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Dissociations and similarities in motor intention and motor awareness: the case of anosognosia for hemiplegia and
motor neglect
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DOI:10.1136/jnnp-2012-302838
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Garbarini F; Piedimonte A; Dotta E; Pia L; Berti A. Dissociations and
similarities in motor intention and motor awareness: the case of anosognosia
for hemiplegia and motor neglect. JOURNAL OF NEUROLOGY,
NEUROSURGERY AND PSYCHIATRY. 84 (4) pp: 416-419.
DOI: 10.1136/jnnp-2012-302838
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http://jnnp.bmj.com/cgi/doi/10.1136/jnnp-2012-302838
When citing, please refer to the published version.
Link to this full text:
Dissociations and similarities in motor intention and
motor awareness: the case of anosognosia for
hemiplegia and motor neglect
Francesca Garbarini, Alessandro Piedimonte, Manuela Dotta, Lorenzo Pia,
Anna Berti
ABSTRACT
Objectives To confront m otor awareness in anosognosia
for hemiplegia (AHP), w here paralyzed patients deny their m otor im pairm ent, and in m otor neglect (M N), w here non-paralyzed patients behave as if they w ere paretic.
M ethods Eight right-brain-dam aged-patients,
4 hem iplegic (2 w ith and 2 w ith o u t AHP) and 4 non- hemiplegic (2 w ith only perceptual-neglect and 2 w ith also M N) w e re evaluated w ith a bimanual m otor battery, before and after examiner's reinforcem ent to use the contralesional limb. The requested bimanual m ovem ents could be either sym m etric or asym m etric, either intransitive or transitive (w ith /w ith o u t objects). W e compared the examiner's evaluation of patients' perform ance w ith the patients' self-evaluation of their ow n m otor capability (explicit knowledge). W e also evaluated the presence/absence of com pensatory unimanual strategies that, if present, suggests im plicit knowledge of the m otor deficit.
Results W e found significant differences between
conditions only in M N patients, w hose perform ance w as better after the examiner's reinforcem ent than before it, during sym m etric than asym m etric m ovem ents and during intransitive than transitive m ovem ents. As for m otor awareness, w e found a lack of explicit and im plicit knowledge in both AHP and M N patients.
Conclusion Although different in term s of motor
intention and m otor planning, AHP and M N are both characterised by anosognosia for the m otor im pairm ent.
Som etim es described as ‘pseudo-hem iplegia’, m otor neglect (M N) is characterised by a spontaneous underuse o f the contralesional lim b w ithout any m otor deficits. N o tab ly w hen the exam iner actively encourages the patient to use the affected lim b (exam iner’s reinforcement), norm al m ove m ent and strength are observed.1 From a clinical point of view, M N represents an antithetic pathology w ith respect to anosognosia for hemi plegia (AHP) in w hich patients, not aware of their m otor im pairm ent, approach everyday actions as if they could use both limbs.
Recently,2 w e described a dissociation betw een M N and AHP in term of m otor intention, using a bim anual m otor task in w hich patients were asked to sim ultaneously draw lines w ith one hand and circles w ith the other hand. In AHP patients, w ith impaired m otor execution but spared m otor intention,0 w e found that the trajectories of the
intact hand were influenced by the intended but not executed m ovem ent of the paralysed hand and tended to assum e an oval shape (coupling effect). By contrast, M N patients, w ith spared m otor execution but dam aged m otor intention, did not show these bim anual constraints.
The aim of the present study w as to exam ine the relationship betw een M N and AHP in term of motor a w aren ess, by using a bim anual m otor battery where both explicit and im plicit aspects of aw are ness were evaluated. It is w orth noting that w hen M N patients are asked to perform bim anual m ovem ents they only perform ipsilesional hand m ovem en ts,1 show ing an overt m otor response similar to th at of AHP patients. The explicit m otor aw areness w as tested through a verbal task com paring the exam in er’s evaluation of the p atien ts’ bim anual performance w ith the p atien ts’ self-evaluation. Im plicit aw areness w as, instead, inferred by the w ay in w hich patients approached bim anual actions.4 The assum ption w as that the presence of an im plicit aw areness is verified if patients approached bim anual tasks planning to use only one lim b (unim anual strategies), show ing covert knowledge of their m otor im pairm ent. On the contrary, im plicit unaw areness is verified if patients approached bim anual actions as if they could use both limbs.
METHODS Participants
We recruited eight right-brain-damaged patients: four hemiplegic patients, tw o w ithout (HP) and tw o w ith anosognosia (AHP); and four patients w ithout hemiplegia, tw o w ith only neglect (N) and tw o w ith also M N . Neurological/neuro- psychological assessm ent is sum m arised in online supplem entary figure 1A. Patients’ lesional m apping is showed in online supplem entary figure IB.
Experimental task
A bim anual m otor battery, containing either sym m etric or asym m etric, intransitive or transitive (w ith/w ithout objects) m ovem ents (see details in figure 1A), w as adm inistrated before and after the exam iner’s reinforcement to use the contralesional limb. We evaluated the p atien ts’ ability to perform the bim anual m ovem ents w ith a score ranging from 0 to 2 and w e asked the patients a self-eval- uation judgem ent using the sam e score:
Movement* example*
Bimanual movements list
Sym m etric without ob jects:---1. T o clap the hands
2. T o opcn/closc both hands
3. T o lift up both arms
4. T o tapping on the table with both index fingers
Sym m etric w ith objects: ---1. T o lift up a tray with both hands
2. T o open a cupboard with both hands
3. T o grasp two pencils with both hands
4. T o reach the exam iner's arm s w ith both hands
Asym m etric without objects: | 1. T o bend one arm while extending the other
2. T o touch the table with each hand using alternate rhythm
3. T o lift up one arm while moving to the side the other
4. T o tap with one Index finger while closing the other hand
Asym m etric with objects: j 1. T o open a bottle
2. T o close a t-shirt clasp
3. T o open an umbrella 4. T o tie a knot MN7
HI
c s jm
REINFORCEMENT ASYM SYM SYMMETRY W ITH W ITHOUT 20 1 1.9 1.8 1.7 1.6 1.5 1.4 1,3 _ 1.2 <N é 11 § ,o ? 0.9 > 0.8 UJ 0.7 0.8 0.5 0.4 0.3 0.2 0.1 0.0 SYM ASYMPRE POST AHP MN
Figure 1 (A) Bimanual motor battery. (B) Examiner’s evaluation of motor neglect (MN) patients’ performance during different experimental conditions of the bimanual motor battery: pre-examiner’s and postexaminer’s reinforcement; asymmetric and symmetric movements; movements w ith and w ithout object. (C) Crucial contrast between sym m etric-with- and sym m etric-without-object movements and asymm etric-with- and asymmetric- w ithout-object movements in both pre-examiner and postexaminer’s reinforcement conditions. (D) Comparison between examiner’s evaluation and patient’s self-evaluation: explicit motor unawareness in AHP and MN patients.
0 = left hand m ovem ent w as not performed;
1 = left hand m ovem ent w as performed but n o t at the same tim e of the right hand m ovem ent;
2 = left and right hand m ovem ents w ere sim ultaneously performed.
W hen the left hand m ovem ent w as n o t performed, w e also evaluated the presence/absence o f com pensatory unim anual strategies.
RESULTS
In all conditions, b o th HP and AHP patients received from the exam iner the m inim um score (0), w hile N patients the m axim um score (2). We found significant differences betw een conditions only in M N patients. As show n in figure IB , the M N p atien ts’ perform ance w as better (a) after the exam in er’s rein forcem ent th an before it; (b) during sym m etric th en asym m etric m ovem ents; and (c) during ‘w ith o u t’ than ‘w ith ’ o b ject m ove m ents (W ilcoxon test, for each com parison, W (8 )= 3 6 , Z = 2 .5 , p = 0 .0 1 ). Furtherm ore, as show n in figure 1C, before the exam in e r’s reinforcem ent, w e found a significant difference betw een sym m etric-w ith- and sym m etric-w ith o u t-o bject m ovem ents
w hile, after the exam in er’s reinforcem ent, w e found a significant difference betw een asym m etric-w ith- and asym m etric-w ithout- o b ject m ovem ents (for each com parison, W (8 )= 2 8 , Z = 2 .3 , p = 0 .0 1 ). We also found a significant difference betw een the
exam iner's evaluation and the patients' self-evaluation b o th w ith in AHP patients (W (8 )= 3 6 , Z = 2 .5 , p = 0.01) and w ith in M N patients (W (6 )= 2 1 , Z = 2 .2 , p = 0 .0 3 ), suggesting th at th ey both w ere ‘exp licitly ’ n o t aware o f the lack of their contralesional m ovem ents (see figure ID ).
We also calculated the presence/absence of com pensatory unim anual strategies. We only found them in HP patients, suggesting th at bo th AHP and M N patients were also ‘im plic itly ’ unaw are of the lack of their contralesional m ovem ents (see table 1).
DISCUSSION
O ur results showed that, although AHP and M N are dissociated in term s of prim ary m oto r capabilities and o f m otor in ten tion ,2 M N patients can be unaw are o f their m otor abnorm alities in a sim ilar w ay as AHP patients. T h is sim ilarity contributes to m ake som ehow difficult the clinical d istinction betw een the tw o
Table 1 Presence/absence of compensative unimanual strategies: im plicit4 motor unawareness in AHP and MN patients
Movement Compensatory strategy CS patients No compensatory strategy NCS patients
To clap hands Placing the affected hand open on the table and clapping w ith the unaffected one
H PpI; HPp2 Moving only the unaffected hand as if also the affected hand w as clapping
AHPp3; AHPp4; MNp7; MNp8
To lift up a two-handle tray
Placing the unaffected hand below and in the middle of the tray
H PpI; HPp2 Grasping one handle w ith the unaffected hand as if the affected hand was grasping the other
AHPp3; AHPp4; MNp7; MNp8
To open a bottle Placing the bottle between legs and then opening it w ith the unaffected hand
HPpI; HPp2 Holding the top w ith the unaffected hand and turning it as if the affected hand was holding the bottle
AHPp3; AHPp4; MNp7; MNp8
To close a t-shirt zip Placing the t-shirt extrem ity between legs and then close the zip w ith the unaffected hand
HPpI; HPp2 Trying to close the zip w ith the unaffected hand as if the affected hand was holding the t-shirt extrem ity
AHPp3; AHPp4; MNp7; MNp8
To open an umbrella Placing the handle between legs and then opening the umbrella w ith the unaffected hand
HPpI; HPp2 Trying to open the umbrella w ith the unaffected hand as if the affected hand was holding the handle
AHPp3; AHPp4; MNp7; MNp8
To tie a knot Placing the string on the table and tying a knot using only the unaffected hand
HPpI; HPp2 Holding one end of the string w ith the unaffected hand and trying to tie a knot as if the affected hand was holding the other end
AHPp3; AHPp4; MNp7; MNp8
Neglect patients were not included because they actually performed all bimanual movements proposed (In each condition score = 2). Only six out of 16 bimanual movements have been considered: for the other 10, alternative unlmanual strategies were not possible.
AHP, anosognosla for hemiplegia; CS, compensatory strategy; MN, motor neglect; NCS, no compensatory strategy.
syndromes. Here, w e propose th at the lack of knowledge for m otor problems m ay depend on the im pairm ent at different levels o f the chain o f m oto r events described by the com puta tional model o f m otor con trol.5 C onceptualising m otor aw are ness w ith in this model, anosognosia in AHP patients can be ascribed to a damage at a com parator system th at, in norm al conditions, com pares m ovem ent anticipation w ith the feedback com ing from m ovem ent execution.6 Because o f the brain lesion, the com parator cannot d etect the m ism atch betw een intended but n ot executed m ovem ents, causing the p atien t’s unawareness of the m otor deficits. However, the norm al activ ity o f the structures im plem enting m otor in ten tio n ality gives rise to the subjective feeling of m ovem ent th at AHP patients (erroneously) report experiencing. O n the contrary, the m otor unawareness showed by M N patients can be explained by brain lesions involving the intention-program m ing-system netw ork. In this perspective, M N patients, because o f the in ten tio n ality impair m ent, do n ot attem p t any m ovem ent and, therefore, cannot discover the abnorm ality o f their behaviour (see also7). Inter estingly, our AHP and M N patients did n o t show any dissocia tion betw een explicit and im plicit anosognosia (but see4 8 for different findings), indicating the presence of a severe and pervasive deficit o f awareness.
T h is interpretation is in keeping w ith our anatom o-clinical data. Indeed, AHP patients had lesions affecting som e structures (AHP-P3: pre-m otor; AHP-P4 insular areas) o f the proposed com parator system ,0 w hile sparing the intention-program m ing- system netw ork; on the contrary, M N patients had lesions m ostly involving th at n etw ork (M N-P7: inferior parietal areas;9 M N -P8: pre-frontal areas10). Interestingly, HP and AHP patients, w ith prim ary m otor deficits, had lesions involving subcortical structures (basal ganglia and internal capsule) typically associ ated w ith lim b paresis, w hile in N and M N patients these structures were spared (see online supplem entary figure IB). It m u st be noted th at, due to the small size of our sample, further studies are needed in order to reach definite anatom ical conclusions.
From a behavioural point of view, w e confirmed the role of the exam in er’s verbal reinforcem ent1 in determ ining the im prove m en t o f M N p atients’ perform ance. T h is suggests th at m otor unawareness due to lack of m otor in ten tio n (as in M N ) is less
severe than m oto r unawareness due to a direct damage to the com parator system (as in AHP).
Furtherm ore, our results show for the first tim e a dissociation betw een sym m etric and asym m etric m ovem ents in M N p atien ts’ perform ance. Previous neuroim aging evidence11 suggested th at the (left) dom inant hem isphere would play a dom inant role in bim anual sym m etric m ovem ents, whereas the (right) non-dom inant fronto-parietal n etw ork exerts its key role during the execution of bim anual asym m etric m ovem ents. H ence, w hen our right-brain-dam aged M N patients were requested to perform a sym m etric m ovem ent, the (intact) dom inant hem isphere allowed m ovem ent execution, whereas w hen the requested m ovem ent w as asym m etric the (lesioned) non-dom inant hem isphere w as n ot able to plan it correctly. This hypothesis is in accordance w ith previous dem onstration o f M N p atien ts’ failure to inhibit ipsilesional lim b m otor plans.12 If m oto r planning for the left arm is intruded by m ovem ent plans for the right arm, the sym m etric m ovem ents w ill be facilitated and the asym m etric m ovem ents w ill be impaired.
We also described here a specific M N p atients’ deficit in ecological interactions w ith objects. Indeed, intransitive m ove m en t w as performed better than transitive m ovem ents. This m ight be explained by lesions affecting fronto-parietal circuits underpinning grasping fu n ctio n s.10 It is interesting to note that, w hile sym m etric-w ith -o bject m ovem ents improved after the exam in er’s reinforcem ent, asym m etric-w ith-ob ject m ovem ents w ere the only conditions in w h ich M N patients did n o t improve their perform ance. Indeed, before the exam in er’s reinforcem ent, the p atien ts’ perform ance w as significantly w orse in sym m etric- w ith - than in sym m etric-w ith o u t-ob ject m ovem ents, w hile, after the exam in er’s reinforcem ent, no difference w as found. O n the contrary, for the asym m etric m ovem ents, before the exam in e r’s reinforcem ent there w as no difference betw een w ith - and w ith o u t-o b ject m ovem ents (patients’ score w as low in bo th conditions) w hile, after the exam in er’s reinforcem ent, p atients’ scores were significantly low er in asym m etric-w ith- than in asym m etric-w ith o u t-ob ject m ovem ents. It is w o rth noting th at although proxim al m ovem ents (shoulder) can be mediated by the ipsilateral cortex more than distal m ovem ents (fingers),14 we did not find any difference in proxim al versus distal m ovem ent execution (both tested in our bim anual battery).
Finally, our study m ay also provide som e helpful hints for 2. rehabilitation of M N p atien ts’ m otor disability indicating the im portance of focusing p atien ts’ atte n tio n on m otor awareness through verbal reinforcem ent and by m eans o f bim anual 4.
sym m etric m ovem ents w hich, being preserved in M N patients, m ay help in recovering contralesional m otor functions.
6.
A cknow ledgem ents The authors appreciate the help given by Dr Anna Cantagallo
in recruiting neurological patients. The authors also acknowledge Dr Sara Bochicchio
for her help in collecting data.
7-Contributors FG, AP and AB designed the study. LP conducted patients' lesion
mapping. FG and MD selected the patients, gathered behavioural data and collected 8. the instrumental data. AP and FG conducted statistical analysis. FG, AP, LP and AB interpreted the data. FG and AB w ro te the paper. All authors reviewed the first draft of
the paper. 9.
Funding Professor Anna Berti received a grant (PRIN project) from the Italian M inistry iq
of University and Research.
Competing interests None. ^
P atien t consent Obtained.
Ethics approval Ethics approval provided by the Local Ethical Commitee. 12
Provenance and peer re v ie w Not commissioned; externally peer reviewed.
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