A

(sawttcfilWt©

K

1

ofBpoptHto

af

0d

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

bstract

The aim of this work was to investigate ocular control in patients with optic ataxia (OA). Following a lesion in the posterior parietal cortexPPC), these patients exhibit a deficit for fast visuo-motor control of reach-to-grasp movements. Here, we assessed the fast visuo-motor control ofaccades as well as spontaneous eye–hand coordination in two bilateral OA patients and five neurologically intact controls in an ecological “looknd point” paradigm. To test fast saccadic control, trials with unexpected target-jumps synchronised with saccade onset were randomly intermixedith stationary target trials. Results confirmed that control subjects achieved visual capture (foveation) of the displaced targets with the same

iming as stationary targets (fast saccadic control) and began their hand movement systematically at the end of the primary saccade. In contrast,he two bilateral OA patients exhibited a delayed visual capture, especially of displaced targets, resulting from an impairment of fast saccadicontrol. They also exhibited a peculiar eye–hand coordination pattern, spontaneously delaying their hand movement onset until the execution of anal corrective saccade, which allowed target foveation. To test whether this pathological behaviour results from a delay in updating visual target

ocation, we had subjects perform a second experiment in the same control subjects in which the target-jump was synchronised with saccade offset.ith less time for target location updating, the control subjects exhibited the same lack of fast saccadic control as the OA patients. We propose

hat OA corresponds to an impairment of fast updating of target location, therefore affecting both eye and hand movements.2007 Elsevier Ltd. All rights reserved.

rol; P

odi(h((Dau

eywords: Optic ataxia; Saccades; Eye–hand coordination; On-line motor cont

. Introduction

Eye–hand coordination is necessary for reaching to visualbjects in order to interact with the environment. Whether thisunctional link between saccade and reach (see Neggers &ekkering, 2001) involves common neural substrates within theosterior parietal cortex (PPC) remains a crucial question in thengoing debate about the function of the PPC in visuo-motorrogramming, i.e., how (Andersen & Buneo, 2002) versus spa-ial visual processing, i.e. where (Colby & Goldberg, 1999).

istorically, the Balint–Holmes syndrome described concomi-

ant ocular and reach impairments, with similar interpretationsf visuo-motor disconnection (Balint, 1909) versus “visual dis-

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

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

rip1aoOi

028-3932/$ – see front matter © 2007 Elsevier Ltd. All rights reserved.oi:10.1016/j.neuropsychologia.2007.08.028

osterior parietal cortex

rientation” (Holmes, 1918). More recent studies however haveemonstrated that saccade and reach impairments can occurn isolation. Isolated impairments of contralesional saccadesincluding direction-specific hypometry and increased latency)ave been observed after lesions of the inferior parietal lobuleIPL) of the PPC without concomitant reaching impairmentsPierrot-Deseilligny, Rivaud, Gaymard, & Agid, 1991; Pierrot-eseilligny & Muri, 1997). Conversely, patients with optic

taxia (OA) arising from damage of the superior parietal lob-le (SPL) of the PPC have been described as exhibiting isolatedeaching impairments. In the latter, visuo-manual guidance ismpaired in peripheral vision, without any primary visual, pro-rioceptive and motor deficits (Garcin, Rondot, & de Recondo,967; Jeannerod, 1986). This definition of OA is supposed to

lso exclude any oculomotor deficits. The slight impairmentf saccadic eye movements detected in clinical tests in someA patients have not been considered relevant to the misreach-

ng deficits (e.g. Baylis & Baylis, 2001; Perenin & Vighetto,

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 superioro e invo

1chvaDD2

tra&am2w&(sctmvdri1ctrmtms

BaEhkttuGc1

i((ectceatvesanloiI

ccipital lobes (V3a). IG’s cerebral MRI scans indicate bilateral parietal damag

988; Rondot, de Recondo, & Dumas, 1977). Isolated sac-ade or reach errors as a consequence of lesions of the PPC inumans have thus provided supporting arguments for the currentiew of a segregated parietal eye field (PEF: Pierrot-Deseillignynd Muri, 1997; Pierrot-Deseilligny & M ri, 1997Pierrot-eseilligny et al., 1991) and parietal reach region (PRR: Calton,ickinson, & Snyder, 2002; Connolly, Andersen, & Goodale,003).

However, such a motor segregation within the PPC is ques-ioned by several results: (i) a lesion of parietal saccadicegion in monkeys (lateral intraparietal area: LIP) does notffect saccadic programming and execution (Wardak, Olivier,

Duhamel, 2002); (ii) electrophysiological activity of LIPnd PRR neurons could represent reach- and saccade-relatedodulations respectively (Snyder, Batista, & Andersen, 1997,

000) and show motor commands which encode target locationith respect to the eyes (Constantin, Wang, Martinez-Trujillo,Crawford, 2007; Pesaran, Nelson, & Andersen, 2006); and

iii) fMRI experiments tend to distinguish between at least twoegregated regions activated during saccades in humans, oneorresponding potentially to the macaque LIP and the othero the PRR (Schluppeck, Glimcher, & Heeger, 2005). Further-

ore, OA patients, who are reported to show only isolatedisuo-manual impairment, have been classically tested in con-ition where they are asked to maintain their eyes fixed whileeaching immediately and quickly toward objects presentedn peripheral vision (Milner et al., 2001; Perenin & Vighetto,988; Rossetti et al., 2005). Their behaviour in unconstrainedonditions in which subjects spontaneously look and pointo the target, which allows the investigation of saccades andeaches, and their coordination, has never been studied. In nor-

al individuals, in such a “look and point” paradigm, the same

arget-related signal from peripheral vision is used both for theotor command initially sent to the arm and for the primary

accadic eye movement (Biguer, Jeannerod, & Prablanc, 1982).

ciit

lving Brodmann’s areas 18, 19, 7 and a limited part of area 39.

ecause of the arm inertia however, the hand movement actu-lly begins roughly when the primary saccade ends (Prablanc,challier, Komilis, & Jeannerod, 1979). In addition, the eye andand motor planning based on peripheral visual information isnown to be inaccurate (Prablanc et al., 1979). The comple-ion of the primary saccade allows accurate perifoveal signalso update target location. This updated visual information issed to adjust the ongoing hand trajectory (fast manual control,oodale, Pelisson, & Prablanc, 1986) and the amplitude of the

orrective saccade (fast ocular control, Prablanc & Jeannerod,975).

An impairment of fast manual control has already been shownn two patients with bilateral OA when reaching in centralGrea et al., 2002; Pisella et al., 2000) or peripheral visionMilner, Dijkerman, McIntosh, Rossetti, & Pisella, 2003; Milnert al., 2001; Rossetti et al., 2005). Protocols of reaching inentral vision (Grea et al., 2002; Pisella et al., 2000) used aarget displacement (target-jump) at hand movement onset toompel visual updating during manual execution. In the firstxperiment here, the same two bilateral OA patients performed“look and point” paradigm with target-jumps occurring at

he onset of the primary saccadic eye movement to compelisual updating during ocular execution. Under the hypoth-sis of non-segregated visuo-motor modules for reaches andaccades within the PPC, we predict that OA patients wouldlso exhibit a deficit of fast ocular control. Such a deficit hasever been described in the literature. Since the control of ocu-ar capture, contrary to manual capture, involves the executionf additional (corrective) saccade, one could predict either annadequate or a delayed execution of the corrective saccade.n the second experiment, we delayed the target-jump (at sac-

ade offset) to simulate the same deficit of fast ocular controln our group of 5 normal subjects as a demonstration that OAmpairment results from a delay to update visual target loca-ion.

sychologia 46 (2008) 475–486 477

2

2

wcHc

ttetcOaopsinseibgert

eptefdsHaibtit2

2

svw1psdsraLt2oFeI

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 appearous

Pfi

2

patiaa

ptamfbTtsseo

2

ip&bitiacawflat

V. Gaveau et al. / Neurop

. Subjects and methods

.1. Subjects

Five naıve control subjects (all right-handed, mean age 31) and two patientsith OA participated in the study. The study was conducted with their informed

onsent, in agreement with the ethical standards laid down in the Declaration ofelsinki of 1964. The patients were only involved in Exp. 1. The same group of

ontrol 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-

ic attack which provoked bilateral haemorrhagic softening in the region aroundhe parieto-occipital arteries. Structural MRI revealed bilateral parietal damagextending toward the upper section of the occipital regions (see Fig. 1a). Duringhe initial 2 weeks after the lesion, AT presented a severe visual deficit resemblingortical blindness. Subsequently, AT showed with a set of diverse symptoms:A, right-left disorientation, simultanagnosia, constructional apraxia, spatialgraphia and acalculia. On the other hand, she showed no clinical indicationsf occipito-temporal damage (e.g. alexia, object agnosia, achromatopsia, orrosopagnosia). She showed a normal visual field except for a small parafovealcotoma in the right inferior homonymous quadrant and near normal visual acu-ty. At the time of testing for the current study, she was able to lead a surprisinglyormal life despite her extensive lesions but she still faced difficulties in visuo-patial tasks and in tasks requiring precise and fast control within personal andxtrapersonal space (Michel & Henaff, 2004). OA has remained stable, impair-ng reaching movements toward objects in peripheral vision. Her eye movementehaviour was mentioned in Michel and Henaff (2004): AT complained that “heraze would not reach directly what she wanted to see”; yet pursuit and saccadicye movements were apparently normal at clinical examination except visualeaction times which were abnormally high compared to her auditory reactionimes.

Patient IG was a 32-year old woman at the time of testing, 6 years after bilat-ral parieto-occipital infarctions related to acute vasospastic angiopathy in theosterior cerebral arteries. MRI revealed a hyperintense signal on T2 sequenceshat was near-symmetrically located in the posterior parietal and upper and lat-ral occipital cortico-subcortical regions (see Fig. 1b). She initially sufferedrom severe headaches, dysarthria and bilateral blindness, which lasted for 3ays. Subsequently, bilateral OA and simultanagnosia became apparent. By thetart of our first testing (Pisella et al., 2000) her simultanagnosia had subsided.er visual acuity and ocular fundi were normal though visual fields showedpartial right inferior homonymous quadranopia with temporal crescent spar-

ng. Routine recordings of saccadic and smooth pursuit eye movements elicitedy a LED in the dark showed normal latencies, gains, directions and veloci-ies (Grea et al., 2002). Her reaction time to a target change in position wasdentical to that of control subjects when evaluated by the production of an arbi-rary motor response to the target-jump (“location-stop” task in Pisella et al.,000).

.2. Experimental setup

Exp. 1 and Exp. 2 were conducted on the same experimental set-up withimply the instruction to look and point at visual targets presented in peripheralisual field in the dark. Subjects were placed in front of a 45◦ tilted pointing tableith their head fixed with a bite board (Fig. 2a). A tactile circle placed sagitally6 cm distant from the trunk served as hand start position. Four target lights wererojected on the table surface along the fronto-parallel line at the level of theubject’s gaze (Fig. 2b). These targets were virtual images of red light-emittingiodes (LEDs, diameter 3 mm) reflected on a mirror. This apparatus preventsubjects from detecting their pointing errors (no visual feedback of the handelative to the target) and consequently from developing strategic behaviours todjust their pointing movements. Subjects were instructed to initially fixate aED, designated as the eye start position, located 10◦ to the left with respect

o their trunk. They then had to look and point to three targets located 12.5◦,

0◦ and 27.5◦ to the right with respect to the trunk or at 22.5◦, 30◦ and 37.5◦f eccentricity in the right visual field, with respect to initial eye fixation (seeig. 2b). Coordinates in visual degrees are used throughout this paper. Horizontalye movements were recorded with an infrared optometric system (EyeLink, SR Research, Ontario) at a frequency of 250 Hz with an accuracy of 0.1◦.

tctcp

n the level of the table where the subjects reached. (b) Locations of the LEDsed as (saccadic and pointing) targets and eye fixation, with respect to the handtarting location.

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

.3. Behavioural paradigm

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

Among these 200 trials, 84% were ‘stationary trials’: the target LED wasresented at 22.5 (R2), 30 (R3) or 37.5 (R4) visual degrees until the end of therial; 16% of the trials were ‘jump trials’: the target LED was initially presentedt 30◦ (R3) and was suddenly extinguished at the beginning of the saccade (byeans of a two-point central difference velocity detection algorithm, adapted

rom Bahill & McDonald, 1983) and replaced by a target LED at 22.5 (J2:ackward jump) or 37.5 (J4: forward jump) degrees till the end of the trial.his target-jump was not consciously detected by subjects as it occurred during

he time of “saccadic suppression” (Goodale et al., 1986), which avoided anytrategic motor behaviour. When questioned at the end of the experiment, noubject was able to report the occurrence of the target jump. Exp. 2 was identicalxcept that the target-jump was synchronised to primary saccade offset insteadf onset.

.4. Analysis

The horizontal eye position signal was filtered (50 Hz cut-off frequency, finitempulse response filter FIR) and eye velocity was computed from the filteredosition signal using a two-point central difference derivative algorithm (Bahill

McDonald, 1983). In order to determine the sequence of eye movements, theeginning and the end of the primary and corrective saccades were automat-cally detected using a velocity threshold procedure (30◦ s−1). The results ofhis automatic procedure were then inspected off-line and corrected manually,f necessary. Several saccade-related parameters were computed; for primarynd corrective saccades, saccadic gain was calculated as the ratio between sac-adic amplitude and desired amplitude. Note that in the jump trials, the desiredmplitude of the primary saccade corresponded to the initial target location,hereas the desired amplitude of corrective saccades corresponded to the dif-

erence between eye position at the end of the primary saccade and final targetocation. Saccadic errors for the primary and corrective saccades were computeds the difference between final eye position and target position. In jump trials,he initial and the final target locations were used to compute saccadic errors for

he primary and the corrective saccades, respectively. Reaction times (RT) wereomputed with respect to target onset for primary saccades and with respect tohe end of the primary saccade for corrective saccades. Finally, the number oforrective saccades and the time of visual capture (period elapsing from targetresentation to the end of the last corrective saccade) were computed.

4 sychologia 46 (2008) 475–486

afmpttaet

2

2

spAtami

2

aWf1etoa

3

3

33dtrt

(gieio(spiFtswptp

eter

sin

stat

iona

rytr

ials

(mea

nan

dS.

D.)

for

the

cont

rolg

roup

(C)

and

the

two

patie

nts

with

OA

(AT

and

IG)

Targ

etpo

sitio

n(◦

)Pr

imar

ysa

ccad

esC

orre

ctiv

esa

ccad

esT

ime

ofvi

sual

capt

ure

(ms)

Err

or(◦

)R

T(m

s)G

ain

Num

ber

Err

or(◦

)R

T(m

s)

22.5

−2.0

0(1

.50)

248

(39)

0.91

(0.0

5)0.

34(0

.41)

−0.7

4(0

.64)

155

(42)

467

(28)

30−2

.39

(1.5

2)24

1(3

8)0.

92(0

.04)

0.42

(0.4

4)−0

.78

(1.2

3)16

5(6

0)49

1(6

8)37

.5−3

.68

(1.7

1)25

1(4

0)0.

90(0

.06)

0.62

(0.4

3)−1

.18

(1.3

1)15

5(4

1)50

9(6

7)

22.5

−2.3

3(2

.08)

461

(105

)0.

90(0

.07)

0.36

(0.4

9)−1

.22

(0.5

6)26

9(6

8)80

2(1

32)

30−3

.02

(2.3

5)43

7(1

12)

0.90

(0.0

6)0.

40(0

.50)

−0.9

3(0

.99)

232

(73)

792

(117

)37

.5−6

.03

(2.2

8)45

6(8

4)0.

84(0

.08)

0.95

(0.4

3)−1

.57

(1.4

2)24

7(4

1)82

5(9

6)

22.5

1.20

(2.3

5)23

5(3

7)1.

06(0

.12)

0.95

(0.9

5)−0

.58

(1.0

5)17

1(5

5)56

3(1

15)

30−4

.80

(3.1

1)23

8(4

5)0.

84(0

.10)

1.22

(0.6

8)−0

.61

(1.2

6)17

6(3

9)59

4(1

12)

37.5

−12.

26(3

.64)

237

(27)

0.67

(0.0

8)1.

74(0

.93)

−1.2

8(1

.27)

156

(55)

641

(106

)

78 V. Gaveau et al. / Neurop

For arm movements, the x, y, and z position signals were filtered at 10 Hz withsecond-order Butterworth dual-pass filter. Movement velocity was computed

rom the filtered position signal using a least square second-order polynomialethod (10 points moving window). The same method was used to com-

ute the acceleration of the hand from the velocity signal. The onset andhe end of the movements were computed automatically using the followinghresholds: hand velocity 80 mm/s and hand acceleration 150 mm/s2. Aftern automatic detection, a visual inspection of the results was performed forach trial. The hand-related parameter analysed in this study was hand reactionime.

.5. Statistics

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

cores of patients reliably differed from the control ones. For each patient, thesearameters were compared to those of the control group with repeated measuresNOVAs with Group as a factor. We adjusted the critical value of F in order to

ake the variance of the control group and the patient (AT or IG) into account,s proposed by Mycroft, Mitchell and Kay (2002). Note that in this statisticalethod for single-case studies, a significant effect at the 5% level (p′) is accepted

f the revised F-value exceeds 10.

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

nd in the control group the effect of target eccentricity and of target-jump.ithin each patient, a one-way ANOVA was performed with Trial type as a

actor. For the control group, a repeated-measures ANOVA was used. In Exp., contrast analyses (planned comparisons) were used to test the effect of targetccentricity or occurrence of target-jump on ocular or pointing behaviour. Theime of occurrence of the target-jump (at saccade onset in Exp. 1 versus saccadeffset in Exp. 2) was then used as an additional factor for the within-groupnalyses.

. Results

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

.1.1. Saccadic behaviour

.1.1.1. Control Group. Within-group analyses were con-ucted to determine the effect of target eccentricity or ofarget-jump on saccadic behaviour. All saccadic parameters areeported in Tables 1 and 2 for stationary and jump trials respec-ively.

The classical hypometry of primary saccades was observedmean gain of 0.91). The gain remained constant with tar-et eccentricity (F(2,8) = 0.8; p > 0.05), leading to a significantncrease of the absolute error of the primary saccade when targetccentricity increased (F(2, 8) = 10.4, p < 0.01) (Fig. 3a). Despitenitial saccadic hypometry, neither mean error nor reaction timef the corrective saccade differed across target eccentricitiesF(2, 8) < 1.30, p > 0.05). The reaction time of the correctiveaccade was significantly shorter than the reaction time of therimary saccade (F(1, 4) = 90, p < 0.01), in agreement with find-ngs from the literature (Prablanc & Jeannerod, 1975; Becker &uchs, 1969). The mean error and reaction time of the correc-

ive saccades showed no differences between target-jump andtationary trials (between stationary trials at 37.5◦ and trials

ith target displaced forward from 30◦ to 37.5◦: F(1,4) < 1.4,> 0.05 and between stationary trials at 22.5◦ and trials with

arget displaced backward from 30◦ to 22.5◦: F(1,4) < 5.4,> 0.05). Ta

ble

1Sa

ccad

icpa

ram

Gro

ups

C AT

IG

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)

nscljtssrIcrtc

3ttcItBbtTctWpgatsat

wa(e3b

mj

g(NpotteO

rrbrtsjarctcas

wFcPsIbp(te

In stationary trials, visual capture was usually achieved witho or a single corrective saccade (mean number of correctiveaccades = 0.46), the mean gain of the corrective saccade waslose to 1 (1.08) and thus accurate target capture (final errors ofess than 1◦) was achieved despite initial saccadic hypometry. Inump trials, control subjects achieved visual capture of the per-urbed target both by increasing the occurrence of a correctiveaccade (F(1,4) > 9.8, p < 0.05) and by changing its amplitudeo that the gain of the first corrective saccades computed withespect to the final target location remained close to 1 (1.03).n fact, visual capture was systematically achieved with a singleorrective saccade for backward jumps (mean number of cor-ective saccade = 1 with S.D. = 0) and with one or exceptionallywo corrective saccades for forward jumps (mean number oforrective saccade = 1.21).

.1.1.2. OA patients. The classical relationship between ampli-ude and duration (the main sequence) was observed for thewo patients, attesting that the dynamic characteristics of sac-ades were not altered by the lesion (see Supplementarynformation). Therefore, only the spatial (error and gain) andemporal (reaction time) saccadic parameters are detailed below.etween-group comparisons (Mycroft et al., 2002) revealed thatoth patients exhibited a larger hypometry of primary saccadeshan control subjects (revised F(1,4) > 10.2; p′ < 0.05; Table 1).his hypometry appeared outside the confidence interval of theontrol group for the most eccentric targets (Fig. 3b: only forhe 37.5◦ target in AT and for the 30 and 37.5◦ targets in IG).

ithin-group analysis revealed that with a mean gain of 0.84 forrimary saccades, patient IG, in fact, showed a higher saccadicain than that of the control group for the 22.5◦ target (1.06),gain of 0.84 for the 30◦ target and a reduced gain (0.67) for

he 37.5◦ target. Rather than a general gain reduction of primaryaccades, the deficit of patient IG is therefore best described aspathological decrease of the slope of the saccadic gain versus

arget eccentricity relationship.Yet, in both patients, the visual capture of the target

as always achieved with normal accuracy as the final errorfter the last corrective saccade did not differ from controls

revised F(1,4) < 6; p′ > 0.05 for both patients) at all targetccentricities and whenever the target-jump occurred (Figs.c and 4b). Thus OA patients could eventually correct foroth their own initial error resulting from hypometric pri-

ac1p

ary saccades and the experimental error due to the target-ump.

The time of visual capture computed with respect to tar-et onset was significantly delayed with respect to controlsTables 1 and 2; revised F(1,4) > 13; p′ < 0.05 for both patients).ote that if we consider the time of visual capture with respect torimary saccade onset, the two patients exhibited a similar delayf 100 ms for stationary targets, corresponding to an increasedime needed for ocular control. Detailed inspection revealed thathis common increase of the duration of the saccadic sequencexecution was expressed differently in the behaviour of the twoA patients.

Patient AT delayed her corrective saccade significantly withespect to the control group (revised F(1,4) = 25.3; p′ < 0.05) byoughly 100 ms for stationary (Table 1) and jump trials (Table 2)ut visual capture was achieved with a normal number of cor-ective saccades (revised F(1,4) = 8.0; p′ > 0.05). In stationaryrials, visual capture was achieved with no or a single correctiveaccade (mean number of corrective saccade = 0.57). The target-ump trials implied a significant increase of the occurrence ofcorrective saccade (F(1,66) = 61.97, p < 0.01). Similar to that

eported above for the control group, the mean gain of the firstorrective saccade computed with respect to the final target loca-ion remained close to 1 (0.98) in jump trials, such that visualapture was achieved with one systematic corrective saccadend very exceptionally with two (mean number of correctiveaccade = 1.16).

In patient IG, the reaction time of the first corrective saccadeas even significantly shorter than in the control group (revised(1,4) = 13.7; p′ < 0.05) but the number of corrective sac-ades was significantly higher (revised F(1,4) = 21.1; p′ < 0.05).atient IG needed one or two corrective saccades to capturetationary targets (mean number of corrective saccade = 1.30).n response to target-jumps, a further increase of the num-er of corrective saccades was observed (F(1,150) = 15.23,< 0.01), consequently delaying even more visual capture

F(1,150) = 17.9, p < 0.01). Indeed, in 65% of the backward jumprials and in 85% of the forward jump trials, the primary saccadicrror and the error due to the target-jump were compensated seri-

lly. In these trials, the mean gain of the first corrective saccadeomputed with respect to the final target location was far from(0.47 for forward and 2.08 for backward jumps). When com-

uted instead with respect to the initial target location (30◦), the

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

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.

V. Gaveau et al. / Neuropsychologia 46 (2008) 475–486 481

Conti

gttosTwmaItawccsqVs

ttatTpaol

33tt

tesm

3drgtdtrbgrcwcwshttic

3

Fig. 3. (

ain reached a mean value of 1.02, showing that the first correc-ive saccade was actually directed toward the first (extinguished)arget location. The first corrective saccade of IG allowed hernly to compensate her primary saccade error and at least aecond one was needed to compensate for the target-jump error.his is particularly clear from the example provided in Fig. 4a, inhich patient IG and the illustrated control subject exhibited pri-ary saccades with similar hypometry. Then, in both backward

nd forward jump trials, the first corrective saccade of patientG brought the eye to the position of the initial (extinguished)arget, whereas that of the control subject directly reached thectual (displaced) target position. This behaviour of patient IGas particularly striking for the backward target-jumps which

alled for a backward corrective saccade. In contrast to theontrol subject, patient IG executed a first forward correctiveaccade, away from the actual target location. Only the subse-uent corrective saccades were executed in the correct direction.isual capture was finally achieved by the fourth corrective

accade.This ‘serial’ behaviour characterised by normal reaction

imes of the first corrective saccade but a significant increase ofhe number of saccades was predominant in patient IG but shelso exhibited the same ‘parallel’ behaviour as patient AT. Thesewo behaviours in response to target-jump are distinguished inable 2 using the criteria of the number of corrective saccadesroduced to capture the displaced target (one or more than one;ccordingly, the reaction time of the first saccade is delayedr not relative to controls). The ‘serial’ behaviour caused theongest delay of visual capture.

.1.2. Eye–hand coordination

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

dtws

nued ).

he pointing movement consistently began at approximately thend of the primary saccade, and consequently, (2) a correctiveaccade was made during the execution of the pointing move-ent.

.1.2.2. OA patients. The temporal sequence of eye–hand coor-ination was consistently modified in the two patients withespect to that observed in healthy controls. Indeed, between-roup statistics (Mycroft et al., 2002) revealed in both patientshat the reaction time of the reaching response was markedlyelayed relative to controls (revised F(1,4) > 33; p′ < 0.05), sohat the pointing movement began at the time of the final cor-ective saccade (see Fig. 5). When patient IG exhibited the sameehaviour as patient AT, consisting of capturing the visual tar-et with a single but much delayed corrective saccade, the handeaction time temporally matched to the execution of the singleorrective saccade (IG left panel in Fig. 5). In the other trials, inhich patient IG captured the visual target with more than one

orrective saccade, the hand reaction time temporally matchedith the execution of the last corrective saccade. There was no

ignificant main effect of the occurrence of a target-jump onand reaction time. The lack of change of this temporal parame-er indicates that the distinct eye–hand coordination exhibited byhe two patients was not adopted in response to target-jumps butnstead corresponded to their standard behaviour in ecologicalonditions.

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

The main aspect of the saccadic deficit of OA patients was the

elayed time of visual capture. In order to test the hypothesis thathis deficit resulted from a delay in updating the target location,e conducted a second experiment in which the target-jump was

ynchronised on saccade offset instead of saccade onset. We

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

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)

V. Gaveau et al. / Neuropsychologia 46 (2008) 475–486 483

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 targetsw d ends atienb

eonpficdjo

3

tsbrpcbg(pdaEt

pgtvdt

3

rjcmipdtcc

4

apa

ith backward (J2) and forward (J4) jump. The parameters are: beginning ( ) anaccades (S2), beginning ( ) and end (�) of the hand pointing movement. In peen distinguished in two separate panels.

xpected to observe a behaviour similar in control subjects as inur two patients with bilateral OA, if the visual information of theew target location is provided with a delay of about 80 ms (meanrimary saccade duration). This delay shortens the time availableor visual updating and may therefore produce, as in OA, anmpairment of fast motor control. Within-group analyses wereonducted on the target-jump trials in order to test the effect ofelaying the visual information of the new target location (target-ump synchronised at primary saccade onset versus offset) oncular behaviour and on eye–hand coordination.

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

ime of visual capture (F(1, 4) = 14.70, p = < 0.05) in controlubjects (Table 3) resulting from both an increase of the num-er of corrective saccades (F(1, 4) = 61.45, p < 0.05) and of theeaction time of the (first) corrective saccade (F(1,4) = 17.46,< 0.05). In fact, in response to the delayed target-jump, theontrol subjects exhibited the two types of saccadic controlehaviours observed in the OA patients, which can be segre-ated based on the number of corrective saccades (see Table 3):1) ‘parallel’ behaviour: when only one corrective saccade wasroduced to achieve foveal capture, its occurrence was largely

elayed (257 ms in target-jump trials with respect to 158 ms onverage in stationary trials, and 172 ms in target-jump trials inxp. 1) leading to delayed visual capture (625 ms with respect

o 580 ms in Exp. 1); (2) ‘serial’ behaviour: the control subjects

eawp

nd for backward and forward jump trials (J2 and J4 respectively). The left panel deosition for the control group; the middle and right panels depict the means and stanctual final target positions.

( ) of primary saccades (S1), beginning ( ) and end ( ) of the last correctivet IG, the two saccadic behavioural types (“parallel” and “serial”, see text) have

roduced several corrective saccades to capture displaced tar-ets when the first corrective saccade was not delayed (reactionime of 170 ms as in Exp. 1: 172 ms) leading to a largely delayedisual capture (736 ms). The ‘parallel’ behaviour was used pre-ominantly by the control subjects (in 73.25% of the target-jumprials).

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

eaction time was not affected by the delay of the target-ump occurrence (F(1,4) = 1.18, p > .05). The classical eye–handoordination was observed, with the pointing movement onsetatching the offset of the primary saccade (as in Fig. 5). Point-

ng accuracy was also not significantly impaired (F(1,4) = 2.28,> .05) but the duration of pointing movement was significantlyelayed (F(1,4) = 8.60, p = .046): about 33 ms longer when thearget-jump occurred at saccade offset (Exp. 2) compared to sac-ade onset (Exp. 1); however this slight pointing delay was notomparable to the delay of saccadic capture.

. Discussion

Patients with bilateral OA have been shown in the literature to

xhibit a lack of fast motor control for hand movements (Grea etl., 2002; Pisella et al., 2000). In the present paper, we investigatehether this deficit resulting from a lesion of the PPC causes aathological delay in updating the location of the visual target.

picts the mean and confidence interval (1.96*standard deviation) of final eyedard deviations for patients AT and IG respectively. Dashed lines indicate the

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

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)

−1.9

Tslttpicts

4

pRrs(tentmP(wgtdop

4

Oc1hrs(pstr(

jocs

tmatsictw(pth

asvaf“s

OvPttrs

4

tstooa

Forward 1.54 (0.32)1 (53.5%) N = 30�2 (46.5%) N = 26

he slow visual processing of the target location is first demon-trated by showing that patients with bilateral OA also exhibit aack of fast motor control for saccadic eye movements (Exp. 1,arget-jump at primary saccade onset) and second by showinghat normal subjects exhibit the same ocular behaviour as OAatients if the visual information (of the final target location)s provided with a delay (Exp. 2, target-jump at primary sac-ade offset). After a detailed discussion of the results leading tohese conclusions, we will discuss the anatomical segregation ofaccade and reach modules within the PPC.

.1. Saccadic behaviour

The saccadic deficit included temporal and spatial com-onents, which can be expressed differently in patients (seeossetti, Pisella, & Vighetto, 2003 for a review of the tempo-

al and spatial aspects of OA). In the two OA patients of thistudy, the saccadic deficits mainly addressed fast ocular controlcharacterised by a delayed visual capture, especially when thearget jumped) and the pathological hypometry for large targetccentricities (>30 visual degrees). The experimental conditionsecessary to reveal these deficits are not used routinely in clinicalests, which may explain usual clinical reports that eye move-

ents are relatively preserved in OA (e.g. Baylis & Baylis, 2001;erenin & Vighetto, 1988; Rondot et al., 1977). A recent studyTrillenberg et al., 2007) reported intact saccades in a patientith optic ataxia, but the authors computed a global saccadicain related to the final saccadic accuracy which did not allowhem to reveal the hypometry of the primary saccade and theeficit of saccadic control (suggested by the closed inspectionf the typical eye trace presented on their Fig. 4) in their OAatient.

.2. Fast motor control

We argue that the delayed time of visual capture in the twoA patients reveals an impaired fast ocular control of the sac-adic sequence. Indeed, data from our control subjects in Exp.indicated that normal foveal capture is achieved by a slightly

ypometric primary saccade, sometimes followed by one cor-ective saccadic movement. In target-jump trials, the correctiveaccade is systematically initiated, and its spatial parametersamplitude, direction) are adjusted in order to capture the dis-laced visual target without the need for additional corrective

accades (Becker & Jurgens, 1979). In addition, it was shownhat the latency (and duration) of the single corrective saccadeemained similar in target jump and in stationary target trialsabout 160 ms). These observations indicate that in control sub-

swAi

2 (0.26) 244 (80)279(73)

692 (87)643 (75)

174 (35) 749 (64)

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

Patient AT produced a pairing of two saccades, irrespective ofhe trial type (stationary or jump), with a large temporal “safety

argin” for both primary and secondary saccades. Patient IGlso exhibited a single, delayed, corrective saccade in 25% ofhe target-jump trials (parallel compensation of intrinsic primaryaccade errors and errors due to the target-jump). However,n most trials, she instead produced an increased number oforrective saccades to achieve visual capture of the displacedargets. Strikingly, in these trials, her first “corrective” saccadeas generated with no RT increase and was directed to the initial

extinguished) target location (serial compensation of intrinsicrimary saccade error and error due to the target-jump). Clearly,his observation indicates that her oculomotor system did notave immediate access to the new retinal target location.

It is worth noting that despite the different “serial” and “par-llel” behaviours in target-jump trials, the patients showed theame additional delay of about 100 ms to capture stationaryisual targets. This pathological delay of visual capture revealedcommon deficit in fast ocular control. This conclusion is rein-

orced by Exp. 2, in which control subjects exhibited the sameserial” and “parallel” behaviours in response to a target-jumpynchronised on primary saccade offset.

Our prediction was that the deficit of fast ocular control inA patients results from an inability to update “on-line” theisual target location, as suggested by a previous study (Khan,isella, Rossetti, Vighetto, & Crawford, 2005). Consequently,

he time normally sufficient to implement the new target locationurns out to be too short. Accordingly, in Exp. 2 we showed thateducing the time available for visual updating could cause theame abnormal ocular control in control subjects.

.3. Eye–hand coordination

In the present “look and point” task, both OA patients spon-aneously delayed their hand movement onset to the end of theaccadic sequence (see Fig. 5 and reaction times on Table 3), i.e.o when the visual target location was eventually updated basedn central vision. Note that a similar behaviour can be observedn the typical eye–hand trace of the OA patient of Trillenberg etl. (2007, Fig. 4). This temporal sequence of eye–hand responses

uppresses the need for reaching in peripheral vision, and like-ise limits the need for fast control of hand reaching movement.ccordingly, bilateral OA patients are known to be specifically

mpaired for reaching in peripheral vision (Milner et al., 2003;

sycho

R2hintitwiet

4w

tvPerepnmlt

weetIiie

petreteufwlintupTal

ollv(otTae

C

A

fg

R

A

B

B

B

B

B

B

B

C

C

C

C

D

V. Gaveau et al. / Neurop

ossetti et al., 2005) and for fast reaching corrections (Grea et al.,002; Pisella et al., 2000). This eye–hand coordination patternas not been reported before, even in other neurological patientsmpaired for reaching (e.g. Desmurget et al., 2004) and was alsoot observed in the control group of the second experiment. It ishus probably not a strategy developed for the present task butnstead a spontaneous and unconscious behaviour adopted by thewo OA patients for all reach-and-grasp actions. This behaviourould explain why OA patients actually rarely complain from

naccuracy of hand movements in their everyday life (Rossettit al., 2003), and may thus reflect a functional compensation forheir lesion.

.4. Common or segregated saccade and reach regionsithin the PPC?

It is interesting to compare the deficit of fast ocular controlo the impairment of fast manual control demonstrated in pre-ious studies involving patients IG and AT (Grea et al., 2002;isella et al., 2000). For example, the “serial” saccadic behaviourxhibited by patient IG (Fig. 4a) is directly comparable to hereaching behaviour presented in Fig. 2A of the study of Great al. (2002). In both cases, and in contrast to control subjects,atient IG responded to the target-jump by performing first aon-modified response (either hand movement or eye move-ent sequence) toward the initial target location, followed by at

east one supplementary movement allowing her to achieve finalarget position.

The second aspect of the oculomotor deficits in OA patientsas the hypometry of primary saccades. Both OA patients

xhibited a primary saccadic error that increased with targetccentricity, with accuracy outside the confidence interval ofhe control group, at least for the most eccentric target (37.5◦).nterestingly again, pointing data from previous studies involv-ng patients IG and AT also revealed hypometric errors thatncreased with target eccentricity (Milner et al., 2003; Rossettit al., 2005).

Anatomically, one cannot rule out the possibility that theatients’ parietal lesions encroached upon nearby but segregatedye- and hand-related regions. However, the similarity betweenhe saccadic deficits demonstrated here and the reach deficitseported in the literature raises the possibility of a common pari-tal module for saccade and reach. This similarity concerns thearget localisation in peripheral vision (pathological increase ofye and hand hypometry with target eccentricity) and the fastpdating of target localisation (absence of fast corrections bothor hand and eye movements). Interestingly, the POJ region,hich has recently been identified as the focus of lesions in a

arge group of OA patients (Karnath & Perenin, 2005), is specif-cally activated in relation to reaching movements performed byormal subjects in peripheral vision (Prado et al., 2005). Fur-hermore, the same POJ region has been involved in dynamicpdating of the eye-centred spatial representation of peripheral

ointing targets (Medendorp, Goltz, Vilis, & Crawford, 2003).herefore, POJ is a potential anatomical candidate to subservecore visuo-spatial mechanism (“Where”), and a lesion at this

ocation would affect both eye and hand movements. The study

G

logia 46 (2008) 475–486 485

f unilateral OA patients (Perenin & Vighetto, 1988) has estab-ished a pattern of hand reaching deficits that combines errorsinked to the location of the visual target in the contralesionalisual field (field effect) and to the use of the contralesional handhand effect). The present results do not rule out the existencef a specific visuo-manual deficit (hand effect) correspondingo a mislocalisation of the ataxic hand (Blangero et al., 2007).hese deficits could correspond to the impairment of the twonatomical modules demonstrated in normal subjects by Pradot al. (2005).

onflict of interest

The authors report no conflicts of interest.

ppendix A. Supplementary data

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

eferences

ndersen, R. A., & Buneo, C. A. (2002). Intentional maps in posterior parietalcortex. Annual Review of Neuroscience, 25, 189–220.

ahill, A. T., & McDonald, J. D. (1983). Frequency limitations and optimal stepsize for the two-point central difference derivative algorithm with appli-cations to human eye movement data. IEEE Transactions on BiomedicalEngineering, 30, 191–194.

alint, R. (1909). Seelenlahmung des “Schauens”, optische Ataxie, raumlicheStorung der Aufmerksamkeit. Monatschrift fur Psychiatrie und Neurologie,25, 5–81.

aylis, G. C., & Baylis, L. L. (2001). Visually misguided reaching in Balint’ssyndrome. Neuropsychologia, 39, 865–875.

ecker, W., & Fuchs, A. F. (1969). Further properties of the human saccadicsystem: Eye movements and correction saccades with and without visualfixation points. Vision Research, 19, 1247–1258.

ecker, W., & Jurgens, R. (1979). An analysis of the saccadic system by meansof double step stimuli. Vision Research, 19, 967–983.

iguer, B., Jeannerod, M., & Prablanc, C. (1982). The coordination of eye, headand arm movements during reaching at a single visual target. ExperimentalBrain Research, 46, 301–304.

langero, A., Ota, H., Delporte, L., Revol, P., Vindras, P., Rode, G., et al. (2007).Optic ataxia is not only ‘optic’: impaired spatial integration of proprioceptiveinformation. Neuroimage, 36(Suppl. 2), T61–T68.

alton, J. L., Dickinson, A. R., & Snyder, L. H. (2002). Non-spatial, motor-specific activation in posterior parietal cortex. Nature Neuroscience, 5(6),580–588.

olby, C. L., & Goldberg, M. E. (1999). Space and attention in parietal cortex.Annual Review of Neuroscience, 22, 319–349.

onnolly, J. D., Andersen, R. A., & Goodale, M. A. (2003). FMRI evidence fora ‘parietal reach region’ in the human brain. Experimental Brain Research,153(2), 140–145.

onstantin, A. G., Wang, H., Martinez-Trujillo, J. C., & Crawford, J. D. (2007).Frames of reference for gaze saccades evoked during stimulation of lateralintraparietal cortex. Journal of Neurophysiology, (Jun 6)

esmurget, M., Gaveau, V., Vindras, P., Turner, R. S., Broussolle, E., & Thobois,

S. (2004). On-line motor control in patients with Parkinson’s disease. Brain,127, 1755–1773.

arcin, R., Rondot, P., & de Recondo, J. (1967). Optic ataxia localized in 2left homonymous visual hemifields (clinical study with film presentation).Revue Neurologique, 116, 707–714.

4 sycho

G

G

H

J

K

K

M

M

M

M

M

N

P

P

P

P

P

P

P

P

R

R

R

S

S

S

T

86 V. Gaveau et al. / Neurop

oodale, M. A., Pelisson, D., & Prablanc, C. (1986). Large adjustments invisually guided reaching do not depend on vision of the hand or perceptionof target displacement. Nature, 320, 748–750.

rea, H., Pisella, L., Rossetti, Y., Desmurget, M., Tilikete, C., Grafton, S., et al.(2002). A lesion of the posterior parietal cortex disrupts on-line adjustmentsduring aiming movements. Neuropsychologia, 40, 2471–2480.

olmes, G. (1918). Disturbances of vision caused by cerebral lesions. BritishJournal of Ophtalmology, 2, 353–384.

eannerod, M. (1986). Mechanisms of visuomotor coordination: A studyin normal and brain-damaged subjects. Neuropsychologia, 24(1), 41–78.

arnath, H. O., & Perenin, M. T. (2005). Cortical control of visually guidedreaching: Evidence from patients with optic ataxia. Cerebral Cortex, 15(10),1561–1569.

han, A. Z., Pisella, L., Rossetti, Y., Vighetto, A., & Crawford, J. D. (2005).Impairement of gaze-centered updating of reach targets in bilateral parietal-occipital damaged patients. Cerebral Cortex, 15(10), 1547–1560.

edendorp, W. P., Goltz, H. C., Vilis, T., & Crawford, J. D. (2003). Gaze-centered updating of visual space in human parietal cortex. The Journal ofNeuroscience, 23, 6209–6214.

ichel, F., & Henaff, M. A. (2004). Seeing without the occipito-parietal cortex:Simultagnosia as a shrinkage of the attentional visual field. BehaviouralNeurology, 15, 3–13.

ilner, A. D., Dijkerman, H. C., McIntosh, R. D., Rossetti, Y., & Pisella, L.(2003). Delayed reaching and grasping in patients with optic ataxia. Progressin Brain Research, 142, 225–242.

ilner, A. D., Dijkerman, H. C., Pisella, L., McIntosh, R. D., Tilikete, C.,Vighetto, A., et al. (2001). Grasping the past delay can improve visuomotorperformance. Current Biology, 11, 1896–1901.

ycroft, R., Mitchell, D. C., & Kay, J. (2002). An evaluation of statisticalprocedures for comparing an individual’s performance with that of a groupof controls. Cognitive Neuropsychology, 19, 291–299.

eggers, S. F., & Bekkering, H. (2001). Gaze anchoring to a pointing target ispresent during the entire pointing movement and is driven by a non-visualsignal. Journal of Neurophysiology, 86, 961–970.

esaran, B., Nelson, M. J., & Andersen, R. A. (2006). Dorsal premotor neurons

encode the relative position of the hand, eye, and goal during reach planning.Neuron, 51(1), 125–134.

erenin, M. T., & Vighetto, A. (1988). Optic ataxia: A specific disruption invisuomotor mechanisms. I. Different aspects of the deficit in reaching forobjects. Brain, 111(3), 643–674.

W

logia 46 (2008) 475–486

ierrot-Deseilligny, C., & Muri, R. M. (1997). Posterior parietal cortex controlof saccades in humans. In P. Thier & H.-O. Karnath (Eds.), Parietal lobecontribution to orientation in 3D space (pp. 135–148). Springer Verlag:Heidelberg.

ierrot-Deseilligny, C., Rivaud, S., Gaymard, B., & Agid, Y. (1991). Corticalcontrol of reflexive visually-guided saccades. Brain, 114(Pt. 3), 1473–1485.

isella, L., Grea, H., Tilikete, C., Vighetto, A., Desmurget, M., Rode, G., et al.(2000). An ‘automatic pilot’ for the hand in human posterior parietal cortex:Toward reinterpreting optic ataxia. Nature Neuroscience, 3, 729–736.

rablanc, C., Echallier, J. F., Komilis, E., & Jeannerod, M. (1979). Optimalresponse of eye and hand motor system in pointing. I. Spatio-temporal char-acteristics of eye and hand movements and their relationships when varyingthe amount of visual information. Biological Cybernetics, 35, 113–124.

rablanc, C., & Jeannerod, M. (1975). Corrective saccades: Dependence onretinal reafferent signals. Vision Research, 15, 465–469.

rado, J., Clavagnier, S., Otzenberger, H., Scheiber, C., Kennedy, H., & Perenin,M. T. (2005). Two cortical systems for reaching in central and peripheralvision. Neuron, 48, 849–858.

ondot, P., de Recondo, J., & Dumas, J. L. (1977). Visuomotor ataxia. Brain,100, 355–376.

ossetti, Y., Pisella, L., & Vighetto, A. (2003). Optic ataxia revisited: Visuallyguided action versus immediate visuomotor control. Experimental BrainResearch, 153, 171–179.

ossetti, Y., Revol, P., McIntosh, R., Pisella, L., Rode, G., Danckert, J., et al.(2005). Visually guided reaching: Bilateral posterior parietal lesions causea switch from fast visuomotor to slow cognitive control. Neuropsychologia,43, 162–177.

chluppeck, D., Glimcher, P., & Heeger, D. J. (2005). Topographic organiza-tion for delayed saccades in human posterior parietal cortex. Journal ofNeurophysiology, 94, 1372–1384.

nyder, L. H., Batista, A. P., & Andersen, R. A. (1997). Coding of intention inthe posterior parietal cortex. Nature, 386, 167–170.

nyder, L. H., Batista, A. P., & Andersen, R. A. (2000). Saccade-related activityin the parietal reach region. Journal of Neurophysiology, 83, 1099–1102.

rillenberg, P., Sprenger, A., Petersen, D., Kompf, D., Heide, W., & Helmchen,C. (2007). Functional dissociation of saccade and hand reaching control with

bilateral lesions of the medial wall of the intraparietal sulcus: Implicationsfor optic ataxia. Neuroimage, 36(Suppl. 2), T69–T76.

ardak, C., Olivier, E., & Duhamel, J. R. (2002). Saccadic target selectiondeficits after lateral intraparietal area inactivation in monkeys. The Journalof Neuroscience, 22, 9877–9884.