Is Grasping Impaired in Hemispatial Neglect?

Behavioural Neurology 13 (2001/2002) 17–28 17 IOS Press

Is grasping impaired in hemispatial neglect?

Monika Harveya,∗, Stephen R. Jacksonb, Roger Newportb, Tanja Kramer¨ a, D. Llewlyn Morrisc and Lindsay Dowd aDepartment of Psychology, University of Glasgow, Glasgow, UK bSchool of Psychology, University of Nottingham, Nottingham, NG7 2RD, UK cCentre for Perception, Attention, and Motor Sciences, University of Wales, Bangor, Gwynedd LL57 2DG, UK dCare of the Elderly, Frenchay Hospital, University of Bristol, BS8 1PN, UK

Abstract. Patients with right unilateral cerebral stroke, four of which showed acute hemispatial neglect, and healthy aged-matched controls were tested for their ability to grasp objects located in either right or left space at near or far distances. Reaches were performed either in free vision or without visual feedback from the hand or target object. It was found that the patient group showed normal grasp kinematics with respect to maximum grip aperture, grip orientation, and the time taken to reach the maximum grip aperture. Analysis of hand path curvature showed that control subjects produced straighter right hand reaches when vision was available compared to when it was not. The right hemisphere lesioned patients, however, showed similar levels of curvature in each of these conditions. No behavioural differences, though, could be found between right hemisphere lesioned patients with or without hemispatial neglect on either grasp parameters, path deviation or temporal kinematics.

1. Introduction The areas of the human brain that control prehension are not defined in detail and patients with focal lesions Prehension requires the integration of visual and primarily affecting prehension seem to be rare [18,19]. somatosensory information into a co-ordinated motor One of the first researchers to highlight a specific grasp- plan for transporting the arm to a target while shaping ing impairment as a result of bilateral posterior parietal the hand to match the target geometry. The role of vi- lesions was Rudolf Balint´ [1]. He described the dis- sion in grasping is not only to activate proper schemas order as ‘optic ataxia’, a specific deficit of the visual and specify the composition of the fingers but also to control of movement unrelated to motor, somatosensory, visual acuity or visual field deficits. More re- determine the relative positions of the hand and the ob- cent studies into the visuomotor behaviour of humans ject to be grasped, as accurate positioning of the fingers have confirmed Balint’s observation. Jeannerod [17] on the object surface are a prerequisite for the subse- and Perenin and Vighetto [31] reported patients with quent handling and manipulation of the object. The parietal lesions whose reaching movements proved information of the grasp before contact with the object accurate, often erred in one direction and were also is therefore the critical factor that governs the move- kinematically altered, with increased movement dura- ments of the other segments of the upper limb during tions and lower peak velocities. Additionally, during the reach (see [20] for review). Although reach and prehension of objects the finger grip proved too wide, grasp can be described as separate subsystems [18,19], with either no or poor preshaping and the grasp clos- studies of reaching in isolation from grasping ignore ing on contact with the object only, a finding replicated many of these key aspects of its control. more recently by Jakobson et al. [16]. It thus seems that lesions that do affect goal-directed behaviour are

∗ most commonly centred in the posterior parietal lobe Corresponding author: Dr. Monika Harvey, Department of Psy- and indeed imaging studies [11,37] conﬁrm this. In chology, 58 Hillhead Street, Glasgow, G12 8QB, UK. Tel.: +44 141 330 6174; Fax: +44 141 330 4606; E-mail: M.Harvey@ fact, a recent study by Binkofski et al. [2] that inves- psy.gla.ac.uk. tigated grasping behaviour in patients with parietal le-

ISSN 0953-4180/01/02/$8.00  2001/2002 – IOS Press. All rights reserved 18 M. Harvey et al. / Is grasping impaired in hemispatial neglect? sions showed that patients with lesions of the anterior the reach trajectory, as well as a larger terminal error part of the intraparietal sulcus had distinct impairments for the right hemisphere lesioned patients, were found in grasping. Moreover, these lesion data were supple- only in the absence of visual feedback but not in the mented by functional MRI data showing specific acti- closed loop pointing and bisection tasks. Although one vation of this area during grasping in normal subjects. might be tempted to explain the differences between the Patients suffering from hemispatial neglect after two studies in terms of patient population (Goodale’s right hemisphere lesions, usually to the parietal lobe patients had recovered from neglect but Harvey’s pa- (although frontal and subcortical structures have been tients had never shown any sign of it) this interpretation shown to be involved as well [38]), unsurprisingly also seems unlikely in view of a recent result by Karnath show a characteristic disturbance of visuospatial be- and colleagues. For the first time Karnath et al. [22] haviour. They typically demonstrate a deficient re- actually tested acute neglect patients, as well as right sponse to stimuli located contralaterally to the lesion hemisphere lesioned patients without neglect, with a and fail to explore the contralesional space with ei- simple pointing task and found no evidence of a right- ther eye or limb movements. Despite these striking vi- ward bias in the reach trajectory neither in the closed suospatial impairments the substantial majority of ex- nor the open loop condition. In fact, neither patient isting research into hemispatial neglect has been con- group varied from the healthy controls in terms of ei- cerned with the biased selection of ipsi-over contrale- ther reach deviation or final accuracy. This finding sional input (see [33] for review). Although a number seems surprising in the light of the severe visuospatial of investigations have looked at reaction and movement disturbance these patients generally experience. How- times towards points and objects in the contralesional ever, a similarly good result was found by Chieffi and hemispace, and have generally found these to be in- colleagues [4] in a grasping experiment in which a re- creased in hemispatial neglect (see [25] for review), covered neglect patient showed normal reaching and only very few studies to date have examined the visuo- grasping towards single objects. Only when distractor motor output patterns of these patients, i.e., their reach- objects where presented simultaneously to the right of ing and grasping parameters in terms of reach trajectory the target, did she show a rightward deviation of the and grasp kinematics. This lack of investigations is wrist trajectory, her grip aperture, however, was never striking since there is now abundant evidence that per- affected. This last finding was also repeated in an ex- ceptual processes in humans and many other species are periment by Pritchard et al. [32] whose acute neglect tightly constrained by the kinds of responses they con- patient showed normal grip aperture towards targets of trol (see [26,27] for review). Studies that have in fact different sizes. Unfortunately reach trajectory was not directly investigated pointing and grasping behaviour reported in this study. in hemispatial neglect have revealed partly diverging The main objective of the present study was thus to results: clarify the issue of goal-directed behaviour in hemispa- In 1990, Goodale and colleagues [9] investigated vi- tial neglect. Are these patients impaired while grasping sually guided pointing in right hemisphere lesioned pa- for single objects in right and left space? It is inher- tients who had recovered from neglect. Patients were ently difficult to accurately assess hemispatial reach- asked to point either midway between two lights or di- ing and grasping differences in a neglect population rectly on top of a single light. It was found that all as hemiplegia prevents left hand movements in almost patients made large rightward directional errors at the all the cases. However, it has been clearly shown that outset of the reach. These initial errors were observed ipsi-and contralesional reaches differ in terms of their not only in bisection, but also in simple pointing; how- mechanics [3]. It is thus difficult to disentangle these ever they were more poorly corrected in the bisection mechanical hemispatial from visuomotor effects unless task, so that the final rightward errors remained much reaches are performed to identical positions under dif- larger than those seen in pointing. A related study on ferent feedback conditions [12,22,15]. Both the Chieffi pointing and bisecting (this time including open loop et al. [4] and Pritchard et al. [32] studies indicate that reaches) was run by Harvey et al. [12] using a wider there might not be hemispatial grasping effects but then sample of right-and-left hemisphere lesioned patients, only single cases were studied and none of the condi- none of them revealing signs of hemispatial neglect at tions required an open loop grasp. Secondly, even if the time of testing (only two right hemisphere lesioned the grasp component is intact, will the path curvature patients had ever shown any sign of neglect). In con- prove unbiased as shown by Karnath and colleagues? trast to the results of Goodale et al. rightward biases in We thus asked four neglect patients to grasp towards M. Harvey et al. / Is grasping impaired in hemispatial neglect? 19 objects in right and left hemispace, either with or with- fects [4,32] and would have resulted in too many trials out visual feedback of the hand and measured their and independent variables. grasp kinematics as well as their path curvature and Subjects began each trial with their hand placed flat velocity profiles. Performance was compared to right upon the starting position, oriented along the saggital hemisphere lesioned patients without neglect as well as plane, and with their thumb closed against their index to matched healthy controls. finger. All subjects executed four types of prehension movements: unimanual near and far reaches in right hemispace and unimanual near and far reaches in left 2. Method hemispace. To control viewing conditions, subjects wore a set 2.1. Subjects of glasses that were fitted with liquid crystal lenses throughout the experiment (Plato Systems, Translucent Two groups of subjects were tested: 7 patients with Technologies Inc.). It is important to note that occlu- unilateral right hemisphere infarct [R CVA] (mean age sion with these lenses does not significantly decrease = 68, SD = 9.7, 5 male, 2 female), four of which levels of illumination to the eye. Each trial commenced showed evidence of hemispatial neglect at the time of with the glasses clearing. On half the trials the glasses testing when assessed with the BIT [40] and 5 normal control subjects (mean age = 68, SD. = 5.7). Ethi- remained clear throughout the reach (binocular view- cal approval had been given by Frenchay Healthcare ing). On the remaining trials vision was occluded again Trust and all subjects gave their informed consent to at movement onset, i.e., as soon as the subject lifted the participate in the experiment prior to testing. All sub- fingers from the start block (open loop condition). jects in the two patient groups had suffered cerebrovas- Each subject completed six trials towards each of the cular accidents within the previous 43 months of test- four target locations (24 trials) in both the open and ing. CT scans were available on all the patients, and closed loop conditions thus performing a total of 48 none of these aroused any suspicion of bilateral dam- trials. Testing was done in four blocks of 12 trials with age. All subjects were right handed and it was ensured blocked presentation of open and closed loop trials to that none of the subjects in the control group had any avoid fatigue and allow breaks between blocks. Order appreciable medical, neurological or psychiatric his- of presentation of trials for each block was individu- tory. There were no significant differences between the ally randomised for each subject and presentation of control group and the patient group in age or education blocks balanced across patients and controls. Subjects (mean R CVA = 9.8 years, SD = 5.8; mean controls = were instructed to reach at normal speed and maintain 10.6 years, SD = 1.4). Clinical and neuropsychological accuracy. A brief practice session for both open loop details of all the patients are listed in Table 1. and binocular viewing conditions was conducted prior to the presentation of the experimental sessions. 2.2. Apparatus and procedures

Subjects were seated at a 1000 mm square table and 2.3. Movement recording and data analysis – from a fixed starting position, that was indicated by a T-shaped mark 3 cm tall by 4 cm wide, placed cen- trally in front of them – executed prehension move- Hand movements were recorded using a MacReflex ments toward target objects presented in the frontal infra-red motion-analysis system (Qualisys Inc.) with × plane (red wooden dowels 50 mm high with a diame- a sampling rate of 50 Hz. 5 mm 5 mm reflective ter of 22.5 mm). None of the patients could use their markers were placed on the distal portion of the thumb- contralesional hand so only ipsilesional reaches were nail, on the distal portion of the index finger and on the tested. The control subjects used their right hand also. wrist of the right hand. An additional marker was also Targets were placed at one of four locations, two fixed to the target object. The 3D spatial co-ordinates to the left and two to the right equidistant (100 mm) of these markers were analysed off-line using custom from the subject’s mid-saggittal axis positioned at ei- software with Labview (National Instruments Inc.) and ther 200 mm (near) or 250 mm (far) from the starting Matlab (The Mathworks Inc.) programming environ- position. Target size was not manipulated as this had ments. Data were low pass filtered using an 4th-order been done in previous studies with no significant ef- Butterworth filter (cut-off frequency of 10 Hz). 20 M. Harvey et al. / Is grasping impaired in hemispatial neglect?

Table 1 Clinical data for the three patient groups. BIT-Score:Total score achieved in the Behavioural Inattention Test, conventional subtests (max. score 146, cut off 129) Patients Lesion Post- Hemianopia Neglect BIT-Score stroke (Cut off (days) 129) D.K. R temporo-parietal 1340 No Yes 115 E.R. R fronto-temporal 196 No Yes 116 L.C. R occipital, inferior-temporal, 570 Yes Yes 115 basal ganglia M.B.H. R temporo-parietal 857 No Yes 125 E.E. R temporo-parietal 197 Yes No 133 A.W. R fronto-parietal 633 No No 135 M.A.H. R superior parietal 195 No No 140

2.4. Dependent measures the hand path curved leftwards or rightwards, are positive. As leftward and rightward movements can often Kinematic and hand path parameters were calculated show a roughly mirror symmetric curvature, we also for each hand separately. Movement onset was defined carried out analyses to examine the sign of the hand as the first frame in which the wrist marker exceeded path curvature (HPC) in both the controls and patients, a velocity of 25 mm/s in the direction of movement. assigning positive values for rightward curving hand Movement end-point was defined as the first frame in paths and negative values for leftward curving hand which displacement of the target marker exceeded 1.0 paths. mm in any direction. 1. Movement duration (MD) was The following dependent measures were computed defined as movement end-point minus movement on- from the 3D co-ordinates for the wrist marker, and were set. The following dependent measures were computed used to analyse the kinematics of the transport phase: from the 3D co-ordinates for the markers placed on the 5. Peak velocity in the direction of movement (PV) thumb, index finger and wrist, and were used to anal- and, 6. the deceleration phase measured as the time yse the kinematics of the grasp phase of the prehension from peak velocity to endpoint as a percentage of the task: 2. Peak grip aperture (PGA) between index finger total movement duration (DT%). and thumb (measured in mm). 3. The time taken to 2.5. Statistical analyses reach PGA as a percentage of total movement duration (TTPGA%). 4. To calculate a hand path curvature Two sets of ANOVA’s were performed on each of index (HPC-index) subjects’ hand paths were spatially the dependent measures. The first set compared the resampled and translated (see also Jackson et al. [15] RCVA group with the controls using their right hand for a description of this procedure). Spatial resampling (mixed 4-way ANOVA with Group, Loop, Hemispace was carried out to produce hand paths which each con- and Distance as the factors). For the final analysis the tained 100 equally spaced spatial segments, thereby al- RCVA group was further split into patients with acute lowing comparisons between movements. The spatial neglect (RCVAN+) and the rest (RCVAN−) and again resampling did not change the shape of each individual compared to the controls using their right hand. Since hand path, and did not result in the normalisation of this ANOVA yielded no differences between patients movement amplitude. Hand paths were also translated with and without neglect on any of the dependent mea- spatially so that movements to different target locations sures, these results will be reported in a complementary within the workspace could be compared. This pro- manner only. cedure resulted in a set of hand paths aligned along a single axis. The HPC-index consisted of the ratio between the magnitude of the maximum lateral deviation 3. Results achieved at any point during the movement (mm), and the straight line joining the kinematically-determined 3.1. Trajectory and grasp phase kinematics start and end positions of the movement (mm). Note that the HPC-index produces a measure of hand path 3.1.1. Peak Grip Aperture (PGA) curvature that is (a) independent of movement ampli- Overall the maximum grip aperture of the patients tude, and, (b) in which all values, regardless of whether (means: RCVA N+=93 mm, SD = 10.8; RCVA M. Harvey et al. / Is grasping impaired in hemispatial neglect? 21

130 Binocular Viewing 120 Open Loop

110

100

Peak Grip Aperture in mm Peak Grip 70

60 R CVA (+) R CVA (-) Controls

Fig. 1. Overall Peak Grip Aperture for the R CVA patients with and without neglect (R CVA (+), R CVA (−)) and the control group using their right hand. Error bars indicate SE’s.

N− = 93mm, SD = 10.6) did not differ from the 3.1.3. Hand path curvature (HPC) and hand path aperture shown by the controls (mean = 97.3 mm, SD curvature index (HPC-index) = 17.8) on any of the ANOVA’s (Fig. 1). Only viewing Looking at the hand path curvature (HPC) is was condition affected the opening of the hand with the found that grasping movements made with the right maximum grip aperture proving larger in the open than hand resulted in rightward curvatures. This proved the the closed loop condition for all subjects (RCVA’s vs case for patient and control groups over all locations Controls, F (1, 10) = 58.9,p<0.001). and distances (Fig. 2). With regard to the HPC-index, the ANOVA com- 3.1.2. Percentage of Time taken to reach PGA paring the RCVA group with the controls revealed a (TTPGA%) significant Group by Viewing Condition interaction Similarly to PGA there were no group effects with (F (1, 10) = 6.9,p =0.02). Further analyses showed regards to the time taken to reach maximum peak grip that the RCVA group showed curvature of similar mag- aperture on any of the ANOVA’s (means: RCVAN+= nitude on both open and closed loop conditions whereas 76%, SD = 20.3; RCVA N− = 75%, SD = 12.4; the controls showed significantly less curvature under Controls right hand = 84%, SD = 6) and no other binocular viewing than open loop conditions (Fig. 3). effects were found. RCVA N+ and RCVA N- patients showed no differ- An additional attempt was made to ensure that the ences with regard to the magnitude of curvature (RCVA grasp kinematics were indeed unimpaired, by assessing N+=0.07, SD = 0.03; RCVA N− = 0.08, SD = the consistency and spatial accuracy of the subjects’ 0.03). grip orientation at the end of the reach. Since no group There was also a main effect of hemispace (F (1, 10) = effects were found for the different viewing conditions 54.75,p< 0.001) with contralateral reaches revealing in relation to the grip aperture parameters,this was done less curvature than ipsilateral reaches and a distance for binocular viewing only. The angle of the opposition effect (F (1, 10) = 27.1,p < 0.01) with near targets axis formed between the index finger and the thumb giving rise to larger curvature than far targets. These was calculated one sample (20 ms) prior to contact with effects were shown equally by patients and controls. the target object. This opposition axis was calculated by taking the angle formed between the XY position of 3.2. Velocity analyses the thumb marker and the XY position of the marker located on the index finger. 3.2.1. Movement Duration (MD) In line with the PGA data no group effects were Overall, the reaches of the RCVApatients took much found (means: RCVA N+=48◦,SD= 11; RCVA longer than those performed by the controls (main N− = 50◦,SD= 13, Controls right hand = 40◦,SD effect of group, F (1, 10) = 21.6,p =0.009), see = 9) although there was a general effect of hemispace Fig. 4. There were, however, no significant differences (F (1, 10) = 113.06) with contralateral reaches giving in movement duration between the RCVA N+ whose rise to larger opposition angles (mean: 52 ◦,SD= 12) mean duration time was 1057msec (SD = 186) and than ipsilateral reaches (mean: 35◦,SD= 10). the RCVA N− group who showed a mean duration 22 M. Harvey et al. / Is grasping impaired in hemispatial neglect?

Fig. 2. Mean Hand paths for the control subjects and the R CVA patients (RH patients) plotted separately for viewing condition (Bi = Binocular, OL = Open Loop) and hemispace).

0.1

0.09

0.08

0.07

Binocular Viewing 0.06

Hand Path Curvature Index Hand Path Open Loop

0.05 R CVA (+) R CVA (-) Controls (RH)

Fig. 3. Mean hand-path -curvature-index (HPC-index) for control subjects and RCVA patients (with and without neglect) under binocular and open loop viewing conditions. See text for HPC-index calculation. Error bars indicate SE’s. time of 1205msec (SD = 226), although both groups RCVA patients (main effect of group, F (1, 10) = were significantly slower than the control group (mean 24.2,p =0.008). There were, however, no signifi- 672 msec, SD = 168), Tukey-test. cant differences between the RCVA N+ whose mean There were also main effects of space (1,10) = 12.6, peak velocity reached 480 mm/sec (SD = 89) and the p =0.006) and distance (F (1, 10) = 85.7,p<0.001) RCVA N− group who showed a mean peak velocity of with ipsilateral reaches taking less time than contralat- 478 mm/sec (SD = 89) although they were both signifi- eral reaches and far reaches taking longer than near cantly slower than the control group (mean 919 mm/sec, reaches. SD = 198), Tukey-test. There was also a Group by Distance interaction 3.2.2. Peak Velocity (PV) (F (1, 10) = 5.9,p=0.03). Further analyses revealed Overall, the reaches of the controls reached much that target distance had no effect on the RCVA patients higher peak velocities than those performed by the whereas the controls reached significantly higher peak M. Harvey et al. / Is grasping impaired in hemispatial neglect? 23

Fig. 4. Mean Velocity profiles for control subjects and RCVA patients (RH patients) plotted separately for viewing condition (Bi = Binocular, OL = Open Loop) and hemispace (Contra = Contralateral, Ipsi = Ipsilateral). velocities for the far targets. There was also a Loop hemisphere lesioned patients showed the same amount by Hemispace interaction (F (1, 10) + 7.6,p =0.02). of curvature with and without visual feedback, whereas Planned contrasts showed that ipsilateral reaches led to the trajectory of the controls proved straighter in the higher velocities than contralateral reaches. Addition- closed loop condition. There was, however, no differ- ally contralateral reaches proved faster in the open loop ence between patients with and without neglect with than the binocular viewing condition. This was not the regard to the extent of curvature shown. case for ipsilateral reaches. Both patient groups proved markedly slower on the velocity measures of MD and PV although there were 3.2.3. Percentage of Time spent Decelerating (DT%) no differences in the velocity profiles of RCVApatients The ANOVA comparing the RCVA group with the with or without acute neglect. DT% revealed an in- controls using their right hand revealed a significant teresting Group by Loop effect. Whereas the control Loop by Distance by Group interaction (F (1, 10) = group spent less time decelerating under binocular as 11.76p =0.006). Further analyses showed that the tar- opposed to open loop viewing conditions, this was not get distance and viewing condition had no effect on the the case for the RCVAgroup suggesting that they might time spent decelerating by the patients. Target distance be less efficient in using visual guidance to home in on did also not affect the controls. The controls, how- the target, an interpretation that also fits with the lack ever, spent significantly less time decelerating under of curvature differences found between presence and binocular as opposed to open loop viewing conditions absence of visual feedback in these patients. (Fig. 5). There was also a main effect of hemispace (F (1, 10) = 7.1,p =0.02) with less time spent on deceleration in contralateral space. 4. Discussion

3.3. Summary of the main results 4.1. Grasp kinematics

As the main motivation of this study was to investi- The most interesting result of this study was the ﬁnd- gate the effects of brain damage on the control of grasping that neither peak grip aperture nor the time taken ing, discussion of the results will mainly focus on the to reach peak aperture was impaired in any of the pa- reported group effects: tient groups. Additionally grasp orientation was also It was shown clearly that neither of the two patient normal. In line with Paulignan et al. [29] we found a groups differed from the control groups in relation to signiﬁcant hemispatial effect with contralateral reaches the peak grip aperture or the grip orientation shown nor producing larger opposition axis angles than ipsilateral the time taken to reach the peak grip aperture. There reaches for both subject groups. The authors suggest was, however, an effect of path curvature in that right that prehension movements aimed at cylindrical objects 24 M. Harvey et al. / Is grasping impaired in hemispatial neglect?

45 Binocular Viewing Open Loop

Percentage of Time spent decelerating Time Percentage of 40 R CVA Controls

Fig. 5. Percentage of Time spent decelerating under binocular and open loop viewing conditions, separately for the R CVA patients (with and without neglect) and the control subjects using their right hand. Again, error bars indicate SE’s. are organised to minimise changes in the posture of though the optic ataxia patients tested by Perenin and the lower arm and that this position is thus not deter- Vighetto [31] had lesions mainly confined to the su- mined with respect to (external ) visual co-ordinates perior parietal lobe, both Jeannerod et al.’s [19] and but mainly with respect to body centred co-ordinates. Jakobson et al.’s [16] patients had lesions in both the These three findings clearly show that neglect pa- superior and inferior parietal lobes and although the tients have no problems in scaling their grip size when lesions were not mapped, we can assume that this was reaching to objects placed in near and far locations, also the case for some of the patients presented here. both in left and right hemispace. Although similar re- Chieffi et al.’s [4] patient had a subcortical and Pritchard sults have already been reported [4,32], we now report et al.’s [32] patient an occipito-temporal lesion. It is this in a group of neglect patients and also extend the thus hard to make specific anatomical predictions from finding to grasp orientation and grasping movements such diverse data and probably more useful to look at executed in the absence of visual feedback. The pos- the findings in terms of function: sibility that visuomotor grip scaling might be normal Although hemispatial neglect is typically described under open and closed loop conditions in neglect pa- as a disturbance of spatial behaviour, the main prob- tients clearly dissociates this syndrome from the ob- lem is a failure to attend to or represent objects pre- served cases of optic ataxia [16,31] and also directly sented in the contralesional space. This then results in contrasts with the behaviour of patient AT reported by a variety of symptoms, i.e., ignoring part of the objects Jeannerod et al. [19]. This patient presented a bilateral completely [5,39], misrepresenting their size [2,28] deficit in grasping simple objects, both in the presence or failing to explore or localise them adequately in and absence of visual feedback, without a concurrent space [10,21]. However, these problems may not be deficit in reaching towards the location of these objects. directly related to goal-directed behaviour. The pro- It is tempting to link the observed dissociations to gramming and on-line control of a particular action typ- varying lesion sites within the parietal lobe. Both Mil- ically requires a unique set of transformations of the ner and Goodale [27] and Perenin [30] have recently visual array, so that each component of the action can argued that lesions resulting in optic ataxia tend to lie be correctly executed with respect to the goal object. in the upper part of the parietal lobe around the intra- Thus, to fixate and then reach towards a goal object, it parietal sulcus but that the focus for neglect lies more is necessary that the location and motion of that object ventrally, in the region of the supramarginal and an- be specified in egocentric co-ordinates (that is, coded gular gyri. Indeed the previously described study by with respect to the observer). To form the hand and fin- Binkofski et al. supports this: only patients whose gers appropriately for the grasp, the coding of the goal lesions included the intraparietal sulcus showed ab- object’s shape and size would also need to be largely normalities in grasping, whereas in the three patients viewer based. Finally, since the relative position of in which this area was spared no abnormalities were the observer and the goal object will change, it is ob- found. However, although this distinction might be vious that the egocentric co-ordinates of the object’s generally acceptable, no conclusive interpretations can location and its surface and contours must be computed be made when other grasping studies are analysed. Al- on each occasion. It is possible that neglect may not M. Harvey et al. / Is grasping impaired in hemispatial neglect? 25 operate within these broad co-ordinates of egocentric of sensorimotor transformations involved in converting space, but within the internal co-ordinates of objects or visual target information into motor output to muscles, figures themselves. One interesting example of this in- although, as they also argue, the neural correlate of this ternal object representation is the metric relating sizes seems elusive. Their other explanation maintains that to weights. This ratio determines expectations when hand trajectory is determined largely at a perceptual lifting objects and there is recent evidence from normal rather than motor level. This argument is supported by subjects that grip force miscalibrations can occur when the findings that with the availability of visual feedback observers are deceived about the size of objects under of the hand, subjects maintain relatively straight hand the influence of the ‘Ponzo’ illusion [14]. However, the trajectories at the expense of curved joint trajectories experiment also showed that the opening movements and vice versa when vision is available for the joint of the fingers prior to contact with the object were not trajectories [7]. This explanation seems also likely to miscalibrated. This same dissociation holds true for hold for the data presented here. It is possible that the some neglect patients. Shaw et al. [36] who studied right hemisphere lesioned patients were less efficient in grip force calibrations in such patients found that, com- using the visual feedback possibly due to their distorted pared to controls, neglect patients dramatically over- topography of the visual representation. The lack of grip objects, especially those presented in left space. visual feedback may have thus affected them less than Two of the patients tested in that study (LC and DK) it did the controls. This relative increase in curvature were also included in this experiment and showed no in comparison to the control subjects is also consistent miscalibration of their hand opening in either right or with the Jackson et al. [15] finding who reported that left space. Although these data seem to suggest that three patients recovering from neglect showed signifi- neglect patients might be less impaired in egocentric as cantly more curved trajectories to visually over propri- opposed to allocentric coding, the path curvature data oceptively defined targets. of this experiment do not entirely fit with that interpre- On the surface, our data also seem consistent with tation (see below). Chieffi et al.’s [4] result of a normal trajectory towards A caveat also has to be made regarding the fact that single targets in conditions with visual feedback. Sim- in this experiment object size was not explicitly manip- ply looking at the closed loop condition we also found ulated. The subjects therefore did not have to rely on this, as there was no group effect. The interaction ef- the visual size of the object for the scaling of their hand fect however, is at odds with other studies. Goodale as indeed they could have used kinaesthetic memory of et al. [9] found increased rightward curvature in closed the object size. It thus has to be granted that the lack of loop pointing. We also found this but not when com- abnormalities of the grasp components may have been paring the trajectory to control data but by comparison a result of the experimental design. However, our data to the open loop condition. Both Harvey et al. [12] are in accordance with two previous studies [5,34] who and Karnath et al. [22] found that controls show similar did manipulate object size but also found no abnormal- reach trajectories in conditions with or without visual ity in the grasp aperture. feedback. Karnath et al. found this pattern in the patient subjects as well, whereas Harvey et al. found right 4.2. Path curvature hemisphere lesioned patients to make large rightward deviations under open loop. We found that our control The main finding with respect to reach trajectory subjects made straighter reaches when vision was avail- was the group by loop interaction: right hemisphere able, whereas the trajectories of the right hemisphere lesioned patients showed the same amount of curvature lesioned patients were curved to the same degree in with and without visual feedback, whereas the trajec- both conditions. Part of the differences in these stud- tory of the controls proved straighter in the closed loop ies might be explained by physiological findings that condition. Reach trajectories did, however, not differ reaches and grasps may rely on different neural subsys- between patients with and without neglect. The find- tems [24,37] and it may thus not be appropriate to com- ings of the controls are in line with Sergio and Scot- pare pointing and grasping experiments directly. This t’s [35] data who also found significantly decreased path does, however, not explain the discrepancies within the curvature when subjects grasped with visual feedback pointing experiments. These discrepancies might boil as opposed to a blindfolded condition. They give two down to differences in the individual experimental set- possible explanations for this effect, one stating that up. Maybe illumination was much lower in the Harvey hand trajectory may be explicitly defined in the series et al. [12] than the Karnath et al. [22] open loop con- 26 M. Harvey et al. / Is grasping impaired in hemispatial neglect? dition, which might have resulted in a larger disorien- ity profiles of RCVA patients with or without acute ne- tation in their patients. It is possible that the pointing glect. Not many studies looking at goal-directed be- condition in the Goodale et al. [9] study was somehow haviour in brain lesioned patients have reported veloc- harder than the one used in the other two studies. One ity profiles as well as reach trajectory and grasp kine- of the things that can be said, though, is that even if matics. No mention of temporal kinematics is made in a bias in the trajectory occurs, there is no evidence so the Goodale et al. [9], Karnath et al. [22] or Pritchard far that this bias is typical for neglect patients only. et al. [32] studies. Chieffi et al.’s [4] patient showed Like Karnath et al. [22] we found no differences in the normal execution time but then it was only a single trajectories of our neglect patients when compared to case. Harvey et al. [12] again, did not report movement the right hemisphere lesioned controls and Harvey et time. The temporal kinematics were, however, anal- al. [12] found a bias in right hemisphere lesioned pa- ysed in these patients [11] and comparable to the pre- tients without neglect. It thus seems that if there is an sented data, movement time and peak velocity proved impairment in goal-directed behaviour it is not confined longer and lower for both RCVA and LCVA groups to hemispatial neglect. when compared to the control subjects. This was also However, unlike the two studies mentioned here [12, found in two other studies by Konczak and Karnath [23] 22] our experiment had a relatively small number of and Hermsdorfer¨ et al. [13] whose patients were slowed patients which might have contributed to the lack of in all movement kinematics although again there were differential effects. Further, although there were clear no differences between patients with and without ne- differences between the two patients groups in terms of glect. The main finding is that these slowings are not their neglect behaviour (the four neglect patients only directionally specific, i.e., there is no relative slowing ever omitted items on the left whereas the three con- in movements towards leftwardly compared to right- trol patients omitted items more generally in both left wardly located targets (this was not explicitly analysed and right space and less frequently overall), it has to by Hermsdorfer¨ et al. [13]). Also in the present study, be granted that the neglect patients did not exhibit very there was no contralesional slowing beyond that shown severe neglect scores and the control patients were not by the control group in terms of movement duration perfect on this test. These could well be contributing and peak velocity, a general effect that is certainly due factors to the fact that no differences were found be- to mechanical constraints (see [3]). It thus seems that tween these two patient groups and in future it may patients with right damage exhibit a general slowing well be informative to test patients with more severe of their kinematics but that this bradykinesia does not neglect. seem to be directionally specific towards targets located So bearing these caveats in mind, when compar- in contralesional space. ing these right hemisphere lesioned patients to controls Additionally to the general slowing of arm move- what we seemed to have found are unimpaired grasp as ments in both patient groups, RCVA patients with and well orientation parameters, whereas the path curvature without neglect proved specifically impaired with re- seems to be relatively greater under visual feedback. spect to deceleration time: the control group spent less This latest parameter thus seems the most sensitive in time decelerating under binocular as opposed to open reflecting any perceptual misrepresentations these pa- loop viewing conditions, suggesting on-line use of vi- tients may experience possibly because (as argued by sual feedback. This was not the case for the RCVA Jackson et al., [15]) at least initially, the trajectory is group indicating that they may be less efficient in using less driven by a monitoring of the moment by moment visual guidance to home in on the target, an interpreta- changes on the hand relative to the target. Thus move- tion that also fits with the lack of curvature differences ments may be anchored at both the beginning and the found between presence and absence of visual feed- end of the movement but less so during mid reach when back in these patients. Hermsdorfer¨ et al. [13] also re- they may be maximally susceptible to misrepresenta- ported prolonged deceleration times in their right brain tions. damaged patients compared to the control groups and there is a trend for prolonged deceleration in Konzcak 4.3. Velocity profiles and Karnath’s [23] data a well. However, these data are different from those of Fisk Both patient groups proved markedly slower on the and Goodale [6,8] who demonstrated no impairment velocity measures of movement duration and peak ve- on any of the kinematic measures for their right hemi- locity although there were no differences in the veloc- sphere damaged subjects, while pointing under closed M. Harvey et al. / Is grasping impaired in hemispatial neglect? 27 loop conditions. Nonetheless, the results presented [2] F. Binkofski, C. Dohle, S. Posse, K.M. Stephan, H. Hefter, here indicate a right parietal involvement during the R.J. Seitz and H.-J. Freund, Human anterior intraparietal area adjustment phase, suggesting a less efficient use of the subserves prehension. A combined lesion and functional MRI activation study. Neurology 50 (1998), 1253–1259. available visual feedback. If one accepts the assump- [3] E. Bisiach, M.L. Rusconi, V.A.Peretti and G. Vallar, Challeng- tion that the RCVA patients had difficulty in determin- ing current accounts of unilateral neglect, Neuropsychologia ing the target position (see also path curvature, above), 23 (1994), 1431–1434. [4] D.P. Carey, E.L. Hargreaves and M.A. Goodale, Reaching it is possible that the initial direction of the movement to ipsilateral or contralateral targets: within hemisphere vi- while accelerating was less driven by a monitoring of suomotor processing cannot explain hemispatial differences the moment by moment changes of the hand relative to in motor control, Experimental Brain Research 112 (1996), the target and consequently modifications of the trajec- 496–504. [5] S. Chieffi, M. Gentilucci, A. Allport, E. Sasso and G. Riz- tory would need to occur during deceleration. 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Unpub- lished PhD thesis University of St. Andrews, 1993. [14] M. Harvey, A.D. Milner and R.C. Roberts, Spatial bias in Acknowledgements visually-guided reaching and bisection following right cerebral stroke, Cortex 30 (1994), 343–350. [15] J. Hermsdorfer,¨ S. Ulrich, C. Marquardt, G. Goldenberg and We would like to thank all the patients and other N. Mai, Prehension with the ipsilesional hand after unilateral participants for their co-operation and the two anony- brain damage, Cortex 35 (1999), 139–161. mous reviewers for very insight and helpful comments [16] S.R. Jackson and A. Shaw, The effects of the Ponzo illusion on on a previous version of this manuscript. This work grip aperture and grip force scaling, Journal of Experimental Psychology (in press). was supported by Wellcome grants to M Harvey (No: [17] S.R. Jackson, R. Newport, M. Husain, M. Harvey and J.V.Hin- 050184/Z) and SR Jackson (No: 054665). 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