Electrocortical signs of word categorization in saccade-related brain potentials and visual evoked potentials

International Journal of Psychophysiology Elsevier

131

3 (1985) 131-144

PSP 00084

ELECTROCORTICAL SIGNS OF WORD CATEGORIZATION POTENTIALS AND VISUAL EVOKED POTENTIALS

MAGDA

MARTON,

JGZSEF

SZIRTES

and PETER

IN SACCADERELATED

BRAIN

BREUER

Institute /or Psychology, Hungarian Academy of Sciences, Budapest (Hungaryl (Accepted

July 25th, 1985)

Key words: visual evoked potential-saccade-brain

potential--semantic

categorization

Visual evoked potentials (VEPs) elicited by fovea1 presentation of words were compared to brain potentials evoked by the same words in a condition where subjects had to make a saccadic eye movement in order to perceive the words (saccade-related brain potentials, SRPs). Subjects had to categorize the words responding with a button press to stimuli belonging to the target (infrequent, P = 0.2) category. The VEP and SRP waveforms showed divergences in the early (up to 250 ms) components, but a marked similarity between the late components. Principal Component Analysis also revealed the same relationship between the two types of brain responses. Peak latency of the late SRP components measured from saccade offset showed an apparent processing advantage over the corresponding late components of VEPs. The N3 component, indexing semantic processing of visual patterns, peaked between 310 and 375 ms in the SRPs, while in the VEPs it appeared between 410 and 470 ms. The P4 component, associated with final stimulus evaluation, showed a similar latency benefit in favour of SRPs (420-500 ms vs 530-590 ms in VEPs). The mean reaction time was 74 ms shorter in the eye movement condition (measured from saccade offset) than in the VEP condition (703 vs 777 ms). The question of what kind of processes may contribute to the differences in mean RTs and to the latencies of the late components between the two conditions are discussed. We suggest that the late components (P3, N3 and P4) of the VEP and the SRP, respectively, index identical brain processes.

INTRODUCTION In early reports sharp waves appearing in the occipital EEG during saccadic eye movements across an illuminated environment were labelled “lambda waves” (Evans, 1953). Subsequent studies introducing computer techniques for averaging lambda responses considered the possibility that this saccade-related brain potential (SRP) might contain visual evoked potential (VEP) components. The amplitude of lambda responses was generally reported to be attenuated when the field luminance was reduced (Remand and Lesevre, Correspondence: M. Marton, Institute for Psychology, Hungarian Academy of Science, H-1394 Budapest 62, Pf. 398, Hungary.

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1956; Gaarder et al., 1964; Remend et al., 1965), and the waveform associated with scanning of complex pictures was characterized as one resembling VEPs (Scott and Bickford, 1967). Using vertical stripes as stimuli, it was found that high luminance and a 13 per cycle spatial frequency stimulus field lead to optimal lambda responses (called by the authors “saccadecontingent VEP”, Armington et al., 1967; Armington, 1977). Several researchers have found that the lambda responses accompanying saccades are similar to brain potentials elicited by the displacement of the same pattern (e.g. pattern reversal) while the subject is fixating (Barlow and Cigatrek, 1969; Remand and Lesevre, 1971; Kurtzberg and Vaughan, 1973, 1977; Morton and Cobb, 1973; Brook, 1977). Using pattern reversal stimulation there is no

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change in the total amount of illumination reaching the eye as the patterns are interchanged. A similar situation arises when the pattern is kept steady and its image is displaced on the retina as the subject makes a voluntary saccade. The authors have therefore suggested that in both experimental situations pattern-related VEPs might have been recorded. Several reports were published about the characteristic components of pattern-reversal VEPs and their relationships to those of pattern-onset and -offset VEPs (Jeffreys, 1969, 1971; Estevez and Spekreijse, 1974; Lesevre and Remend, 1972; Halliday and Michael, 1970; Skrandies et al., 1980). A general finding was that the reversal VEP shows a prominent positive peak at around loo-120 ms (PlOO) and a subsequent negative component at 150 ms. In a study by Lehmann and Skrandies (1980) the scalp distribution of VEPs evoked by checkerboard reversal was analyzed simultaneously in 47 channels. Two evoked components were identified which showed occipitally positive and anteriorly negative extreme values at 100 ms and vice versa at 14Oms. It was shown that the topographic distribution of the averaged VEPs in the occipitoparietal region shows a similar pattern when the eyes are fixated while a checkerboard reverses or when the subjects move their eyes across the same stationary pattern (Rtmond et al., 1965; Kurtzberg and Vaughan, 1973). Furthermore, similar morphological and temporal characteristics were observed for the two types of responses (Kurtzberg and Vaughan, 1973). On the other hand, differences between pattern-reversal VEPs and the lambda responses have also been noted (e.g. Scott et al., 1981). Both types of brain responses show at Oz a prominent PlOO component (between 100 and 125 ms both from stimulus onset, and from saccade onset, although the exact latencies for lambda responses depend on saccade amplitude). Differences emerged in two components, however; the lambda responses had a prominent preceding negative component and a smaller subsequent negative peak at 150 ms as opposed to the pattern-reversal VEPs. In most of the experiments mentioned above the lambda responses associated with saccades across continuously patterned fields were supposed

to be elicited by the stimulation arising at the beginning of the eye movement. Recently, the question concerning the association of lambda components with the onset and offset of saccades has been the subject of detailed studies (Kurtzberg and Vaughan, 1977; Yagi, 1979). By systematically manipulating the saccade amplitudes, it was possible to separate the components which appear at constant latencies from those which shift with increasing amplitudes. For the lambda responses recorded with ear reference it was reported that a positive component appearing at around 100 ms after saccade offset (the lambda wave) represents a VEP component that is elicited by the visual input at saccade offset. Kurtzberg and Vaughan (1977) also showed that further “fixational” (i.e. offsetlinked) components with negative and positive polarity can be observed at 150 and 200 ms after saccade termination. Kurtzberg and Vaughan (1979) and Yagi (1981, 1982) using tasks with either spatial versus verbal, or detection versus distraction conditions, established that the main positive-negative components of lambda response showed an increase of amplitude when the processing requirements of the task were increased. Few studies were, however, devoted to investigating the late components of lambda responses. A P300-like component in the lambda response was observed during reading (Barlow, 1971) and in association with the saccade leading to the target stimulus in a complex visual scene (Cooper et al., 1978). These results led us to investigate the late components of saccade-related brain potentials (SRPs) in paradigms which have traditionally been used to study the late positive components (P300) of EPs. The tasks employed were modified in such a way that subjects had to perform a saccade in order to perceive the task-relevant stimuli. We recorded SRPs in a guessing task (see Sutton et al., 1965) and found that guessing, as compared to the control condition, led to the appearance of a parietal late positive component in the SRP at 375 ms from saccade onset (Marton et al., 1983). In a counting or “oddball” task (see Duncan-Johnson and Donchin, 1977) we demonstrated that the late positive component of the SRP associated with infrequent stimuli showed significantly greater am-

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plitude than that associated with frequent stimuli (Marton et al., 1984). Furthermore, in a word categorization task (adopted from Kutas et al., 1977) we observed an increase in the latency of the late positivity of SRP with increasing complexity of categorization (Marton et al., 1985). Thus, our results demonstrated that the experimental variables influence the late components of SRPs similarly to the way they had been shown to affect the late component of EPs. On the basis of our findings we concluded that the late components appearing after 200 ms in the SRPs might be equivalent to the late components of VEPs. The present study was designed to compare directly the late components of SRPs and VEPs of the same subjects recorded in the same experimental paradigm. For this purpose we have again employed the paradigm developed by Kutas et al. (1977) in which subjects have to categorize words in two conditions: (a) with eyes kept steady and stimuli presented at the fixation point; and (b) where a saccadic eye movement was necessary to perceive the stimulus.

METHOD Subjects Eleven right-handed adults (7 female, 4 male, mean age = 26 years) with normal or corrected-tonormal vision were paid to participate in the experiments. Stimulus conditions and procedure Subjects were seated in front of a translucent screen with head position maintained by a chinrest. The stimuli were different male and female names and were back-projected on the screen. They subtended 1.3-2.3“ visual angle horizontally and 0.4” vertically. The luminance of these whiteon-black slides was on the average 0.3 cd/m’ at the screen as measured by a Tektronix 516 photometer. Two stimulus conditions were employed. In the eye movement or SRP condition subjects had to perform a saccadic eye movement in order to perceive the stimulus. Subjects fixated a white fixation point located at 12” from the midline. The

word also appeared at 12” from the midline but on the opposite side of the screen. Subjects were instructed to wait about 1 s after the stimulus appeared on the periphery, then to perform the saccade to the stimulus and fixate it while it was present (3.5 s), and finally, to make a return eye movement to the original fixation area. Two runs, each consisting of 70 stimuli, were presented. There were 14 “target” male names in the infrequent category and 56 “non-target” female names in the frequent category, presented in random order. The two runs differed only in that the respective positions of the fixation point and the stimuli were reversed. In a given run subjects always performed the saccade leading to the names in the same direction. The two runs with opposite saccade directions were necessary in order to eliminate the possibility of EOG contamination of the records, and in each individual SRP average an equal number of responses with left and right saccades was included (see Kurtzberg and Vaughan, 1982). The interstimulus interval ranged between 7 and 9 s. The subjects’ task was to press a microswitch with the index finger of the right hand whenever a name belonging to the target category (male names with 20% probability) was presented. They were instructed to respond only when they were certain in their decision. The experiment began with practice trials during which subjects learned to perform the eye movements accurately and to avoid blinking during the behavioral response. In the second, visual evoked potentials (VEP) condition brain responses were recorded to the same stimuli which were now presented foveally for 2 s. Subjects fixated a small fixation point in the middle of the screen and they were instructed to avoid eye movement, blinks, etc. during the presence of the stimulus. Here too, they had to press the switch only when seeing the infrequent target names, and to avoid responding to the non-target stimuli. The interstimulus interval was varied between 6 and 8 s. Recording and data evaluation The EEG was recorded from Fz, Cz, Pz, Oz, P3 and P4 scalp locations referenced to linked ears using Beckman and SLE Ag-AgCl electrodes. The electro-oculogram (EOG) was recorded between

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electrodes at the outer canthus of each eye, and above and below one eye. Brain activity and the EOG were amplified on a Beckman Accutrace EEG machine (with a time constant of 1 s) and stored on FM tape (Analog 14, Philips). The overall bandpass of the system was 0.16-1250 cps. Averaging was performed off-line on a small computer with a sampling rate of 4 ms per point. The analysis epoch extended from 172 ms prior to saccade/stimulus onset to 852 ms after it. For SRPs the onset of the horizontal saccades leading to the names served as trigger for averaging. The exactness of the triggering was controlled individually on a memory scope. Furthermore, the EOG record was averaged along with the brain potentials which made it possible to establish the exact relation of saccade onset to the SRP components. In the VEP condition a pulse synchronized with the appearance of the names served for averaging the VEPs. In both conditions, VEPs and SRPs were averaged separately for the target and for the non-target categories. Records were edited before movement averaging, i.e. frials with blinks, artifacts, or poorly performed saccades (in the SRP condition) were left out from the analysis. Due to editing, the number of sweeps in the averages varied between 24 and 28 across subjects (there were 28 targets in each condition). Responses were written out on X-Y plotter. Components were visually identified within the latency ranges indicated at each component and the peak latenties were measured from saccade onset and presentation onset (VEP), respectively. Amplitudes were measured relative to the baseline defined as the average amplitude of EEG activity preceding stimulus and saccade onset, respectively. Two-way analysis of variance was used to evaluate the effects of stimulus category and electrode site. SRP and VEP waveforms were separately subjected to Principal Component Analysis (PCA) to objectively identify the components and to deal with their possible overlaps. In both conditions the input for the PCA consisted of 11 (subjects) X 2 (stimulus categories) x 6 (electrodes) = 132 averages. The waveforms were condensed to 64 points by using every fourth data point only. Based on the algorithm of the SPSS program package (Nie et al. , 1972) covariance matrices were computed

and factored on TPA 11/40 computer. The extracted factors were rotated using the normalized Varimax criterion. Factor scores were also derived to assess the magnitude of each factor in the different averages.

RESULTS Behavioral data Subjects solved the task without error. The average duration of the saccades were 69.9 ms (S.D. = 9.8). The mean RT in the saccadic eye movement (SRP) condition was 773 ms (S.D. = 79.7) measured from saccade onset, and 703 ms from saccade offset. The mean RT in the VEP condition was 777 ms (S.D. = 87.2) measured from stimulus onset. VEPs and SRPs to target and non-target words The grand mean VEPs elicited by target and non-target stimuli are depicted in Fig. 1. The first negative component appears between 120 and 156 ms. Following this negativity the waveforms are somewhat different at anterior and posterior locations. In the parieto-occipital leads a positive peak (P2) appears between 220 and 250 ms followed by a further positive peak (P3) between 310 and 350 ms ‘. When measuring the following component, in the target VEPs we identified as N3 the negative-going deflection appearing between the P3 and the second late positivity (time-range 330-470 ms), while in the non-target VEPs it was the negative deflection following the P3 that we considered to be the N3 (time range 340-530 ms). In most subjects in the frontal lead two negative peaks were present in this time range. In both the target and non-target frontal VEPs we chose to measure the second of these peaks because it showed greater amplitude, it was more recognizable over the posterior scalp areas, and it also

’ In the frontal lead the P2 and P3 components could not be identified because here the two positivities were not so clearly separated in the individual averages. When a single positive peak was present, it peaked later than the P2 but earlier than the P3.

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Fig. 1. Grand mean VEP waveforms (across all subjects) for target (infrequent) and non-target (frequent) stimuli recorded over the six scalp areas. The solid line represents the VEPs to non-target words, the dotted line stands for the VEPs to target words. The arrow indicates mean reaction time (RT).

corresponded more to the N3 measured in the SRPs. The ANOVA of N3 latencies showed a significant category effect ( Ft,tzO = 36.41, P < O.OOl), reflecting the fact that this deflection peaked earlier in target than in non-target VEPs. The amplitude of N3 was greater in the non-target VEPs (F1,izO = 23.22, P < 0.001) and greatest at the Fz and Cz locations ( F5,120= 15.07, P < 0.001). The next positive component (P4 or P300) appears in the target VEPs between 530 and 590 ms, while in the non-target VEPs the late negativity is followed by a slow positive shift between 600 and 800 ms. This difference in P4 latencies was highly significant (F,,,,, = 76.86, P < 0.001). The amplitude of P4 showed a significant difference both between target and non-target VEPs (F,,,,, =

73.68, P -c 0.001) and between electrodes ( F5,120= 33.56, P < 0.001). Furthermore, the stimulus category x electrode site interaction was also significant (F,,,,, = 5.34, P c 0.001) which reflects the difference in P4 topography between VEP categories: the target P4 showing pronounced amplitudes in the occipito-parietal leads (see Fig. 3A), the non-target P4 being more anteriorly distributed. The P4 was followed by a negative wave in the fronto-central leads of the target VEPs which peaked about 70 ms before the behavioral response. Therefore, this negativity is presumably associated with brain processes underlying the movement response. The morphology of the SRP waveforms (Fig. 2) is very similar to the one we observed in the “variable names” condition of our earlier study (Marton et al., 1985). In the present experiment the peak latencies were measured also from saccade onset, but the latencies of the fixational and late components are shown from saccade offset as well. A positive “spike-like” component appearing simultaneously with saccade onset is followed in the SRPs by an early negative complex which develops during the saccade and peaks at around and after the end of the saccade. Between 90 and 110 ms this negative complex shows a peak primarily in the parieto-occipital leads. A further negative component appears between 170 and 190 ms (i.e. loo-120 ms from offset) over the frontal region. At Oz the SRP shows a positive component between 160 and 190 ms (90-120 ms from offset) which corresponds to the “lambda wave”. A smaller positive wave, riding on a broader positivity, follows the lambda wave component. In the individual averages this peak (P2) appears between 240 and 280 ms (170-210 ms from offset), while the broader positivity (P3) peaks between 290-370 ms. Here, however, these two positivities are not so clearly separated by a negative wavelet as they are in the parieto-occipital VEPs. The P3 amplitude showed a significant electrode site effect (&o = 9.53, P < O.OOl), being the greatest at Pz. Following the P3 peak, a negative wave (N3) emerges between 420 and 520 ms (340-450 ms from offset) in the frontal lead of the non-target SRP, and a similar negative-going deflection is apparent in the other leads. In the target SRPs the

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Fig. 3. A: the distribution over scalp midline of the mean P4 amplitude in target VEP and SRP, respectively. B: score distribution over the midline of the factors corresponding to the P4 component in target VEP and SRP waveforms, respectively. The ordinate scale is in arbitrary units. +

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Fig. 2. Grand mean SRP waveform (across all subjects) for target and non-target stimuli recorded over the six scalp areas. The solid line represents the SRPs to non-target words, the dotted line stands for the SRPs to target words. The bottom curves illustrate the averaged EOG activity in both horizontal directions. The arrow indicates mean reaction time (RT).

negative deflection appears earlier, between 380 and 445 ms (310-375 ms from offset; stimulus category F,,,,, = 60.04, P < 0.001). The significant electrode effect is due to the earlier appearance of this negativity at Fz ad Cz (F, r2 = 6.73, P < 0.001). The ANOVAs for N3 amphtudes revealed both the effect of stimulus category (F,.,,, = 59.42, P <

0.001) and of electrode site ( Fs,120 = 8.45, P < 0.001) to be significant. The stimulus category effect is due to this negativity being greater in the non-target SRPs, while the electrode site effect corresponds to the fact that N3 is largest over the frontal area. The most prominent positive component (P4) appears in the target SRPs between 490 and 570 ms (420-500 ms from offset), while in the non-target responses the broad N3 component shifts gradually into positivity and reaches a peak at around 700 ms (stimulus category F,,,,, = 671.68, P < 0.001). The amplitude of the P4 peak differed significantly both between categories = 7.66, P -cO.Ol), and between electrodes 5,120= 21.25, P < 0.001). The stimulus category I :,*20 X electrode site interaction also reached significance (F5,12o = 4.10, P -cO.OOS), which reflects a difference in P4 topography between SRP categories that is similar to what was found between target and non-target VEPs: the target SRPs show a distinct parietal focus (see Fig. 3A also), while in the case of the non-target SRPs the P4 is more anteriorly distributed with its maximum at Cz. Finally, a late negative peak, with a distinct fronto-central maximum, appears only in the target SRPs, as it does in the case of the target VEPs as well. This wave peaks 50-80 ms earlier than the

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mean RT, which reflects processes sponse.

suggests that this component related to the behavioral re-

The relationship between SRP and VEP waveforms In the literature, when pattern-reversal VEPs and SRPs (lambda responses) are compared, the early pattern-related components of these waveforms are typically brought into correspondence with reference to reversal onset and saccade onset, respectively, as in both cases these indicate the moment when the stimulus is displaced on the retina. In our study, however, subjects were executing saccades of considerable amplitude across a homogeneous, non-patterned dim field, and so the relevant pattern information could only be picked up at the end of the saccade. Therefore, when comparing the component characteristics of the VEPs and SRPs, the peak latencies of the late SRP components (as well as the RT) will be considered starting from saccade offset *. According to our results, the late components of the SRPs show shorter peak latencies than those of the VEP: the latency benefit for the P3 component is 30-70 ms, while for the N3 and P4 components it is about 70-100 ms. In the eye movement condition the mean RT shows a 74 ms advantage over the RT measured in the VEP condition. The difference in component latencies measured in our two experimental conditions can obscure the overall similarity between the two types of potentials. Since the processes underlying the organization of the behavioral response are presumably the same in both conditions, in order to demonstrate the similarity between VEPs and SRPs we superimposed the two types of responses according to the mean RT of each condition. Using this procedure the similarity between the later portions of the VEP and SRP waveforms becomes quite apparent (Fig. 4) being especially clear in the parietal derivations. There is, however, a difference between the occipital waveforms of the VEP and the SRP, respectively, which deserves comment. The late ’ The EOG was always averaged along with the brain potentials and the end of the averaged EOG deflection allowed for an accurate measurement of saccade offset.

Fig. 4. The comparison of target VEPs and SRPs. The two types of brain potentials are superimposed according to the mean reaction times (RT).

SRP components at Oz are less marked than in the centro-parietal waveforms, while in the occipital VEPs, the N3 and especially the P4 components were at least as prominent as they were in the central and parietal waveforms. Principal Component Analysis In the case of VEPs, the first six factors extracted by the PCA accounted for 85% of the variance in the original waveforms, while for the SRPs this figure was 89%. Fig. 5 shows these factors superimposed according to the mean RT. The first two factors show the greatest differences between the two conditions. In the PCA of VEPs the first factor shows a maximum score at Cz and peaks at around 160 ms from presentation onset. It can therefore be identified with the Nl component of VEPs. The second factor of VEPs shows a peak in its loading at 220 ms and thus corresponds to the P2 component. In the SRPs the first factor shows the greatest negative score at Oz and contributes to the early negative complex in the SRP waveform. The second factor

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Fig. 5. Factor loadings for the factors extracted from the covariance matrix of VEPs and SRPs performed by separate Principal Component Varimax Analyses. Factors are arranged according to the time range of their most significant loadings. The polarities were adjusted so that the major peak of each factor corresponds to the polarity of the original data waveforms. The factors were superimposed according to the mean RT in each condition. Numbers on the right indicate the percentage of variance accounted for by each factor.

shows a peak loading at the period corresponding to the “lambda wave” component of SRPs and shows the greatest positive score at Oz. However, the PCA of SRPs did not disclose a factor that could have been identified with a P2 component, as in the case of the PCA of the VEPs. Since the third, P3 factor of the SRP waveforms shows

significant loadings over a broad time range (about 250 ms duration) encompassing the mean latencies of both the P2 and P3 peaks of the SRPs, it might be the case that the P2 and P3 peaks represent parts of a single broad positivity in the SRPs. The fourth factor explains a small part of the variance only. In the VEP this factor loads maximally around 370 ms and shows the greatest negative scores at Fz and Cz. This factor seems to contribute to the early part of the negative deflection (N3) 3. In the SRPs this factor appears between 380 and 460 ms and is negative at Fz. It seems to represent activity associated with the N3 deflection of SRPs. The fifth and sixth factors were identified as corresponding to the P4 and Slow Wave components of the responses, respectively. There were differences in scalp topography of scores between the respective SRP and VEP factors which deserve being mentioned. In the case of VEPs, the P3 and P4 factors demonstrated at least as great scores at the occipital as the parietal area, while in the PCA of SRPs, the P3 and P4 factors showed a clear maximum of scores at Pz and a much smaller contribution to the waveform at Oz (see Fig. 3B). These differences in score topography are in accord with those observed in the respective waveforms (Figs. 1 and 2) and in the amplitude topography of the P4 component (Fig. 3A): the P4 component of target VEPs appears with the greatest amplitude at Oz, while in the target SRPs, the P4 shows a distinct focus at Pz.

DISCUSSION Information processing benefit in the eye movement condition? We found that in a word categorization task the form and time-course of the late components of the SRP waveforms on the one hand, and the VEP ’ The lack of a prominent late negative factor might be due to the simultaneous time-course of the negativity in non-target responses on the one hand, and of the P4 component in target responses on the other. Separate PCAs of the two VEP categories point to this possibility..Another reason could be that part of the late negativity simply represents the onset of the subsequent P4 component.

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waveforms on the other, show a marked similarity. This similarity emerges even more clearly when the curves are superimposed relative to the mean RT of each condition (Fig. 4). The two responses match especially well in the parietal recordings. However, if we take into consideration that the processing of the stimuli should be related to the offset of the saccade, then we find shorter peak latencies of the late components (with 30-100 ms) and faster RTs (with about 74 ms) in the eye movement condition as opposed to the VEP condition. There are several reasons why in the eye movement condition the processing of stimuli should be measured from saccade offset. Firstly, it was demonstrated that even during reading, when contextual cues may help stimulus identification, the area from which useful pattern information can be obtained extends only about 5’ from fixation (e.g. Rayner et al., 1980). In our experiment the stimuli appeared at 24” on the periphery. Secondly, during the saccade, inhibitory processes suppress the transmission and processing of figural information (saccadic suppression). The RT and the component latency benefits in the eye movement condition point to a faster processing following a saccade as compared to the processing of flash-presented pattern stimuli. This result poses an intriguing problem which may be explained on the basis of neuronal and psychophysical observations. Authors generally agree that masking phenomena ensure that figural information pickup does not occur during saccades (Matin, 1974; Breitmeyer and Ganz, 1976; Rayner, 1978). The nature of the afferent component of the saccadic suppression (as well as that of masking phenomena) has been characterized in terms of interactions between the transient and sustained channels of the visual system (for a review, see Breitmeyer and Ganz, 1976). Efferent activity, in the form of central processes corollary to the programming and generation of saccades, may also play an important role in postsaccadic visual information processing. Though corollary discharges that enhance saccadic suppression have been shown to exist (Duffy and Burchfield, 1975), there is also substantial evi-

dence that extraretinal discharges accompanying saccades may facilitate the processing of visual information by counteracting afferent mechanisms of saccadic suppression (Breitmeyer, 1983; Breitmeyer and Ganz, 1976). Therefore, the response produced by the saccade consists of two phases: saccadic suppression is followed by a sustained response facilitation (lasting for about 150 ms) produced by extraretinal (corollary) discharges. Due to these extraretinal discharges there is a curtailment of saccadic suppression, as a result suppression is present only during the saccade but not after it. The extraretinal facilitation acting on the cortical sustained neurons comes from more than one source. Transient fibers from the retinotopically organized superficial layers of the superior colliculus travel through the pulvinar to the primary visual cortex and the secondary visual association areas (Chalupa et al. 1976; Goldberg and Robinson, 1978; Gross, 1973; see also Goldberg and Wurtz, 1972). While the collicular facilitation occurs maximally during the saccade, the facilitation enhancing the sustained response and arriving from the frontal eye fields is maximal shortly after the saccade is completed (Tsumoto and Suzuki, 1976). Facilitation signals from the midbrain reticular formation (Singer, 1977) converge on the sustained cells also after the saccade has been executed. It was suggested that the mechanisms responsible for saccadic facilitation on the one hand, and for shift of attention on the other, are closely related (Goldberg and Wurtz, 1972; Mohler and Wurtz, 1976; Breitmeyer and Ganz, 1976). Wurtz et al. (1980) proposed that the selective visual enhancement effect of the posterior parietal cortex may participate in the mechanisms underlying selective attention that is independent of the specific saccadic response. The saccade-related facilitation of attention can be brought into connection with the results of psychophysical studies. Using grating stimulus it was demonstrated that visibility can also be facilitated after initial saccadic suppression (Volkmann et al., 1978a and b). Furthermore, it was shown that a saccade to a spot of light lowers its detection threshold (Singer et al., 1977). The existence of a facilitation effect on information processing

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due to spatially directed selective attention was also demonstrated (Eriksen and Hoffman, 1974; Posner et al., 1978). These observations have led us to hypothesize the existence of a specific kind of saccadic facilitation present in the SRP condition. This facilitation, of course, cannot appear in the VEP condition. The question might be raised then, whether it is this saccadic facilitation effect, present in the SRP but not in the VEP condition, that results in the observed differences between the latencies of the late components and the RTs of the two conditions, or whether other aspects of the situation may also play a role. It is possible that an anticipation of the time of information pick-up linked to the programming of a saccade might accompany self-initiated saccades which, in turn, could promote subsequent processing. Since the interstimulus interval was varied between 6 and 8 s in the VEP condition, no such anticipation could function there. Another difference 4 between the conditions was the fact that the SRP condition possesses an intrinsic foreperi,od between stimulus appearance and saccade execution (information pick-up), while in the VEP condition subjects react immediately. Therefore, in two further subjects we examined VEPs when a warning tone preceded with 1 s the appearance of the word. The mean RT was 685 ms and the N3 and P4 peaked at 356 and 489 ms at Pz, respectively. After subtracting mean saccade duration, the mean RT and the peak latencies in the SRP condition of these two subjects were as follows: RT 628 ms, N3 353 ms, and P4 470 ms. Thus, there still remained a small gain in favour of the SRP condition as compared to the values of the VEP condition. This suggests that both the temporal anticipation of information pick-up and saccade-related facilitation processes may contribute to faster processing in the SRP condition. The functional significance of the components of the VEPs and SRPs. An attempt to identify VEP and SRP components In the light of the above hypothesis we can

4 We thank one of the referees for raising this possibility.

suggest that in the case of SRPs the positive lambda component around 170 ms from saccade onset (i.e. at 100 ms from offset), and the simultaneously appearing frontal negative component may both reflect facilitated pattern processing. On the other hand, in the VEPs, the Nl component (peaking between 120 and 160 ms) might be associated with selective attentional “ tuning” for the processing of the pattern characteristics of the flash-presented stimuli (see Harter and Previc, 1978). Such a process seems to be unnecessary in the SRP condition where an anticipatory selective attention process is independently present. The subsequent P3 component, which did not differ between stimulus categories in either type of brain potentials, seems to be related to the recognition of the visual pattern of words. Concerning the frontally maximal negativegoing deflection around 400 ms it seems possible that the topographic distribution of this negativity reflects the influence of later processes (such as the P300 and the Slow Wave). In theory, this negativity could either be a distinct negative component superimposed on a broad positivity or it could simply correspond to the onset of the subsequent late positivity. We presently think that our results point to the existence of an independent negative process around 400 ms and this suggestion is supported by the observation of several authors (e.g. McCallum et al., 1984) that this negativity is frequently encountered as a negative-going change rather than as a peak showing absolute negativity. (To a certain degree the PCA has also supported the hypothesized presence of a negativity; in both analyses there was a frontally negative, although somewhat weak, factor extracted.) The functional interpretation of a frontal N3 wave is, as yet, unresolved and there is also considerable disagreement in the literature concerning the functional significance and topography of the late negativity around 400 ms. The discussion centers around whether the N400 reflects lexical or semantic processes, or other processes not specific to verbal tasks. According to Kutas and Hillyard (1983) an N400 with a broad centro-parietal distribution is elicited whenever a word is unexpected (anomalous or improbable) in a given semantic context. Other authors suggested that the N400

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may be a delayed manifestation of the more general N200 component (for a review, see Ritter et al., 1984). Stuss et al. (1983) argue that the late negativity (Ny or N400) represents the initiation of the specific procedures necessary for the evaluation of the stimuli. Thus, when words have to be discriminated the N400 might reflect the fact that the visually presented stimuli require immediate semantic processing (Stuss et al. 1983). The frontal N3 wave in our experiment seems more similar to the fronto-temporal negativity (N410) obtained in a reading condition (Neville et al., 1982) and to the late negative component (Ny) following unexpected words (Stuss et al., 1983) than to the centro-parietal negativity observed by Kutas and Hillyard (1980). Negativities with more anterior distribution are generally followed by a parietal positivity (Neville et al., 1982; Stuss et al., 1983). Therefore, following Stuss et al. we interpret the frontally maximal negative-going deflection in our study as the sign of the semantic processing of a visually presented complex pattern (word). We found that in both kinds of brain potentials the amplitude of the second late positivity (P4) was significantly greater in the target category. The general finding of an inverse relationship between the amplitude of the late positivity (P300) of EPs and the probability of the task-relevant stimuli (Tueting et al., 1970; Friedman et al., 1973; N. Squires et al., 1975; Duncan-Johnson and Donchin, 1977) has also been demonstrated in the visual modality (K. Squires et al., 1977; see also Courchesne et al., 1975). Similarly in the present experiment the second late positivity (P4) was sensitive to probability and task relevance. Thus, from this point of view the SRPs showed the same characteristics as the VEPs. The P4 component may index the consequence of the final evaluation of the stimuli (Donchin 1975, 1979; Kutas et al. 1977). It is a further question why the late components in the occipital VEP record emerged in a much more pronounced manner than did the corresponding components cf the occipital SRP waveform. Data from a more recent study suggest that this topographic difference could be a consequence of the particular stimulus presentation technique

used. In this study (Szirtes and Marton, in preparation) we compared VEPs to whole field grating presentation, VEPs to the displacement of the grating, and SRPs associated with saccades across the same grating pattern. We found that in the VEP to flash-presented grating a very pronounced positive component appeared at around 260 ms both in the centroparietal and in the occipital waveforms. On the other hand, both in the SRP and in the VEP to pattern displacement the occipital waveform remained at around the baseline after 200 ms. Thus, the SRPs on the one hand, and the VEPs to pattern displacement, on the other, behaved similarly in one respect: they gave more localized responses in contrast to the VEP to the flash-presented pattern which was more widespread over the scalp. These observations suggest that in our present experiment the late parietal positivity (P300 or P4) may be more localized in the SRPs than in the VEPs to flash-presented patterns. The suggestion of identity of the late components of SRPs and VEPs is also supported by the PCA results. When the factor loadings were superimposed according to the mean RTs, the factors corresponding to the late components showed a good fit. In contrast, the loading patterns of the factors associated with the early components of SRPs and VEPs suggest different underlying neural events. In summary, we suggest that the P3, N3 and P4 components of the VEP and the SRP, respectively, index identical brain processes. In other words, the late components of the SRP and the VEP reflect the later phases of information processing similarly-with a processing benefit in the eye movement condition.

ACKNOWLEDGEMENT We are grateful to our anonymous their useful comments.

referees

for

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