Neuropsychologia 50 (2012) Contents lists available at SciVerse ScienceDirect. Neuropsychologia

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1 Neuropsychologia 50 (2012) Contents lists available at SciVerse ScienceDirect Neuropsychologia journal homepage: The role of saccade preparation in lateralized word recognition: Evidence for the attentional bias theory Dorine Vergilino Perez a,c,n, Christelle Lemoine a, Eric Siéroff b,c, Anne-Marie Ergis b, Redha Bouhired a,c, Emilie Rigault a,c, Karine Doré-Mazars a,c a Laboratoire Vision Action Cognition, IUPDP, Université Paris Descartes, Sorbonne Paris Cité, Institut de Psychologie, 71 Avenue Edouard Vaillant, Boulogne Billancourt, Cedex, France b Neuropsychologie du vieillissement (EA 4468), IUPDP, Université Paris Descartes, Sorbonne Paris Cité, Institut de Psychologie, Boulogne Billancourt, France c Institut Universitaire de France, Paris, France article info Article history: Received 24 February 2012 Received in revised form 17 July 2012 Accepted 30 July 2012 Available online 7 August 2012 Keywords: Hemispheric asymmetry Right visual field advantage Saccadic eye movements Language Attention abstract Words presented to the right visual field (RVF) are recognized more readily than those presented to the left visual field (LVF). Whereas the attentional bias theory proposes an explanation in terms of attentional imbalance between visual fields, the attentional advantage theory assumes that words presented to the RVF are processed automatically while LVF words need attention. In this study, we exploited coupling between attention and saccadic eye movements to orient spatial attention to one or the other visual field. The first experiment compared conditions wherein participants had to remain fixated centrally or had to make a saccade to the visual field in which subsequent verbal stimuli were displayed. The orienting of attention by saccade preparation improved performance in a lexical decision task in both the LVF and the RVF. In the second experiment, participants had to make a saccade either to the visual field where verbal stimuli were presented subsequently or to the opposite side. For RVF as well as for LVF presentation, saccade preparation toward the opposite side decreased performance compared to the same side condition. These results are better explained by the attentional bias theory, and are discussed in the light of a new attentional theory dissociating two major components of attention, namely preparation and selection. & 2012 Elsevier Ltd. All rights reserved. 1. Introduction The human visual system is organized so that stimuli presented to the right visual field (RVF) are initially projected to the left primary visual cortex whereas stimuli presented to the left visual field (LVF) are projected to the right primary visual cortex. Many studies have examined whether this neuroanatomical contralateral organization is responsible for perceptual asymmetries observed on behavioral measures. One of the most studied asymmetries is the right visual field superiority (RVFS) for words, which accounts for the fact that words presented to the right visual field are recognized more readily than those presented to the left visual field (Mishkin & Forgays, 1952). Whatever the verbal task identification, lexical decision response time and accuracy measures improve when verbal stimuli are presented to the right of the fixation point rather than to the left (e.g., Nicholls & Clode, 1996; Faust, Babkoff, & Kravetz, 1995). n Correspondence author. Tel.: þ ; fax: þ address: dorine.vergilino-perez@parisdescartes.fr (D. Vergilino Perez). The RVFS may be explained by the structural model of cerebral asymmetry, assuming that the left hemisphere is solely responsible for verbal processing, or is at least the most efficient (Kimura, 1966; Allen, 1983), as contralateral organization of the human visual system implies a direct access to the language centers located in the left hemisphere for words presented to the RVF. LVF word presentation may require an inter-hemispheric transfer via the callosum corpus that explains longer reaction times in verbal tasks. Arguments for the structural hypothesis come from the work of Cohen, Dehaene and colleagues, who have shown that a portion of the left mid fusiform gyrus called the visual word form area (VWFA) is particularly responsive to visual words (McCandliss, Cohen, & Dehaene, 2003). The VWFA was initially considered as being invariant for spatial position, as it was activated for words regardless of their position of presentation in the visual field (Cohenet al., 2000; Cohen et al., 2002). However, a recent magnetoencephalography study found stronger VWFA responses for words presented to the RVF than to the LVF (Barca et al., 2011). Moreover, a direct relationship between individual language lateralization and visual half field advantages measured by behavioral studies has been reported recently (Hunter & Brysbaert, 2008; Van der Haegen, Cai, Seurinck, & /$ - see front matter & 2012 Elsevier Ltd. All rights reserved.

2 D. Vergilino Perez et al. / Neuropsychologia 50 (2012) Brsybaert, 2011). Left-handers with left hemisphere language dominance assessed by fmri responses during a word naming task showed an RVFS whereas left-handers with right hemisphere language dominance showed an LVF superiority. However, other explanations of the RVFS have been proposed based on a different allocation of spatial attention across the visual field that could depend on the hemisphere involved in the task processing or on how written language is processed by each hemisphere. In that, attentional hypotheses are not incompatible with the structural model. The attentional bias theory proposed by Kinsbourne (1970) suggests that visual field asymmetries are the result of an attentional imbalance between the hemispheres. The theory suggests that at rest, the two hemispheres are in a state of mutual inhibition resulting in distribution of attention over the two visual fields. However, preferential activation of one hemisphere by a task leads to deployment of attentional resources to the contralateral visual field. Thus, presentation of verbal material in a reading task, resulting in an activation of the left hemisphere, causes a bias of attentional resources to the right side of space. For left-to-right readers, this bias may be strengthened by reading habits, as attention constantly shifts in the direction of most eye movements. Considering spatial attention to be a component of visual asymmetries allows the attentional effects reported in numerous studies to be explained. A first attentional effect refers to the fact that when a word and a distractor are simultaneously presented in opposite visual fields, word identification is more impaired by presentation of the distractor to the RVF (i.e., the visual field in which the attention is mainly allocated) than to the LVF (Siéroff & Urbanski, 2002; Siéroff & Riva, 2011). Interestingly, such distractor effect is reversed when both the word and the distractor were presented in foveal vision, attached to each other in such a way that the word was presented to the left or to the right of the fixation position (Van der Haegen & Brysbaert, 2011). In such case, word presented to the LVF was better recognized than word presented in the RVF. Such a left visual field advantage has been explained in the context of the SERIOL model (Whitney, 2001) by considering that in this situation, both word and nonword were considered as a single unit that has to be processed serially. This model assumes that the letters of a word have to be processed serially with the help of an activation gradient that is based on the decreasing visual acuity from the fovea to the periphery. Whereas such gradient is adapted to RVF presentation, it has to be reversed for LVF information processing. Moreover in case of a single foveal word, information about RVF letter has to be inhibited until LVF letter information is transmitted to the left hemisphere. Such inversion gradient as well as inhibition processes require attention to focus on the initial word letters. A second attentional effect occurs in classical cueing paradigms in which the RVF Superiority is reduced when parafoveal word location is previously cued. This indicates that the LVF benefits more from the valid cue than the RVF (e.g., Mondor & Bryden, 1992; Ducrot & Grainger, 2007; Nicholls & Wood, 1998; Gatheron & Siéroff, 1999). This suggests that the LVF valid cue may counteract the RVF attentional bias by increasing attentional resources in the LVF whereas the RVF valid cue does not further increase the amount of attentional resources in the RVF. Whereas the attentional bias theory assumes that more attention is allocated to the RVF than to the LVF, the attentional advantage theory (Mondor & Bryden, 1992) proposes that the processing of verbal material in the RVF does not require as much attention as in the LVF. According to this model, the word is processed as a whole by the left hemisphere and letter-by-letter by the right hemisphere. Word-level processing and letter-level processing make different demands on attentional processing, the former requiring little or no attentional resources, the latter requiring important attentional resources (Lindell & Nicholls, 2003). Such automatic processing of verbal stimuli in the RVF also explains why an RVF valid cue does not help word recognition any further and why a distractor presented in the RVF decreases recognition of the word in the LVF. A recent neuroimaging study has provided arguments for the attentional advantage theory by showing that the fast and parallel RVF word recognition is underpinned by a network involving the left ventral occipitotemporal pathway including the VWFA, whereas serial letter-byletter scanning involved in LVF word processing is underpinned by the dorsal parietal attention system (Cohen, Dehaene, Vinckier, Jobert, & Montavont, 2008). Whether the RVF Superiority may be explained by the attentional bias theory or by the attentional advantage theory is still under debate. Siéroff and Riva (2011) provide an argument in favor of the attentional bias theory, as they show the same larger distractor effect on LVF words than on RVF words in young children and adults, although the effect of the distractor is globally much stronger in children indicating less automatic reading. If the asymmetric distractor effect was explained by automatic word processing of the left hemisphere, then one would expect a greater asymmetric distractor effect in adults for whom reading is more automatic. On the other hand, the greater word length effect for words as well as the larger effects of letter distortion such as case alternation for LVF words than for RVF words argue in favor of whole-word processing as assumed by the attentional advantage theory (see Ellis, 2004 and Lindell, 2006 for a review). Recently, Siéroff et al., 2012 proposed an attentional theory that could reconcile the two attentional hypotheses by taking into consideration two attentional components, namely preparation and selection (LaBerge, 1995). Divided visual field studies generally involve a first phase in which a warning signal allows the subjects to get ready to answer to the subsequent verbal task by allocating processing resources in the location where words are likely to occur. During this preparatory phase, distribution of attentional resources could be influenced by hemispheric activation as proposed by Kinsbourne (1970), as well as by reading habits. In the second phase, word presentation implies a deployment of selective attention that helps its identification. Different modes of selective attention may exist depending on visual field and reading direction. For left-to-right language, RVF word presentation implies that selective attention initially oriented to the first letters of the word could smoothly move to the other letters resulting in a very fast word processing. On the contrary, LVF word presentation implies that selective attention be oriented to the left which contradicts the natural tendency to read from left to right and takes more time, explaining the poorer performance in word recognition. Such mechanism may be compared to the cost of acuity gradient inversion proposed in the SERIOL model (Whitney, 2001). Thus, the attentional theory distinguishing preparatory and selective aspects of attention may help to understand why the distractor effect is reversed in foveal and attached presentation of the word and distractor, compared to parafoveal and separated presentation (Siéroff et al., 2012). It should be noted that in previously cited studies, covert attention is generally oriented by instructions or by a cueing paradigm with the gaze having to be fixated to the center of the screen. Lateralized verbal stimuli were presented briefly to avoid any eye movement in their direction, even if only recording of eye movement can really ensure that the eyes remain fixated on the central fixation point (see Bourne, 2006 for other methodological constraints in divided visual field studies). Some authors monitored eye movement but simply to discard trials with eye movement (e.g., Nicholls & Wood, 1998; Lindell & Nicholls, 2003; Calvo & Nummenmaa, 2009). It is quite surprising that

3 2798 D. Vergilino Perez et al. / Neuropsychologia 50 (2012) none of these studies exploited coupling between attention and saccade to orient attention. Indeed, it is now well known that preparation of a saccade to a spatial location induces a concomitant deployment of spatial attention at this location. This leads, in a detection task, to better performances at the saccade target location than at any other location of the visual field (Hoffman & Subramaniam, 1995; Kowler, Anderson, Dosher, & Blaser, 1995; Deubel & Schneider, 1996, Doré-Mazars, Pouget, & Beauvillain, 2004). To our knowledge, only one study has examined the effect of orienting attention by saccade preparation on the RVF superiority (Hyönä & Koivisto, 2006). Participants had to perform a lexical decision task on verbal stimuli presented 100 ms to the RVF or in the LVF. The fixation condition in which the participants had to remain fixated on the screen center did not involve any manipulation of attention as verbal stimuli were not preceded by any cue or any instructions. The move condition, in which the participants had to execute a saccade to the verbal stimuli before making their lexical decision, involved an overt attentional engagement. As expected, a RVFS was found in the fixation condition. However, in the move condition, saccade preparation toward verbal stimuli improved performance only in the LVF, leading to a cancellation of the RVFS. The authors interpreted their results in the context of the attentional advantage theory, suggesting that orientation of attention by saccade preparation allowed to cancel out the initial poorer performance in the LVF but did not increase the RVF performance due to automatic word processing. However, we trust that the results of Hyönä and Koivisto were not incompatible with the attentional bias theory. Indeed, if we consider that there is a maximal amount of attention that could be allocated to a region of visual space, then attention allocated to the RVF by saccade preparation may not be cumulated with the attentional resources due to the preexisting bias. Moreover, the fact that the deployment of attention linked to the saccade preparation compensated for the RVFS is surprising as most of the studies looking at the cueing effect have found a reduction rather than a cancellation of the RVFS (e.g., Ducrot & Grainger, 2007). The main objective of the two experiments presented here was to disentangle the attentional bias and the attentional advantage theories by building on coupling between spatial attention and saccade preparation. Moreover, we also tried to evaluate the respective contributions of covert and overt attention in the RVF Superiority. Indeed, it was previously shown that covert attention is sufficient to identify words in a divided visual field study, with better performance in the RVF than in the LVF (Calvo & Nummenmaa, 2009) and Hyönä and Koivisto s study suggests that the overt attention linked to saccade preparation increases performance in the LVF, but not in the RVF. In our study, spatial attention was oriented by both a cueing procedure and preparation of a saccade. The first experiment was inspired from Hyönä and Koivisto s as we asked participants to do a lexical decision task while remaining fixated on the screen centre during all the trial or while executing a saccade to the verbal stimuli. However, our study differs as we used a central cue, always valid, to indicate spatial location of the subsequent verbal stimuli as well as saccade direction. In the second experiment, the participants had to make a saccade in each trial. However, the central cue that indicated saccade direction was valid or invalid relative to the hemifield of presentation for verbal stimuli. We were particularly interested in the condition in which stimuli were presented to the RVF and a saccade executed on the opposite side, as this was the critical condition to disambiguate between the two attentional hypotheses. Indeed, since the attentional advantage theory assumes an automatic processing of verbal stimuli in the RVF, RVF performance should not be deteriorated by deployment of attention linked to saccade preparation to the LVF. Conversely, since the attention bias theory assumes that more attention is allocated to the RVF, RVF performance should decrease when attention is oriented to the LVF by saccade preparation. 2. Experiment Method Participants Sixteen French students (8 men) from the University of Paris Descartes took part in the experiment. All subjects had normal or corrected to normal vision, were between 19 and 32 (mean age: 23) and were right-handed (mean laterality score: 91%, from 81% to 100%). Their hand preference was determined by using the Humphrey Laterality Questionnaire modified by (Hécaen and Ajuriaguerra (1963), 22 items testing hand, eye and foot preferences). The study adhered to the principles of the Declaration of Helsinki Apparatus Stimuli were presented on an Iiyama HM240DT monitor with a refresh rate of 170 Hz and a resolution of pixels. The experimental sessions took place in a dimly lit room. Subjects were seated 57 cm away from the screen and their head kept stable with a chin and forehead rest. Eye movements were recorded with an Eyelink 1000 s (SR Research, Ontario, Canada), with a temporal resolution of 1000 Hz, and a spatial resolution of Viewing was binocular but only movements of the right eye were monitored. Each session began with a 9 point calibration over the entire screen. Before each trial, central fixation was checked and compared to the calibration. If the distance between the fixation check and the calibration was greater than 0.751, fixation was refused and a new calibration was initiated. When successful calibration was detected, the trial began. Online saccade detection corresponded to above-threshold velocity (301/s) and acceleration (80001/s 2 ) Stimuli The experimental material comprised 120 French four-letter nouns and 120 French four-letter pseudo-words, each divided in 4 lists of 30 items. The word frequency computed from the Lexique 3.71 database (New, Pallier, Ferrand, & Matos, 2001; New, Pallier, Brysbaert, & Ferrand, 2004) did not vary across word lists (mean: 47.8 occurrences per million, all t-tests non significant). The pseudo-words were constructed from real words by changing only one letter and conformed to the phonotactic rules of French. The stimuli were displayed in lowercase black letters on a white background in 14-point Bold Courier New Font. Each letter covered a visual angle of 0.51 horizontally and 0.51 vertically Procedure and design The participants performed the fixation and the saccade tasks in separate sessions. Each trial began with the presentation of a black double arrow for 500 ms at the screen s center (see Fig. 1). Four dashes were presented at 21 degrees of eccentricity (from the arrow center to the closest edge of the dashes) on both sides, at the same position of the stimuli when they were presented to the right or to the left of the fixation point. The double arrow was then replaced by a single arrow pointing to the right or to the left for 500 ms. In the Fixation task, the single arrow indicated the visual field in which the stimulus would appear. In the Saccade task, it also indicated the direction of the saccade as all the trials were valid. A trial was cancelled and replaced later if the participant s gaze deviated by more than

4 D. Vergilino Perez et al. / Neuropsychologia 50 (2012) from the arrow. Simultaneously to the extinction of the arrow (go-signal in the saccade task), a letter string was displayed for a duration adapted for each participant on a pre-experiment (see description below). For each participant, the stimulus duration was the same in the fixation and the saccade conditions, and should be shorter than the mean latency of a saccade. Indeed, in both fixation and saccade tasks, the stimulus should be processed only in parafoveal vision when the participants fixated the centre of the screen. In other words, in the saccade condition, the stimulus was expected to have disappeared at the time the eye movement started. Otherwise, the data were excluded (see Section 2.2). The participant had to decide whether or not the stimulus was a French word. A manual response was given at the end of the trial, after the stimulus extinction, by pressing one of the two designated buttons in the gamepad. Responses were always given with one hand, with the index finger for the yes response and the middle finger for the no. The hand of response was counterbalanced across participants. For each participant, a pre-experiment was conducted before the experimental sessions in which we adapted the time of presentation of the verbal stimuli in order to avoid chance performance and ceiling effects. Four blocks of 16 trials were presented, using the same procedure as the Fixation task. The stimuli differed from the experimental sessions. The duration of stimulus presentation was fixed at 80 ms for the first block. At the end of the block, the duration was increased or decreased depending on participants performance. The procedure was repeated for following blocks until a percentage of correct answers of approximately 80% was obtained. The mean duration was 76 ms (standard deviation: 16.3, range from 50 to 100). Each participant had to do the two tasks in two sessions of 120 trials each. The tasks order was maintained constant across subjects. They began by the fixation task in which they were asked to keep fixating the screen centre until responding. In the Fig. 1. Procedure used in the first experiment. After the verification of the calibration, a double arrow was displayed during 500 ms in the center of the screen. Four dashes were presented on either side, at the same position of the stimuli when they were presented to the right or to the left of the fixation point. The double arrow was then replaced by a single arrow pointing to the right or to the left for 500 ms and indicating the hemifield of the stimulus presentation in the fixation task, and the saccade direction. The verbal stimulus was displayed during a time adapted for each participant. saccade task, they were instructed to execute a saccade towards the visual field indicated by a cue at the moment of its disappearance. In each session, two lists of words and two lists of pseudo-words were presented. The presentation of the lists was counterbalanced between participants so that each list was presented in each of the 4 experimental conditions resulting from the crossing of the task instructions (Fixation vs. Saccade) and the visual field of presentation (Left or Right). Each item was seen only once by each participant but appeared in each of the four experimental conditions across them all. In each session, trials were randomized, so that participants could not anticipate on which side the stimulus would be presented Results Trials in which blinks occurred (0.1%) were eliminated from further analyses. In the Fixation task, we also eliminated trials in which a saccade was executed (7.4%). In the Saccade task, we eliminated trials in which a participant did not make an eye movement (5.75%), made it in the opposite direction relative to the arrow (0.7%), made a saccade with a latency shorter than the stimulus duration implying that the letter string was still on the screen when the saccade landed (3.78%), or made a saccade with short (o80 ms) or long (4800 ms) saccade latencies (2.96%). We first report data on saccadic latency and amplitude obtained with the saccade task. We ran a 2 2 Anova including visual field of presentation (Left or Right) and stimulus type (words vs. pseudo-words). For data focused on the RVF superiority (percentage of correct responses, sensitivity index d 0 and reaction time), we first verified that the responding hand did not modulate the results pattern by adding it to the analyses as a between-subject factor. As we did not find any effect of the responding hand, as well as no interaction with the withinsubject factors, we collapsed the data across the two modalities. So for the percentage of correct responses and the mean reaction time for correct responses, we ran a Anova including stimulus type (words vs. pseudo-words), visual field of presentation (Left or Right) and task instructions (Fixation vs. Saccade). As noted by Hyönä and Koivisto (2006), data on reaction time should be interpreted with caution as in the saccade task, the psychological refractory period could induce delayed secondary manual response due to the preceding saccadic eye movement (Wolf, Deubel, & Hauske, 1984). However, we have chosen to report these data as we did not find significant differences between mean reaction times obtained in fixation and saccade tasks. The means for correct responses and reaction times are shown in Table 1. As Hyönä and Koivisto, we computed the parametric sensitivity index of d 0 that measures detection accuracy in the context of the signal detection theory (see formula in Gescheider (1985)) and the index C that reflects a possible response bias (see formula in Snodgrass and Corwin (1988)). For these two measures, we ran a 2 2 Anova including visual field of presentation (Left or Right) and task instructions (Fixation vs. Saccade). Table 1 Percentage of correct response and reaction time (in ms) relative to the task instructions (fixation vs. saccade), hemifield of stimulus presentation (LVF vs. RVF) and stimulus type (word vs. pseudo-words). Fixation Saccade LVF RVF LVF RVF Word Pseudo-word Word Pseudo-word Word Pseudo-word Word Pseudo-word % of correct response 69.7 (17.8) 79.9 (11.3) 84.7 (9.2) 83.7 (8.6) 72.5 (12.8) 82.7 (12.8) 88.9 (8.3) 86.4 (11.2) Reaction time (ms) 885 (285) 1163 (493) 765 (236) 945 (309) 880 (288) 1112 (418) 738 (194) 942 (290)

5 2800 D. Vergilino Perez et al. / Neuropsychologia 50 (2012) Saccadic latency and amplitude The mean latency was of ms739 ms with no significant differences between words and pseudo-words (177 ms742 ms, and 174 ms738 ms, Fo1) and between LVF and RVF (174 ms740 ms, and 177 ms739 ms, Fo1). The interaction between both factors failed to reach significance (F(1,15)¼3.83, po06). The mean saccade amplitude was of However, the analysis of variance revealed a significant effect of the visual field of presentation (F(1,15)¼5.04, po04), indicating that saccades directed to the LVF had larger amplitudes ( ) than saccades to the RVF ( ). Such an effect interacted with the type of stimulus (F(1,15)¼6.31, po03) as it was only marginal for words ( vs , F(1,15)¼2.88, po10) and significant for pseudo-words ( vs , F(1,15)¼6.88, po01). Note, however, that the effect of 0.21 was below the spatial accuracy of eye movement. and Koivisto, as the RVFS was maintained in the saccade condition. We estimated a possible bias in performance by computing the index C. A completely neutral bias has a C value of 0 whereas a conservative bias induces a positive value and a liberal bias a negative value. As shown in Fig. 2, we obtained C values relatively close to 0 in each experimental condition. However, the analysis of variance revealed a significant effect of the visual field of presentation (F(1,15)¼19.10, po0006), indicating that the participants presented a conservative bias when they responded to stimuli presented to the LVF and a tendency to be liberal for stimuli to the RVF. The greater bias to respond word with RVF presentation compared to that of the LVF has already been reported in other studies (e.g., Babkoff, Faust, & Lavidor, 1997). There was no task effect and no interaction between the two factors (Fso1) Probability of correct response The Anova ran on the probability of correct responses revealed significant effects of the visual field of presentation (F(1,15)¼ 22.02, po0003) and the task instructions (F(1,15)¼4.35, po05). We found a right visual field superiority as the percentage of correct response was significantly better for stimuli presented in the RVF than in the LVF. The percentage of correct response was also greater in the saccade than in the fixation task. The interaction between the two factors was not significant (Fo1), indicating that a right visual field superiority was found for the fixation task but also for the saccade task. This differs from Hyönä and Koivisto (2006) who found a disappearance of right visual field superiority in the saccade condition, with equally good performance in both hemifields. The main effect of the stimulus type was not significant (F(1,15)¼1.94, ns). However, the type of stimulus interacted with the visual field of presentation (F(1,15)¼19.35, po0005), indicating an effect of the visual field presentation for words (F(1,15)¼28.91, po0005) that was only marginal for pseudowords (F(1,15)¼3.75, po07). Moreover, performance was better for words than for pseudo-words in the LVF (F(1,15)¼7.03, po02) but not in the RVF (Fo1). Finally, there was no interaction between the three factors (Fo1) Sensitivity index d 0 and response bias index C Data presented in Fig. 2 seem to be in accordance with results obtained on the probability of correct responses. A RVFS appears for both fixation and saccade tasks, even if performance is better in the latter. The analysis of variance confirmed these descriptive results: the main effects of visual field presentation and of task instructions were significant (F(1,15)¼19.41, po0005 and F(1,15)¼4.70, po04, respectively), with no interaction between the two (Fo1). Again, we failed to replicate the results of Hyönä Fig. 2. Sensitivity index d 0 (left panel) and response bias index C (right panel) as a function of the task instructions (fixation vs. saccade) and the hemifield of stimulus presentation (LVF vs. RVF) Reaction time Reaction times for correct responses yielded a main effect of the stimulus type (F(1,15)¼19.37, po0005), with longer reaction times for pseudo-words than for words and as expected a main effect of the visual field presentation (F(1,15)¼16.87, po0009), with longer reaction times for stimuli presented in the LVF than in the RVF. There was no effect of the task instructions (Fo1) as well as no interactions (Fo1) Discussion In this experiment, we used fixation and saccade conditions similar to those of Hyönä and Koivisto (2006), except that a central cue, always valid, indicated the visual field in which verbal stimuli appeared. We did not replicate their results. Indeed, they found equally good performance in both visual fields when the participants had to make a saccade to the LVF or RVF and performance in the RVF identical in the fixation and saccade conditions. Using the context of the attentional advantage theory, they concluded that saccade preparation allowed deployment of attentional resources to the LVF, overcoming its disadvantage found in a fixation condition but did not benefit the RVF in which word processing required less attention. Our results differed as we found a RVFS in the fixation as well as in the saccade conditions, with better performance in both LVF and RVF when participants had to make a saccade. This suggests that if attentional resources due to saccade planning help performance in both visual fields, this does not cancel out the RVFS. This is in agreement with previous studies showing that cue or instructions reduce RVFS but do not cancel it (e.g., Ducrot & Grainger, 2007). Increased performance for words presented to the RVF in the saccade condition compared to the fixation condition are better explained by the attentional bias theory, assuming that deployment of attention due to saccade preparation leads to better performance in the LVF, that has initially limited attentional resources, but also in the RVF by cumulating with the existing attentional bias due to hemispheric activation and reading habits (Kinsbourne, 1970). However, a critical condition to disambiguate between the two attentional theories would consist in using invalid cues to direct the saccade to the opposite visual field from the one in which verbal stimuli will appear. Whereas the attentional advantage theory assumes that performance in the RVF should not be deteriorated by engagement of attentional resources due to saccade preparation in the LVF, the attention bias theory predicts that it should. In order to test these hypotheses, we conducted a second experiment, in which the participants had to make a saccade to the visual field in which verbal stimuli appeared subsequently or to the opposite one.

6 D. Vergilino Perez et al. / Neuropsychologia 50 (2012) Experiment Method Participants Thirty-two French students (16 men) from the University of Paris Descartes took part in the experiment. All subjects had normal or corrected to normal vision, were between 19 and 31 (mean age: 24) and were right-handed (mean laterality score: 94%, from 81, 81% to 100%) Apparatus and stimuli The apparatus and stimuli were the same as in Experiment Procedure and design The procedure was similar to the one used in the first experiment, except that the participants only performed the saccade task (240 trials). As in the first experiment, they had to execute a saccade toward the visual field indicated by the single arrow. However, verbal stimuli could be displayed in the same visual field (valid trials) or in the opposite visual field (invalid trials) with a proportion of 50/50. The presentation of the lists was counterbalanced between participants so that each list was presented in each of the 4 experimental conditions resulting from crossing the visual field of stimulus presentation (Left or Right) and the saccade direction (Same vs. opposite direction relative to the visual field of presentation). Each item was seen only once by each participant but appeared in each of the four experimental conditions across all participants. Experimental trials were randomized. The mean duration of verbal stimuli was 85 ms (standard deviation: 18.9 ms, range from 50 ms to 120 ms) Results Trials in which blinks occurred (0.03%) were eliminated from further analyses. We also eliminated trials in which a participant did not make an eye movement (8.7%), made it in the opposite direction relative to the arrow (10.35%), made a saccade with a latency shorter than the stimulus duration implying that the letter string was still on the screen when the saccade landed (15.18%), or made a saccade with short (o80 ms) or long (4800 ms) saccade latencies (4.03%). As in the first experiment, we first checked a potential effect of the responding hand on the percentage of correct response, the d 0 and the reaction time. Again, we did not find any effect of the responding hand and collapsed the data across the two modalities Saccadic latency and amplitude Saccade latency was longer when the saccade was planned to the opposite side than to the same side of the stimulus presentation (248 ms768 ms, and 161 ms731 ms, respectively). Although the participants had 500 ms to prepare a saccade in the direction indicated by the central arrow, the abrupt onset of verbal stimuli in the opposite visual field automatically triggered the execution of a saccade towards it that had to be inhibited. Such a latency difference between the same side and the opposite side conditions may be related to the classical differences found between pro- and anti-saccades (Munoz & Everling, 2004). Here, the difference of 87 ms between the two saccadic conditions was significant (F(1,31)¼99.93, po0005). Moreover, we also found a smaller but significant difference of 16 ms between the latency of saccades directed to the LVF or RVF, the former being longer than the latter (212 ms754 ms vs. 196 ms745 ms, F(1,31)¼10.85, po002). The interaction between the visual field of stimulus presentation and the saccade direction failed to reach significance (F(1,31)¼3.07, po08). We did not find any other significant effect or interactions (Fso1). Saccade amplitudes were only affected by the saccade direction, the amplitude of saccades directed to the opposite side of visual stimulus presentation being larger than the amplitude of saccades directed to the same side ( vs , respectively, F(1,31)¼7.63, po009).this difference of 0.81 could be understood as an inaccuracy of the saccade directed to the visual field with no stimulation Probability of correct response Table 2 presents the percentage of correct response for words and pseudo-words displayed in the LVF and in the RVF when a saccade is directed to either the same or the opposite visual field. The Anova ran on the data indicated a main effect of the visual field presentation (F(1,31)¼53.41, po0005) as well as a main effect of the saccade direction (F(1,31)¼14.06, po0008) with no interaction between the two factors (Fo1). This showed that although performance is better when the participant planned a saccade to the visual field in which a stimulus subsequently appeared, a RVFS was found in this condition as well as when the saccade was planned in the opposite direction. Note that the type of stimulus interacted with the saccade direction (F(1,31)¼18.39, po0002) as well as with the visual field of presentation (F(1,31)¼11.36, po002), its main effect being not significant (Fo1). The first interaction means that the effect of the saccade direction was shown for words (F(1, 31)¼24.52, po0005) but not for pseudo-words (F(1,31)¼2.03, ns). The second interaction indicated a stronger RVFS for words, although the RVFS was significant for both words and pseudo-words (F(1,31)¼38.65, po0005 and F(1,31)¼11.72, po002, respectively) Sensitivity index d 0 and response bias index C As in the first experiment, we analyzed our data in the context of the signal detection theory by computing the d 0 and the index C. As shown in Fig. 3, performance in terms of perceptual capacity is better for stimuli presented in the RVF than in the LVF in both same- and opposite-side conditions. As for the probability of correct response, the performance increased when the saccade was planned to the visual field in which the stimulus Table 2 Percentage of correct response and reaction time (in ms) relative to the saccade direction (same side vs. opposite side from the stimulus), hemifield of stimulus presentation (LVF vs. RVF) and stimulus type (word vs. pseudo-words). Same side Opposite side LVF RVF LVF RVF Word Pseudo-word Word Pseudo-word Word Pseudo-word Word Pseudo-word % of correct response 74,1 (11.8) 72.7 (14.9) 91.9 (7.3) 78.6 (11.1) 60.1 (23.8) 75.4 (14.8) 78 (21.7) 81.7 (17) Reaction time (ms) 985 (506) 1171 (537) 813 (367) 1033 (548) 1281 (689) 1205 (683) 1156 (654) 1136 (616)

7 2802 D. Vergilino Perez et al. / Neuropsychologia 50 (2012) General discussion Fig. 3. Sensitivity index d 0 (left panel) and response bias index C (right panel) as a function of saccade direction (same side vs. opposite side from the stimulus) and the hemifield of stimulus presentation (LVF vs. RVF). subsequently appeared. The Anova confirmed these results, by showing a main effect of the visual field of presentation (F(1, 31)¼63.75, po0005) and a main effect of the saccade direction (F(1,31)¼14.23, po0007), with no interaction between these factors (Fo1). As in the first experiment, the analysis of the index C showed that the participants presented a conservative bias for stimuli presented in the LVF and a liberal bias for stimuli presented in the RVF, the difference being significant (F(1, 31)¼18.71, po0001). The Anova also revealed an effect of the saccade direction (F(1, 31)¼18.97, po0001), indicating a conservative bias when the saccade was made to the visual field opposite that of the verbal stimulus presentation and a liberal bias when the saccade was made in the same visual field. There was no interaction between the two factors (F(1, 31)¼1.79, ns) Reaction time As expected, the Anova ran on mean reaction times showed a main effect of the visual field of presentation (F(1,31)¼23.47, po0005), with longer times for stimuli presented in the LVF than in the RVF. The saccade direction also affected the mean reaction times (F(1,31)¼11.04, po002) that were longer when the saccade was made to the visual field opposite that of the verbal stimulus presentation. We also found a main effect of the type of stimulus (F(1,31)¼5.51, po02), with longer reaction time for pseudo-words than for words. The interaction between the type of stimulus and the saccade direction was significant (F(1,31)¼32.48, po0005) indicating that the saccade direction effect occurred only for words (F(1,31)¼24.42, po0005) Discussion In the second experiment, we used the central cue to indicate the visual field in which the saccade had to be executed. The cue could be valid when verbal stimuli appeared on the same visual field or invalid when it appeared on the opposite visual field. In valid trials which correspond to the saccade condition of the first experiment, again we did not replicate Hyönä and Koivisto s results: the allocation of attentional resources to the LVF induced by the saccade preparation did not cancel out the RVFS. However, the condition of interest to distinguish between the attentional bias and attentional advantage theories relied on trials in which the central cue oriented attention to the LVF whereas verbal stimuli appeared in the RVF. In this condition, the attentional advantage theory predicts that the performance for words presented in the RVF should not be affected by the LVF cue and so should be equal to valid RVF cue whereas the attentional bias theory predicts a decrease in performance compared to the valid RVF cue. Our results clearly argue in favor of the attentional bias theory as the performance measured by the percentage of correct response and by the d 0 clearly decreased for verbal stimuli presented in the RVF preceded by an invalid cue compared to a valid cue. In this study, we conducted two experiments, inspired from the work of Hyönä and Koivisto (2006), in which we examined the effect of orienting attention by saccade preparation on the RVFS. In the first experiment, we used similar fixation and saccade conditions. In the fixation condition, the participants had to do a lexical decision task on verbal stimuli displayed in the LVF or RVF by remaining fixated on the center of the screen, whereas in the saccade condition, they had to execute a saccade toward the visual field in which verbal stimuli were displayed. Whereas both studies found a RVFS in the fixation condition, they differed in the saccade condition. In Hyönä and Koivisto s work, saccade preparation toward the stimulus improved performance only in the LVF, cancelling the RVFS. In the RVF, performance was equivalent in the two conditions. They concluded, in the context of the attentional advantage theory, that orientation of attention by saccade preparation increased performance in the LVF where little attention was allocated, but did not benefit the RVF, where automatic word processing did not necessitate much attention. Their results are coherent with the work of Mondor & Bryden (1992) showing also a cancellation of the RVFS when a cue oriented attention to the LVF, even in the case of short delays between the apparition of the cue and the verbal stimuli. In Hÿonä and Koivisto s study, attention was simply oriented by saccade preparation. The mean saccade latency, which represented the delay to orient attention, was of 156 ms, and so coherent with Mondor & Bryden s delays. However, it should be noted that many other studies found reduction rather than cancellation of the RVFS (e.g., Nicholls & Wood, 1998; Nicholls, Wood, & Hayes, 2001; Ducrot & Grainger, 2007). Our results are in agreement with these studies as deployment of attention by saccade preparation increased performance in both LVF and RVF, without overcoming the RVFS. The benefit in the RVF as well as in the LVF argues for the attentional bias theory. Moreover, this suggests that overt attention can be cumulated with covert attention to increase performance in both visual fields. This result fits in with a previous study showing that covert attention is sufficient to identify words in a divided visual field study, with better performance in the RVF than in the LVF (Calvo & Nummenmaa, 2009). In the second experiment, we contrasted trials with valid and invalid cue involving the execution of a saccade in the same or in the opposite visual field in which the verbal stimuli were displayed. We were particularly interested in the condition in which the stimuli were presented to the RVF and the saccade executed toward it or on the opposite side. The decreased performance in the latter condition compared to the former argues again for the attentional bias theory. The question may arise of the differences between our works and Hÿonä and Koivisto s? Methodological differences can be put forward. Indeed, in Hÿonä and Koivisto s study, verbal stimuli were briefly presented during 100 ms for all participants. Here, we adapted in a pre-experiment the time of presentation of verbal stimuli that was on average between 75 ms and 85 ms in the first and second experiment, respectively. It is possible that a 100-ms presentation made the lexical decision task too easy in the saccade condition. However, in this case, ceiling effects should have been highlighted on both the percentage of correct responses and d 0. Another methodological difference, and, to our view, the crucial difference, is related to the way attention is directed to one or the other visual field, involving preparatory attention or not, in addition to attentional selection components (Laberge, 1995). In Hÿonä and Koivisto s study, there was no manipulation of spatial attention other than that due to saccade preparation. The authors did not use any cue or instructions to orient covert attention. In other words, their experiment did not

8 D. Vergilino Perez et al. / Neuropsychologia 50 (2012) allow any preparatory phase and attention could only select the word target location when it appeared. As proposed by the new attentional bias theory presented by Siéroff et al. (2012), selective attention could be naturally directed to the right in left-to-right languages, implying that the initial orientation to the first letters could be smoothly moved to the final letter resulting in a very fast word processing in the RVF, in the fixation as in the saccade conditions. On the contrary, our task allows the dissociation of the two components of attention. Indeed, the central cue presented during 500 ms induced a preparatory phase during which our participants could prepare for the subsequent verbal task by allocating processing resources at the location where words are likely to occur. Siéroff et al. (2012) expanded on Kinsbourne, 1970 theory and proposed that distribution of attentional resources during this preparatory phase might be influenced by hemispheric activation. Riva and Siéroff (2010) have provided arguments for that by showing that a distractor deteriorates the performance more significantly when it is presented before the word than simultaneously for RVF as well as LVF words. The RVF attentional bias occurring during the preparatory phase before word presentation is also compatible with the larger visual half field differences observed with bilateral than with unilateral presentation (Boles, 1987; Boles, 1990; Hunter & Brysbaert, 2008). Boles (1990) had suggested that activation of homologous areas in the two hemispheres by a bilateral presentation caused a disruption of the inter-hemispheric transfer, resulting in even worse performance for stimuli presented to the LVF (Boles, 1990). However, one can expect that such disruption of the inter-hemispheric transfer does not deteriorate good performance for RVF stimuli presentation due to distribution of attentional resources. It should be noted that the RVFS, consistently found in our data regardless of whether the experiment was conducted in the fixation or saccade conditions, can also be explained by the structural hypothesis (Kimura, 1966; Allen, 1983), considering that the left hemisphere is solely responsible for verbal processing, or is at least the most efficient. However, as mentioned in the introduction, structural and attentional factors were not incompatible and our results clearly argue for a role of attention in the RVFS, in addition to structural factors. Indeed, we show a modulation of performance by the attentional component due to saccade preparation to the LVF as well as to the RVF. Thus, the performance improves when the subject has to prepare a saccade to the visual field in which verbal stimuli will be displayed and decreases when the subject prepares a saccade to the opposite visual field. Another argument for a role of attention comes from the fact that in the second experiment, saccades directed to the LVF had longer latencies than saccades directed to the RVF. Earlier studies looking at the saccade characteristics have shown such left-right asymmetry for right-handers but not for left-handers (e.g., Pirozzolo & Rayner, 1980; Hutton & Palet, 1986). The leftright asymmetry has been taken as a behavioral indicator of hemispheric specialization for oculomotor control, the left hemisphere being more efficient than the right one at executing visuomotor tasks. This difference in efficiency was hypothetically enhanced by reading habits. However, another study failed to replicate it in data averaged over subjects but found it at the individual level, arguing for a cognitive explanation linked to a visuospatial attention bias specific to individuals (Honda, 2002). Note that we also failed to find the left-right asymmetry on saccade latencies in the first experiment. To orient attention by preparation of an eye movement appears to be an interesting line of research in the study of lateralized word recognition. The eye movement recording is now made easier by the development of new systems and opens new possibilities. By manipulating the mode of triggering of the saccades involving reactive or voluntary saccades or the delay of their preparation, it could be possible to further investigate the two attentional components preparatory attention and selection in line with the recent theory proposed by Siéroff et al. 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