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Neuropsychologia 46 (2008) 475–486

Saccade control and eye–hand coordination in optic ataxia

Valerie Gaveau a,b, Denis Pelisson a,b, Annabelle Blangero a,b, Christian Urquizar a,b,Claude Prablanc a,b, Alain Vighetto a,b,c, Laure Pisella a,b,∗a «Espace et Action» INSERM Unite 864, Bron, France, Universite Claude Bernard, Lyon, France

b Institut Federatif des Neurosciences de Lyon IFNL, Hopital Neurologique, Lyon, Francec Hospices Civils de Lyon, Hopital Neurologique Pierre Wertheimer, Lyon, France

Received 4 May 2007; received in revised form 2 August 2007; accepted 24 August 2007Available online 14 September 2007

Abstract

The aim of this work was to investigate ocular control in patients with optic ataxia (OA). Following a lesion in the posterior parietal cortex(PPC), these patients exhibit a deficit for fast visuo-motor control of reach-to-grasp movements. Here, we assessed the fast visuo-motor control ofsaccades as well as spontaneous eye–hand coordination in two bilateral OA patients and five neurologically intact controls in an ecological “lookand point” paradigm. To test fast saccadic control, trials with unexpected target-jumps synchronised with saccade onset were randomly intermixedwith stationary target trials. Results confirmed that control subjects achieved visual capture (foveation) of the displaced targets with the sametiming as stationary targets (fast saccadic control) and began their hand movement systematically at the end of the primary saccade. In contrast,the two bilateral OA patients exhibited a delayed visual capture, especially of displaced targets, resulting from an impairment of fast saccadiccontrol. They also exhibited a peculiar eye–hand coordination pattern, spontaneously delaying their hand movement onset until the execution of afinal corrective saccade, which allowed target foveation. To test whether this pathological behaviour results from a delay in updating visual targetlocation, we had subjects perform a second experiment in the same control subjects in which the target-jump was synchronised with saccade offset.With less time for target location updating, the control subjects exhibited the same lack of fast saccadic control as the OA patients. We proposethat OA corresponds to an impairment of fast updating of target location, therefore affecting both eye and hand movements.© 2007 Elsevier Ltd. All rights reserved.

Keywords: Optic ataxia; Saccades; Eye–hand coordination; On-line motor control; Posterior parietal cortex

1. Introduction

Eye–hand coordination is necessary for reaching to visualobjects in order to interact with the environment. Whether thisfunctional link between saccade and reach (see Neggers &Bekkering, 2001) involves common neural substrates within theposterior parietal cortex (PPC) remains a crucial question in theongoing debate about the function of the PPC in visuo-motorprogramming, i.e., how (Andersen & Buneo, 2002) versus spa-tial visual processing, i.e. where (Colby & Goldberg, 1999).Historically, the Balint–Holmes syndrome described concomi-tant ocular and reach impairments, with similar interpretationsof visuo-motor disconnection (Balint, 1909) versus “visual dis-

∗ Corresponding author at: “Espace et Action” UMR-S INSERM U864, 16avenue Lepine, Case 13, 69676 Bron, France. Tel.: +33 4 72913405;fax: +33 4 72913401.

E-mail address: pisella@lyon.inserm.fr (L. Pisella).

orientation” (Holmes, 1918). More recent studies however havedemonstrated that saccade and reach impairments can occurin isolation. Isolated impairments of contralesional saccades(including direction-specific hypometry and increased latency)have been observed after lesions of the inferior parietal lobule(IPL) of the PPC without concomitant reaching impairments(Pierrot-Deseilligny, Rivaud, Gaymard, & Agid, 1991; Pierrot-Deseilligny & Muri, 1997). Conversely, patients with opticataxia (OA) arising from damage of the superior parietal lob-ule (SPL) of the PPC have been described as exhibiting isolatedreaching impairments. In the latter, visuo-manual guidance isimpaired in peripheral vision, without any primary visual, pro-prioceptive and motor deficits (Garcin, Rondot, & de Recondo,1967; Jeannerod, 1986). This definition of OA is supposed toalso exclude any oculomotor deficits. The slight impairmentof saccadic eye movements detected in clinical tests in someOA patients have not been considered relevant to the misreach-ing deficits (e.g. Baylis & Baylis, 2001; Perenin & Vighetto,

0028-3932/$ – see front matter © 2007 Elsevier Ltd. All rights reserved.doi:10.1016/j.neuropsychologia.2007.08.028

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476 V. Gaveau et al. / Neuropsychologia 46 (2008) 475–486

Fig. 1. Lesions of the patients. AT’s cerebral MRI scans indicate bilateral parietal damage involving Brodmann’s areas 18, 19, 39 and 7 and extending to the superioroccipital lobes (V3a). IG’s cerebral MRI scans indicate bilateral parietal damage involving Brodmann’s areas 18, 19, 7 and a limited part of area 39.

1988; Rondot, de Recondo, & Dumas, 1977). Isolated sac-cade or reach errors as a consequence of lesions of the PPC inhumans have thus provided supporting arguments for the currentview of a segregated parietal eye field (PEF: Pierrot-Deseillignyand Muri, 1997; Pierrot-Deseilligny & M ri, 1997Pierrot-Deseilligny et al., 1991) and parietal reach region (PRR: Calton,Dickinson, & Snyder, 2002; Connolly, Andersen, & Goodale,2003).

However, such a motor segregation within the PPC is ques-tioned by several results: (i) a lesion of parietal saccadicregion in monkeys (lateral intraparietal area: LIP) does notaffect saccadic programming and execution (Wardak, Olivier,& Duhamel, 2002); (ii) electrophysiological activity of LIPand PRR neurons could represent reach- and saccade-relatedmodulations respectively (Snyder, Batista, & Andersen, 1997,2000) and show motor commands which encode target locationwith respect to the eyes (Constantin, Wang, Martinez-Trujillo,& Crawford, 2007; Pesaran, Nelson, & Andersen, 2006); and(iii) fMRI experiments tend to distinguish between at least twosegregated regions activated during saccades in humans, onecorresponding potentially to the macaque LIP and the otherto the PRR (Schluppeck, Glimcher, & Heeger, 2005). Further-more, OA patients, who are reported to show only isolatedvisuo-manual impairment, have been classically tested in con-dition where they are asked to maintain their eyes fixed whilereaching immediately and quickly toward objects presentedin peripheral vision (Milner et al., 2001; Perenin & Vighetto,1988; Rossetti et al., 2005). Their behaviour in unconstrainedconditions in which subjects spontaneously look and pointto the target, which allows the investigation of saccades andreaches, and their coordination, has never been studied. In nor-mal individuals, in such a “look and point” paradigm, the sametarget-related signal from peripheral vision is used both for themotor command initially sent to the arm and for the primarysaccadic eye movement (Biguer, Jeannerod, & Prablanc, 1982).

Because of the arm inertia however, the hand movement actu-ally begins roughly when the primary saccade ends (Prablanc,Echallier, Komilis, & Jeannerod, 1979). In addition, the eye andhand motor planning based on peripheral visual information isknown to be inaccurate (Prablanc et al., 1979). The comple-tion of the primary saccade allows accurate perifoveal signalsto update target location. This updated visual information isused to adjust the ongoing hand trajectory (fast manual control,Goodale, Pelisson, & Prablanc, 1986) and the amplitude of thecorrective saccade (fast ocular control, Prablanc & Jeannerod,1975).

An impairment of fast manual control has already been shownin two patients with bilateral OA when reaching in central(Grea et al., 2002; Pisella et al., 2000) or peripheral vision(Milner, Dijkerman, McIntosh, Rossetti, & Pisella, 2003; Milneret al., 2001; Rossetti et al., 2005). Protocols of reaching incentral vision (Grea et al., 2002; Pisella et al., 2000) used atarget displacement (target-jump) at hand movement onset tocompel visual updating during manual execution. In the firstexperiment here, the same two bilateral OA patients performeda “look and point” paradigm with target-jumps occurring atthe onset of the primary saccadic eye movement to compelvisual updating during ocular execution. Under the hypoth-esis of non-segregated visuo-motor modules for reaches andsaccades within the PPC, we predict that OA patients wouldalso exhibit a deficit of fast ocular control. Such a deficit hasnever been described in the literature. Since the control of ocu-lar capture, contrary to manual capture, involves the executionof additional (corrective) saccade, one could predict either aninadequate or a delayed execution of the corrective saccade.In the second experiment, we delayed the target-jump (at sac-cade offset) to simulate the same deficit of fast ocular controlin our group of 5 normal subjects as a demonstration that OAimpairment results from a delay to update visual target loca-tion.

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V. Gaveau et al. / Neuropsychologia 46 (2008) 475–486 477

2. Subjects and methods

2.1. Subjects

Five naıve control subjects (all right-handed, mean age 31) and two patientswith OA participated in the study. The study was conducted with their informedconsent, in agreement with the ethical standards laid down in the Declaration ofHelsinki of 1964. The patients were only involved in Exp. 1. The same group ofcontrol subjects was involved in both Exp. 1 and Exp. 2.

Patient AT was 47 at the time of testing, which was 15 years after an eclamp-tic attack which provoked bilateral haemorrhagic softening in the region aroundthe parieto-occipital arteries. Structural MRI revealed bilateral parietal damageextending toward the upper section of the occipital regions (see Fig. 1a). Duringthe initial 2 weeks after the lesion, AT presented a severe visual deficit resemblingcortical blindness. Subsequently, AT showed with a set of diverse symptoms:OA, right-left disorientation, simultanagnosia, constructional apraxia, spatialagraphia and acalculia. On the other hand, she showed no clinical indicationsof occipito-temporal damage (e.g. alexia, object agnosia, achromatopsia, orprosopagnosia). She showed a normal visual field except for a small parafovealscotoma in the right inferior homonymous quadrant and near normal visual acu-ity. At the time of testing for the current study, she was able to lead a surprisinglynormal life despite her extensive lesions but she still faced difficulties in visuo-spatial tasks and in tasks requiring precise and fast control within personal andextrapersonal space (Michel & Henaff, 2004). OA has remained stable, impair-ing reaching movements toward objects in peripheral vision. Her eye movementbehaviour was mentioned in Michel and Henaff (2004): AT complained that “hergaze would not reach directly what she wanted to see”; yet pursuit and saccadiceye movements were apparently normal at clinical examination except visualreaction times which were abnormally high compared to her auditory reactiontimes.

Patient IG was a 32-year old woman at the time of testing, 6 years after bilat-eral parieto-occipital infarctions related to acute vasospastic angiopathy in theposterior cerebral arteries. MRI revealed a hyperintense signal on T2 sequencesthat was near-symmetrically located in the posterior parietal and upper and lat-eral occipital cortico-subcortical regions (see Fig. 1b). She initially sufferedfrom severe headaches, dysarthria and bilateral blindness, which lasted for 3days. Subsequently, bilateral OA and simultanagnosia became apparent. By thestart of our first testing (Pisella et al., 2000) her simultanagnosia had subsided.Her visual acuity and ocular fundi were normal though visual fields showeda partial right inferior homonymous quadranopia with temporal crescent spar-ing. Routine recordings of saccadic and smooth pursuit eye movements elicitedby a LED in the dark showed normal latencies, gains, directions and veloci-ties (Grea et al., 2002). Her reaction time to a target change in position wasidentical to that of control subjects when evaluated by the production of an arbi-trary motor response to the target-jump (“location-stop” task in Pisella et al.,2000).

2.2. Experimental setup

Exp. 1 and Exp. 2 were conducted on the same experimental set-up withsimply the instruction to look and point at visual targets presented in peripheralvisual field in the dark. Subjects were placed in front of a 45◦ tilted pointing tablewith their head fixed with a bite board (Fig. 2a). A tactile circle placed sagitally16 cm distant from the trunk served as hand start position. Four target lights wereprojected on the table surface along the fronto-parallel line at the level of thesubject’s gaze (Fig. 2b). These targets were virtual images of red light-emittingdiodes (LEDs, diameter 3 mm) reflected on a mirror. This apparatus preventssubjects from detecting their pointing errors (no visual feedback of the handrelative to the target) and consequently from developing strategic behaviours toadjust their pointing movements. Subjects were instructed to initially fixate aLED, designated as the eye start position, located 10◦ to the left with respectto their trunk. They then had to look and point to three targets located 12.5◦,20◦ and 27.5◦ to the right with respect to the trunk or at 22.5◦, 30◦ and 37.5◦of eccentricity in the right visual field, with respect to initial eye fixation (seeFig. 2b). Coordinates in visual degrees are used throughout this paper. Horizontaleye movements were recorded with an infrared optometric system (EyeLinkI, SR Research, Ontario) at a frequency of 250 Hz with an accuracy of 0.1◦.

Fig. 2. Experimental set-up (a) Side view: the LED target array was locatedabove the subjects and was projected using a half-reflecting mirror to appearon the level of the table where the subjects reached. (b) Locations of the LEDused as (saccadic and pointing) targets and eye fixation, with respect to the handstarting location.

Pointing movements were recorded by an infra-red marker fixed on the indexfingertip (Optotrak, NDI, Ontario; 200 Hz).

2.3. Behavioural paradigm

Each subject performed 200 trials divided into two sessions. Each trial tookplace as follows: (1) the subject put his pointing finger on the hand start positionand (2) looked at the eye start position (illumination period, 2 s ± 300 ms); (3)the eye start position was extinguished while one of the three target LEDs wasilluminated (for 2 s ∓ 300 ms) signalling the subject to make a rightward saccadeand a pointing movement as fast and as accurately as possible (4) the trialacquisition ended when LED target switched off.

Among these 200 trials, 84% were ‘stationary trials’: the target LED waspresented at 22.5 (R2), 30 (R3) or 37.5 (R4) visual degrees until the end of thetrial; 16% of the trials were ‘jump trials’: the target LED was initially presentedat 30◦ (R3) and was suddenly extinguished at the beginning of the saccade (bymeans of a two-point central difference velocity detection algorithm, adaptedfrom Bahill & McDonald, 1983) and replaced by a target LED at 22.5 (J2:backward jump) or 37.5 (J4: forward jump) degrees till the end of the trial.This target-jump was not consciously detected by subjects as it occurred duringthe time of “saccadic suppression” (Goodale et al., 1986), which avoided anystrategic motor behaviour. When questioned at the end of the experiment, nosubject was able to report the occurrence of the target jump. Exp. 2 was identicalexcept that the target-jump was synchronised to primary saccade offset insteadof onset.

2.4. Analysis

The horizontal eye position signal was filtered (50 Hz cut-off frequency, finiteimpulse response filter FIR) and eye velocity was computed from the filteredposition signal using a two-point central difference derivative algorithm (Bahill& McDonald, 1983). In order to determine the sequence of eye movements, thebeginning and the end of the primary and corrective saccades were automat-ically detected using a velocity threshold procedure (30◦ s−1). The results ofthis automatic procedure were then inspected off-line and corrected manually,if necessary. Several saccade-related parameters were computed; for primaryand corrective saccades, saccadic gain was calculated as the ratio between sac-cadic amplitude and desired amplitude. Note that in the jump trials, the desiredamplitude of the primary saccade corresponded to the initial target location,whereas the desired amplitude of corrective saccades corresponded to the dif-ference between eye position at the end of the primary saccade and final targetlocation. Saccadic errors for the primary and corrective saccades were computedas the difference between final eye position and target position. In jump trials,the initial and the final target locations were used to compute saccadic errors forthe primary and the corrective saccades, respectively. Reaction times (RT) werecomputed with respect to target onset for primary saccades and with respect tothe end of the primary saccade for corrective saccades. Finally, the number ofcorrective saccades and the time of visual capture (period elapsing from targetpresentation to the end of the last corrective saccade) were computed.

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478 V. Gaveau et al. / Neuropsychologia 46 (2008) 475–486

For arm movements, the x, y, and z position signals were filtered at 10 Hz witha second-order Butterworth dual-pass filter. Movement velocity was computedfrom the filtered position signal using a least square second-order polynomialmethod (10 points moving window). The same method was used to com-pute the acceleration of the hand from the velocity signal. The onset andthe end of the movements were computed automatically using the followingthresholds: hand velocity 80 mm/s and hand acceleration 150 mm/s2. Afteran automatic detection, a visual inspection of the results was performed foreach trial. The hand-related parameter analysed in this study was hand reactiontime.

2.5. Statistics

2.5.1. Between-group analysesOur goal was to establish on which eye and hand motor parameters the mean

scores of patients reliably differed from the control ones. For each patient, theseparameters were compared to those of the control group with repeated measuresANOVAs with Group as a factor. We adjusted the critical value of F in order totake the variance of the control group and the patient (AT or IG) into account,as proposed by Mycroft, Mitchell and Kay (2002). Note that in this statisticalmethod for single-case studies, a significant effect at the 5% level (p′) is acceptedif the revised F-value exceeds 10.

2.5.2. Within-group analysesThe objective of these analyses was to assess separately in each patient

and in the control group the effect of target eccentricity and of target-jump.Within each patient, a one-way ANOVA was performed with Trial type as afactor. For the control group, a repeated-measures ANOVA was used. In Exp.1, contrast analyses (planned comparisons) were used to test the effect of targeteccentricity or occurrence of target-jump on ocular or pointing behaviour. Thetime of occurrence of the target-jump (at saccade onset in Exp. 1 versus saccadeoffset in Exp. 2) was then used as an additional factor for the within-groupanalyses.

3. Results

3.1. Exp. 1: target-jumps at saccade onset

3.1.1. Saccadic behaviour3.1.1.1. Control Group. Within-group analyses were con-ducted to determine the effect of target eccentricity or oftarget-jump on saccadic behaviour. All saccadic parameters arereported in Tables 1 and 2 for stationary and jump trials respec-tively.

The classical hypometry of primary saccades was observed(mean gain of 0.91). The gain remained constant with tar-get eccentricity (F(2,8) = 0.8; p > 0.05), leading to a significantincrease of the absolute error of the primary saccade when targeteccentricity increased (F(2, 8) = 10.4, p < 0.01) (Fig. 3a). Despiteinitial saccadic hypometry, neither mean error nor reaction timeof the corrective saccade differed across target eccentricities(F(2, 8) < 1.30, p > 0.05). The reaction time of the correctivesaccade was significantly shorter than the reaction time of theprimary saccade (F(1, 4) = 90, p < 0.01), in agreement with find-ings from the literature (Prablanc & Jeannerod, 1975; Becker &Fuchs, 1969). The mean error and reaction time of the correc-tive saccades showed no differences between target-jump andstationary trials (between stationary trials at 37.5◦ and trialswith target displaced forward from 30◦ to 37.5◦: F(1,4) < 1.4,p > 0.05 and between stationary trials at 22.5◦ and trials withtarget displaced backward from 30◦ to 22.5◦: F(1,4) < 5.4,p > 0.05). Ta

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V. Gaveau et al. / Neuropsychologia 46 (2008) 475–486 479

Table 2Corrective saccade parameters in jump trials (mean and S.D.) for the control group (C) and the two patients with OA (AT and IG), obtained for target-jumps atsaccade onset (Exp. 1)

In stationary trials, visual capture was usually achieved withno or a single corrective saccade (mean number of correctivesaccades = 0.46), the mean gain of the corrective saccade wasclose to 1 (1.08) and thus accurate target capture (final errors ofless than 1◦) was achieved despite initial saccadic hypometry. Injump trials, control subjects achieved visual capture of the per-turbed target both by increasing the occurrence of a correctivesaccade (F(1,4) > 9.8, p < 0.05) and by changing its amplitudeso that the gain of the first corrective saccades computed withrespect to the final target location remained close to 1 (1.03).In fact, visual capture was systematically achieved with a singlecorrective saccade for backward jumps (mean number of cor-rective saccade = 1 with S.D. = 0) and with one or exceptionallytwo corrective saccades for forward jumps (mean number ofcorrective saccade = 1.21).

3.1.1.2. OA patients. The classical relationship between ampli-tude and duration (the main sequence) was observed for thetwo patients, attesting that the dynamic characteristics of sac-cades were not altered by the lesion (see SupplementaryInformation). Therefore, only the spatial (error and gain) andtemporal (reaction time) saccadic parameters are detailed below.Between-group comparisons (Mycroft et al., 2002) revealed thatboth patients exhibited a larger hypometry of primary saccadesthan control subjects (revised F(1,4) > 10.2; p′ < 0.05; Table 1).This hypometry appeared outside the confidence interval of thecontrol group for the most eccentric targets (Fig. 3b: only forthe 37.5◦ target in AT and for the 30 and 37.5◦ targets in IG).Within-group analysis revealed that with a mean gain of 0.84 forprimary saccades, patient IG, in fact, showed a higher saccadicgain than that of the control group for the 22.5◦ target (1.06),a gain of 0.84 for the 30◦ target and a reduced gain (0.67) forthe 37.5◦ target. Rather than a general gain reduction of primarysaccades, the deficit of patient IG is therefore best described asa pathological decrease of the slope of the saccadic gain versustarget eccentricity relationship.

Yet, in both patients, the visual capture of the targetwas always achieved with normal accuracy as the final errorafter the last corrective saccade did not differ from controls(revised F(1,4) < 6; p′ > 0.05 for both patients) at all targeteccentricities and whenever the target-jump occurred (Figs.3c and 4b). Thus OA patients could eventually correct forboth their own initial error resulting from hypometric pri-

mary saccades and the experimental error due to the target-jump.

The time of visual capture computed with respect to tar-get onset was significantly delayed with respect to controls(Tables 1 and 2; revised F(1,4) > 13; p′ < 0.05 for both patients).Note that if we consider the time of visual capture with respect toprimary saccade onset, the two patients exhibited a similar delayof 100 ms for stationary targets, corresponding to an increasedtime needed for ocular control. Detailed inspection revealed thatthis common increase of the duration of the saccadic sequenceexecution was expressed differently in the behaviour of the twoOA patients.

Patient AT delayed her corrective saccade significantly withrespect to the control group (revised F(1,4) = 25.3; p′ < 0.05) byroughly 100 ms for stationary (Table 1) and jump trials (Table 2)but visual capture was achieved with a normal number of cor-rective saccades (revised F(1,4) = 8.0; p′ > 0.05). In stationarytrials, visual capture was achieved with no or a single correctivesaccade (mean number of corrective saccade = 0.57). The target-jump trials implied a significant increase of the occurrence ofa corrective saccade (F(1,66) = 61.97, p < 0.01). Similar to thatreported above for the control group, the mean gain of the firstcorrective saccade computed with respect to the final target loca-tion remained close to 1 (0.98) in jump trials, such that visualcapture was achieved with one systematic corrective saccadeand very exceptionally with two (mean number of correctivesaccade = 1.16).

In patient IG, the reaction time of the first corrective saccadewas even significantly shorter than in the control group (revisedF(1,4) = 13.7; p′ < 0.05) but the number of corrective sac-cades was significantly higher (revised F(1,4) = 21.1; p′ < 0.05).Patient IG needed one or two corrective saccades to capturestationary targets (mean number of corrective saccade = 1.30).In response to target-jumps, a further increase of the num-ber of corrective saccades was observed (F(1,150) = 15.23,p < 0.01), consequently delaying even more visual capture(F(1,150) = 17.9, p < 0.01). Indeed, in 65% of the backward jumptrials and in 85% of the forward jump trials, the primary saccadicerror and the error due to the target-jump were compensated seri-ally. In these trials, the mean gain of the first corrective saccadecomputed with respect to the final target location was far from1 (0.47 for forward and 2.08 for backward jumps). When com-puted instead with respect to the initial target location (30◦), the

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Fig. 3. Saccadic behaviour in stationary trials. (a) Individual saccadic traces for stationary trials at the three target eccentricities (22.5◦, 30◦ and 37.5◦) for the mosthypometric control subject, and for patients IG and AT. Horizontal eye position is plotted with respect to time of data acquisition (from target presentation at 0 msuntil 1500 ms). Filled and opened arrows indicate onset of primary and corrective saccades respectively. (b) The left panel represents the mean and confidence interval(∓1.96*standard deviation) of the endpoints of the primary saccade for the control group and for the three target eccentricities (22.5◦, 30◦ and 37.5◦). The two otherpanels represent the mean and standard deviation of the primary saccade endpoints for patients AT (middle panel) and IG (right panel), for the same three targeteccentricities. Dashed lines indicate actual target locations. (c) The left panel represents the mean final positions of the eye (after corrective saccades) and confidenceinterval (1.96*standard deviation) for the control group and for the three target eccentricities (22.5◦, 30◦ and 37.5◦). The middle and the right panels represent themeans and standard deviations of the final eye position for AT and IG respectively, for the same three target eccentricities. Dashed lines indicate the actual targetpositions.

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Fig. 3. (Continued ).

gain reached a mean value of 1.02, showing that the first correc-tive saccade was actually directed toward the first (extinguished)target location. The first corrective saccade of IG allowed heronly to compensate her primary saccade error and at least asecond one was needed to compensate for the target-jump error.This is particularly clear from the example provided in Fig. 4a, inwhich patient IG and the illustrated control subject exhibited pri-mary saccades with similar hypometry. Then, in both backwardand forward jump trials, the first corrective saccade of patientIG brought the eye to the position of the initial (extinguished)target, whereas that of the control subject directly reached theactual (displaced) target position. This behaviour of patient IGwas particularly striking for the backward target-jumps whichcalled for a backward corrective saccade. In contrast to thecontrol subject, patient IG executed a first forward correctivesaccade, away from the actual target location. Only the subse-quent corrective saccades were executed in the correct direction.Visual capture was finally achieved by the fourth correctivesaccade.

This ‘serial’ behaviour characterised by normal reactiontimes of the first corrective saccade but a significant increase ofthe number of saccades was predominant in patient IG but shealso exhibited the same ‘parallel’ behaviour as patient AT. Thesetwo behaviours in response to target-jump are distinguished inTable 2 using the criteria of the number of corrective saccadesproduced to capture the displaced target (one or more than one;accordingly, the reaction time of the first saccade is delayedor not relative to controls). The ‘serial’ behaviour caused thelongest delay of visual capture.

3.1.2. Eye–hand coordination3.1.2.1. Control group. The eye–hand coordination in the con-trol subjects (left panel of Fig. 5) followed a well-establishedtemporal sequence with the following two characteristics: (1)

the pointing movement consistently began at approximately theend of the primary saccade, and consequently, (2) a correctivesaccade was made during the execution of the pointing move-ment.

3.1.2.2. OA patients. The temporal sequence of eye–hand coor-dination was consistently modified in the two patients withrespect to that observed in healthy controls. Indeed, between-group statistics (Mycroft et al., 2002) revealed in both patientsthat the reaction time of the reaching response was markedlydelayed relative to controls (revised F(1,4) > 33; p′ < 0.05), sothat the pointing movement began at the time of the final cor-rective saccade (see Fig. 5). When patient IG exhibited the samebehaviour as patient AT, consisting of capturing the visual tar-get with a single but much delayed corrective saccade, the handreaction time temporally matched to the execution of the singlecorrective saccade (IG left panel in Fig. 5). In the other trials, inwhich patient IG captured the visual target with more than onecorrective saccade, the hand reaction time temporally matchedwith the execution of the last corrective saccade. There was nosignificant main effect of the occurrence of a target-jump onhand reaction time. The lack of change of this temporal parame-ter indicates that the distinct eye–hand coordination exhibited bythe two patients was not adopted in response to target-jumps butinstead corresponded to their standard behaviour in ecologicalconditions.

3.2. Exp. 2: target-jumps at saccade offset

The main aspect of the saccadic deficit of OA patients was thedelayed time of visual capture. In order to test the hypothesis thatthis deficit resulted from a delay in updating the target location,we conducted a second experiment in which the target-jump wassynchronised on saccade offset instead of saccade onset. We

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Fig. 4. Saccadic behaviour in target-jump trials. (a) Individual saccadic traces for backward and forward target-jump trials (initial target eccentricity of 30◦, finaltarget eccentricities of 22.5◦ and 37.5◦ respectively) for the most hypometric control subject, and for patients AT and IG. Horizontal eye position is plotted withrespect to time of data acquisition (from initial target presentation at 0 ms until 1500 ms). The time of target-jump is synchronised to the occurrence of the primarysaccade (as indicated by the step in the dotted line). Filled and opened arrows indicate onset of primary and corrective saccades respectively, grey arrows indicatethe onset of an inadequate corrective saccade. (b) Final saccadic accuracy (after all corrective saccades) for stationary targets at 22.5◦ and 37.5◦ (R2 and R4 respectively)

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Fig. 5. Temporal relationships between saccadic and pointing responses. For each parameter, the mean values (∓1.96*standard deviation) computed in each subjectgroup (CONTROLS, IG and AT) are plotted against target eccentricity for the stationary targets at 22.5◦ (R2), 30◦ (R3) and 37.5◦ (R4) and for the perturbed targetswith backward (J2) and forward (J4) jump. The parameters are: beginning ( ) and end ( ) of primary saccades (S1), beginning ( ) and end ( ) of the last correctivesaccades (S2), beginning ( ) and end (�) of the hand pointing movement. In patient IG, the two saccadic behavioural types (“parallel” and “serial”, see text) havebeen distinguished in two separate panels.

expected to observe a behaviour similar in control subjects as inour two patients with bilateral OA, if the visual information of thenew target location is provided with a delay of about 80 ms (meanprimary saccade duration). This delay shortens the time availablefor visual updating and may therefore produce, as in OA, animpairment of fast motor control. Within-group analyses wereconducted on the target-jump trials in order to test the effect ofdelaying the visual information of the new target location (target-jump synchronised at primary saccade onset versus offset) onocular behaviour and on eye–hand coordination.

3.2.1. Saccadic behaviourDelaying the occurrence of target-jump induced a delayed

time of visual capture (F(1, 4) = 14.70, p = < 0.05) in controlsubjects (Table 3) resulting from both an increase of the num-ber of corrective saccades (F(1, 4) = 61.45, p < 0.05) and of thereaction time of the (first) corrective saccade (F(1,4) = 17.46,p < 0.05). In fact, in response to the delayed target-jump, thecontrol subjects exhibited the two types of saccadic controlbehaviours observed in the OA patients, which can be segre-gated based on the number of corrective saccades (see Table 3):(1) ‘parallel’ behaviour: when only one corrective saccade wasproduced to achieve foveal capture, its occurrence was largelydelayed (257 ms in target-jump trials with respect to 158 ms onaverage in stationary trials, and 172 ms in target-jump trials inExp. 1) leading to delayed visual capture (625 ms with respectto 580 ms in Exp. 1); (2) ‘serial’ behaviour: the control subjects

produced several corrective saccades to capture displaced tar-gets when the first corrective saccade was not delayed (reactiontime of 170 ms as in Exp. 1: 172 ms) leading to a largely delayedvisual capture (736 ms). The ‘parallel’ behaviour was used pre-dominantly by the control subjects (in 73.25% of the target-jumptrials).

3.2.2. Eye–hand coordinationIn contrast to the behaviour of the two OA patients, pointing

reaction time was not affected by the delay of the target-jump occurrence (F(1,4) = 1.18, p > .05). The classical eye–handcoordination was observed, with the pointing movement onsetmatching the offset of the primary saccade (as in Fig. 5). Point-ing accuracy was also not significantly impaired (F(1,4) = 2.28,p > .05) but the duration of pointing movement was significantlydelayed (F(1,4) = 8.60, p = .046): about 33 ms longer when thetarget-jump occurred at saccade offset (Exp. 2) compared to sac-cade onset (Exp. 1); however this slight pointing delay was notcomparable to the delay of saccadic capture.

4. Discussion

Patients with bilateral OA have been shown in the literature toexhibit a lack of fast motor control for hand movements (Grea etal., 2002; Pisella et al., 2000). In the present paper, we investigatewhether this deficit resulting from a lesion of the PPC causes apathological delay in updating the location of the visual target.

and for backward and forward jump trials (J2 and J4 respectively). The left panel depicts the mean and confidence interval (1.96*standard deviation) of final eyeposition for the control group; the middle and right panels depict the means and standard deviations for patients AT and IG respectively. Dashed lines indicate theactual final target positions.

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Table 3Corrective saccade parameters in jump trials (mean and S.D.) for control group (C) obtained for target-jumps at saccade offset (Exp. 2)

Groups Jump trials Number Final Error (◦) RT (ms) Time of visual capture (ms)

CBackward 1.08 (0.02)

1 (93%) N = 64 −0.50 (0.79) 233 (48)238(42)

618 (30)610 (51)

�2 (7%) N = 5 162(66) 724 (118)

Forward 1.54 (0.32)1 (53.5%) N = 30 −1.92 (0.26) 244 (80)

279(73)692 (87)

643 (75)�2 (46.5%) N = 26 174 (35) 749 (64)

The slow visual processing of the target location is first demon-strated by showing that patients with bilateral OA also exhibit alack of fast motor control for saccadic eye movements (Exp. 1,target-jump at primary saccade onset) and second by showingthat normal subjects exhibit the same ocular behaviour as OApatients if the visual information (of the final target location)is provided with a delay (Exp. 2, target-jump at primary sac-cade offset). After a detailed discussion of the results leading tothese conclusions, we will discuss the anatomical segregation ofsaccade and reach modules within the PPC.

4.1. Saccadic behaviour

The saccadic deficit included temporal and spatial com-ponents, which can be expressed differently in patients (seeRossetti, Pisella, & Vighetto, 2003 for a review of the tempo-ral and spatial aspects of OA). In the two OA patients of thisstudy, the saccadic deficits mainly addressed fast ocular control(characterised by a delayed visual capture, especially when thetarget jumped) and the pathological hypometry for large targeteccentricities (>30 visual degrees). The experimental conditionsnecessary to reveal these deficits are not used routinely in clinicaltests, which may explain usual clinical reports that eye move-ments are relatively preserved in OA (e.g. Baylis & Baylis, 2001;Perenin & Vighetto, 1988; Rondot et al., 1977). A recent study(Trillenberg et al., 2007) reported intact saccades in a patientwith optic ataxia, but the authors computed a global saccadicgain related to the final saccadic accuracy which did not allowthem to reveal the hypometry of the primary saccade and thedeficit of saccadic control (suggested by the closed inspectionof the typical eye trace presented on their Fig. 4) in their OApatient.

4.2. Fast motor control

We argue that the delayed time of visual capture in the twoOA patients reveals an impaired fast ocular control of the sac-cadic sequence. Indeed, data from our control subjects in Exp.1 indicated that normal foveal capture is achieved by a slightlyhypometric primary saccade, sometimes followed by one cor-rective saccadic movement. In target-jump trials, the correctivesaccade is systematically initiated, and its spatial parameters(amplitude, direction) are adjusted in order to capture the dis-placed visual target without the need for additional correctivesaccades (Becker & Jurgens, 1979). In addition, it was shownthat the latency (and duration) of the single corrective saccaderemained similar in target jump and in stationary target trials(about 160 ms). These observations indicate that in control sub-

jects, an update of the visual error takes place between the endof the primary saccade and the initiation of the corrective sac-cade without any additional time cost. This fast control of thesaccadic sequence is clearly lacking in the two OA patients.

Patient AT produced a pairing of two saccades, irrespective ofthe trial type (stationary or jump), with a large temporal “safetymargin” for both primary and secondary saccades. Patient IGalso exhibited a single, delayed, corrective saccade in 25% ofthe target-jump trials (parallel compensation of intrinsic primarysaccade errors and errors due to the target-jump). However,in most trials, she instead produced an increased number ofcorrective saccades to achieve visual capture of the displacedtargets. Strikingly, in these trials, her first “corrective” saccadewas generated with no RT increase and was directed to the initial(extinguished) target location (serial compensation of intrinsicprimary saccade error and error due to the target-jump). Clearly,this observation indicates that her oculomotor system did nothave immediate access to the new retinal target location.

It is worth noting that despite the different “serial” and “par-allel” behaviours in target-jump trials, the patients showed thesame additional delay of about 100 ms to capture stationaryvisual targets. This pathological delay of visual capture revealeda common deficit in fast ocular control. This conclusion is rein-forced by Exp. 2, in which control subjects exhibited the same“serial” and “parallel” behaviours in response to a target-jumpsynchronised on primary saccade offset.

Our prediction was that the deficit of fast ocular control inOA patients results from an inability to update “on-line” thevisual target location, as suggested by a previous study (Khan,Pisella, Rossetti, Vighetto, & Crawford, 2005). Consequently,the time normally sufficient to implement the new target locationturns out to be too short. Accordingly, in Exp. 2 we showed thatreducing the time available for visual updating could cause thesame abnormal ocular control in control subjects.

4.3. Eye–hand coordination

In the present “look and point” task, both OA patients spon-taneously delayed their hand movement onset to the end of thesaccadic sequence (see Fig. 5 and reaction times on Table 3), i.e.to when the visual target location was eventually updated basedon central vision. Note that a similar behaviour can be observedon the typical eye–hand trace of the OA patient of Trillenberg etal. (2007, Fig. 4). This temporal sequence of eye–hand responsessuppresses the need for reaching in peripheral vision, and like-wise limits the need for fast control of hand reaching movement.Accordingly, bilateral OA patients are known to be specificallyimpaired for reaching in peripheral vision (Milner et al., 2003;

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Rossetti et al., 2005) and for fast reaching corrections (Grea et al.,2002; Pisella et al., 2000). This eye–hand coordination patternhas not been reported before, even in other neurological patientsimpaired for reaching (e.g. Desmurget et al., 2004) and was alsonot observed in the control group of the second experiment. It isthus probably not a strategy developed for the present task butinstead a spontaneous and unconscious behaviour adopted by thetwo OA patients for all reach-and-grasp actions. This behaviourwould explain why OA patients actually rarely complain frominaccuracy of hand movements in their everyday life (Rossettiet al., 2003), and may thus reflect a functional compensation fortheir lesion.

4.4. Common or segregated saccade and reach regionswithin the PPC?

It is interesting to compare the deficit of fast ocular controlto the impairment of fast manual control demonstrated in pre-vious studies involving patients IG and AT (Grea et al., 2002;Pisella et al., 2000). For example, the “serial” saccadic behaviourexhibited by patient IG (Fig. 4a) is directly comparable to herreaching behaviour presented in Fig. 2A of the study of Greaet al. (2002). In both cases, and in contrast to control subjects,patient IG responded to the target-jump by performing first anon-modified response (either hand movement or eye move-ment sequence) toward the initial target location, followed by atleast one supplementary movement allowing her to achieve finaltarget position.

The second aspect of the oculomotor deficits in OA patientswas the hypometry of primary saccades. Both OA patientsexhibited a primary saccadic error that increased with targeteccentricity, with accuracy outside the confidence interval ofthe control group, at least for the most eccentric target (37.5◦).Interestingly again, pointing data from previous studies involv-ing patients IG and AT also revealed hypometric errors thatincreased with target eccentricity (Milner et al., 2003; Rossettiet al., 2005).

Anatomically, one cannot rule out the possibility that thepatients’ parietal lesions encroached upon nearby but segregatedeye- and hand-related regions. However, the similarity betweenthe saccadic deficits demonstrated here and the reach deficitsreported in the literature raises the possibility of a common pari-etal module for saccade and reach. This similarity concerns thetarget localisation in peripheral vision (pathological increase ofeye and hand hypometry with target eccentricity) and the fastupdating of target localisation (absence of fast corrections bothfor hand and eye movements). Interestingly, the POJ region,which has recently been identified as the focus of lesions in alarge group of OA patients (Karnath & Perenin, 2005), is specif-ically activated in relation to reaching movements performed bynormal subjects in peripheral vision (Prado et al., 2005). Fur-thermore, the same POJ region has been involved in dynamicupdating of the eye-centred spatial representation of peripheralpointing targets (Medendorp, Goltz, Vilis, & Crawford, 2003).Therefore, POJ is a potential anatomical candidate to subservea core visuo-spatial mechanism (“Where”), and a lesion at thislocation would affect both eye and hand movements. The study

of unilateral OA patients (Perenin & Vighetto, 1988) has estab-lished a pattern of hand reaching deficits that combines errorslinked to the location of the visual target in the contralesionalvisual field (field effect) and to the use of the contralesional hand(hand effect). The present results do not rule out the existenceof a specific visuo-manual deficit (hand effect) correspondingto a mislocalisation of the ataxic hand (Blangero et al., 2007).These deficits could correspond to the impairment of the twoanatomical modules demonstrated in normal subjects by Pradoet al. (2005).

Conflict of interest

The authors report no conflicts of interest.

Appendix A. Supplementary data

Supplementary data associated with this article can befound, in the online version, at doi:10.1016/j.neuropsychologia.2007.08.028.

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