Exp Brain Res (2010) 205:521–531 DOI 10.1007/s00221-010-2390-4

RESEARCH ARTICLE

Event-related potentials before saccades and antisaccades and their relation to reaction time Marianna Papadopoulou • Ioannis Evdokimidis Evangelos Tsoukas • Asimakis Mantas • Nikolaos Smyrnis



Received: 10 March 2010 / Accepted: 31 July 2010 / Published online: 14 August 2010 Ó Springer-Verlag 2010

Abstract In the present study, reaction time (RT) was measured in 12 healthy subjects in a saccade and antisaccade task while recording electroencephalographic activity (EEG) from 62 electrodes on the scalp. Event-related potentials averaged both on target appearance and on saccade onset were larger in amplitude (increased negativity) for the antisaccade task compared to the saccade task. The relation of RT variability to EEG amplitude was studied by averaging stimulus-aligned and movement-aligned individual trials for each subject into four RT quartile groups. The analysis showed a relation of EEG amplitude to RT for both saccades and antisaccades. More specifically, the ERP negativity at 100–120 ms after stimulus onset in the saccade task and at 160–200 ms after stimulus onset in the antisaccade task for stimulus-aligned ERPs decreased monotonically with increasing RT as would be expected if this signal would be related to the eye movement preparation processes. This was much more pronounced and wide spread for the antisaccades than for visually triggered saccades. The peak negativity before movement onset for movement-aligned ERPs also covaried with RT suggesting no relation of this activity to movement preparation processes. This study then confirmed that only a particular ERP signal variation was related to the saccadic eye

M. Papadopoulou  I. Evdokimidis  E. Tsoukas  A. Mantas  N. Smyrnis Cognition and Action Group, Neurology Department, Medical School, National University of Athens, Aeginition Hospital, 72-74 Vas. Sofias Av, 11528 Athens, Greece N. Smyrnis (&) A’ Psychiatry Department, National University of Athens, Medical School, Aeginition Hospital, 74 Vas. Sofias Av, 11528 Athens, Greece e-mail: [email protected]

movement preparatory processes while other components of the ERP have no specific relation to the movement preparation. This particular signal was more prominent for antisaccades compared to visually triggered saccades supporting previous evidence for the cortical involvement in the preparation of these voluntary eye movements. In conclusion, this study validates the use of ERPs in the study of the planning and execution of saccadic eye movements. Keywords EEG  Saccade  Antisaccade  Reaction time  Event-related potentials

Introduction The cortical mechanisms underlying the generation of saccadic eye movements have been the focus of a large body of literature (Johnston and Everling 2008; PierrotDeseilligny et al. 2004). One method to study these mechanisms in humans has been the use of electroencephalography (EEG) and more specifically the use of event-related potentials (ERPs) that are the average electroencephalographic responses aligned to an event, either the target appearance or the saccade onset (Richards 2003). In humans, saccadic eye movements are preceded by two distinct ERPs when the EEG responses are aligned to the onset of the saccadic eye movement toward either a visual stimulus or the remembered location of a previously presented visual stimulus. The first potential is the presaccadic negativity that is similar to the readiness potential recorded before finger movements, and the second potential is the presaccadic positivity that is similar to the premotor positivity prior to finger movements (Becker et al. 1972). The negative potential begins at approximately 1 s

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before saccade onset and reaches its maximum over the vertex (Becker et al. 1972; Klostermann et al. 1994; Kurtzberg and Vaughan 1980, 1982; Moster and Goldberg 1990). The positive presaccadic potential begins 30–300 ms before saccade onset and is located primarily over the parietal regions contralateral to saccade direction (Becker et al. 1972; Csibra et al. 1997; Kurtzberg and Vaughan 1980, 1982; Moster and Goldberg 1990). A sharp positive potential that was named ‘‘spike potential’’ is also recorded over parietal electrodes 10–20 ms before saccade onset (Balaban and Weinstein 1985; Becker et al. 1972; Csibra et al. 1997; Kurtzberg and Vaughan 1980, 1982; Weinstein et al. 1991). The presaccadic ERPs have been shown to be influenced by task parameters. Thus, they are larger and more widespread when saccades are generated toward expected peripheral stimuli in time or predicted locations in space (Evdokimidis et al. 1991, 1992, 1997; Kurtzberg and Vaughan 1982; Thickbroom and Mastaglia 1985). ERPs are also larger for voluntary compared to reflexive saccades (Balaban and Weinstein 1985; Evdokimidis et al. 1991). When EEG responses are aligned to the target appearance, a negative potential emerges about 100 ms after target appearance over central electrodes (Brickett et al. 1984; Evdokimidis et al. 1996; Everling et al. 1998). A task where a reflexive saccade has to be suppressed and a voluntary saccade has to be performed in the opposite direction is the antisaccade task (Hallett and Adams 1980). ERPs elicited when subjects performed the antisaccade task have also been studied. Brickett et al. (1984) observed significantly larger negativity at central locations for the antisaccade task when ERPs were averaged on target appearance (Brickett et al. 1984). When ERPs were averaged on saccade onset, the presaccade positivity was greater for the saccade task compared to the antisaccade task at parietal locations. Evdokimidis et al. (1996) observed that ERPs in the antisaccade task are characterized by a more pronounced activity during the last 100 ms prior to saccade onset over central-anterior locations with a slight ipsilateral lateralization (Evdokimidis et al. 1996). In contrast to Brickett et al. (1984), they also observed that the negative potential 100–120 ms after target appearance with maximum amplitude over central electrodes was not significantly different between the two tasks. Instead, a statistically significant difference was observed for the latter part (350 ms after target appearance) where the positive shift in the saccade task had a steeper slope than in the antisaccade task. Everling et al. (1998) found that in both visually guided saccades and antisaccades a slow negative shift before saccade onset was observed at dorsomedial central-frontal locations and this negativity was significantly larger for antisaccades at the central locations. They also observed that the integral of a subsequent positivity

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before saccade onset was significantly lower for antisaccades compared to saccades at the central locations. These authors also studied the stimulus-aligned ERPs and compared correct antisaccades with incorrect pro-saccades to observe that the negative shift associated with target appearance was higher prior to correct antisaccades than prior to incorrect prosaccades over the dorsomedial frontal cortex (Everling et al. 1998). Although there are many studies investigating the effect of different task requirements on the ERPs preceding saccadic eye movements, there are very few studies that have addressed the question of whether these ERPs are directly related to the processes of saccadic preparation in the cortex. The hypothesis here would be that a direct relation of the ERP preceding the saccadic eye movement and the preparation of that movement should be reflected in the relation of the saccadic reaction time (RT) and the ERP. Indeed, in animal studies, where activity was measured from single neurons in the Frontal Eye Field (FEF), it was observed that variability in saccadic RT was negatively correlated with neuronal activity before the presentation of the saccade target stimulus (Everling and Munoz 2000). In yet another study Hanes and Schall (1996) showed that RT variability was correlated with the rate of increase in neuronal activity of FEF after the presentation of the saccade target stimulus (Hanes and Schall 1996). These correlations were also observed in the Superior Colliculus (SC) (Dorris et al. 1997; Everling et al. 1999). These studies have correlated the cortical activity and the RT for each saccadic eye movement and tried to explain the intertrial RT variability with the variation in neuronal activity. One could then ask the same question in EEG studies in humans namely is there a correlation between EEG and RT? There is though a basic problem one faces in order to address this question and that is the low signal to noise ratio of the EEG method. ERP signals can only be detected by averaging a large number of individual trials precluding a correlation of single-trial EEG to RT. On the other hand, RTs could be grouped in a small set of categories (using for example four quartiles of increasing RT) and the effect of category of RT on EEG could be measured. Everling et al. (1997b) correlated ERPs averaged on saccade onset to RTs that were grouped in 3 categories: fast (130–180 ms), median (180–230 ms) and slow (230–280 ms). The parameter of ERP that was correlated was the overall activity 100 ms prior to movement onset. It was observed that fast trials were preceded by a more negative potential than slow trials. Although this study provided evidence for a relation of ERP to RT, it still did not conclusively answer the question of whether ERP reflected the saccadic eye movement preparation processes. If an EEG signal would be specifically related to the movement preparation processing, this signal should covary with RT only for

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stimulus-aligned EEG activity while it should remain constant when EEG activity would be aligned to the movement onset (see Fig. 1). Thus, conclusive evidence for this relation would be given if one would study the relation of EEG and RT for stimulus-aligned EEG signals. In this study, we measured the RT and EEG for saccades and antisaccades in healthy subjects. We first examined the task effect (saccade versus antisaccade) on RT and ERP. Then, in order to explore the hypothesis of whether these ERPs are specifically related to the cortical processing of the upcoming saccade and antisaccade, we divided all trials for each subject and each task (saccade, antisaccade) into four quartiles of increasing RT. We then measured for each trial the stimulus-aligned electroencephalographic activity (EEG) at different time points until the onset of the fastest of the eye movements (140 ms for saccades and 200 ms for antisaccades). We hypothesized that if the EEG signal reflected the processing of the saccadic eye movement then as time progressed there would be a difference in activation namely more activation for fast RTs and less activation for slower RTs. More specifically, we hypothesized the

Fig. 1 a These are two theoretically possible EEG waveforms averaged on target appearance that correspond to a short (upper trace) and long (lower trace) RT. The shaded area presents the measurement of EEG at a specific time point after target appearance and the small inset figure presents the expected amplitude of the EEG negativity for the two traces at the particular time. The negativity for the trial with short RT is larger at time T (shaded area) than the negativity for the trial with the long RT. b The same two theoretically possible EEG waveforms averaged on movement onset that correspond to a short (upper trace) and long (lower trace) RT. The shaded area presents the measurement of EEG at a specific time point before movement onset and the small inset figure presents the expected amplitude of the EEG negativity for the two traces at the particular time. The negativity for the both the trial with short RT and the trial with the long RT are of the same magnitude

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presence of a monotonic relation between increasing RT quartile and EEG activity.

Materials and methods Participants Twelve, right-handed healthy subjects, six women and six men, aged 22–42 years, mean age 33.58 years, SD = 5.265, were recruited voluntarily in the study. All subjects had normal or corrected-to-normal vision. The experimental protocol and the aim of the study were explained to all participants and they gave written informed consent for their participation. The study protocol was approved by the Aeginition Hospital ethics committee. Behavioral task design All subjects were seated comfortably in a dimly illuminated and quiet room. A specially designed table was used that had a head holder with a chinrest adjusted at one end and a 17-inch computer monitor mounted at the other end (1 m distance from the head holder). Subjects were instructed to fixate a white-colored disk of 0.5° diameter (FP) in the center of the black screen of the computer monitor. After a 2,500–3,500 ms (at steps of 125 ms) display period, the FP was extinguished and a white-colored disk of the same diameter, 0.5°, appeared at various distances (2°, 3°, 4°, 5°, 6°, 7°, 8°, 9°) either to the left or to the right in a pseudorandom order for 1,000 ms (peripheral target). Subjects were instructed to look toward the target. When the peripheral target was extinguished, a black screen (stimulus-free interval) remained for 4,000 ms before a new trial begun. A calibration procedure was performed before each block using a sequence of four saccadic eye movements, two to the left and two to the right of the central fixation target at an eccentricity of 5° and 10°. Each subject completed a block of 150 trials. Then, the subject was instructed to perform another block of 150 antisaccades. The procedure was the same but now the instruction was to look to the opposite site of the target. The block order was kept constant for all subjects. Data acquisition Eye movement recording Eye movements were recorded from both eyes using the IRIS SCALAR infrared device. The sampling rate of eye position acquisition was 1,024 Hz. Stimulus presentation and recording of the responses were accomplished with a

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Scalp EEG was obtained from 62 surface electrodes (resistance \10 KX, monopolar recordings, interlinked ears as reference). Electrodes were placed at the following sites (10/20 international system): OZ, POZ, PZ, CPZ, CZ, FCZ, FZ, FPZ, O1, O2, PO3, PO4, PO5, PO6, PO7, PO8, P1, P2, P3, P4, P5, P6, P7, P8, CP1, CP2, CP3, CP4, CP5, CP6, C1, C2, C3, C4, C5, C6, C7, C8, FC1, FC2, FC3, FC4, FC5, FC6, TP7, TP8, T7, T8, FT7, FT8, F1, F2, F3, F4, F5, F6, F7, F8, AF3, AF4, AF7, AF8, FP1, FP2). Using a digital data acquisition system (ISO-1064CE and CONTROL-1164 Braintronics, the Netherlands), the EEG and IRIS signals were amplified with a 10 s time constant and a 100 Hz low pass filter and sampled at 1,024 Hz from a data acquisition Analog-to-Digital card on a desktop PC.

trace) and presented graphically this trace and the instantaneous position trace for each saccade trial. The program then searched for a value of instantaneous speed greater than 80 deg/s for 500 ms after stimulus onset. If such a value was detected, the program searched backward from this value and marked with a cursor the point where the instantaneous speed was lower than 15 deg/s. This was the onset of the saccade. In the same fashion, the program searched forward from the 80 deg/s instantaneous speed value to find the point where the instantaneous speed was lower than 15 deg/s. This point was marked using a second cursor as the end of the saccade. The onset and end of each saccade were then visually inspected by one of the authors and corrected manually if needed by moving the relevant cursor. The program operator discarded the trial if there was no detection of saccade for 500 ms after stimulus onset or if the first saccade detected was in the wrong direction as observed in the position record only for antisaccades. For each subject, a mean RT was computed for saccades and antisaccades. These mean RTs were compared between the two different tasks using a paired sample t-test.

Preprocessing

ERP analysis

EEG data acquisition began 1,000 ms before target appearance to 1,000 ms after. Trials with artifacts (large amplitude shifts, no eye movement, and blinks) were excluded from averaging. All trials were visually inspected for correct identification of saccade onset and for artifacts. Saccades with RT below 80 ms (anticipatory saccades) or above 500 ms (no response trials) were also excluded. As a result, the final data set for analysis comprised of 1,415 (78.6%) from the total 1,800 saccades (12 subjects 9 150 trials per subject). Also from a total of 1,800 antisaccades, 1,525 (84.7%) antisaccades were included. From this pool, we excluded incorrect antisaccades, eye movements that were falsely made toward the target and then were corrected. There were 162 incorrect antisaccades in total. The remaining 1,363 (75.7%) correct antisaccades were finally included for further analysis. We also excluded from further analysis the EEG data from 6 temporal electrodes (TP7, TP8, T7, T8, FT7, and FT8) because of large muscular artifacts probably induced by the temporalis muscles.

ERP averaged at target appearance

program written in Turbo Pascal 7.0 for DOS. A 12-bit A/D converter was used for stimulation (Advantech PC-Lab Card 818L). EEG recording

Statistical analysis Behavioral data analysis Saccade onset and offset were computed using an interactive program written in Delphi 7.0 by one of the authors (A.M.). The program first computed the instantaneous saccade speed trace (first-order derivative of the position

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Single-trial EEG data were averaged from 1,000 ms before to 500 ms after target appearance. A baseline was defined by the mean voltage over the initial 200 ms of the averaged epoch. In each averaged ERP signal from each subject and electrode, we computed the following indices: (a) time of post-stimulus negativity peak amplitude, (b) Peak amplitude of post-stimulus negativity. We analyzed the differences in these indices between the saccade and the antisaccade task for each electrode using paired sample t-tests. ERP averaged on saccade onset Single-trial EEG data were averaged from 1,000 ms before to 100 ms after saccade onset. A baseline was defined by the mean voltage over the initial 200 ms of the averaged epoch. In each averaged ERP signal from each subject and each electrode, we computed the following indices: (a) Time of premovement negativity peak amplitude. (b) Peak amplitude of premovement negativity. We analyzed the differences in these indices between the saccade and the antisaccade task for each electrode using paired sample t-tests.

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RT effect on EEG activity

Table 1 Mean RT and standard deviation (SD) for each subject in the saccade and antisaccade task

In this analysis, the stimulus-aligned and the movementaligned saccade and antisaccade trials for each electrode (56 electrodes) were analyzed separately. For the stimulusaligned trials, the single-trial EEG was measured at 20, 40, 60, 80, 100, 120 and 140 ms after target appearance for the saccade task and at 20, 40, 60, 80, 100, 120, 140, 160, 180 and 200 ms after target appearance for the antisaccade task. The selection of these cutoff points was based on the requirement that about 5% of the total number of saccadic eye movements for all subjects would have an RT lower than the cutoff point. For the movement-aligned trials, the single-trial EEG was measured at 20, 40, 60, 80, 100, 120, 140, 160, 180 and 200 ms before saccade onset, for both the saccade and the antisaccade task. EEG activity at each time point was measured as the mean of ten samples centered at the particular time point, (for example the term OZ_20ms represents mean activity at the OZ electrode averaged from 15.625 to 23.4375 ms (sampling rate 1,024 Hz). The single-trial EEG data for each time point at each electrode site for each one of the two tasks (saccade, antisaccade) were pooled within each subject and across subjects for analysis. The single-trial EEG data (time point, electrode, and task) for each subject were grouped in four quartiles using the RT distribution of the subject and a continuous predictor variable was computed reflecting RT quartile. The predictor value 1 was assigned to the first quartile (25% fastest trials of the particular subject), and the predictor value 4 was assigned to the last quartile (25% slowest trials). Predictor values 2 and 3 were assigned to the second and third quartiles accordingly. A general linear model analysis (GLM) was performed using the RT quartile continuous predictor and subject as a random categorical predictor (12 levels) to the pooled single-trial EEG data for all subjects at each time point, each electrode and each task. The F value for the RT quartile effect was calculated, and the significance level was set at p \ 0.05. F values with significance at the p \ 0.1 level are also presented showing a trend toward significance. The Statistica 7.0 software (StatSoft Inc., 1984–2004) was used for all analyses.

Subject

Saccade RT ± SD (ms)

Antisaccade RT ± SD (ms)

1

169 ± 22

250 ± 45

2

172 ± 27

226 ± 36

3 4

190 ± 25 193 ± 37

248 ± 40 227 ± 63

5

203 ± 32

335 ± 63

6

203 ± 39

306 ± 52

7

204 ± 31

245 ± 38

8

215 ± 28

267 ± 39

9

222 ± 61

353 ± 80

10

246 ± 57

311 ± 43

11

265 ± 35

265 ± 39

12

333 ± 95

334 ± 60

Grand mean

215 ± 59

279 ± 67

Subjects were sorted by increasing mean RT in the saccade task

Effect of task on ERP ERPs averaged at target appearance The peak amplitude of the post-stimulus negativity was larger in the antisaccade task compared to the saccade task (see Fig. 2). The difference was highly significant for all electrode sites (paired t test p \ 0.05) except for electrodes P6, F1, F7. The time of the peak ERP amplitude did not differ significantly between the two tasks for most electrode sites. ERP averaged on saccade onset The peak amplitude of the premovement negativity was larger in the antisaccade task compared to the saccade task for many electrode sites (see Fig. 3). Figure 4 presents a map of the significance level (paired t-tests) of this difference for each electrode site. The time of the peak ERP amplitude did not differ significantly between the two tasks for most electrode sites. Relation of single-trial EEG to RT

Results

Stimulus-aligned trials

Effect of task on RT

In the saccade task, the GLM analysis confirmed a significant effect of RT quartile on EEG activity at 100 and 120 ms after the appearance of the target while there was no significant effect for all other time points (20–80 ms and 140 ms after target appearance). Figure 5 presents a map of the p values for the significance of the effect of RT quartile

Table 1 presents the mean RTs for each subject in the saccade and the antisaccade task, respectively. Mean RTs for all subjects were significantly slower in the antisaccade task compared to the saccade (t11 = -5, p \ 10-4).

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Fig. 2 Grand average ERPs aligned at target appearance for the saccade task (gray line) and antisaccade task (black line)

Fig. 3 Grand average ERPs aligned at movement onset for the saccade task (gray line) and antisaccade task (black line)

on EEG for each time point. The significant effect was observed for only one electrode site (PO7). Figure 6 shows the relation of RT to EEG activity for PO7 at 100 and 120 ms. A monotonic decrease in negativity with increasing RT can be observed as predicted by our original hypothesis. In the antisaccade task, the GLM analysis confirmed a significant effect of RT quartile on EEG activity at 160,

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180 and 200 ms after the appearance of the target while there was no significant effect for all other time points (20–140 ms after target appearance). Figure (7) presents a map of the p values for the significance of the effect of RT quartile on EEG for each time point. The significant effect was observed for many electrode sites bilaterally mostly at central and frontal electrode sites. The effect became more pronounced at later time points as would be expected.

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Fig. 6 This plot shows the mean saccade EEG activity (negativity up) recorded at electrode P07 for each one of the four RT quartiles at 100 ms (black line and diamonds) and 120 ms (gray line and squares)

Fig. 4 Map of the significance level (paired t tests) comparing peak negativity between the saccade and antisaccade task for ERPs averaged on movement onset for all electrodes. The rectangle signifies a difference significant at p \ 0.05 and the ellipse signifies a difference significant at p \ 0.1

Figure (8) shows the relation of RT to EEG activity at electrode F2, at 160, 180 and 200 ms. A monotonic decrease in negativity with increasing RT can be observed as expected. Also this effect is more pronounced at later time points again confirming the hypothesis that this negativity is related to movement preparation processes.

Movement-aligned trials In the saccade task, the GLM analysis confirmed a significant effect of RT quartile on EEG activity in every electrode site at 20 ms before saccade onset, except in electrodes PO6, PO7 and F7. A decrease in negativity with increasing RT is observed (Fig. 9). In the antisaccade task, the GLM analysis confirmed a significant effect of RT quartile on EEG activity in every electrode site at 20, 40, 60, 80 ms before saccade onset, except in electrodes O1 and PO7. A monotonic decrease in negativity with increasing RT was observed (Fig. 10).

Fig. 5 a Map of the p values for the significance of the effect of RT quartile on EEG at 100 ms after target appearance, for the saccade task. The rectangle signifies an effect significant at p \ 0.05 and the ellipse signifies an effect significant at p \ 0.1. b Map of the p values for the significance of the effect of RT quartile on EEG at 120 ms after target appearance, for the saccade task

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Fig. 7 a Map of the p values for the significance of the effect of RT quartile on EEG at 160 ms after target appearance, for the antisaccade task. b Map of the p values for the significance of the effect of RT quartile on EEG at 180 ms after target appearance, for the antisaccade

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task. c Map of the p values for the significance of the effect of RT quartile on EEG at 200 ms after target appearance, for the antisaccade task

Fig. 9 This plot shows the mean saccade EEG activity (negativity up) recorded at electrode P3 for each one of the four RT quartiles at 20 ms before saccade onset Fig. 8 This plot shows the mean antisaccade EEG activity (negativity up) recorded at electrode F2 for each one of the four RT quartiles at 160 ms (black line and diamonds), 180 ms (light gray line and squares) and 200 ms (dark gray line and triangles)

Discussion In the present study, we measured mean RT for 12 healthy subjects in a saccade and antisaccade task and simultaneously recorded EEG activity aligned either to the stimulus or to the onset of the saccadic eye movement. The main findings were a significant increase in RT and ERP negativity for antisaccades versus visually guided saccades and a significant relation between RT and EEG for both tasks. According to our prediction (presented in Fig. 1), faster movements were preceded by a higher early negativity (at 100–120 ms for saccades and at 160–200 ms for

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antisaccades). Finally, the relation of RT to EEG was much more pronounced for antisaccades compared to saccades. Human behavior is dominated by variability in responses to identical stimuli (Kupfermann et al. 1974; Sherrington 1910; Wise et al. 1996). Since the midst of 19th century, Helmholtz (1886) noted that RT in sensorimotor tasks varied from trial to trial even though stimulus and response did not change. This inter-trial variability is also apparent in the reaction time for the generation of a saccadic eye movement toward a visual stimulus. Saccadic RTs of normal adults range from 90 to over 400 ms with a mean around 200 ms (Westheimer 1954). The large inter-trial variability observed for saccadic RTs is also reflected in a large inter-subject variability of the mean saccadic RT (Evdokimidis et al. 2002; Michell et al. 2006). This large

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Fig. 10 This plot shows the mean antisaccade EEG activity (negativity up) recorded at electrode P1 for each one of the four RT quartiles at 20 ms (black line and Xs), 40 ms (dark gray line and triangles), 60 ms (light gray line and squares), 80 ms (black line and diamonds) before saccade onset

RT variability gave us the opportunity to ask the question of whether EEG activity could account for this RT variability of saccadic eye movements. The effects of task on both the behavioral and the electrophysiological data replicated previous findings. Mean RTs are shorter in the antisaccade task compared to the saccade task. Mean RT for saccades is 200 ms and for antisaccades 280 ms (Clementz et al. 2001; McDowell et al. 2005). Many explanations have been proposed to explain this difference. A very prominent such hypothesis attributes the ‘delay’ of the antisaccades to the need of inhibiting the reflex saccades and at the same time generate a new saccade to the opposite side (Olk and Kingstone 2008). This function has been proposed to be cortical in origin, involving the FEF and the dorsolateral prefrontal cortex (DLPFC). ERPs also differ between the two tasks. Although they are similar in shape, peak negativity is larger in antisaccades compared to saccades. This finding has been consistently reported previously in the literature (Evdokimidis et al. 1996; Everling et al. 1997a). It is not very easy to interpret the observed difference merely due to the discrepancy concerning the origin of cortical potentials. Kurtzberg and Vaughan attribute the negative element of ERP to activation of FEF because they detected its maximum over the fontal areas (Kurtzberg and Vaughan 1982). Others support the notion that negativity in ERP originates in the supplementary eye field (SEF) since they found its maximum over the vertex (Moster and Goldberg 1990). Their explanation is further supported by findings on PET (O’Driscoll et al. 1995). The close relation between FEF and saccade RT has also been previously reported by studies using either fMRI(Connolly et al. 2005; Neggers et al. 2005) or TMS (Terao et al. 1998).

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Finally, the main finding in this study was a significant relation between EEG negativity and RT for the stimulusaligned ERPs. This relation was predicted by our original hypothesis presented in Fig. 1 namely that shorter RTs would be accompanied by an earlier onset of the negativity preceding the eye movement; thus, the negativity would be larger early (at 100–120 ms in the saccade task and at 160–200 ms in the antisaccade task). On the other hand, the significant correlation between RT and EEG activity observed for the movement-aligned ERPs suggests that the peak of the ERP negativity is not related to the saccadic eye movement preparation processes as suggested by our original hypothesis. In a previous study, Everling et al. (1997a, b) found a significant relation of RT and EEG activity for movement-aligned ERPs that were the same as the one observed in this study. This relation was interpreted as showing a differential processing for fast compared to slow movements in cortical areas. Our interpretation though of this correlation is that the peak of the ERP negativity observed close to movement onset in movementaligned EPRs is not related to movement preparatory processes. In order for this activity to predict the preparation of the upcoming saccade, one would expect that this activity would be coupled to movement onset thus would not co vary with RT as shown in Fig. 1. In summary, this study provided evidence that only the onset of the negativity for the stimulus-aligned ERP is predictive of a movement preparation process in the sense that the sooner the onset of the negativity after stimulus presentation appears the sooner the movement onset will occur (faster RT). This study further showed that this preparatory activity is more pronounced for antisaccades than for saccades, confirming the specific role of cortical areas in the preparation of these voluntary eye movements. Finally, it was observed that movementaligned and stimulus-aligned ERPs before saccades might reveal different sources of information concerning underlying cognitive processes. A final point to be made concerns the large difference in the magnitude and significance of the RT, EEG covariation between saccades and antisaccades. An explanation of this difference could be that scalp EEG reflects mainly cortical activity. Processing that originates and completes in subcortical areas cannot be detected by EEG using surface electrodes. Indeed, the integration of the saccades, after stimulus perception by the occipital cortex, is solely subcortical, with the superior colliculi in the brainstem playing a major role (Dorris et al. 1997). On the other hand, antisaccades require the participation of frontal areas, more specifically FEF and DLPFC (Everling and Munoz 2000). Our findings are in close relation with this notion, since correlation of EEG data and RT was clearly observed in the antisaccade task that involves mainly

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cortical processing. This is in accordance with findings from studies using fMRI (Ford et al. 2005). In conclusion, this study demonstrated that the EEG negativity preceding voluntary saccades is related to the cortical processes of saccade preparation thus validating the use of EEG in the exploration of the cortical substrate of saccadic eye movement planning. These results could thus be used in the study of saccade planning in healthy humans and individuals suffering from disorders in which cortical control of saccades is affected such as schizophrenia (Gooding and Basso 2008) or dementia (Fletcher and Sharpe 1986). Acknowledgments M. Papadopoulou was supported by the Greek State Scholarship Foundation.

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Event-related potentials before saccades and ...

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