented similarly to Condition3, but, before stimulus onset, the participant was asked to declare theexpected position of the target according to a predefined sequence.

. Condition 8 (stimuli: square, triangle and X): Three different stimuliwere presented similarly to Condition 4, but, before stimulus onset,the participant was asked to declare the expected position of the targetaccording to a predefined sequence.

Each experimental condition consisted of 15 trials, the first three trialswere considered as run-in, hence the score for each condition ranged from0 to a maximum of 12 (see Figure 2). AC first performed the test with hisaffected hand and then with his unaffected hand. Controls carried out thetest with both hands, using their right hand first.

RESULTS

Accuracy

The healthy controls carried out all the tasks with good accuracy. AC alsoperformed all the tasks without errors with his left hand; the performanceof AC’s right AH, while without errors for the exogenous conditions, had

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Figure 2. Experimental conditions.

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peculiar aspects for the endogenous conditions. A summary of his errors isreported in Table 3.

Differences in accuracy between endogenous and exogenousmovements

With his right hand, AC performed exogenous movements (conditions 1 and 2)without errors. He made 3 errors out of 12 trials (25%) during the sequentialtasks without distractors (condition 3). The number of errors increased duringendogenous movements in the presence of distractors (10/12, 83%). A distractorinterference effect was, in fact, evident in condition 4. Error analysis showed that5 out of 10 errors were perseverations (touch of visual target X) while theremaining 5 were sequential non-perseverative errors. This would indicatethat AC had difficulty when planning and programming sequential actions(endogenous movements) with his right AH in the presence of distractors.

The effect of verbal commands

The performance of AC’s AH in the sequential tasks without distractors(baseline condition 3: score 3/12 errors) became normal (no errors) withverbal cues provided either externally (condition 5) or when he was askedto generate verbally his own goal (condition 7). Verbal aid reduced thenumber of errors in the sequential movements also under conditions ofendogenous movements with distractors (baseline condition 4 scored 10/12errors). In condition 6 the patient’s AH produced 4/12 errors (two were per-severations and two were sequential errors) and, in condition 8, 3/12 errors(two were perseverations and one was a sequential error).

There was a significant difference between all the conditions of endogen-ous movement with distractors: condition 4 (without aid), condition 6 (withexternal verbal command) and condition 8 (with internal verbal command),

TABLE 3Number of errors in the endogenous conditions of patient AC performing the task with his

anarchic right hand

Endogenous movements

TASK B TASK C TASK D

Conditions without aid External verbal command Self-verbal command

Condition 3

No

distractors

Condition 4

With

distractors

Condition 5

No

distractors

Condition 6

With

distractors

Condition 7

No

distractors

Condition 8

With

distractors

3 10 0 4 0 3

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x2(2) ¼ 7.091; p ¼ .029: Cochran Test. In the couple comparisons with theMcNemar Test, there is just one significant difference: A reduction of errors isevident from condition 4 to condition 8 (z ¼ 2.64, p ¼ .008).

Anticipatory responses

Responses faster than 180 ms, which, according to the literature, is the thresholdfor a simple visual reaction, were considered anticipatory responses (Woodworth& Schlosberg, 1954). Sometimes participants anticipated the appearance ofvisual stimuli; negative values and anticipated responses were less than 10% ofthe total number of trials (see Table 4). These responses did not enter the analyses.

Response times

Data (response times in seconds) were analysed by means of repeatedmeasures ANOVA with the Participant (AC patient/control 1/control 2) asbetween-factor and Hand (right hand/left hand) and Task (exogenousmovements/endogenous movements without aid/endogenous movementswith external command/endogenous movements with self-command) andDistractor Effect (no distractors/distractors) as within subjects factors.Newman-Keuls tests were adopted for post-hoc analyses.

Does verbal command influence the timing of endogenouslydriven movements?

As expected, AC’s responses times were slower than those of the two healthycontrols, F(2, 10) ¼ 153,61, p , .0001. A post hoc test showed that thedifference was significant for both comparisons (AC vs. control 1; AC vs.control 2). Significant main effects of Hand, F(1, 10) ¼ 84.053, p , .0001,Task, F(3, 30) ¼ 63,224, p , .0001, and Distractor Effect, F(1, 10) ¼151,36, p , .0001, factors were present. The Hand � Participants interactionwas also significant, F(2, 10) ¼ 68,006, p , .0001. The results indicate thatAC’s right AH was slower than his intact left hand (p , .0005) and slower

TABLE 4Number of anticipatory responses in each task in the patient (AC) and controls

Hand Task A Task B Task C Task D

AC Right hand 4 3 12 4

AC Left hand 0 0 14 1

Control 1 Right hand 0 0 12 4

Control 1 Left hand 0 0 2 3

Control 2 Right hand 0 0 1 0

Control 2 Left hand 0 0 1 0

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than the averaged performance of the right hand of the controls. The perform-ance of AC’s intact left hand did not differ significantly from the averaged per-formance of the left hand of the two healthy controls.

The Hand� Task� Participant interaction was also significant, F(6, 30)¼98,227, p , .0001. Observing the response times in the four tasks, it can beseen that the patient’s right AH showed the worst performances in Task C(endogenous movements with external command). A summary of responsetime results is reported in Figure 3.

A post hoc test showed that the response times of AC’s right AH in Task B(endogenous movement without aid) were slower than response times in TaskA (exogenous movements), and response times in Task C (endogenous move-ments with external verbal aids) were significantly slower than all the otherconditions (p , .0005 for all comparisons). Response times in Task D didnot differ from Task A.

Figure 3. Means (the vertical bars indicate the confidence interval) of response times of patient AC

and controls in the four Tasks. AC’s right hand is the anarchic hand. TASK A: exogenous movements;

TASK B: endogenous movements without aid; TASK C: endogenous movements with external

command; TASK D: endogenous movements with self-command.

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The Hand � Task � Distractor � Participant interaction was also signifi-cant, F(6, 30) ¼ 94,320, p , .0001. We found a significant effect of the pres-ence of distractor stimuli influencing the performance of the patient’s AH. Apost hoc test (Newman-Keuls) showed that the response times of AC’s rightAH in conditions 4 and 6 were slower than in all the other conditions (p , .05for all comparisons). Condition 4 assessed endogenous movements (with dis-tractor stimuli) without aid and condition 6 assessed sequential movementsunder external verbal command with distractors. In this last condition theimprovement of the accuracy induced an increase of the response times.The response time appears to be an important index of motor interference.

DISCUSSION

This is the first study showing the rehabilitative potential of verbal commandto improve sequential movements in a patient with AH. Notably, the presentresults show that the patient’s ability to make sequential movements using hisAH improves under verbal command, both personal and external.

We confirmed that in patients affected by AH syndrome simple exogenousmovements are preserved while endogenous movements are impaired (Kriti-kos et al., 2005), particularly in the presence of distractors. Our results showthat AC was capable, with his AH, of performing reaching movementstowards a single visual target (with or without distractors) flawlessly (exogen-ous movements). Nevertheless, he had some difficulties in performing move-ments in the correct sequence (endogenous movements); these difficultiesincreased if distractors were present.

AC’s right AH was abnormally perseverative. Perseveration is a hallmarkfeature of the AH syndrome that shows a specific difficulty in inhibiting auto-matic responses to distractor stimuli presented near to the hand (Giovannettiet al., 2005). The errors in endogenous movements reflect impairments inselecting targets that are congruent with planning sequential movement:sometimes AC selected the same position, in other instances he touched thesame target (X) more times than necessary, regardless of its position.Annoni, Pegna, Michel, Estate, and Landis (1998) distinguished betweenrecurrent perseverations (repetition of a previous response to a subsequentstimulus) and continuous perseverations (abnormal prolongation of acurrent activity) as two different aspects of motor intentional disorders. ACshows both types of perseveration: when he selected the same spatial positionon the screen he produced continuous perseverations, whereas when hetouched the same target more than once he produced recurrent perseverations.

The results of this present research show that the motor control of an AH canimprove with verbal commands. However, the accuracy improvement in theexternal verbal command condition (condition 6) was coupled with a

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considerable slowing of response times. This slowing occurred when the patienthad to move his AH in a predefined sequence in the presence of distractors. Theverbal commands guided the hand towards a visual target in the correct sequenceand the distractor stimuli were always placed in a different position on thescreen. We suppose that the slowing of response times was due to the presenceof two conflicting external stimuli (visual and verbal). The presence of these twoconflicting stimuli produced an increase of response times due to a greater con-scious motor control. This slowing did not occur in the condition of sequentialmovements with distractor and personal verbal command (condition 8).

The SMA, the key area damaged in AH, plays a major role in the initiationand control of at least some kinds of voluntary movement in man, and theverbal command could help the planning of voluntary movements. Forexample, a positron emission tomography (PET) study (Albani et al., 2001)with patients with Parkinson’s disease (PD) showed that repetitive joystickmovements activated the contralateral SMA and the cerebellum bilaterally.However, when the SMA was assumed to be damaged (PD patients withgait disorders), the contralateral Broca’s area, the contralateral sensorymotor cortex and the ipsilateral cerebellum were activated. The authors main-tained that PD patients with gait disorders and presumably functional SMAdamage have to rely on an internal verbal cue to control the output of the joy-stick movements. Similarly positive results were obtained with the use ofexternal verbal prompts in cases of unilateral motor neglect after frontallobe lesions (Laplane & Degos, 1983). The authors described the dissociationbetween voluntary and automatic movement: normally these patients showunderuse of one side of their body and verbal aids (external command orself-command) seems to be effective in improving the motor control of theaffected limb. The strict connection between language control, semantic infor-mation and programming and execution movement has also been observed inhealthy people (e.g., Kroliczak, Westwood, & Goodale, 2006). In their exper-iment, participants had first to name objects, then reach for the same or differ-ent objects: a congruent cue enhanced performance indicating a preparatoryeffect, whereas an incongruent cue significantly slowed down the reaching.

In conclusion, our results support the hypothesis that the capacity to useverbal command is one of the preserved mechanisms for intermittentvoluntary control in patients with AH syndrome and lesions of the SMA.

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