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N2, P3 and the lateralized readiness potential in a nogo task involving selective response priming
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Electroencephalography and clinical Neurophysiology99 (1996) 19-27
N2, P3 and the lateralized readiness potential in a nogo task involving selective response priming B r u n o K o p p a,*, U w e M a t t l e r b, R a l f G o e r t z a, F r e d R i s t b aHumboldt University at Berlin, Department ~f Psychology, Clinical Psychology and Behavioral Neuroscience, Hausvogteiplatz 5-7, D-lOll 7 Berlin, Germany bCentral Institute of Mental Health, Mannheim, Germany
Accepted for publication: 20 March 1996
Abstract
Motor inhibition and its correlates in the event-related potential (ERP) are often studied in go/nogo tasks. However, go and nogo trials differ in their motor and their attentional requirements, rendering an interpretation of corresponding changes in ERP components difficult. As an alternative strategy to study motor inhibition, a hybrid choice-reaction go/nogo procedure involving selective response priming was used. Eighteen subjects performed the task. Response time (RT) and error measures as well as the lateralized readiness potential (LRP) indicated that responses were primed by flanker stimuli that were associated with one of the two possible responses. In nogo trials, selective response priming influenced the N2 amplitude whereas the P3 amplitude was unaffected. Because the N2 appeared irrespective of whether an erroneous response was correctable (in go trials) or not (in nogo trials), we conclude that the N2 reflects either the detection or the inhibition of an inappropriate tendency to respond. Keywords: N2; P3; LRP; Nogo task; Motor inhibition; Response priming; Error processing
1. I n t r o d u c t i o n
The ability to inhibit thought and action is crucial for the maintenance of coherent sequences of cognitive and motor events (Logan and Cowan, 1984). Traditionally, motor inhibition has been studied by comparing go and nogo trials. Several ERP components have been found to differ between go and nogo trials. These go/nogo effects on ERP amplitudes were interpreted as signs of inhibitory activity in the nogo trial which is related to the interruption of response execution, Roberts et al. (1994) reported that the amplitude of the P3 in nogo trials was enhanced compared to those in go trials and related the P3 go/nogo effect to motor inhibition. In further support of the motor inhibition interpretation of the P3 go/nogo effect, Roberts et al. (1994) point out that the scalp distribution of the nogo P3 is more anterior compared to the distribution of the go P3 (Pfefferbaum and Ford, 1988). The go/nogo effect on the amplitude of the P3 had similarly been re-
* Corresponding author. Tel.: +30 203 77379; fax: +30 203 77308; e-mail: [email protected]
ported by Eimer (1993), Kok (1986), Schr6ger (1993), Simson et al. (1977). Simson et al. (1977) attributed the P3 go/nogo amplitude effect to the sustained negativity that accompanies the motor performance which is required in go trials and which is withheld in nogo trials. However, Pfefferbaum et al. (1985) showed that the more anterior scalp distribution of the nogo P3 compared to the go P3 appeared when covert (cognitive) responses had to be interrupted in nogo trials. This result rules out the possibility that the overlay of (negative) motor potentials in the go trials was solely responsible for the P3 go/nogo effect. Apart from the P3 go/nogo effect, the amplitude of the N2 was found to be enhanced in nogo trials compared to go trials (e.g. Eimer, 1993; Jodo and Kayama, 1992; Kok, 1986; Pfefferbaum et al., 1985). Pfefferbaum et al. (1985) observed the N2 go/nogo effect with both overt motor responses and covert cognitive responses. Although the N2 go/nogo effect was larger with overt than with covert responses, the N2 go/nogo effect was still present with covert responses. Thus, the N2 go/nogo effect cannot be completely attributed to the overlay of motor potentials. In sum, the N2 enhancement in nogo trials is not confined
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B. Kopp et al. / Electroencephalography and clinical Neurophysiology 99 (1996) 19-27
to withholding motor responses, but appears whenever either overt or covert responses have to be interrupted. The purpose of the present study was to clarify whether the N2 or the P3 or both ERP components indicate motor inhibition. Motor inhibition signifies the suppression of a tendency to respond that may be achieved either by inhibitory neuronal activity (cessation of the movement agonist) or by excitatory neuronal activity (activation of the movement antagonist). Apparently, comparing go and nogo trials is a straightforward method to identify ERP components that are associated with motor inhibition. In practice, however, go and nogo trials differ in at least two further features. Firstly, with motor responses, the go ERPs will reflect brain activity that is related to the execution of the responses whereas the nogo ERPs will not (Kok, 1988). Secondly, go and nogo trials differ with respect to the necessity to prepare for a movement and thus may be associated with different attentional requirements. Paying attention might be dispensable once it is recognized that nothing has to be done in a given trial. Thus, nogo trials may be accompanied by a lapse of cortical excitation. In sum, go/nogo effects on the amplitude of ERP components are not unambiguously attributable to motor inhibition because these confounds are not easily disentangled. In order to avoid the inferential difficulties that arise from these ambiguities, we compared ERPs in specifically versus nonspecifically primed nogo trials in a hybrid choice-reaction go/nogo task. The go task was a variant of the original flanker task (Eriksen and Eriksen, 1974). In this task, a centrally presented target letter was flanked by additional stimuli. The target letter was flanked either by congruent (letters that indicated the same response as the target), by neutral (letters with no response assignment) or by incongruent (letters that indicated the opposite response as the target) flanker stimuli. RTs in congruent trials were faster and RTs in incongruent trials were slower than those in neutral trials. In order to explain the effects on RT that are exerted by the flanker stimuli, it is commonly assumed that the activation of responses begins as soon as visual information accumulates. Early in the process, all responses receive initial activation. Because more flanker stimuli than target stimuli were presented, flanker-triggered responses receive a relatively stronger initial activation than target-triggered stimuli. With the target becoming gradually localized, information from this part of the stimulus pattern gains importance. The threshold for the execution of the response is achieved faster if the response had already an initial level of activation. The achievement of the response threshold is prolonged due to interference if the opposite response received initial activation as in the incongruent trials (Eriksen and Schultz, 1979; Coles et al., 1985). Selective response priming can be measured with the asymmetry between the ipsilateral and the contralateral readiness potential. The lateralized readiness potential is a valid
real-time index of hand-specific motor preparation (Kutas and Donchin, 1980; Coles, 1989; Miller and Hackley, 1992). In the flanker task, the LRP was sensitive to even brief preparation for a unimanual response that was primed by the flanker stimuli (Gratton et al., 1988; Kopp et al., 1996). The original flanker task was modified in several respects for the study to be reported. Instead of letters with random response assignment, arrowheads were used both as target stimuli and as flanker stimuli. The relation between an arrow to the left and a left-hand response is considered a population stereotype which does not require learning. The arrowheads should prime their associated responses automatically because of the high compatibility between stimuli and responses (Kornblum et al., 1990). Several studies showed that facilitation and interference were more pronounced when flanker onset preceded target onset (Taylor, 1977; Eriksen and Schultz, 1979; Flowers and Wilcox, 1982; Grice et al., 1984; Grice and Gwynne, 1985; Flowers, 1990). As a consequence, we introduced a constant stimulus onset asynchrony (SOA) of 100 ms. Nogo trials were interspersed with an overall probability of 33%. Nogo stimuli were preceded either by arrowheads (specific priming) or by squares (nonspecific priming) as flanker stimuli. In specifically primed nogo trials, the flanker stimuli were associated with one of the two possible go-responses. Nonspecific flanker stimuli delivered the same temporal information but they were not related to one of the two possible go-responses. The critical difference between specific and nonspecific priming was that response priming could take place in the former but not in the latter case. In our hybrid go/nogo task, go trials (33% left-hand responses and 33% right-hand responses) were twice as probable as nogo trials (33%). It is known that the probability of events influences ERP amplitudes, especially the P3 amplitudes. Therefore, and for the reasons mentioned above, we concentrated our analyses on the comparison between (a) the specifically primed nogo trials and (b) the nonspecifically primed nogo trials. We expected response priming to occur in the specific but not in the nonspecific priming condition of the nogo trials. We further assumed that the interruption of the erroneously primed responses involves motor inhibition. Thus, we examined the effects that selective response priming exerts on the ERP in a nogo task. More specifically, we wanted to know whether the N2 or the P3 or both ERP components are associated with the necessity to withhold a primed response. 2. Method 2.1. Subjects
Eighteen paid volunteers served as subjects (mean age
B. Kopp et al. / Electroencephalography and clinical Neurophysiology 99 (1996) 19-27
21
33 years; 13 men and 5 women). All subjects were righthanded and all had normal or corrected-to-normal vision.
2.2. Stimuli and procedure The target stimulus was an arrowhead pointing either left or right (go stimulus) or an octagon (nogo stimulus) presented at the center of a PC-CRT screen (Beringer, 1994). The arrowheads were constructed as equilateral triangles with an edge length of 21 mm, the squares had an edge length of 15 mm. Triangles, squares and octagons contained identical numbers of pixels. The edge-to-edge distance of flanker and target stimuli was always 1° of visual angle. All stimuli were presented in gray color against a black background. Two thirds of all trials were go trials; in go trials, the three visual context conditions (congruent, neutral, incongruent) appeared with equal probabilities. Subjects had to respond with the index finger that corresponded to the central arrowhead. In congruent go trials, two arrows pointing to the same direction as the target stimulus were presented above and below the target. In incongruent go trials, the two flanker stimuli pointed to the opposite direction. Squares were used as neutral flanker stimuli (cf. Fig. 1). One third of all trials were nogo trials, i.e. responses had to be withheld when an octagon appeared as target stimulus. In nogo trials with specific priming, the flanker stimuli were arrows that primed their associated response. Thus, there were nogo trials in which either a left-hand or a right-hand response was primed. In nogo trials with nonspecific priming, the flanker stimuli were squares without any response assignment. Go trials (67%, summed over left-hand and right-hand responses) occurred twice as often as nogo trials (33%). Within go trials, congruent (33%), neutral (33%) and incongruent (33%) flanker stimuli occurred with equal probabilities. Within nogo trials, specific priming (67%, summed over left-hand and right-hand flanker stimuli) occurred twice as often as nonspecific priming (33%, neutral flanker stimuli). Note that the flanker stimuli did not predict the forthcoming target stimulus. Each flanker stimulus (left-hand stimulus, neutral, right-hand stimulus) was associated with left-hand responses (33%), right-hand responses (33%) or nogo responses (33%). Thus, all three possibilities were equally probable alternatives, given the presence of a particular flanker stimulus. At the beginning of each trial, a central fixation cross appeared for 500 ms. As short SOAs between flanker and target stimuli enhance visual context effects (Taylor, 1977), the onset of the flanker stimuli preceded the onset of the target stimulus by 100 ms. The target stimulus was presented in addition to the flanker stimuli and stayed for 50 ms at the center of the CRT screen. All three stimuli were removed simultaneously. A variable intertrial interval of about 2 s followed. After a practice block of 63 trials, 10 blocks of 63 trials each followed. Thus, at least
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Fig. 1. The design of the experiment. (Top) Go trials. The three visual context conditions (congruent, neutral, incongruent) for fight-hand responses. These visual context conditions occurred with equal frequencies; the overall probability for a go trial was 67%. (Bottom) Nogo trials. The three priming conditions (specific right, nonspecific, specific left). These priming conditions occurred with equal frequencies; the overall probability for a nogo trial was 33%.
630 trials (error trials were repeated) were administered during 45-60 min. Within each block, trial types were presented in random sequence. Subjects were instructed to focus on the central target stimulus and to ignore the flanker stimuli. They were instructed to respond as fast as possible at the expense of accuracy, Subjects were seated 1.20 m in front of the CRT screen. They kept their index fingers resting on analogue response keys that resembled telegraph keys (Giray and Ulrich, 1993). A leaf spring was held by an adjustable clamp at one end, whereas the other end remained free. Strain gauges were attached near the fixed end of the leaf spring. Any force applied to the leaf spring led to a displacement at its free end. The displacement was converted into an analogous electrical signal. The electrical signals from both force keys were fed into a second PC, digitized at 100 Hz and stored on disk. The resolution of this device was about 2 mN. Subjects were asked to rest their fingers on both response keys and to make a response by depressing the appropriate key or to withhold the response. A response was defined as a key displacement equivalent to at least 2 N of force. The responses were evaluated online. RTs were defined as the interval between the target stimulus onset and the time when a level of 2 N force was surpassed with the appropriate key. Subjects were told that they could correct wrong responses in go trials by pressing the correct key immediately after the wrong key (i.e. within 1300 ms after the onset of the flanker stimuli). Uncorrected wrong responses elicited an auditory feedback tone (500 Hz) that began 1300 ms after the onset of the flanker stimuli. Uncorrected errors were rerun within the same block of trials. In go trials, uncorrected errors occurred very rarely (the probability of uncorrected errors did not surpass 0.5% in any of the three visual context conditions) and were not analyzed further. Corrected wrong
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B. Kopp et al. /Electroencephalography and clinical Neurophysiology 99 (1996) 19-2 7
responses were considered errors. Early or late responses and those responses that did not achieve the criterion force level of 2 N were fed back using a 1000 Hz tone. In nogo trials, a response that exceeded the criterion force level of 2 N was an (uncorrectable) error that was fed back using a 500 Hz tone.
2.3. Recording and data analyses The electroencephalogram (EEG) was recorded using Ag-AgC1 electrodes at Fz, Cz, Pz, C3', and C4' referenced to the left ear lobe. 1 The vertical and horizontal electrooculogram (EOG) was recorded from sites above and below the left eye and 1 cm external to the outer canthus of each eye. Trials containing horizontal eye movements were rejected; trials containing blinks were corrected using the regression method described by Berg (1986). A ground electrode was placed on the forehead. The signals were amplified with a Nihon Kohden amplifier (time constant 10 s; high-frequency cutoff 35 Hz). Electrode impedance was kept below 5 kQ. The signals were digitized on-line at a rate of 100 Hz for 1400 ms, starting 100 ms before the presentation of the flanker stimuli. No digital filtering was applied to the signals. Stimulus-synchronized average ERPs were computed from correctly responded trials subtracting the lOOms prestimulus period as the baseline. Separate averages were computed for go trials (visual context (congruent, neutral, incongruent)) and nogo trials (response priming (specific, nonspecific)) for the midline electrode sites (Fz, Cz, Pz). The LRP in go trials was evaluated separately for the three visual context conditions. The LRP in go trials was assessed by using the ERP waveforms recorded at C3' and C4'. The recordings at C3' and C4' were subtracted from one another (left-hand responses C4'-C3', right-hand responses C3'-C4') and averaged separately for left-hand and right-hand responses. These averages were then combined across hands ((left-hand (C4'-C3') + right-hand (C3'-C4'))/2). The LRP in the specific priming condition of the nogo trials was computed in the same way, but averaged separately for specific left- and rightresponse priming conditions. These averages were then combined across both specific priming conditions, ((C4'C3') + (C3'-C4'))/2. It was not possible to compute LRPs in the nonspecific priming condition of the nogo trials
because there was no way to decide whether C4'--C3' or C3'-C4' was to be computed in a particular trial. The LRPs (peak and mean amplitudes) from the various conditions were compared by the permutation test described by Blair and Karniski (1993). By computing t values at each single time point, this waveform analysis indicates the periods during which two waveforms differ significantly. Within the go condition, we compared (a) the neutral and the congruent LRPs to test for the facilitative effect of congruent flanker stimuli and (b) the neutral and the incongruent LRP to test for the interfering effect of incongruent flanker stimuli. In addition, we compared the go and the nogo LRPs, i.e. (a) the congruent LRP from go trials with the LRP from the specific nogo trials (multiplied with -1) and (b) the incongruent LRP from go trials with the LRP from the specific nogo trials. Greenhouse-Geisser adjusted P values are reported, but original degrees of freedom are given. 3. Results
3.1. Behavioral findings Mean RTs from the correct go trials were subjected to a repeated-measures ANOVA (visual context) that revealed a significant effect for visual context, F(2, 34) = 173.0, P < 0.0001. The congruent visual context (mean = 321 ms) yielded faster RTs than the neutral context (mean= 361 ms; F(I, 17)= 115.4, P<0.0001); the incongruent visual context (mean = 388 ms) yielded slower RTs than the neutral context, F(I, 17) = 81.4, P < 0.0001. Arcsin-transformed error scores from the go trials were subjected to the same repeated-measures ANOVA (visual context) that revealed a significant effect for visual context, F(2, 34) = 20.8, P < 0.0002. The incongruent visual context (mean= 15.1%) yielded more errors than the neutral context (mean = 2.7%; F(1, 17) = 20.6, P < 0.0003) with no discernible difference between the congruent visual context (mean = 2.1%) and the neutral context. Arcsin-transformed error scores from the nogo trials were subjected to a repeated-measures ANOVA (priming: specific, nonspecific). The effect for priming was marginally significant, F(1, 17)= 5.4, P < 0.03; specific priming (mean = 4.8%) tended to induce more errors than nonspecific priming (mean = 1.5%).
3.2. LRP findings 1 Using the left ear as the common reference might induce underestimation of the true C3' potential and overestimation of the true C4' potential. Note, that the LRP does not reflect these possible distortions because the lateral differences (i.e. C4'-C3' and C3'-C4') enter the LRP with equal weights (see below). Assume for example, that the true potentials amount to -4/~V, but the distorted potential at C3' is -3 ~uV and the distorted potential at C4' is -5/~V, In this case, the LRP correctly averages (2 - 2)/2 = 0. Thus, we refrained from recalculating the recordings to linked ears as the common reference. In addition, the recording from the right ear (referenced to the left ear) averaged to null.
The next step was to verify that erroneous response priming took in fact place. Fig. 2 plots the LRPs from the go trials and from the specific priming condition of the nogo trials. For the go trials, the LRPs are plotted separately for the visual context conditions (congruent, neutral, incongruent). Incorrect response priming here should be reflected by a positive deflection and correct response
B. Kopp et al. /Electroencephalography and clinical Neurophysiology 99 (1996) 19-2 7
between 150 and 250 ms posttarget were computed (its boundaries were determined by visual inspection of the waveforms). The repeated-measures ANOVA (visual context) for the mean LRP amplitudes from go trials revealed a significant effect for visual context, F(2, 34) = 33.1, P < 0.0001. The congruent visual context (mean = - l .0 HV) yielded greater negativity than the neutral context (mean = - 0 . 1 3 ~ V ; F(I, 17) = 25.4, P < 0.0001); the incongruent visual context (mean = 0.65/~V; F(1, 17) = 26.2, P < 0.0001) yielded greater positivity than the neutral context. The LRPs from the nogo trials lacked the negative deflection that was prominent in all LRPs from the go trials and which accompanies unimanual responses (Kutas and Donchin, 1980). However, there was a positive deflection in the specific priming condition of the nogo trials. The positive deflection differed from zero in the incongruent visual context condition of the go trials (t = 8.1) as well as in the specific priming condition of the nogo trials (t = 8.8). Next, we compared the peak positivities in the incongruent visual context condition of the go trials with those in the specific priming condition of the nogo trials. The ANOVA (trial type) for the peaks and latencies of the LRP positivities yielded nonsignificant effects, F(1, 17) < 2.9. The results of the permutation significance tests replicate and extent the analyses above (cf. Fig. 3). Turning first to the comparison between go trials, we found facilitative and interfering effects of the flanker stimuli on the LRPs. The LRP from congruent trials were more negative than the LRP from neutral trials during the period 175-
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Fig. 2. LRPs, averaged separately for go and nogo trials. ERPs from go trials were broken down by visual context (congruent, solid line; neutral, dotted line; incongruent, dashed line). ERPs from nogo trials stem from the specific priming condition (bold line). F denotes the onset of flanker stimuli, T denotes the onset of target stimuli. These average waveforms were digitally filtered (low pass cutoff frequency 12 Hz).
priming should be reflected by a negative deflection of the LRP. In line with these expectations, the early LRP deflections (beginning at around 100 ms posttarget) were positive in the incongruent flanker condition; they were negative in the congruent flanker condition. These early deflections indicate that flanker-triggered responses were activated. As late as around 260 ms posttarget, the positive LRP deflection in the incongruent flanker condition was reversed towards a negative LRP deflection. Mean LRP amplitudes from go trials within the latency window 8-
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Fig. 3. Plots of t statistics that compare the LRP waveforms at each time point. (Top) Comparisons between go trials (left, congruent versus neutral; right, incongruent versus neutral). (Bottom) Comparisons between go and nogo trials (left, congruent versus specific nogo (multiplied by -1); right, incongruent versus specific nogo). Dashed lines indicate critical t values (P = 0.05).
B. Kopp et al. / Electroencephalography and clinical Neurophysiology 99 (1996) 19-27
24
250 ms posttarget. The LRP from incongruent trials were more positive than the LRP from neutral trials during the period 150-275 ms posttarget. Thus, the influence of the congruent or incongruent flanker stimuli (obviously priming responses) relative to the neutral flanker stimuli (were no response priming was possible) persisted around 100 ms, a duration that corresponds well with the particular SOA that was chosen. The comparison between the go and the nogo LRPs yielded two results. First, neither the congruent LRP from go trials versus the LRP from the specific nogo trials waveforms, nor the incongruent LRP from go trials versus the LRP from the specific nogo trials differed significantly during the periods that were sensitive for flanker-triggered response priming. Second, the go LRP and the nogo LRP differed during later periods (congruent versus nogo = 225-430 ms; incongruent versus nogo= 260--460 ms) reflecting that unilateral responses were emitted during go trials, but not during nogo trials.
pointed out in Section 1, we focused on the comparison between specific and nonspecific priming in the nogo trials. The first question was whether response priming exerted a significant effect on the N2 amplitudes. Because the N2 did not have a definite peak, we refrained from calculating peak and latency measures. Instead of these measures, we took the mean activity across the latency range between 250 and 350 ms because the mean N2 latency in the incongruent visual context condition of the go trials amounted to 294 ms. The mean N2 amplitudes were computed separately for specific (collapsed across left- and right-hand priming) and nonspecific priming. The ANOVA (priming, electrode site) for the mean nogo N2 amplitudes revealed significant main effects for electrode site, F(2,34)=40.0, P<0.0001, and priming, F(1, 17) = 25.2, P <0.0001. Specifically primed nogo trials (mean = 6.2 ktV) yielded larger mean N2 amplitudes than the nonspecifically primed nogo trials (mean = 9.0/~V). In addition, the interaction electrode site × priming proved significant, F(2, 34) = 7.6, P < 0.004. Priming yielded less pronounced effects on the mean N2 amplitudes at the Fz (mean = - 2 . 2 ~ V ) and Pz (mean = -2.7/tV) electrodes than at the Cz electrode (mean = -3.6/~V; F(1, 17) > 8.8, P < 0.009). Thus, response priming was associated with N2 activity in the nogo trials. This result is in line with the hypothesis that N2 indicates an inhibitory process. The second question was whether the P3 amplitude in the nogo trials was influenced by response priming. The
3.3. ERP findings A detailed analysis of the visual context effects on the ERPs in the flanker task had already been presented (Kopp et al., 1996). Most importantly, the N2 appeared specifically in the incongruent visual context condition of the go trials, thus replicating our former result (cf. Fig. 4, left, especially at the Cz electrode). To avoid the problems that arise in comparisons between go and nogo trials
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B. Kopp et al. / Electroencephalography and clinical Neurophysiology 99 (1996) 19-27
P3 amplitudes were computed separately for specific (collapsed across left- and right-hand priming) and nonspecific priming. Because the P3 had a definite peak, we measured the peak and latency of this component (cf. Fig. 4, right). The ANOVA (priming, electrode site) for P3 amplitudes from the nogo trials revealed a significant effect for electrode site, F(2, 34) = 52.0, P < 0.0001, whereas priming and the interaction electrode × priming yielded non-significant effects. The Fz and Pz electrodes yielded less positive peaks than the Cz electrode, F(1, 17)> 30.2, P < 0 . 0 0 0 1 . Contrary to the hypothesis that P3 indicates motor inhibition, response priming clearly did not affect the nogo P3 amplitudes. Visual inspection of the waveforms (cf. Fig. 4) suggested that the P3 latencies were prolonged in the specific priming versus nonspecific response priming condition. The repeated-measures ANOVA (priming, electrode site) for the nogo P3 latencies revealed a significant effect for electrode site, F(2, 34) = 7.9, P < 0.004, and for priming, F(1, 17) = 26.2, P < 0.0001, indicating a prolonged P3 latency in the specifically primed nogo trials compared to the nonspecifically primed nogo trials (cf. Table 1). The latency of the P3 at Pz was prolonged compared to that at Cz (F(1, 17) = 26.8, P < 0.0001). Next, we compared the P3 amplitudes from the nogo trials with the P3 amplitudes from the go trials. In order to enhance the comparability with former go/nogo studies, we decided to restrict this comparison to trials without response priming, i.e. the neutral go trials and the nonspecific nogo trials. The ANOVA (response type (go, nogo), electrode site) for the P3 peak amplitudes revealed significant main effects for electrode site, F(2, 34) = 41.4, P < 0 . 0 0 0 1 , and response type, F(I, 17)= 26.8, P<_ 0.0001. The go P3 was less positive than the nogo P3 (cf. Table 1). In addition, the interaction electrode site x response type proved significant, F(2, 34)=24.5, P < 0.0001. The go P3 was maximum at Pz and showed a clear posterior-anterior gradient whereas the nogo P3 reached its maximum amplitude at Cz (cf. Table 1). The differential topography of the go and nogo P3 was reflected in significant interactions response type x (Cz versus Fz) and response type x (Cz versus Pz), F(1, 17) > 40.3, P _<0.0001.
Table 1 P3 peak amplitudes ~ V ) and latencies (ms) and standard errors of the mean (in parentheses) for go and nogo trials at Fz, Cz, Pz. Amplitudes
Fz Cz Pz
Latencies
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Nogo spec
Nogo nonspec
Nogo spec
Nogo nonspec
7.6 (0.9) 10.5 (1.4) 11.3(1.3)
9.8 (0.9) 17.0 (1.5) 13.6(1.3)
9.3 (0.8) 16.6 (1.4) 13.4(1.2)
403 (5.6) 387 (8.4) 413(7.0)
373 (8.0) 368 (6.0) 383(5.4)
25
4. Discussion Selective response priming was demonstrated in the present hybrid go/nogo task as a function of the information conveyed in the visual context. In go trials, flanker compatibility exerted large facilitative and interfering effects on performance as assessed by RTs and error scores. LRPs showed that flanker-triggered responses were partially primed at the cortical level. The execution of target-triggered responses was associated with more negative waveforms over the contralateral hemisphere. These negativities reflect the lateralized part of the readiness potential accompanying unimanual responses (Kutas and Donchin, 1980). As assessed by the LRP, cortical response priming to flanker and target stimuli began about 150 ms after the appearance of the stimuli. Cortical response priming to flanker and target stimuli differed with respect to their duration (100 versus 200ms) and amplitude (i.6 versus 4 ~V). Although the P3 go/nogo effect was replicated, we are reluctant to interpret it as reflecting motor inhibition. Our reasoning focuses on the occurrence of motor potentials in go trials but not in nogo trials. LRP deflections were observed in go trials but not in nogo trials during the interval between 250 and 450 ms posttarget. These lateral negativities in go trials amounted to around -4/zV. They reached their peak amplitudes within the interval between 300 and 400 ms after the onset of the target stimuli. Because the P3 latencies fell within this latency range, the P3 amplitude in go trials was probably reduced by the (partially lateralized) motor potentials that accompanied the execution of target-triggered responses. The P3 go/ nogo effect reached its maximum at the vertex where it amounted to around 6/zV. Note, that the topography of the P3 go/nogo effect is thus in line with the motor potential overlay hypothesis. In the present investigation, a substantial part of the P3 go/nogo effect may be attributed to a probability effect because go trials (67%) were more probable than nogo trials (33%). In addition, the comparison between go and nogo trials confounds motor inhibition with at least one other variable: Nogo stimuli (but not go stimuli) may be associated with a lapse of excitation following the revelation that nothing more has to be done in the given trial. The priming conditions in the nogo trials revealed that the necessity to withhold selectively primed responses had no effect on the P3 amplitude. Because the P3 amplitude did not vary as a function of erroneous response priming, the P3 is not associated with the interruption of erroneous response tendencies. We conclude that the interpretation of the P3 go/nogo effect as indicating motor inhibition (Roberts et al., 1994) is undesired (Simson et al., 1977). With respect to the investigation of motor inhibition, comparing various response priming conditions seems to be the more valuable tool than comparing go and nogo trials. A distinct N2 appeared most prominently at the vertex
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B. Kopp et al. / Electroencephalography and clinical Neurophysiology 99 (1996) 19-27
in the incongruent visual context condition of the go trials and in the specific priming condition of the nogo trials. These two conditions had in common that responses were primed erroneously, as indicated by the LRPs. Thus, the erroneous tendency to respond was generally accompanied by a distinct N2. In ERPs, errors in choice RT tasks are associated with increased negativity in the latency range between 300 and 500 ms after the onset of the imperative stimulus (Falkenstein et al., 1991). This negativity was called 'error negativity' (NE). Because the errors were uncorrected, the initiation of a correction response cannot be regarded as the critical processing component underlying the ArE. NE had a fronto-central maximum and was larger in response-triggered than in stimulustriggered averages. Gehring et al. (1993) analyzed ERPs that were obtained from (partial) errors in the flanker task. The 'error-related negativity' (ERN) began around the time of the incorrect response and peaked about 100 ms later. The ERN amplitude was larger when response accuracy was stressed, whereas the ERN amplitude was smaller when the subjects were encouraged to respond quickly. Larger ERN amplitudes were associated (1) with reduced response strength of the incorrect responses, (2) with increased probability that an incorrect response was followed immediately by a correct response, (3) with slower RTs on correct trials following error trials. Because the morphology, the latency and the scalp distribution of the N2 was very similar to those described for the NE/ERN (Dehaene et al., 1994), we infer that both these deflections similarly reflect motor inhibition. Although the N2 and the NE/ERN seem to be equivalent with respect to their underlying processes, it could be argued that the NE/ERN reflects rather unspecifically the activation of attentional processes due to the low frequency of errors and/or the usual consequences of errors (feedback) in choice RT tasks. In contrast, frequency and/or consequence of errors are surely not critical for eliciting the N2 because we restricted our analyses to the correct trials. These analyses indicate that the study of motor inhibition does not presuppose the presence of uncorrected or corrected errors. Error corrections were possible the incongruent visual context condition of the go trials (cf. Section 2) but not in the specific priming condition of the nogo trials (exceeding the criterion force level led irresistibly to an error in nogo trials). Because the N2 appeared irrespective of whether an error was correctable (as in go trials) or not (as in nogo trials), we conclude that the N2 reflects either the detection or the inhibition of an inappropriate tendency to respond. Importantly, we thus exclude that the N2 is associated with the initiation of the correction of an error. 2 We suggest that the response priming effect on the N2 amplitude reflects the recruitment of neuronal activity that serves to suppress the execution an otherwise inap2 This conclusion was pointed out by Michael Coles.
propriate response. Note that this leaves open whether the neuronal activity underlying the N2 is itself inhibitory (deactivation of the agonist) or excitatory (activation of the antagonist). What do we know about the neuronal activity that serves to suppress the execution of an inappropriate response? Our subjects committed much more (correctable) errors in the incongruent visual context condition of the go trials (15.1%) than (uncorrectable) errors in the specific priming condition of the nogo trials (4.8%). In contrast, the flanker-triggered cortical response priming had comparable peaks in both conditions (1.58 versus 1.60/zV). In addition, flanker-triggered response priming at the cortex lasted equally long in the congruent and incongruent visual context condition. If the neuronal activity underlying the N2 specifically interrupts the cortical preparation for errors, cortical error preparation should have a shorter time course than cortical preparation of appropriate responses. These results together imply that some of the activity that underlies the N2 exerts its influence on more peripheral stages, most probably the corticospinal efferents (De Jong et al., 1990, 1995; Gratton et al., 1992).
Acknowledgements This research was supported by a grant from the Deutsche Forschungsgemeinschaft (Ri 342/4). Portions of this work were presented at the 33rd Meeting of the Society for Psychophysiological Research, Rottach-Egern, October 1993. We greatly appreciate the support we obtained from Patrick Berg, University of Konstanz, who let us have his EEG data analysis programs. We thank Hartmut Leuthold, Humboldt University at Berlin, for his valuable comments on an earlier draft of this article, and Michael Coles, University of Illinois at Urbana-Champaign, as well as Michael Falkenstein, Institut fiJr Arbeitsphysiologie, Dortmund, for their helpful discussion and correspondence.
References Berg, P. The residual after correcting event-related potentials for blink artifacts. Psychophysiology, 1986, 23: 354-364. Beringer, J. Software Announcements: ERTS: a flexible software tool for developing and running psychological reaction time experiments on IBM PCs. Behav. Res. Methods, Instrum., Comp., 1994, 55: 1. Blair, R.C. and Karniski, W. An alternative method for significance testing of waveform difference potentials. Psychophysiology, 1993, 30: 518-524. Coles, M.G.H. Modem mind-brain reading: psychophysiology, physiology, and cognition. Psychophysiology, 1989, 26:251-269. Coles, M.G.H., Gratton, G., Bashore, T.R., Eriksen, C.W. and Donchin, E. A psychophysiological investigation of the continuous flow model of human information processing. J. Exp. Psychol.: Hum. Percept. Perform., 1985, 11: 529-553. Dehaene, S., Posner, M.I. and Tucker, D.M. Localization of a neural system for error detection and compensation. Psychol. Sci., 1994, 5: 303-305. DeJong, R., Coles, M.G.H., Logan, G.D. and Gratton, G. In search of
B. Kopp et al. /Electroencephalography and clinical Neurophysiology 99 (1996) 19-27 the point of no return: the control of response processes. J. Exp. Psychol.: Hum. Percept. Perform., 1990, 14: 164--182. DeJong, R., Coles, M.G.H. and Logan, G.D. Strategies and mechanisms in nonselective and selective inhibitory motor control. J. Exp. Psychol.: Hum. Percept. Perform., 1995, 21,498-511. Eimer, M. Effects of attention and stimulus probability on ERPs in a go/nogo task. Biol. Psychol., 1993, 35: 123-138. Eriksen, B.A. and Eriksen, C.W. Effects of noise letters upon the identification of a target letter in a nonsearch task. Percept. Psychophys., 1974, 16: 143-149. Eriksen, C.W. and Schultz, D.W. Information processing in visual search: a continuous flow conception and experimental results. Percept. Psychophys., 1979, 25: 249-263. Falkenstein, M., Hohnsbein, J., Hoormann, J. and Blanke, L. Effects of crossmodal divided attention on late ERP components. I1. Error processing in choice reaction tasks. Electroenceph. clin. Neurophysiol., 1991,78: 447-455. Flowers, J.H. Priming effects in perceptual classification. Percept. Psychophys., 1990, 47: 135-148. Flowers. J.H and Wilcox, N. The effect of flanking context on visual classification: the joint contribution of interactions at different processing levels. Percept. Psychophys., 1982, 32: 581-591. Gehring, W.J., Goss, B., Coles, M.G.H., Meyer, D.E. and Donchin, E. A neural system for error detection and compensation. Psychol. Sci., 1993, 4: 385-390. Giray, M. and Ulrich, R. Motor coactivation revealed by response force in divided and focused attention. J, Exp. Psychol.: Hum. Percept. Perform., 1993, 19: 1278-1291. Gratton, G., Coles, M.G.H., Sirevaag, E.J., Eriksen, C.W. and Donchin, E. Pre- and poststimulus activation of response channels: a psychophysiological analysis. J. Exp. Psychol.: Hum. Percept. Perform., 1988, 14: 331-344. Gratton, G . Coles, M.G.H. and Donchin, E. Optimizing the use of information: strategic control of activation of responses. J. Exp. Psychol.: General, 1992, 12: 480-506. Grice, GR., Boroughs, J.M. and Canham, L. Temporal dynamics of associative interference and facilitation produced by visual context. Percept. Psychophys., 1984, 36: 499-507. Grice. G.R. and Gwynne, J.W. Temporal characteristics of noise conditions producing facilitation and interference. Percept. Psychophys., 1985, 37: 495-501.
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Jodo, E. and Kayama, Y. Relation of a negative ERP component to response inhibition in a go/no-go task. Electroenceph. clin. Neurophysiol., 1992, 82: 477-482. Kok, A. Effects of degradation of visual stimulus components of the event-related potential (ERP) in go/nogo reaction tasks. Biol. Psychol., 1986, 23: 21-38. Kok, A. Overlap between P300 and movement-related potentials: a response to Verleger. Biol. Psychol., 1988, 27: 51-58. Kopp, B., Rist, F. and Mattler, U. N200 in the flanker task as a neurobehavioral tool for investigating executive control. Psychophysiology, 1996, 33: 282-294. Kornblum, S., Hasbroucq, T. and Osman, A. Dimensional overlap: cognitive basis for stimulus-response compatibility - a model and taxonomy. Psychol. Rev., 1990, 97: 253-270. Kutas, M. and Donchin, E. Preparation to respond as manifested by movement-related brain potentials. Brain Res., 1980, 202:95-115. Logan, G.D. and Cowan, W.B. On the ability to inhibit thought and action: a theory of an act of control. Psychol. Rev., 1984, 91: 295327. Miller, J. and Hackley, S.A. Electrophysiological evidence for temporal overlap among contingent mental processes. J. Exp. Psychol.: General, 1992, 121: 195-209. Pfefferbaum, A. and Ford, J.M. ERPs to stimuli requiting response production and inhibition: effects of age, probability and visual noise. Electroenceph. clin. Neurophysiol., 1988, 71: 55-63. Pfefferbaum, A., Ford, J.M., Weller, B.J. and Kopell, B.S. ERPs to response production and inhibition. Electroenceph. clin. Neurophysiol., 1985, 60: 423-434. Roberts, L.E., Rau, H., Lutzenberger, W., and Birbaumer, N. Mapping P300 waves onto inhibition: Go/No-Go discrimination. Electroenceph. clin. Neurophysiol., 1994, 92: 44-55. Schr6ger, E. Event-related potentials to auditory stimuli following transients shifts of spatial attention in a go/nogo task. Biol. Psychol., 1993, 36: 183-207. Simson, R.. Vaughan, H.G. and Ritter, W. The scalp topography of potentials in auditory and visual go/nogo tasks. Electroenceph. clin. Neurophysiol., 1977, 43: 864-875. Taylor, D.A. Time course of context effects. J. Exp. Psychol.: General, 1977, 106: 404-426.
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ELSEVIER
Electroencephalography and clinical Neurophysiology99 (1996) 19-27
N2, P3 and the lateralized readiness potential in a nogo task involving selective response priming B r u n o K o p p a,*, U w e M a t t l e r b, R a l f G o e r t z a, F r e d R i s t b aHumboldt University at Berlin, Department ~f Psychology, Clinical Psychology and Behavioral Neuroscience, Hausvogteiplatz 5-7, D-lOll 7 Berlin, Germany bCentral Institute of Mental Health, Mannheim, Germany
Accepted for publication: 20 March 1996
Abstract
Motor inhibition and its correlates in the event-related potential (ERP) are often studied in go/nogo tasks. However, go and nogo trials differ in their motor and their attentional requirements, rendering an interpretation of corresponding changes in ERP components difficult. As an alternative strategy to study motor inhibition, a hybrid choice-reaction go/nogo procedure involving selective response priming was used. Eighteen subjects performed the task. Response time (RT) and error measures as well as the lateralized readiness potential (LRP) indicated that responses were primed by flanker stimuli that were associated with one of the two possible responses. In nogo trials, selective response priming influenced the N2 amplitude whereas the P3 amplitude was unaffected. Because the N2 appeared irrespective of whether an erroneous response was correctable (in go trials) or not (in nogo trials), we conclude that the N2 reflects either the detection or the inhibition of an inappropriate tendency to respond. Keywords: N2; P3; LRP; Nogo task; Motor inhibition; Response priming; Error processing
1. I n t r o d u c t i o n
The ability to inhibit thought and action is crucial for the maintenance of coherent sequences of cognitive and motor events (Logan and Cowan, 1984). Traditionally, motor inhibition has been studied by comparing go and nogo trials. Several ERP components have been found to differ between go and nogo trials. These go/nogo effects on ERP amplitudes were interpreted as signs of inhibitory activity in the nogo trial which is related to the interruption of response execution, Roberts et al. (1994) reported that the amplitude of the P3 in nogo trials was enhanced compared to those in go trials and related the P3 go/nogo effect to motor inhibition. In further support of the motor inhibition interpretation of the P3 go/nogo effect, Roberts et al. (1994) point out that the scalp distribution of the nogo P3 is more anterior compared to the distribution of the go P3 (Pfefferbaum and Ford, 1988). The go/nogo effect on the amplitude of the P3 had similarly been re-
* Corresponding author. Tel.: +30 203 77379; fax: +30 203 77308; e-mail: [email protected]
ported by Eimer (1993), Kok (1986), Schr6ger (1993), Simson et al. (1977). Simson et al. (1977) attributed the P3 go/nogo amplitude effect to the sustained negativity that accompanies the motor performance which is required in go trials and which is withheld in nogo trials. However, Pfefferbaum et al. (1985) showed that the more anterior scalp distribution of the nogo P3 compared to the go P3 appeared when covert (cognitive) responses had to be interrupted in nogo trials. This result rules out the possibility that the overlay of (negative) motor potentials in the go trials was solely responsible for the P3 go/nogo effect. Apart from the P3 go/nogo effect, the amplitude of the N2 was found to be enhanced in nogo trials compared to go trials (e.g. Eimer, 1993; Jodo and Kayama, 1992; Kok, 1986; Pfefferbaum et al., 1985). Pfefferbaum et al. (1985) observed the N2 go/nogo effect with both overt motor responses and covert cognitive responses. Although the N2 go/nogo effect was larger with overt than with covert responses, the N2 go/nogo effect was still present with covert responses. Thus, the N2 go/nogo effect cannot be completely attributed to the overlay of motor potentials. In sum, the N2 enhancement in nogo trials is not confined
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B. Kopp et al. / Electroencephalography and clinical Neurophysiology 99 (1996) 19-27
to withholding motor responses, but appears whenever either overt or covert responses have to be interrupted. The purpose of the present study was to clarify whether the N2 or the P3 or both ERP components indicate motor inhibition. Motor inhibition signifies the suppression of a tendency to respond that may be achieved either by inhibitory neuronal activity (cessation of the movement agonist) or by excitatory neuronal activity (activation of the movement antagonist). Apparently, comparing go and nogo trials is a straightforward method to identify ERP components that are associated with motor inhibition. In practice, however, go and nogo trials differ in at least two further features. Firstly, with motor responses, the go ERPs will reflect brain activity that is related to the execution of the responses whereas the nogo ERPs will not (Kok, 1988). Secondly, go and nogo trials differ with respect to the necessity to prepare for a movement and thus may be associated with different attentional requirements. Paying attention might be dispensable once it is recognized that nothing has to be done in a given trial. Thus, nogo trials may be accompanied by a lapse of cortical excitation. In sum, go/nogo effects on the amplitude of ERP components are not unambiguously attributable to motor inhibition because these confounds are not easily disentangled. In order to avoid the inferential difficulties that arise from these ambiguities, we compared ERPs in specifically versus nonspecifically primed nogo trials in a hybrid choice-reaction go/nogo task. The go task was a variant of the original flanker task (Eriksen and Eriksen, 1974). In this task, a centrally presented target letter was flanked by additional stimuli. The target letter was flanked either by congruent (letters that indicated the same response as the target), by neutral (letters with no response assignment) or by incongruent (letters that indicated the opposite response as the target) flanker stimuli. RTs in congruent trials were faster and RTs in incongruent trials were slower than those in neutral trials. In order to explain the effects on RT that are exerted by the flanker stimuli, it is commonly assumed that the activation of responses begins as soon as visual information accumulates. Early in the process, all responses receive initial activation. Because more flanker stimuli than target stimuli were presented, flanker-triggered responses receive a relatively stronger initial activation than target-triggered stimuli. With the target becoming gradually localized, information from this part of the stimulus pattern gains importance. The threshold for the execution of the response is achieved faster if the response had already an initial level of activation. The achievement of the response threshold is prolonged due to interference if the opposite response received initial activation as in the incongruent trials (Eriksen and Schultz, 1979; Coles et al., 1985). Selective response priming can be measured with the asymmetry between the ipsilateral and the contralateral readiness potential. The lateralized readiness potential is a valid
real-time index of hand-specific motor preparation (Kutas and Donchin, 1980; Coles, 1989; Miller and Hackley, 1992). In the flanker task, the LRP was sensitive to even brief preparation for a unimanual response that was primed by the flanker stimuli (Gratton et al., 1988; Kopp et al., 1996). The original flanker task was modified in several respects for the study to be reported. Instead of letters with random response assignment, arrowheads were used both as target stimuli and as flanker stimuli. The relation between an arrow to the left and a left-hand response is considered a population stereotype which does not require learning. The arrowheads should prime their associated responses automatically because of the high compatibility between stimuli and responses (Kornblum et al., 1990). Several studies showed that facilitation and interference were more pronounced when flanker onset preceded target onset (Taylor, 1977; Eriksen and Schultz, 1979; Flowers and Wilcox, 1982; Grice et al., 1984; Grice and Gwynne, 1985; Flowers, 1990). As a consequence, we introduced a constant stimulus onset asynchrony (SOA) of 100 ms. Nogo trials were interspersed with an overall probability of 33%. Nogo stimuli were preceded either by arrowheads (specific priming) or by squares (nonspecific priming) as flanker stimuli. In specifically primed nogo trials, the flanker stimuli were associated with one of the two possible go-responses. Nonspecific flanker stimuli delivered the same temporal information but they were not related to one of the two possible go-responses. The critical difference between specific and nonspecific priming was that response priming could take place in the former but not in the latter case. In our hybrid go/nogo task, go trials (33% left-hand responses and 33% right-hand responses) were twice as probable as nogo trials (33%). It is known that the probability of events influences ERP amplitudes, especially the P3 amplitudes. Therefore, and for the reasons mentioned above, we concentrated our analyses on the comparison between (a) the specifically primed nogo trials and (b) the nonspecifically primed nogo trials. We expected response priming to occur in the specific but not in the nonspecific priming condition of the nogo trials. We further assumed that the interruption of the erroneously primed responses involves motor inhibition. Thus, we examined the effects that selective response priming exerts on the ERP in a nogo task. More specifically, we wanted to know whether the N2 or the P3 or both ERP components are associated with the necessity to withhold a primed response. 2. Method 2.1. Subjects
Eighteen paid volunteers served as subjects (mean age
B. Kopp et al. / Electroencephalography and clinical Neurophysiology 99 (1996) 19-27
21
33 years; 13 men and 5 women). All subjects were righthanded and all had normal or corrected-to-normal vision.
2.2. Stimuli and procedure The target stimulus was an arrowhead pointing either left or right (go stimulus) or an octagon (nogo stimulus) presented at the center of a PC-CRT screen (Beringer, 1994). The arrowheads were constructed as equilateral triangles with an edge length of 21 mm, the squares had an edge length of 15 mm. Triangles, squares and octagons contained identical numbers of pixels. The edge-to-edge distance of flanker and target stimuli was always 1° of visual angle. All stimuli were presented in gray color against a black background. Two thirds of all trials were go trials; in go trials, the three visual context conditions (congruent, neutral, incongruent) appeared with equal probabilities. Subjects had to respond with the index finger that corresponded to the central arrowhead. In congruent go trials, two arrows pointing to the same direction as the target stimulus were presented above and below the target. In incongruent go trials, the two flanker stimuli pointed to the opposite direction. Squares were used as neutral flanker stimuli (cf. Fig. 1). One third of all trials were nogo trials, i.e. responses had to be withheld when an octagon appeared as target stimulus. In nogo trials with specific priming, the flanker stimuli were arrows that primed their associated response. Thus, there were nogo trials in which either a left-hand or a right-hand response was primed. In nogo trials with nonspecific priming, the flanker stimuli were squares without any response assignment. Go trials (67%, summed over left-hand and right-hand responses) occurred twice as often as nogo trials (33%). Within go trials, congruent (33%), neutral (33%) and incongruent (33%) flanker stimuli occurred with equal probabilities. Within nogo trials, specific priming (67%, summed over left-hand and right-hand flanker stimuli) occurred twice as often as nonspecific priming (33%, neutral flanker stimuli). Note that the flanker stimuli did not predict the forthcoming target stimulus. Each flanker stimulus (left-hand stimulus, neutral, right-hand stimulus) was associated with left-hand responses (33%), right-hand responses (33%) or nogo responses (33%). Thus, all three possibilities were equally probable alternatives, given the presence of a particular flanker stimulus. At the beginning of each trial, a central fixation cross appeared for 500 ms. As short SOAs between flanker and target stimuli enhance visual context effects (Taylor, 1977), the onset of the flanker stimuli preceded the onset of the target stimulus by 100 ms. The target stimulus was presented in addition to the flanker stimuli and stayed for 50 ms at the center of the CRT screen. All three stimuli were removed simultaneously. A variable intertrial interval of about 2 s followed. After a practice block of 63 trials, 10 blocks of 63 trials each followed. Thus, at least
J congruent
0
neutral
I
i i ,
specific right
!
incongruent
• •
• •
nonspecific
specific left
Fig. 1. The design of the experiment. (Top) Go trials. The three visual context conditions (congruent, neutral, incongruent) for fight-hand responses. These visual context conditions occurred with equal frequencies; the overall probability for a go trial was 67%. (Bottom) Nogo trials. The three priming conditions (specific right, nonspecific, specific left). These priming conditions occurred with equal frequencies; the overall probability for a nogo trial was 33%.
630 trials (error trials were repeated) were administered during 45-60 min. Within each block, trial types were presented in random sequence. Subjects were instructed to focus on the central target stimulus and to ignore the flanker stimuli. They were instructed to respond as fast as possible at the expense of accuracy, Subjects were seated 1.20 m in front of the CRT screen. They kept their index fingers resting on analogue response keys that resembled telegraph keys (Giray and Ulrich, 1993). A leaf spring was held by an adjustable clamp at one end, whereas the other end remained free. Strain gauges were attached near the fixed end of the leaf spring. Any force applied to the leaf spring led to a displacement at its free end. The displacement was converted into an analogous electrical signal. The electrical signals from both force keys were fed into a second PC, digitized at 100 Hz and stored on disk. The resolution of this device was about 2 mN. Subjects were asked to rest their fingers on both response keys and to make a response by depressing the appropriate key or to withhold the response. A response was defined as a key displacement equivalent to at least 2 N of force. The responses were evaluated online. RTs were defined as the interval between the target stimulus onset and the time when a level of 2 N force was surpassed with the appropriate key. Subjects were told that they could correct wrong responses in go trials by pressing the correct key immediately after the wrong key (i.e. within 1300 ms after the onset of the flanker stimuli). Uncorrected wrong responses elicited an auditory feedback tone (500 Hz) that began 1300 ms after the onset of the flanker stimuli. Uncorrected errors were rerun within the same block of trials. In go trials, uncorrected errors occurred very rarely (the probability of uncorrected errors did not surpass 0.5% in any of the three visual context conditions) and were not analyzed further. Corrected wrong
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B. Kopp et al. /Electroencephalography and clinical Neurophysiology 99 (1996) 19-2 7
responses were considered errors. Early or late responses and those responses that did not achieve the criterion force level of 2 N were fed back using a 1000 Hz tone. In nogo trials, a response that exceeded the criterion force level of 2 N was an (uncorrectable) error that was fed back using a 500 Hz tone.
2.3. Recording and data analyses The electroencephalogram (EEG) was recorded using Ag-AgC1 electrodes at Fz, Cz, Pz, C3', and C4' referenced to the left ear lobe. 1 The vertical and horizontal electrooculogram (EOG) was recorded from sites above and below the left eye and 1 cm external to the outer canthus of each eye. Trials containing horizontal eye movements were rejected; trials containing blinks were corrected using the regression method described by Berg (1986). A ground electrode was placed on the forehead. The signals were amplified with a Nihon Kohden amplifier (time constant 10 s; high-frequency cutoff 35 Hz). Electrode impedance was kept below 5 kQ. The signals were digitized on-line at a rate of 100 Hz for 1400 ms, starting 100 ms before the presentation of the flanker stimuli. No digital filtering was applied to the signals. Stimulus-synchronized average ERPs were computed from correctly responded trials subtracting the lOOms prestimulus period as the baseline. Separate averages were computed for go trials (visual context (congruent, neutral, incongruent)) and nogo trials (response priming (specific, nonspecific)) for the midline electrode sites (Fz, Cz, Pz). The LRP in go trials was evaluated separately for the three visual context conditions. The LRP in go trials was assessed by using the ERP waveforms recorded at C3' and C4'. The recordings at C3' and C4' were subtracted from one another (left-hand responses C4'-C3', right-hand responses C3'-C4') and averaged separately for left-hand and right-hand responses. These averages were then combined across hands ((left-hand (C4'-C3') + right-hand (C3'-C4'))/2). The LRP in the specific priming condition of the nogo trials was computed in the same way, but averaged separately for specific left- and rightresponse priming conditions. These averages were then combined across both specific priming conditions, ((C4'C3') + (C3'-C4'))/2. It was not possible to compute LRPs in the nonspecific priming condition of the nogo trials
because there was no way to decide whether C4'--C3' or C3'-C4' was to be computed in a particular trial. The LRPs (peak and mean amplitudes) from the various conditions were compared by the permutation test described by Blair and Karniski (1993). By computing t values at each single time point, this waveform analysis indicates the periods during which two waveforms differ significantly. Within the go condition, we compared (a) the neutral and the congruent LRPs to test for the facilitative effect of congruent flanker stimuli and (b) the neutral and the incongruent LRP to test for the interfering effect of incongruent flanker stimuli. In addition, we compared the go and the nogo LRPs, i.e. (a) the congruent LRP from go trials with the LRP from the specific nogo trials (multiplied with -1) and (b) the incongruent LRP from go trials with the LRP from the specific nogo trials. Greenhouse-Geisser adjusted P values are reported, but original degrees of freedom are given. 3. Results
3.1. Behavioral findings Mean RTs from the correct go trials were subjected to a repeated-measures ANOVA (visual context) that revealed a significant effect for visual context, F(2, 34) = 173.0, P < 0.0001. The congruent visual context (mean = 321 ms) yielded faster RTs than the neutral context (mean= 361 ms; F(I, 17)= 115.4, P<0.0001); the incongruent visual context (mean = 388 ms) yielded slower RTs than the neutral context, F(I, 17) = 81.4, P < 0.0001. Arcsin-transformed error scores from the go trials were subjected to the same repeated-measures ANOVA (visual context) that revealed a significant effect for visual context, F(2, 34) = 20.8, P < 0.0002. The incongruent visual context (mean= 15.1%) yielded more errors than the neutral context (mean = 2.7%; F(1, 17) = 20.6, P < 0.0003) with no discernible difference between the congruent visual context (mean = 2.1%) and the neutral context. Arcsin-transformed error scores from the nogo trials were subjected to a repeated-measures ANOVA (priming: specific, nonspecific). The effect for priming was marginally significant, F(1, 17)= 5.4, P < 0.03; specific priming (mean = 4.8%) tended to induce more errors than nonspecific priming (mean = 1.5%).
3.2. LRP findings 1 Using the left ear as the common reference might induce underestimation of the true C3' potential and overestimation of the true C4' potential. Note, that the LRP does not reflect these possible distortions because the lateral differences (i.e. C4'-C3' and C3'-C4') enter the LRP with equal weights (see below). Assume for example, that the true potentials amount to -4/~V, but the distorted potential at C3' is -3 ~uV and the distorted potential at C4' is -5/~V, In this case, the LRP correctly averages (2 - 2)/2 = 0. Thus, we refrained from recalculating the recordings to linked ears as the common reference. In addition, the recording from the right ear (referenced to the left ear) averaged to null.
The next step was to verify that erroneous response priming took in fact place. Fig. 2 plots the LRPs from the go trials and from the specific priming condition of the nogo trials. For the go trials, the LRPs are plotted separately for the visual context conditions (congruent, neutral, incongruent). Incorrect response priming here should be reflected by a positive deflection and correct response
B. Kopp et al. /Electroencephalography and clinical Neurophysiology 99 (1996) 19-2 7
between 150 and 250 ms posttarget were computed (its boundaries were determined by visual inspection of the waveforms). The repeated-measures ANOVA (visual context) for the mean LRP amplitudes from go trials revealed a significant effect for visual context, F(2, 34) = 33.1, P < 0.0001. The congruent visual context (mean = - l .0 HV) yielded greater negativity than the neutral context (mean = - 0 . 1 3 ~ V ; F(I, 17) = 25.4, P < 0.0001); the incongruent visual context (mean = 0.65/~V; F(1, 17) = 26.2, P < 0.0001) yielded greater positivity than the neutral context. The LRPs from the nogo trials lacked the negative deflection that was prominent in all LRPs from the go trials and which accompanies unimanual responses (Kutas and Donchin, 1980). However, there was a positive deflection in the specific priming condition of the nogo trials. The positive deflection differed from zero in the incongruent visual context condition of the go trials (t = 8.1) as well as in the specific priming condition of the nogo trials (t = 8.8). Next, we compared the peak positivities in the incongruent visual context condition of the go trials with those in the specific priming condition of the nogo trials. The ANOVA (trial type) for the peaks and latencies of the LRP positivities yielded nonsignificant effects, F(1, 17) < 2.9. The results of the permutation significance tests replicate and extent the analyses above (cf. Fig. 3). Turning first to the comparison between go trials, we found facilitative and interfering effects of the flanker stimuli on the LRPs. The LRP from congruent trials were more negative than the LRP from neutral trials during the period 175-
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priming should be reflected by a negative deflection of the LRP. In line with these expectations, the early LRP deflections (beginning at around 100 ms posttarget) were positive in the incongruent flanker condition; they were negative in the congruent flanker condition. These early deflections indicate that flanker-triggered responses were activated. As late as around 260 ms posttarget, the positive LRP deflection in the incongruent flanker condition was reversed towards a negative LRP deflection. Mean LRP amplitudes from go trials within the latency window 8-
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Fig. 3. Plots of t statistics that compare the LRP waveforms at each time point. (Top) Comparisons between go trials (left, congruent versus neutral; right, incongruent versus neutral). (Bottom) Comparisons between go and nogo trials (left, congruent versus specific nogo (multiplied by -1); right, incongruent versus specific nogo). Dashed lines indicate critical t values (P = 0.05).
B. Kopp et al. / Electroencephalography and clinical Neurophysiology 99 (1996) 19-27
24
250 ms posttarget. The LRP from incongruent trials were more positive than the LRP from neutral trials during the period 150-275 ms posttarget. Thus, the influence of the congruent or incongruent flanker stimuli (obviously priming responses) relative to the neutral flanker stimuli (were no response priming was possible) persisted around 100 ms, a duration that corresponds well with the particular SOA that was chosen. The comparison between the go and the nogo LRPs yielded two results. First, neither the congruent LRP from go trials versus the LRP from the specific nogo trials waveforms, nor the incongruent LRP from go trials versus the LRP from the specific nogo trials differed significantly during the periods that were sensitive for flanker-triggered response priming. Second, the go LRP and the nogo LRP differed during later periods (congruent versus nogo = 225-430 ms; incongruent versus nogo= 260--460 ms) reflecting that unilateral responses were emitted during go trials, but not during nogo trials.
pointed out in Section 1, we focused on the comparison between specific and nonspecific priming in the nogo trials. The first question was whether response priming exerted a significant effect on the N2 amplitudes. Because the N2 did not have a definite peak, we refrained from calculating peak and latency measures. Instead of these measures, we took the mean activity across the latency range between 250 and 350 ms because the mean N2 latency in the incongruent visual context condition of the go trials amounted to 294 ms. The mean N2 amplitudes were computed separately for specific (collapsed across left- and right-hand priming) and nonspecific priming. The ANOVA (priming, electrode site) for the mean nogo N2 amplitudes revealed significant main effects for electrode site, F(2,34)=40.0, P<0.0001, and priming, F(1, 17) = 25.2, P <0.0001. Specifically primed nogo trials (mean = 6.2 ktV) yielded larger mean N2 amplitudes than the nonspecifically primed nogo trials (mean = 9.0/~V). In addition, the interaction electrode site × priming proved significant, F(2, 34) = 7.6, P < 0.004. Priming yielded less pronounced effects on the mean N2 amplitudes at the Fz (mean = - 2 . 2 ~ V ) and Pz (mean = -2.7/tV) electrodes than at the Cz electrode (mean = -3.6/~V; F(1, 17) > 8.8, P < 0.009). Thus, response priming was associated with N2 activity in the nogo trials. This result is in line with the hypothesis that N2 indicates an inhibitory process. The second question was whether the P3 amplitude in the nogo trials was influenced by response priming. The
3.3. ERP findings A detailed analysis of the visual context effects on the ERPs in the flanker task had already been presented (Kopp et al., 1996). Most importantly, the N2 appeared specifically in the incongruent visual context condition of the go trials, thus replicating our former result (cf. Fig. 4, left, especially at the Cz electrode). To avoid the problems that arise in comparisons between go and nogo trials
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B. Kopp et al. / Electroencephalography and clinical Neurophysiology 99 (1996) 19-27
P3 amplitudes were computed separately for specific (collapsed across left- and right-hand priming) and nonspecific priming. Because the P3 had a definite peak, we measured the peak and latency of this component (cf. Fig. 4, right). The ANOVA (priming, electrode site) for P3 amplitudes from the nogo trials revealed a significant effect for electrode site, F(2, 34) = 52.0, P < 0.0001, whereas priming and the interaction electrode × priming yielded non-significant effects. The Fz and Pz electrodes yielded less positive peaks than the Cz electrode, F(1, 17)> 30.2, P < 0 . 0 0 0 1 . Contrary to the hypothesis that P3 indicates motor inhibition, response priming clearly did not affect the nogo P3 amplitudes. Visual inspection of the waveforms (cf. Fig. 4) suggested that the P3 latencies were prolonged in the specific priming versus nonspecific response priming condition. The repeated-measures ANOVA (priming, electrode site) for the nogo P3 latencies revealed a significant effect for electrode site, F(2, 34) = 7.9, P < 0.004, and for priming, F(1, 17) = 26.2, P < 0.0001, indicating a prolonged P3 latency in the specifically primed nogo trials compared to the nonspecifically primed nogo trials (cf. Table 1). The latency of the P3 at Pz was prolonged compared to that at Cz (F(1, 17) = 26.8, P < 0.0001). Next, we compared the P3 amplitudes from the nogo trials with the P3 amplitudes from the go trials. In order to enhance the comparability with former go/nogo studies, we decided to restrict this comparison to trials without response priming, i.e. the neutral go trials and the nonspecific nogo trials. The ANOVA (response type (go, nogo), electrode site) for the P3 peak amplitudes revealed significant main effects for electrode site, F(2, 34) = 41.4, P < 0 . 0 0 0 1 , and response type, F(I, 17)= 26.8, P<_ 0.0001. The go P3 was less positive than the nogo P3 (cf. Table 1). In addition, the interaction electrode site x response type proved significant, F(2, 34)=24.5, P < 0.0001. The go P3 was maximum at Pz and showed a clear posterior-anterior gradient whereas the nogo P3 reached its maximum amplitude at Cz (cf. Table 1). The differential topography of the go and nogo P3 was reflected in significant interactions response type x (Cz versus Fz) and response type x (Cz versus Pz), F(1, 17) > 40.3, P _<0.0001.
Table 1 P3 peak amplitudes ~ V ) and latencies (ms) and standard errors of the mean (in parentheses) for go and nogo trials at Fz, Cz, Pz. Amplitudes
Fz Cz Pz
Latencies
Go
Nogo spec
Nogo nonspec
Nogo spec
Nogo nonspec
7.6 (0.9) 10.5 (1.4) 11.3(1.3)
9.8 (0.9) 17.0 (1.5) 13.6(1.3)
9.3 (0.8) 16.6 (1.4) 13.4(1.2)
403 (5.6) 387 (8.4) 413(7.0)
373 (8.0) 368 (6.0) 383(5.4)
25
4. Discussion Selective response priming was demonstrated in the present hybrid go/nogo task as a function of the information conveyed in the visual context. In go trials, flanker compatibility exerted large facilitative and interfering effects on performance as assessed by RTs and error scores. LRPs showed that flanker-triggered responses were partially primed at the cortical level. The execution of target-triggered responses was associated with more negative waveforms over the contralateral hemisphere. These negativities reflect the lateralized part of the readiness potential accompanying unimanual responses (Kutas and Donchin, 1980). As assessed by the LRP, cortical response priming to flanker and target stimuli began about 150 ms after the appearance of the stimuli. Cortical response priming to flanker and target stimuli differed with respect to their duration (100 versus 200ms) and amplitude (i.6 versus 4 ~V). Although the P3 go/nogo effect was replicated, we are reluctant to interpret it as reflecting motor inhibition. Our reasoning focuses on the occurrence of motor potentials in go trials but not in nogo trials. LRP deflections were observed in go trials but not in nogo trials during the interval between 250 and 450 ms posttarget. These lateral negativities in go trials amounted to around -4/zV. They reached their peak amplitudes within the interval between 300 and 400 ms after the onset of the target stimuli. Because the P3 latencies fell within this latency range, the P3 amplitude in go trials was probably reduced by the (partially lateralized) motor potentials that accompanied the execution of target-triggered responses. The P3 go/ nogo effect reached its maximum at the vertex where it amounted to around 6/zV. Note, that the topography of the P3 go/nogo effect is thus in line with the motor potential overlay hypothesis. In the present investigation, a substantial part of the P3 go/nogo effect may be attributed to a probability effect because go trials (67%) were more probable than nogo trials (33%). In addition, the comparison between go and nogo trials confounds motor inhibition with at least one other variable: Nogo stimuli (but not go stimuli) may be associated with a lapse of excitation following the revelation that nothing more has to be done in the given trial. The priming conditions in the nogo trials revealed that the necessity to withhold selectively primed responses had no effect on the P3 amplitude. Because the P3 amplitude did not vary as a function of erroneous response priming, the P3 is not associated with the interruption of erroneous response tendencies. We conclude that the interpretation of the P3 go/nogo effect as indicating motor inhibition (Roberts et al., 1994) is undesired (Simson et al., 1977). With respect to the investigation of motor inhibition, comparing various response priming conditions seems to be the more valuable tool than comparing go and nogo trials. A distinct N2 appeared most prominently at the vertex
26
B. Kopp et al. / Electroencephalography and clinical Neurophysiology 99 (1996) 19-27
in the incongruent visual context condition of the go trials and in the specific priming condition of the nogo trials. These two conditions had in common that responses were primed erroneously, as indicated by the LRPs. Thus, the erroneous tendency to respond was generally accompanied by a distinct N2. In ERPs, errors in choice RT tasks are associated with increased negativity in the latency range between 300 and 500 ms after the onset of the imperative stimulus (Falkenstein et al., 1991). This negativity was called 'error negativity' (NE). Because the errors were uncorrected, the initiation of a correction response cannot be regarded as the critical processing component underlying the ArE. NE had a fronto-central maximum and was larger in response-triggered than in stimulustriggered averages. Gehring et al. (1993) analyzed ERPs that were obtained from (partial) errors in the flanker task. The 'error-related negativity' (ERN) began around the time of the incorrect response and peaked about 100 ms later. The ERN amplitude was larger when response accuracy was stressed, whereas the ERN amplitude was smaller when the subjects were encouraged to respond quickly. Larger ERN amplitudes were associated (1) with reduced response strength of the incorrect responses, (2) with increased probability that an incorrect response was followed immediately by a correct response, (3) with slower RTs on correct trials following error trials. Because the morphology, the latency and the scalp distribution of the N2 was very similar to those described for the NE/ERN (Dehaene et al., 1994), we infer that both these deflections similarly reflect motor inhibition. Although the N2 and the NE/ERN seem to be equivalent with respect to their underlying processes, it could be argued that the NE/ERN reflects rather unspecifically the activation of attentional processes due to the low frequency of errors and/or the usual consequences of errors (feedback) in choice RT tasks. In contrast, frequency and/or consequence of errors are surely not critical for eliciting the N2 because we restricted our analyses to the correct trials. These analyses indicate that the study of motor inhibition does not presuppose the presence of uncorrected or corrected errors. Error corrections were possible the incongruent visual context condition of the go trials (cf. Section 2) but not in the specific priming condition of the nogo trials (exceeding the criterion force level led irresistibly to an error in nogo trials). Because the N2 appeared irrespective of whether an error was correctable (as in go trials) or not (as in nogo trials), we conclude that the N2 reflects either the detection or the inhibition of an inappropriate tendency to respond. Importantly, we thus exclude that the N2 is associated with the initiation of the correction of an error. 2 We suggest that the response priming effect on the N2 amplitude reflects the recruitment of neuronal activity that serves to suppress the execution an otherwise inap2 This conclusion was pointed out by Michael Coles.
propriate response. Note that this leaves open whether the neuronal activity underlying the N2 is itself inhibitory (deactivation of the agonist) or excitatory (activation of the antagonist). What do we know about the neuronal activity that serves to suppress the execution of an inappropriate response? Our subjects committed much more (correctable) errors in the incongruent visual context condition of the go trials (15.1%) than (uncorrectable) errors in the specific priming condition of the nogo trials (4.8%). In contrast, the flanker-triggered cortical response priming had comparable peaks in both conditions (1.58 versus 1.60/zV). In addition, flanker-triggered response priming at the cortex lasted equally long in the congruent and incongruent visual context condition. If the neuronal activity underlying the N2 specifically interrupts the cortical preparation for errors, cortical error preparation should have a shorter time course than cortical preparation of appropriate responses. These results together imply that some of the activity that underlies the N2 exerts its influence on more peripheral stages, most probably the corticospinal efferents (De Jong et al., 1990, 1995; Gratton et al., 1992).
Acknowledgements This research was supported by a grant from the Deutsche Forschungsgemeinschaft (Ri 342/4). Portions of this work were presented at the 33rd Meeting of the Society for Psychophysiological Research, Rottach-Egern, October 1993. We greatly appreciate the support we obtained from Patrick Berg, University of Konstanz, who let us have his EEG data analysis programs. We thank Hartmut Leuthold, Humboldt University at Berlin, for his valuable comments on an earlier draft of this article, and Michael Coles, University of Illinois at Urbana-Champaign, as well as Michael Falkenstein, Institut fiJr Arbeitsphysiologie, Dortmund, for their helpful discussion and correspondence.
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