Biological Psychology 33 (1992) 97-114 0 1992 Elsevier Science Publishers B.V. All rights reserved

97 0301-0511/92/$05.00

Visual stimulus change and the orienting reaction: event-related potential evidence for a two-stage process J.L. Kenemans Department of Psychonomics, University of Amsterdam,

M.N. Verbaten,

The Netherlands

C.J. Melis and J.L. Slangen

Psychopharmacology Section, Faculty of Pharmacy, University of Utrecht, The Netherlands Accepted

for publication

19 December

1991

In a previous study it was found that infrequent deviant visual stimuli, in a series of standards, elicited event-related potentials (ERPs) with enhanced P2-N2s and P3 amplitudes, suggesting that these parameters reflect processes related to the orienting reaction (OR). In the present study a similar oddball series was presented against the background of a second class of stimuli. With respect to the latter stimuli, subjects had to perform either a very involved (hard) or an easy task. EEG was recorded to oddball (probe) stimuli from Oz, Pz, Cz, and Fz. Analysis of average ERPs revealed that, in the easy condition, deviant probes elicited both enhanced P2-N2s and enhanced P3s, relative to the standards. In contrast, in the hard condition P2-N2, but not P3, was enhanced by stimulus change. In addition, overall P3 amplitude to probes was smaller in the hard condition (sequence-independent load effect). Analysis of single-trial ERPs (SERPs) with orthogonal polynomial trend analysis largely replicated these effects. In addition, SERP analysis also revealed a sequence-independent load effect on P2, as well as a decreasing P3 to deviant stimuli in the Easy condition, which was observed at Cz and Fz, but not at Pz or Oz. The results are interpreted as suggesting that P2-N2 and P3 reflect different stages of the OR, one of automatic and one of capacity-limited processing. Keywords: Visual event-related processing.

potentials,

Orienting

response,

P2-N2,

P3, capacity-limited

1. Introduction A number of studies have demonstrated that occasional deviant stimuli in a row of standards may elicit event-related potentials (ERPs) marked by enhanced N2 waves (relative to standards). “N2” refers to a class of negative waves with peak latencies between 150 and 450 ms, and scalp distributions which depend on sensory modality and task requirements. Correspondence to: J.L. Kenemans, Department of Psychonomics, Roetersstraat 15, 1018 WB Amsterdam, The Netherlands.

University

of Amsterdam,

98

J.L. Kenemans et al. / ERPs to Gsual stimulus change

For the auditory modality it seems well established that both attended and unattended deviant stimuli elicit a so-called mismatch negativity (MMN) (Naatanen & Gaillard, 1983; Naatanen, Simpson, & Loveless, 1982; Sams, Alho, & Naatanen, 1984; Snyder & Hillyard, 1976; Squires, Donchin, Herning, & McCarthy, 1977). Because of its independence from the direction of attention the MMN is considered an ERP marker of pre-attentive, automatic detection of stimulus change (NBatHnen, 1986). For the visual modality N2 waves enhanced by deviant stimuli independently from the direction of attention have not been clearly demonstrated yet. In fact, Naatanen (1990) recently suggested that a pre-attentive mechanism for the detection of visual stimulus change might not exist. In previous studies (Kenemans, Melis, Verbaten, & Slangen, 1991; Kenemans, Verbaten, Roelofs, & Slangen, 1989) we found that P2-N2 amplitude was enhanced by occasional visual deviant stimuli, relative to standards. In the present study we examined whether this enhancement of P2-N2 could still be observed in a condition designed to withdraw processing capacity from the eliciting stimuli (standards and deviants). Such a finding would suggest that a pre-attentive mechanism for change detection may also operate in the visual modality, as capacity limitations are assumed to affect central, attentive processing only. In addition to P2-N2, a longer-latency peak amplitude was also found to be enhanced by infrequent deviants (Kenemans et al., 1989). This positive deflection, called P3, was identified with the classical “P3b” (Donchin, 1981), because of its midline distribution (parietal maximum) and peak latency (about 550 ms). As will be discussed below, there are reasons to assume that P3 amplitude reflects the amount of central processing elicited by the stimulus. The distinction between pre-attentive and capacity-limited processes is of considerable relevance for orienting response (OR) theory. Following Ghman’s (1979) elaboration of Sokolov’s two-stage model (Sokolov, 1963; see also Lynn, 1966) a pre-attentive, automatic comparison process may reveal a mismatch between the stimulus and an internally held model of the environment. Mismatch detection results in a “call” for central, capacity-limited processing resources, Auditory data seem to fit this model rather well with short inter-stimulus intervals (ISIS), if one views the MMN as (a process immediately preceding) the call contingent upon mismatch detection. The call then may or may not be answered by the invocation of central processes reflected in P3. For the visual modality, an indication for the operation of such a processing structure could be obtained in the present study, if P3 enhancement by deviants would, and P2-N2 enhancement would not be affected by task load. Differences could remain, however, in that a visual analog of the MMN would be expected to have an occipital midline distribution (Naatlnen, 1986). In contrast, the reported visual P2-N2 has a central maximum (Courchesne, Hillyard, & Galambos, 1975; Kenemans et al., 1989;

J.L. Kenemans

et al. / ERPs to visual stimulus change

99

Renault, 1983). In, addition, P2-N2 enhancement by deviants does not depend on IS1 in the range between 2.45 and 8.45 s (Kenemans et al., 19891, whereas the auditory MMN becomes smaller with longer ISIS (Mantysalo & Naatanen, 1987). The proposition that P3 reflects a capacity-limited process is supported by the findings of Isreal, Chesney, Wickens, and Donchin (1980), Isreal, Wickens, Chesney, and Donchin (19801, and Wickens, Kramer, Vanasse, and Donchin (1983). These studies have demonstrated that P3s elicited by counted infrequent changes are substantially reduced by the introduction of a background task, whereas counting performance was not affected. These results have been interpreted as indicating that P3 reflects a process which is controlled and capacity limited (see Donchin, 19811. That is, the involvement in the background task limits the amount of “P3 process” which can be allocated to processing of the counting task stimuli. A corroborative result was reported by Roth, Dorato, and Kopell (19841, who found that while P3 was not enhanced by task instructions pertaining to the evoking stimuli, it was attenuated when subjects had to perform a secondary task not related to the evoking stimuli. These results (Isreal, Chesney, et al., 1980; Isreal, Wickens, et al., 1980) suggest that P3 amplitude reflects the allocation of processing capacity from a relatively undifferentiated resource. Undifferentiated resources have been included in the framework of a multiple-resource theory, by assuming that multiple resources may be structured hierarchically (Wickens, 1984; see also Gopher & Donchin, 19861. In Wickens’ model, two concurrently performed tasks, one more “verbal” and the other more “spatial”, may tap the same higher-level non-specific “general perceptual-processing resource” (Wickens, 1984, p. 88). Response processes, on the other hand, cannot tap this general resource. Accordingly, Isreal, Chesney, et al. (1980) found no reduction in P3 amplitude to secondary-task stimuli when the primary task was made more difficult on the response side. None of the dual-task studies discussed thus far were directed at evaluating the effects of a capacity manipulation on the enhancement of N2-like waves by occasional deviant visual stimuli. For the auditory modality, relevant data from two subjects were reported by Sams, Paavilainen, Alho, and Naatanen (1985). These authors found that elicitation of the MMN by auditory deviants occurred equally in a condition of a concurrent visual discrimination task and in one in which the auditory deviants had to be counted. In contrast, P3 was enhanced by auditory deviants in the latter condition only. In the present study, processing capacity was manipulated by presenting the ERP-eliciting standard and deviant stimuli as probes against the background of an ongoing task. Background task difficulty was varied between conditions. The extent of central processing elicited by the probe stimuli was

100

J.L. Kenemans et al. / ERPs

to visual stimulus change

measured by P3 amplitude, together with background task performance and a posteriori probe recognition. If the processes reflected in P2-N2 and P3 play a role in the generation of the OR, then it is of interest to study their temporal courses across trials, as a defining characteristic of the OR is its decrement with stimulus repetition. In .straightforward habituation studies we found rapid (asymptotic within 5 trials) decrement of the Nl deflection (peak latency about 180 ms). Nl decrement was paralleled by a similar decrease of the skin conductance response (SCR), the commonly used OR index, but was dissociated from the more slowly decreasing P3 (Kenemans, Verbaten, Sjouw, & Slangen, 1988; Verbaten, Roelofs, Sjouw, & Slangen, 1986a, 1986b). In a more oddball-like selective-attention study, Donald and Young (1982; see also Hansen & Hillyard, 1988) found that tuning of the Nl wave to a relevant stimulus feature took about 3 trials, whereas tuning of P3, presumed to reflect a later stage of selection, was instantaneous. In the Kenemans et al. (1989) study the enhancement of P2-N2 and P3 amplitudes by infrequent deviant stimuli was found to be stable across trials. The pattern across trials was estimated by means of orthogonal polynomial trend analysis (OPTA; see Melis, Kenemans, & Verbaten, 1990; Woestenburg, Verbaten, Van Hees, & Slangen, 19831, using 14 standard-deviant pairs. In the present study 42 of such pairs were used, thereby substantially increasing the number of degrees of freedom for the OPTA.

2. Method 2.1. Subjects Subjects were 22 undergraduate university students (13 female) at the University of Utrecht. All subjects were naive as to the purpose of the experiment and the procedure that was used. They were paid for their participation in course credits or money. 2.2. Apparatus Standard Ag-AgCl electrodes were used for monopolar EEG derivations. They were attached with a 5% collodion solution. Scalp locations were at Fz, Cz, Pz and Oz according to the lo-20 system. Linked ear electrodes were used as reference. Horizontal electro-oculogram (EOG) was recorded using Ag-AgCl electrodes in plastic cups attached to the outer canthus of each eye by means of adhesive rings. Similarly, vertical EOG was recorded from

J.L. Kenemans et al. / ERPs to visual stimulus change

101

infra-orbital and supra-orbital electrodes in line with the pupil of the left eye. A ground electrode was attached to the middle of the forehead. For both EEG and EOG, Hellige EEG paste was used. All EOG and EEG signals were amplified and filtered by an Elema universal filter. A time constant of 5 s was employed in conjunction with a low-pass filter setting of 30 Hz (- 3 dB, roll-off 6 dB/ octave). To suppress mains frequency and harmonics, amplifier output was first sent through a 50-Hz notch filter (bandwidth of 4-5 Hz), followed by a 45-Hz passive low-pass network. Subsequently, the signals were sent to the analog inputs of a PDP 11/23 computer for on-line analog-digital conversion. Sampling started 100 ms before stimulus onset and lasted 1024 ms, at a rate of 250 Hz. 2.3. Stimuli 2.3.1. Probes Two probe stimuli of equal brightness were used, both consisting of abstract visual patterns of standardized information content (Attneave, 1954; Spinks & Siddle, 1976; Verbaten, 1983). Stimulus duration was 924 ms, and the interval between two consecutive probes was fixed at 2.45 s. For each subject, one of the two served as standard, the other as deviant, and this order was counterbalanced over conditions. Within this oddball design, standards were presented 372 times, and deviants 42 times (10%). The number of standards between two deviants was quasi-random, ranging from 6 to 14. 2.3.2. Task stimuli Task stimuli consisted of the digits 0 through 9, each of 100 ms duration. Each digit was followed 2374 ms later by an imperative signal (“-“; task described below), lasting 20 ms. Nine hundred milliseconds after the imperative signal, the next digit was presented. The probe stimuli were always presented 700 ms after offset of the digit. All stimuli were presented in the middle of a TV screen. Rise time was 20 ms. During the experimental session, subjects were seated in a dentist’s chair in an acoustically and electrically shielded room. The chair was adjustable, so that the subject’s head could be positioned roughly parallel to a TV monitor (black and white, 26-inch screen), which was positioned above and in front of the subject at a distance of 60 cm from the subject’s eyes. Clamps were attached to the top of the chair in order to fixate the subject’s head in such a way that the center of the TV screen was in the center of the visual field. Eye movements from the center of the TV screen to any of the four corners were 28 degrees of arc. Presentation of stimuli and sampling procedures were controlled by the PDP 11/23.

102

J.L. Kenemans et al. / ERPs to visual stimulus change

2.4. Procedure Subjects were assigned to either one of two task load conditions: easy and hard. In the easy condition subjects were required to push a button with their right hand after each presentation of the imperative signal. In addition, they were required to look at the middle of the screen as much as possible. They were told that they could earn a maximum reward of 15 Dutch guilders, and that failures to respond and to fixate in the middle of the screen would lead to stepwise reductions of the reward. In the hard condition, subjects also had to respond upon presentation of the imperative signal; the nature of this response (i.e., left or right-hand button press), however, depended on the outcome of a decision process. After presentation of the digit, the subject first had to decide whether it was larger or smaller than the preceding digit. Subsequently, he or she had to compare this decision to the one made after the digit presented on the preceding trial. If two consecutive decisions were equal, the button in the left hand had to be pressed, else the right hand button. Subjects in the hard condition were told that they could earn a maximum reward of 15 Dutch guilders, and that incorrect or absent responses would lead to stepwise reductions of the reward. Some days before the experimental session, each of the 22 subjects was given extensive training on the hard task (without probes). After the training sessions, they were divided in two groups (n = ll), which did not differ significantly in training performance. Subjects in one group (easy) were then told that they had to perform a different task (see above). Both groups were told that “they would see some other things as well, but would not have to pay any attention to them.” The recording session started with 30 trials on which task stimuli were presented only, and subjects immediately started performing the task. From the 31st trial on, each digit was followed by a probe, according to the oddball schedule outlined before. After presentation of the last stimulus, the subject was asked to identify the standard stimulus among three other, slightly different figures; an analogous procedure was employed for the deviants. Finally, a second stimulus series was presented, to gather 36 EOG epochs containing large saccadic eye movements. (For a description see Kenemans et al., 1988; Verbaten et al., 1986b). Horizontal and vertical EOG, as well as EEG, were measured in the same way as they were during the first stimulus block. Using these additional data, the regression technique for removing eye movements from the ERPs (Woestenburg, Verbaten, & Slangen, 1983a) could be applied more adequately. 2.5. Data reduction and scoring Eye movements and blinks were measured by vertical and horizontal EOGs and subtracted from the EEG by a regression method in the frequency

J.L. Kenemans et al. / ERPs to visual stimulus change

103

domain (Woestenburg et al., 1983a). After removal of the ocular artifact, three different methods for ERP estimation were applied: classical averaging (yielding average ERPs or AERPs); estimation of single-trial ERPs by means of orthogonal polynomial trend analysis (OPTA, yielding estimated single-trial ERPs or SERPs); and a method in which the EEG epochs were left entirely unchanged (yielding “raw” ERPs or RERPs). SERP results will be reported to the extent that they differ from AERP results with respect to trial-independent effects, so as to probe the validity of the former, and when they show effects involving trials. RERP results will be reported to the extent that they deviate from SERP results on trial-dependent effects, indicating the benefit of the latter. 2.5.1. Trial grouping and peak scoring For the estimation of both AERPs and SERPs, standard and deviant trials were separated, resulting in one standard AERP and one deviant AERP, as well as one series of 42 standard SERPs, and a second series of 42 deviant SERPs. Note that the standards concerned were always presented on the trial immediately preceding the deviant trial. Fig. 1 shows grand average ERPs (across subjects). Although the experiment concerned P2-N2 and P3, Nl and P2 waves were analyzed as well. At first glance fig. 1 suggests modulation of Nl amplitude by experimental factors; variation in P2 amplitude was analyzed to determine the extent to which it contributed to modulations in P2-N2 amplitude. In each AERP, SERP and RERP, four amplitude measures were taken. The Nl was scored as the largest negative peak occurring between 80 and 230 ms after stimulus onset, and P3 as the largest positive peak between 280 and 600 ms. P3 and Nl amplitudes were determined with reference to a lOO-ms pre-stimulus baseline. The largest positive-negative peak-to-peak amplitude in between Nl and P3 was measured as the P2-N2. In a previous study (Kenemans et al., 19891, using exactly the same windows, the N2 deflection seldom went below zero, and therefore the N2 was scored relative to P2. The maximum window for N2 ranged from 225 to 450 ms. P2 itself was scored relative to the baseline, with latency limits of 150-320 ms.

3. Results 3.1. Performance 3.1.1. Task performance In the hard condition, the mean percentage of correct responses (over all 414 trials) was 86.9% (SD = 6.4). For the easy condition, these figures amounted to 98.5% (SD = 1.51. Additional analyses were carried out to determine the effects of trials and change conditions on task performance.

104

J.L. Kenemans et al. / ERPs to visual stimulus change

HARD

15

Nl 15

0

400

-STANDARD -

0

400 TIME (ms)

DEVIANT

Fig. 1. Grand average ERPs (across subjects and trials), separately vs. hard), change levels (standards vs. deviants), and leads.

for task load conditions

(easy

For each deviant and each preceding standard trial, the number of subjects delivering a correct response was counted. For each stimulus pair (deviant and preceding standard), then, the mean and difference scores were computed. These scores were entered into tests for orthogonal polynomial trends (Freund & Minton, 19791, with trends considered up to the second (quadratic) order. None of the effects of interest, however, reached significance. Hence, performance was not influenced by either trials or change. 3.1.2. Recognition In the easy condition, in 13 out of 22 cases the stimulus was identified correctly. In the hard condition, this number amounted to 5, yielding a significant difference between the two load conditions (p < 0.05, x2).

J.L. Kenemans et al. / ERPs to visual stimulus change

105

Table 1 Summary of the overall analysis of trial-independent effects. Non-significant F values are not reported. Results found only with SERP analysis are in italics. Maximum p values are in parentheses. Lo = Load, Ch = Change, Le = Leads Parameter

d.f.

Nl

1,20 1,20 3, 18 1,20 3, 18 3, 18 3, 18

9.6 (0.001) -

P2

P2-N2

P3

Effect Load Change Leads LoxCh LoxLe ChxLe LoxChxLe

_ 8.5 (0.005) _

-

3.6 (0.05) _ _

7.7 (0.005)

10.8 (0.005) 6.6 (0.05) 14.8 (0.0001) 6.7 (0.05) 4.1 (0.05) 3.6 (0.05)

3.2. ERPs

The four ERP parameters (Nl, P2, P2-N2 and P3 amplitudes) were analyzed within a mixed multivariate ANOVA design. This design included load, a two-level (easy and hard) between-subjects factor, and two within-subjects factors: change (two levels: standards and deviants) and leads (four levels: Oz, Pz, Cz and Fz). Change and leads effects were subjected to multivariate tests, using the program MULTIVARIANCE (Finn, 1978). In addition, in the case of SERPs and RERPs, “trials” was included as a third within-subjects factor. For each ERP parameter, the values for each set of 42 trials were reduced to 14 by averaging within each block of three adjoining trials. Subsequently, these 14 values were transformed to constant, linear and quadratic trend components (Schutz & Gessaroli, 19871, which were included in the multivariate analysis. Results from the overall analysis of trial-independent effects are presented in table 1. 3.2.1. Nl There were no effects involving load on Nl. Fig. 1 might suggest a difference between load conditions, in that Nl amplitudes appear to show a decrease from standard stimuli to deviants in the easy condition, as opposed to an increase in the hard condition. The Change x Load effect, however, only approached significance (F(1,20) = 4.1, p < 0.06), and, moreover, change effects were not significant in either separate load condition. Overall, Nl was larger at Cz than at other leads (see table 1); differences between Cz and other leads were significant at p < 0.01 (Oz and Pz) and p < 0.0001 (Fz). SERP analysis of trial-independent effects revealed the same pattern of results. Neither SERP nor RERP analysis revealed any effect involving trials.

J.L. Kenemans et al. / ERPs to L&al stimulus change

106

OZ

PZ

a

Ed

6-

0

=-

0

.

4

.,

. . . . . , . .

wEe*ee*66~6

0

0

10

5

=++%?-,,_ .

cz

.

.

.

5

0

.

.

.

.

.

.

.

4.

10

FZ 12-

12-

x

EASY

0-

Fig. 2. Mean P2 amplitudes, as scored in estimated single-trial ERPs (SERPs). Ordinate: trial blocks (each consisting of three trials). Abcissa: mean P2 amplitude in easy (x) and hard (0) conditions. Change levels pooled.

3.2.2. P2 There were no effects of load or change on P2. The leads main effect reflected larger amplitudes at Oz relative to Pz (p < O.OOOl), Cz (p < O.OOS>, and Fz (p < 0.001) (see fig. 1). SERP analysis, however, revealed a Leads x Load interaction, which can be better appreciated in combination with the only SERP effect involving trials, namely, a Load X Trials (linear) interaction (F(1, 20) = 9.2, p < 0.01). The linear trend was significant (F(1, 9) = 11.2, p < 0.01) in the easy, but not in the hard condition. In fig. 2 it can be seen, most notably at Pz, Cz and Fz, that P2 amplitudes decrease with trials in the easy condition only. At Cz and Fz this decrease leads to the disappearance of the difference between easy and hard, whereas at Pz this difference remains large enough to be reflected in the Leads x Load effect. Indeed, when tested separately for each lead, the load effect appeared to be significant at Pz only (F(1, 20) = 5.7, p < 0.05). Surprisingly, the Trials X Load effect was also found with RERP analysis. 3.2.3. P2-N2 P2-N2 amplitude was not affected by load, but was significantly larger on deviant trials, relative to standards, at Cz and Fz (Leads X Change effect).

J.L. Kenemans et al. / ERPs to visual stimulus change

” STANDARD

DEVIANT

EASY Fig. 3. Average ERPs amplitudes, separately

“STANDARD

107

DEVIANT

HARD

(AERPs): mean P2-N2 (recorded at Cz) and P3 (recorded at Pz) peak for load (easy vs. hard) and change (standards vs. deviants) levels.

Fig. 3 illustrates this finding for mean P2-N2 amplitudes at Cz. Separate tests for each lead revealed significant change effects at Cz (F(1, 20) = 9.7, p < 0.01) and Fz (F(1, 20) = 6.3, p < 0.05). SERP analysis of trial-independent effects revealed the same pattern of results. Neither SERP nor RERP analysis revealed any effect involving trials.

3.2.4. P3 As can be seen in figs. 1 and 3, P3 amplitude was substantially smaller in the hard condition than in the easy condition at Oz, Pz and Cz. This was reflected in load and Leads X Load effects. For separate leads, load effects were significant at Oz (p < 0.01) Pz (p < O.OOS), and Cz (I, < 0.05), but not at Fz. In addition, deviants elicited larger P3s at Oz and Pz (relative to standards) in the easy condition only, as reflected in Change X Load and Leads x Change x Load effects. The Change X Load effect was significant at Oz (p < 0.05) and Pz (p < O.Ol), not at Cz or Fz. Finally, the leads main effect reflected larger overall P3 amplitudes at Oz relative to Pz (p < O.OOOl), Cz (p < O.OOOl), and Fz (p < 0.001). SERP analysis yielded essentially the same results, albeit without leads interactions, including main effects of load @Xl, 20) = 14.3, p < O.OOS), change (F(1, 20) = 6.6, p < 0.05) and a Load X Change interaction Wl, 20) 6.6, p < 0.05). Again, this is better appreciated in light of trial-dependent effects, illustrated in fig. 4. Central and frontal P3s to deviant stimuli show a rapid decrease in the easy condition, but not in the hard condition, nor to standards or at Oz or Pz. This was confirmed by a Trials (quadratic) X Leads x Change x Load interaction (F(3, 18) = 3.2, p < 0.05), and significant Quadratic x Change X Load interactions specifically at Cz (F(1, 20) = 6.6, p < 0.05) and Fz (F = 4.7, p < 0.05), but not at Oz or Pz. Furthermore, Trials (linear) x Load (F(1, 20) = 8.6, p < 0.01) and Trials (linear) X Load X Leads (F(3, 18) = 3.2, p < 0.05) effects reflected significant linear decrease in the

108

J.L. Kenemans

et al. / ERPs to visual stimulus change

PZ

0

0

ft9?+)+9t~ 5

10

FZ

EASY: HARD:

x

STAND-

0

s-r--

Fig. 4. Mean P3 amplitudes, as scored in estimated single-trial ERPs (SERPs). Ordinate: trial blocks (each consisting of three trials). Abcissa: Mean P3 amplitude to easy standards (X ), hard standards (o), easy deviants ( * 1, and hard deviants ( + 1.

easy condition at Oz, Cz and Fz, which was absent in the hard condition or at Pz. The only trial-dependent effect revealed by RERP analysis concerned the Trials (linear) x Load interaction.

4. Discussion The present study replicated earlier findings (Kenemans et al., 1989) in that occasional visual deviant stimuli, with no particular task assigned to them, elicited enhanced P2-N2 and P3 amplitudes, relative to standards (easy condition). As to the main question of the present study, we found that P2-N2 enhancement by deviant stimuli was not affected by the fact that subjects were devoted to an involved background task (hard condition). In contrast, both substantial overall reduction in P3 amplitude and absence of P3 enhancement to deviant stimuli were observed in the hard condition. Furthermore, background task performance was not affected by probe presentation (cf. Rosier et al., 1986), and a posterior probe recognition was at chance level in the hard condition (but not in the easy condition). This

J.L. Kenemans

et al. / ERPs to visual stimulus change

109

pattern of results suggests that the amount of central processing elicited by the probe stimuli in the hard condition was smaller than in the easy condition. The concurrent (sequence-independent) load effects on P3 and on recognition performance are in line with the suggested relationship between these two variables (Fabiani, Karis, & Donchin, 1986; Paller, McCarthy, & Wood, 1988). The combined results for P2-N2 and P3 suggest that ERPs may reflect the operation of a two-stage process in response to infrequently presented deviant visual stimuli. P2-N2 may reflect the outcome of a comparison process; this process may be conceived of as being “automatic” as it was not affected by load. Following Ohman (1979), mismatch detection results in an OR which represents a “call” for central, capacity-limited processing. P3 may reflect this central processing, and accordingly P3 enhancement to deviant stimuli was absent in the hard condition, where presumably much of the central processing capacity was unavailable. As noted before, a similar processing model has been proposed to account for auditory data. An important difference in this respect between visual and auditory results pertains to the effect of ISI. Unlike the MMN (measured as a difference score), visual P2-N2 enhancement to deviants does not decrease when ISIS increase (see section 1). According to Naatanen (19861, there is no differential processing of standards and deviants at the pre-attentive level with long ISIS (as far as ERPs can reveal). ERPs to visual deviants, on the other hand, show a sign of such differential processing with long ISIS as well (Kenemans et al., 1989). A different explanation for the dissociation between P2-N2 and P3 with respect to load effects would be in terms of multiple resources (Wickens, 1984). For example, P3 amplitude could reflect the general perceptual-central resource, while P2-N2 amplitude would depend on allocation of spatial resources, which would be left relatively unaffected by the allocation of verbal resources by the background task. Rather than maintaining a distinction between central and automatic processes, this view asserts that processes may differ as to the specificity of the resources they invoke. This hypothesis might be substantiated by conducting an experiment in which both background and probe stimuli were of the same verbal or visual-spatial nature. The sequence-independent effects on P3 suggest that standards already presented many times may still invoke a substantial amount of central processing (at least relative to standards in the hard condition). This would contradict hhman’s (1979) conjecture that central processing is always preceded by an OR. Such a dissociation was also suggested by earlier findings pertaining to combined observations of slow P3 decrease and rapid SCR decrease in habituation series (Kenemans et al., 1988; Verbaten et al., 1986a, 1986b), and of enhanced P3s to deviants in the absence of similar SCR enhancement (Kenemans et al., 1989).

110

J.L. Kenemans et al. / ERPs to visual stimulus change

The present analysis of the time course of ERPs across trials confirmed the earlier observation of stable P2-N2 and P3 (Pz) responses to successive deviant stimuli (Kenemans et al., 1989). However, in addition to the posterior P3, a second positivity in the same latency range was found to be sensitive to both stimulus change, and the capacity manipulation, and trials. That is, a Trials x Change x Load effect was found specifically at Cz and Fz, but not at Oz or Pz. The enlarging effect of deviants in the easy condition was constant over all 42 trials at posterior leads, but disappeared at anterior leads within the first 9-12 trials (3-4 trial blocks, see fig. 4). This pattern of anterior P3 responses to repeated stimulus change shows some resemblance to the decrease of frontal P3 amplitude in response to repeated novels reported by Courchesne (1978). A comparable concurrence of sustained posterior and decreasing anterior P3 amplitudes, although in a different paradigm, has been reported by Woestenburg, Verbaten, and Slangen (1981, 1983b). Although these findings may be taken as a corroboration of the comment by Fabiani et al. on the Courchesne et al. reports that “it would have been easier to accept the existence of this frontal positivity if there had been reports of this component from other laboratories” (Fabiani, Gratton, Karis, & Donchin, 1987, p. 67; Courchesne, 1978; Courchesne et al., 1975) the sufficient antecedent conditions for elicitation of the anterior P3, let alone its functional significance, remain somewhat obscure. Both Courchesne (1978) and Pritchard (1981) emphasize the possibility that this frontocentral P3 is especially elicited when the invariance of event attributes, and the rules defining the relations between attributes, have not yet been abstracted. Thus, only after a number of presentations of the deviant stimulus in the probe channel would its temporal and visual-spatial relation to the standard stimulus have been derived, and the frontocentral P3 subsequently decrease. A theoretical view linking trial-dependent fluctuation and the concept of multiple resources has been advanced explicitly by Gopher and Donchin (1986). Following Sanders’ adaptation of the three-part resource theory of Pribram and McGuiness (1975; Sanders, 1983) these authors suggest that the considered a specific perceptual resource, can energetical pool of “arousal,” obtain independence from the central “effort” mechanism through a process of increasing automaticity (cf. Schneider, Dumais, & Shiffrin, 1983). It is tempting to speculate that, in the present easy condition, the decrement in frontocentral P3 reflects the decreasing involvement of the central effort mechanism in the processing of the (deviant) probe stimuli. The absence of the frontocentral P3 in the hard condition then would reflect the limited capacity of the central effort mechanism. It remains to be established why the frontocentral P3 effect was obtained in the present easy condition, and not, for example, in the study by Kenemans et al. (1989). At least two alternative explanations may be considered. One pertains to the increased power for detecting trial-dependent variation

J.L. Kenemans

et al. / ERPs to visual stimulus change

111

in the present study, due to the larger number of trials employed. A second explanation takes into account the more complex stimulus configuration of the present experiment, which is due to the inclusion of background task stimuli. The background task per se (i.e., even the easy one) is not likely to be a crucial factor, as the frontocentral P3 decreases with increasing background task load, and hence it might be expected to increase rather than decrease when no background task is used at all (as in Kenemans et al., 1989). The results for the frontocentral P3, together with other effects involving leads, suggest that P3 amplitude, as measured in the present study, is a function of contributions of different neural generators. The leads main effect indicates an occipital focus (i.e., a source close to the Oz electrode). As has been reported before (Verbaten et al., 1986a, 1986b), visual, relatively meaningless stimuli (e.g., presented many times) elicit larger P3s at Oz relative to other leads. Although we recognize that the relation between midline topography and neural generator properties may be anything but straightforward, this interpretation of the occipital P3 maximum is tempting in the light of its putative relation with the concept of the “local OR” (Sokolov, 1963), referring to relatively persistent activity in modality-specific brain areas. Furthermore, differences in scalp topography may be applied to separate different components contributing to a single waveform, without reference to exact properties of the intracranial generators (Gratton, Coles, & Donchin, 1989). Thus, a third apparently functionally independent generator having a parietal scalp focus is suggested by the fact that, in the easy condition, a gradual (linear) decline in P3 amplitude was visible at Oz Cz and Fz, but not at Pz (see SERP results, fig. 4). Although P2 amplitude was affected by load in a sequence-independent manner (i.e., no interaction with change), there are some conspicious parallels between P2 and P3 results. First, the basic occipital focus (leads main effect) found for P3 was also obtained for P2. Second, the Trials (linear) X Load interaction was obtained for both peaks, reflecting gradual decline in the easy condition, towards the constant level of the hard condition. Third, with both peaks, the pattern over trials at Pz was different, relative to other leads. For P2, the load effect was significant at Pz only (Leads X Load effect); for P3, the load effect decreased at all leads, except for Pz. These results suggest that the occipital and parietal components of the P3 (see previous paragraph) may already be observed in the P2 latency range. The appearance of two positive peaks in the final waveform then, may be attributable to the superposition of the N2 wave. An analogous relationship might exist between the auditory P165 and P3 (Goodin, Squires, Henderson, & Starr, 1978; see also Naatanen & Gaillard, 1983). The results of this work suggest that the response to an infrequent deviant stimulus consists of at least two stages. One is reflected in P2-N2 amplitude and may be viewed as “automatic” (or as involving specific resources); it may

112

J.L. Kenemans et al. / ERPs to visual stimulus change

correspond to 6hman’s “call” for central processing (ohman, 1979). The other, reflected in P3 amplitude, would correspond to this very central processing (or as involving more non-specific resources>. Both P2 results and the persistence of P3 to standard stimuli, however, suggest that central processing may also occur independently from a preceding “call”.

References Attneave, F. (1954). Some informational aspects of visual perception Psychological Reuiew, 61, 183-193. Courchesne, E. (1978). Changes in P3 waves with event repetition: Long-term effects on scalp distribution and amplitude. Electroencephalography and Clinical Neurophysiology, 45,754766. Courchesne, E., Hillyard, S.A., & Galambos, R. (1975). Stimulus novelty, task relevance and the visual evoked potential in man. Electroencephalography and Clinical Neurophysiology, 39, 131-143. Donald, M.W., &Young, M.J. (1982). A time-course analysis of attentional tuning of the auditory evoked response. Experimental Brain Research, 46, 357-367. Donchin, E. (1981) Surprise!. Surprise? Psychophysiology, 18, 493-513. Fabiani, M., Gratton, G., Karis, D., & Donchin, E. (1987). The definition, identification, and reliability of measurement of the P300 component of the event-related brain potential. In P.K. Ackles, J.R. Jennings, & M.G.H. Goes (Eds.), AdLlances in psychophysiology (Vol. 2, pp. I-78). Greenwich, CT: JAI Press. Fabiani, M., Karis, D., & Donchin, E. (1986). P300 and recall in an incidental memory paradigm. Psychophysiology, 23, 298-308. Finn, J.D. (1978) Multiuariance: User’s guide. Version V’Z,release 2. Chicago: National Education Resourses. Freund, R.J., & Minton, P. (1979). Regression methods: A tool for data analysis. New York: Marcel Dekker. Goodin, D.S., Squires, K.C., Henderson, B.H., & Starr, A. (1978). An early event-related cortical potential. Psychophysiology, 15, 360-365. Gopher, D., & Donchin, E. (1986). Workload:An examination of the concept. In K.R. Boff, L. Kaufman, & J.P. Thomas (Eds.), Handbook of perception and performance (Vol. 2, pp. 41/l -41/49). New York: Wiley. Gratton, G., Coles, M.G.H, & Donchin, E. (1989). A procedure for using multi-electrode information in the analysis of components of the event-related potential: Vector filter. Psychophysiology, 26, 222-232. Hansen, J.C., & Hillyard, S.A. (1988). Temporal dynamics of human auditory selective attention. Psychophysiology, 25, 316-329. Isreal, J.B., Chesney, G.L., Wickens, C., & Donchin, E. (1980). P300 and tracking difficulty: Evidence for multiple resources in dual-task performance. Psychophysiology, 17, 259-273. Isreal, J.B., Wickens, C., Chesney, G.L., & Donchin, E. (1980). The event-related brain potential as an index of display-monitoring workload. Human Factors, 22, 211-224. Kenemans, J.L., Melis, C.J., Verbaten, M.N., & Slangen, J.L. (1991). Visual ERPs to a single deviant stimulus sensitive to the number of preceding standard stimuli. Journal of Psychophysiology, 5, 349-359. Kenemans, J.L., Verbaten, M.N., Roelofs, J.W., & Slangen, J.L. (1989). “Initial-” and “changeORs”: An analysis based on visual single-trial event-related potentials. Biological Psychology, 28, 199-226.

J.L. Kenemans et al. / ERPs to visual stimulus change

113

Kenemans, J.L., Verbaten, M.N., Sjouw, W., & Slangen, J.L. (1988). Effects of task relevance on habituation of visual single-trial ERPs and the skin conductance orienting response. International Journal of Psychophysiology, 6, 51-63. Lynn, R. (1966). Attention, arousal and the orientation reaction. Oxford: Pergamon Press. Mantysalo, S., & Naltanen, R. (1987). The duration of a neuronal trace of an auditory stimulus as indicated by event-related potentials. Biological Psychology, 24, 183-195. Melis, C.J., Kenemans, J.L., & Verbaten, M.N. (1990). Beyond averaging: Using orthogonal polynomials to estimate response patterns. In C.H.M. Brunia, A.W.K. Gaillard, &A. Kok (Eds.), Psychophysiological brain research (Vol. 1, pp. 77-82). Tilburg: Tilburg University Press. Nlatanen, R. (1986). The orienting response: A combination of informational and energetical apects of brain function. In G.J.L. Hockey, A.W.K. Gaillard, & M.G.H. Coles (Eds.), Energetics and human information processing (pp. 91-111). Dordrecht: Martinus Nijhoff. NIItanen, R. (1990). The role of attention in auditory information processing as revealed by event-related potentials and other brain measures of cognitive function. Behauioral and Brain Sciences, 13, 201-233. Naatanen, R., & Gaillard, A.W.K. (1983). The orienting reflex and the N2 deflection of the event-related potential (ERP). In A.W.K. Gaillard & W. Ritter (Eds.), Tutorials in euent-rehued potential research: Endogenous components (pp. 119-141). Amsterdam: North-Holland. NIZtinen, R., Simpson, M., & Loveless, N.E. (1982). Stimulus deviance and evoked potentials. Biological Psychology, 14, 53-98. Ghman, A. (1979). The orienting response, attention and learning: An information processing perspective. In H.D. Kimmel, E.H. van Olst, & F. Orlebeke (Eds.), The orienting reflex in humans (pp. 443-471). Hillsdale: Erlbaum. Paller, H.A., McCarthy, G., & Wood, CC. (1988). ERPs predictive of subsequent recall and recognition performance. Biological Psychology, 26, 269-276. Pribram, K.H., & McGuiness, D. (1975). Arousal, activation and effort in the control of attention. Psychological Review, 82, 116-149. Pritchard, W. (1981). Psychophysiology of P300. Psychological Bulletin, 89, 506-540. Renault, B. (1983). The visual emitted potentials: Clues for information processing. In A.W.K. Gaillard & W. Ritter (Eds.), Tutorials in event-related potential research: Endogenous components (pp. 159-175). Amsterdam: North-Holland. Riisler, F., Sutton, S., Johnson, R., Jr., Mulder, G., Fabiani, F., Plooij-van Gorsel, E., & Roth, W.T. (1986). Endogenous ERP components and cognitive constructs: A review. In W.C. McCallum, R. Zappoli, & F. Denoth (Eds.), Cerebral psychophysiology: Studies in event-related potentials (pp. 77-82). Amsterdam: Elsevier. Roth, W.T., Dorato, K.H., & Kopell, B.S. (1984). Intensity and task effects on evoked physiological responses to noise bursts. Psychophysiology, ZZ, 466-481. Sams, M., Alho, K., & NaPtanen, R. (1984). Short-term habituation and dishabituation of the mismatch negativity of the ERP. Psychophysiology, 21, 434-441. Sams, M., Paavilainen, P., Alho, K., & Niiatanen, R. (1985). Auditory frequency discrimination and event-related potentials. Electroencephalography & Clinical Neurophysiology, 62,437-448. Sanders, A.F. (1983). Toward a model of stress and human performance. Acta Psychologica, 53, 61-97. Schneider, W., Dumais, S.T., & Shiffrin, R.M. (1983). Automatic and control processing and attention. In R. Parasuraman & R. Davies (Eds.), Varieties ofattention (pp. l-27). New York: Academic Press. Schutz, R.W., & Gessaroli, M.E. (1987). The analysis of repeated measures designs involving multiple dependent variables. Research Quarterly for Exercise and Sport, 58, 132-149. Snyder, E., & Hillyard, S.A. (1976). Long-latency evoked potentials to irrelevant deviant stimuli. Behavioral Biology, 16, 319-331.

114

J.L. Kenemans et al. / ERPs to visual stimulus change

Sokolov, E.N. (1963). Perception and the conditioned reflex. Oxford: Pergamon Press. Spinks, J.A., & Siddle, D.A.T. (1976). Effects of stimulus information and stimulus duration on amplitude and habituation of the electrodermal orienting response. Biological Psychology, 4, 29-39. Squires, K.C, Donchin, E., Herning, R.I., & McCarthy, G. (1977). On the influence of task relevance and stimulus probability on event-related potential components. Electroencephalography and Clinical Neurophysiology, 42, 1- 14. Verbaten, M.N. (1983). The influence of information on habituation of cortical, autonomic and behavioral components of the orienting response (OR). In A.W.K. Gaillard & W. Ritter (Eds.), Tutorials in event-related potential research: Endogenous components (pp. 201-216). Amsterdam: North-Holland. Verbaten, M.N., Roelofs, J.W., Sjouw, W., & Slangen, J.L. (1986a). Different effects of uncertainty and complexity on single trial visual ERPs and the SCR-OR in non-signal conditions. Psychophysiology, 23, 254-262. Verbaten, M.N., Roelofs, J.W., Sjouw, W., & Slangen, J.L. (1986b). Habituation of early and late visual ERP components and the orienting reaction: The effect of stimulus information. International Journal of Psychophysiology, 3, 287-298. Wickens, C.D. (1984). Processing resources in attention. In R. Parasuraman & and R. Davies (Eds.), Varieties of attention (pp. 63-102). New York: Academic Press. Wickens, C., Kramer, A., Vanasse, L., & Donchin, E. (1983). Performance of concurrent tasks: A psychophysiological analysis of the reciprocity of information-processing resources. Science, 221, 1080-1082. Woestenburg, J.C., Verbaten, M.N., Van Hees, H.H., & Slangen, J.L. (1983). Single-trial ERP estimation in the frequency domain using orthogonal polynomial trend analysis (OPTA): Estimation of individual habituation. Biological Psychology, 27, 173-191. Woestenburg, J.C., Verbaten, M.N., & Slangen, J.L. (1981). The influence of information on habituation of the “Wiener” filtered visual event-related potential and the skin conductance reaction. Biological Psychology, 13, 189-201. Woestenburg, J.C., Verbaten, M.N., & Slangen, J.L. (1983a). The removal of the eye-movement artefact from the EEG by regression analysis in the frequency domain. Biological Psychology, 16, 127-147. Woestenburg, J.C., Verbaten, M.N., & Slangen, J.L. (1983b). Stimulus information and habituation of the visual event-related potential and the skin conductance reaction under task-relevance conditions. Biological Psychology, 16, 225-240.