Psychophysiology, 51 (2014), 824–833. Wiley Periodicals, Inc. Printed in the USA. Copyright © 2014 Society for Psychophysiological Research DOI: 10.1111/psyp.12240

Sensation seeking and error processing

YA ZHENG,a WENBIN SHENG,a JING XU,b and YUANYUAN ZHANGc a

Department of Psychology, Dalian Medical University, Dalian, China Department of Neurology and Psychiatry, First Affiliated Hospital, Dalian Medical University, Dalian, China c School of Public Health, Dalian Medical University, Dalian, China b

Abstract Sensation seeking is defined by a strong need for varied, novel, complex, and intense stimulation, and a willingness to take risks for such experience. Several theories propose that the insensitivity to negative consequences incurred by risks is one of the hallmarks of sensation-seeking behaviors. In this study, we investigated the time course of error processing in sensation seeking by recording event-related potentials (ERPs) while high and low sensation seekers performed an Eriksen flanker task. Whereas there were no group differences in ERPs to correct trials, sensation seeking was associated with a blunted error-related negativity (ERN), which was female-specific. Further, different subdimensions of sensation seeking were related to ERN amplitude differently. These findings indicate that the relationship between sensation seeking and error processing is sex-specific. Descriptors: Sensation seeking, Error processing, Event-related potentials, Error-related negativity

ated mainly in the dorsal anterior cingulate cortex (ACC; Debener et al., 2005; Dehaene, Posner, & Tucker, 1994). The functional significance of the ERN component is still a matter of debate. On one hand, this component is regarded as a cognitive/motor process in that it reflects a mismatch detection between an observed and intended response (Bernstein, Scheffers, & Coles, 1995; Falkenstein et al., 1991) or the monitoring of response conflict (van Veen & Carter, 2002; Yeung, Botvinick, & Cohen, 2004). On the other hand, more and more research recently has emphasized the influence of affect and motivation on the ERN amplitude in that it indexes a reinforcement-learning response to unexpected outcomes (Holroyd & Coles, 2002) or an affective response to errors (Hajcak, Moser, Yeung, & Simons, 2005; Luu, Collins, & Tucker, 2000; Vidal, Hasbroucq, Grapperon, & Bonnet, 2000). Following the ERN, the Pe is a positive deflection with a centroparietal distribution between 200 and 400 ms, which may reflect conscious awareness that an error has occurred (Overbeek, Nieuwenhuis, & Ridderinkhof, 2005). As a matter of fact, growing evidence has demonstrated a robust link between ERN and various types of risk-taking behaviors, including external disorders (Brazil et al., 2009; Hall, Bernat, & Patrick, 2007), substance use (Luijten, van Meel, & Franken, 2011), and addiction (I. H. Franken, van Strien, Franzek, & van de Wetering, 2007). Clinical studies, however, failed to exclude disease effects on the relationship between ERN and risk-taking behaviors. In this sense, the study of subclinical samples is of great importance, especially to rule out the neurotoxic effects inherent to disease states (Gottesman & Gould, 2003). Indeed, accumulating evidence is showing that the ERN varies as a function of individual differences in personality trait (for a review, see Segalowitz & Dywan, 2009). For example, impulsivity, as a candidate for the endophenotype of addiction, has been associated with deficient error processing indexed by a reduced ERN component (Pailing,

Sensation seeking is a trait defined by “the seeking of varied, novel, complex, and intense sensations and experiences, and the willingness to take physical, social, legal, and financial risks for the sake of such experience” (Zuckerman, 1994, p. 27). Several theories hold that the insensitivity to negative consequences incurred by risks is one of the hallmarks of sensation-seeking behaviors (R. E. Franken, Gibson, & Rowland, 1992; Horvath & Zuckerman, 1993; Kruschwitz, Simmons, Flagan, & Paulus, 2012). This view is substantiated by several studies showing that sensation seeking is associated with a decreased sensitivity to adverse consequences (R. E. Franken et al., 1992; Horvath & Zuckerman, 1993; Joseph, Liu, Jiang, Lynam, & Kelly, 2009; Kruschwitz et al., 2012; Lissek & Powers, 2003; Zheng et al., 2011). In the present study, we focus on one specific aspect of adverse consequences: the commission of errors. We investigate whether individuals with high sensation seeking exhibit abnormal behavioral and neural mechanisms when making errors. The neural activity associated with error processing can be measured with event-related potentials (ERPs). Two ERP components are associated with the error processing, that is, the errorrelated negativity (ERN) and the error positivity (Pe). The ERN is a frontocentral negative deflection occurring between 0 and 100 ms after an erroneous response during a variety of psychological tasks (Falkenstein, Hohnsbein, Hoormann, & Blanke, 1991; Gehring, Goss, Coles, Meyer, & Donchin, 1993), and appears to be gener-

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This work was supported by the National Natural Science Foundation of China (81171412). The authors thank the editor Dr. Robert Simons and two anonymous reviewers for their helpful comments on previous drafts of this manuscript. Address correspondence to: Jing Xu, Department of Neurology and Psychiatry, First Affiliated Hospital, Dalian Medical University, Dalian, China, 116011. E-mail: [email protected] 824

Sensation seeking and error processing Segalowitz, Dywan, & Davies, 2002; Potts, George, Martin, & Barratt, 2006; Ruchsow, Spitzer, Gron, Grothe, & Kiefer, 2005). In addition, recent research has illustrated an intimate association between error processing and other personality variables (Boksem, Tops, Wester, Meijman, & Lorist, 2006; Dikman & Allen, 2000; Hoffmann, Wascher, & Falkenstein, 2012; Larson, Good, & Fair, 2010; Luu et al., 2000). Sensation seeking is a neurobiological-based trait that is of great significance in public health, due to its close association with a variety of risk-taking behaviors, including promiscuous sexual activity, excessive gambling, substance use, and even psychopathology (Roberti, 2004; Zuckerman, 2007). In this vein, sensation seeking has been regarded as a potential endophenotype for externalizing problems (Benjamin, Ebstein, & Belmaker, 2001; Gottesman & Gould, 2003). Therefore, it seems quite reasonable to investigate the error processing in sensation seeking to provide a basis for future studies on risk-taking behaviors. Actually, the similarity between brain regions engaged in error processing and those related to sensation seeking indicates a potential relationship between ERN and sensation seeking. For instance, sensation seeking is negatively correlated with ACC glutamate concentration (Gallinat et al., 2007), and left ACC is less activated in response to emotional pictures among individuals with high versus low sensation seeking (Joseph et al., 2009). Similarly, sensation seeking is negatively related with ACC activity during the decision-making stage (successive inflation choices) of a balloon analog risk task, indicating a failure of the ACC to drive risk avoidance among individuals with high sensation seeking. In contrast, sensation seeking is positively correlated with ACC activation during the outcome stage (successive successful inflation outcomes), suggesting a reduced sensitivity to the probabilities for success or failure and, hence, greater unexpectedness for high sensation seekers (Bogg, Fukunaga, Finn, & Brown, 2012). To our knowledge, only one previous study investigated the error processing of sensation seeking (Santesso & Segalowitz, 2009) and found that the ERN was negatively correlated with sensation seeking among late adolescent men. However, several limitations in that study may have prevented the conclusion between sensation seeking and ERN from generalization. Firstly, the subjects recruited in Santesso and Segalowitz’s study were comprised of male adolescents aged 18–19 years. In fact, sensation seeking is considerably more common in males than females (Zuckerman, 1979), whereas ERN is more enhanced in male relative to female college students (Larson, South, & Clayson, 2011). Also, given that both ERN (Segalowitz & Davies, 2004) and sensation seeking (Steinberg et al., 2008) are susceptible to age-related changes, the developmental changes (18–19 years) perhaps constitute a confounding variable for the conclusion between sensation seeking and error processing. Secondly, the subjects consisted of an unselected sample, instead of individuals with extreme sensationseeking scores. Specifically, the sensation-seeking score of their sample was mid to high (15–33), excluding individuals with low sensation seeking. In light of these promising findings, the purpose of the present study was to extend the previous work (Santesso & Segalowitz, 2009) by including a sample of both males and females with an age range of 23 to 27 years, and by selecting the extreme high sensation seekers (HSSs, sensation-seeking score: mean = 24.6, range = 22– 29) and low sensation seekers (LSSs, mean = 9.1, range = 5–14). Further, we included the Pe component to examine whether the conscious evaluation of the error commission was different between HSSs and LSSs. Based on the previous findings, we pre-

825 dicted that HSSs relative to LSSs would exhibit reduced ERN amplitudes. As for the Pe component, we did not have a clear hypothesis about the relationship between sensation seeking and the Pe component due to the absence of related studies. In order to examine the entire process of performance monitoring, we also examined two other stimulus-locked ERP components known to be involved in performance monitoring, namely, the stimulus-locked N2 and P3 components. Both N2 and P3 amplitudes are enhanced on incongruent trials compared with congruent trials (e.g., Fruhholz, Godde, Finke, & Herrmann, 2011; Yeung et al., 2004). Whereas the N2 component is thought to reflect the strength of the preresponse conflict on correct trials (Yeung et al., 2004), the P3 component may index response inhibition (Fruhholz et al., 2011). Given the fact that the significances of the stimuluslocked ERP components are generally interpreted within the framework of cognitive control (Botvinick, Braver, Barch, Carter, & Cohen, 2001) and that previous ERP studies about sensation seeking did not provide a potential association between sensation seeking and cognitive control (Fjell et al., 2007; Zheng et al., 2010), we did not expect, therefore, that there would be group differences with respect to these stimulus-related N2 and P3 components. Method Participants One hundred and twenty students participated in a mass screening with the Chinese version of Sensation Seeking Scale Form V (SSS-V; Zuckerman, Eysenck, & Eysenck, 1978). Based on forced choice, the SSS-V is designed to assess four dimensions of sensation seeking (10 items each): thrill and adventure seeking, experience seeking, disinhibition, and boredom susceptibility. The thrill and adventure-seeking dimension refers to the desire to engage in physically risky activities such as skydiving; the experienceseeking dimension comprises the need to seek sensation and new experiences through the mind and senses such as music, art, or travel; the disinhibition dimension involves the desire to seek social stimulation via uninhibited social activities such as “wild” parties; the boredom susceptibility represents an aversion to monotony and restlessness when facing such monotony. Summing all the 40 items derives an overall sensation-seeking score. Reliability and validity of this scale have been proven to be good in Chinese culture (Wang et al., 2000). Participants scoring in the top quartile of the distribution were assigned to the high sensation-seeking group, whereas participants in the bottom quartile to the low sensation-seeking group. Given the gender imbalance in the high and low sensation-seeking sample, the selection criterion was applied within the males and females separately. As a result, 36 participants (mean = 25.1 years, age range = 23–27 years) entered into the experiment with 18 in the high sensation-seeking group (9 female, 9 male) and 18 in the low sensation-seeking group (8 female, 10 male). Demographic variables are presented in Table 1. The two groups differed significantly in sensation-seeking scores in both females and males (ps < .0001). Moreover, female LSSs scored lower in sensation seeking than male LSSs (p = .001), but no difference was found between female HSSs and male HSSs (p = .796). All participants had normal or corrected-to-normal visual acuity and reported not to be recreational drug users or smokers. All participants were righthanded and had no history of neurological or psychiatric disorders. This research was approved by the Ethical Committee of Dalian

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Table 1. Sample Characteristics and Flanker Task Performance (M ± SD) Females

Case (n) Age (years) SSS Correct trials (%) Congruent errors Incongruent errors Reaction time (ms) Correct congruent Correct incongruent Incongruent slowing All-correct trials Pre-error trials Error trials Post-error trials Post-error slowing Pre-error speeding Error rates for all-correct (%) Error rates for post-error (%)

Males

HSSs

LSSs

HSSs

LSSs

9 25.2 ± 0.8 24.4 ± 1.0 88.8 ± 5.9 9.7 ± 9.3 43.9 ± 20.5

8 24.8 ± 0.5 7.4 ± 1.5 86.0 ± 8.3 12.1 ± 13.2 55.3 ± 28.2

9 25.2 ± 0.8 24.7 ± 2.4 88.4 ± 8.3 10.3 ± 9.7 45.6 ± 30.6

10 25.1 ± 1.1 10.5 ± 2.0 87.7 ± 6.6 12.2 ± 10.1 46.8 ± 23.4

365.6 ± 19.8 399.5 ± 15.8 33.9 ± 12.8 384.5 ± 17.1 367.7 ± 21.8 346.3 ± 33.9 406.1 ± 16.0 21.6 ± 10.8 −16.8 ± 13.4 11.2 ± 5.9 8.8 ± 6.4

347.5 ± 11.0 380.7 ± 14.4 33.2 ± 11.7 364.4 ± 12.2 361.5 ± 13.5 334.1 ± 19.4 377.7 ± 12.5 13.2 ± 15.5 −3.0 ± 9.6 14.0 ± 8.8 12.5 ± 8.2

356.1 ± 16.3 384.3 ± 20.2 28.3 ± 11.1 370.8 ± 18.3 354.2 ± 19.9 331.9 ± 13.6 398.3 ± 18.0 27.4 ± 14.5 −16.7 ± 15.9 11.3 ± 8.4 10.5 ± 10.0

353.7 ± 26.0 383.9 ± 21.4 30.2 ± 9.0 369.9 ± 21.8 358.1 ± 21.4 331.0 ± 28.3 384.7 ± 27.9 14.9 ± 15.8 −11.8 ± 14.5 11.3 ± 6.6 13.8 ± 8.7

Note. Incongruent slowing calculated as the difference between incongruent and congruent correct trials. Post-error slowing calculated as the difference between post-error trials and all-correct trials. Pre-error speeding calculated as the difference between pre-error trials and all-correct trials. HSSs = high sensation seekers; LSSs = low sensation seekers; SSS = sensation-seeking score.

Medical University in accordance with the 1964 Declaration of Helsinki, and all participants provided written informed consent prior to the experiment.

& Segalowitz, 2009). A brief training block of 20 trials was used prior to the formal experiment to familiarize participants with the procedure.

Procedure

Recording and Analysis

Participants performed an Eriksen flanker task (Eriksen & Eriksen, 1974). During the task, participants were presented with a fiveletter string. Each string was either congruent (HHHHH or SSSSS) or incongruent (SSHSS or HHSHH), and participants were instructed to respond to the central letter (target) via the left or right button, as accurately and rapidly as possible. Buttons were reversed for half of the participants within each group. All stimuli were presented at the center of a cathode ray tube (CRT) video monitor and viewed from a distance of approximately 60 cm. Each letter was displayed in a white Arial font on a black background and subtended a 0.25° of visual angle vertically and horizontally; the complete five-letter string subtended a 1.44° of visual angle horizontally. Each trial began with a fixation cross that was presented for 500 ms in the center of the screen. A five-letter string then appeared for 100 ms, followed by a blank screen for 800 ms. Participants were required to respond within 450 ms after target onset. The response time (RT) deadline was used to enhance the difficulty of the task and thereby ensure a sufficient number of errors (Amodio, Master, Yee, & Taylor, 2008; Bartholow, Henry, Lust, Saults, & Wood, 2012). Although responses within 900 ms after stimulus onset were registered as hits, a “Too slow!” feedback was presented for 500 ms immediately if subjects missed the RT deadline. Feedback was also given following error responses. Feedback on correct responses was provided on training trials, but not on experimental trials. The intertrial interval varied randomly from 500 to 1,000 ms. The entire experimental task consisted of 480 trials grouped into four blocks (120 trials each). Each block included 40 congruent and 80 incongruent trials, which were delivered randomly, and a rest break was given between blocks. The larger number of incongruent trials was used in order to elicit more errors (Santesso

The electroencephalogram (EEG) was recorded continuously using an elastic cap with a set of 30 sintered Ag/AgCI electrodes (FP1, FP2, F7, F3, Fz, F4, F8, FT7, FC3, FCz, FC4, FT8, T7, C3, Cz, C4, T8, TP7, CP3, CPz, CP4, TP8, P7, P3, Pz, P4, P8, O1, Oz, and O2) mounted according to the extended 10–20 system and referenced to linked mastoids. The horizontal electrooculogram (EOG) was recorded as the voltage between electrodes placed bilateral to the external canthi to monitor horizontal eye movements. The vertical EOG was recorded via a pair of electrodes placed on the left infraorbital and supraorbital areas to detect blinks and vertical eye movements. Electrode impedance was kept below 5 KΩ. The EEG and EOG were amplified and digitalized using a Neuroscan NuAmps amplifier with a band-pass of 0.1–100 Hz and a sampling rate of 1000 Hz. The EOG artifacts were removed from the EEG signals offline using a regression-based procedure (Semlitsch, Anderer, Schuster, & Presslich, 1986). Separate stimulus-locked and response-locked averages were computed, using an epoch of −200 to 1,000 ms with the activity from −200 to 0 ms serving as the baseline for stimuluslocked averages and an epoch of −600 to 800 ms with −600 to −400 ms as the baseline for response-locked averages, respectively. Trials with reaction time either faster than 100 ms or slower than 900 ms, or contaminated with artifacts exceeding ± 100 μV, were excluded from averaging. As the ERN is very susceptible to differences in signal to noise, preliminary analysis was performed on the number of accepted ERN trials, which revealed no significant group or sex effect (ps > .4). For response-locked ERP components, error-trial and correcttrial amplitudes for the ERN were extracted as the mean voltage from 15 ms prepeak to 15 ms postpeak at Fz, FCz, and Cz sites where the ERN was maximum. Error-trial and correct-trial Pe

Sensation seeking and error processing amplitudes were extracted as the mean voltage from 160 to 300 ms at Cz, CPz, and Pz sites due to a posterior distribution of the Pe component. As the ERN on error trials likely includes processes common to error and correct responses, difference waveforms (i.e., ΔERN) reflecting neural activity to errors more purely were obtained by subtracting correct trial activity from error trials (Pailing et al., 2002). The ΔERN was measured with the same parameters for ERN. For stimulus-locked ERP components, we measured the mean voltage of the stimulus-locked N2 and P3 components in a given measurement window poststimulus: N2 from 320 to 360 ms at Fz, FCz, and Cz sites and P3 from 500 to 700 ms at Cz, CPz, and Pz sites. Similarly, difference waveforms (i.e., ΔN2) reflecting neural activity to conflicts were obtained by subtracting congruent trial activity from incongruent trials and measured with the same parameters for N2. For figures, ERP waveforms were filtered with a low-pass filter at 20 Hz (24 dB/octave). Behavioral measures included total accuracy, the number of errors, and average RTs for congruent and incongruent trials. In addition, a sequential analysis was performed. Specifically, we classified each trial n according to its accuracy, as well as the accuracy on trial n − 1 and trial n + 1 (Dudschig & Jentzsch, 2009) and focused on four different trial types: (1) all-correct trial (cCc), where a correct response on trial n is preceded by correct responses on trial n − 1 and followed by correct responses on trial n + 1; (2) pre-error trial (cCe), where a correct response on trial n is preceded by correct responses on trial n − 1 and followed by incorrect responses on trial n + 1, (3) error trial (cEc), where an incorrect response on trial n is preceded by correct responses on trial n − 1 and followed by correct responses on trial n + 1; (4) post-error trial (eCc), where a correct response on trial n is preceded by incorrect responses on trial n − 1 and followed by correct responses on trial n + 1. Moreover, error rates were calculated for all-correct trials [E(all-correct) = cEc/(cCc + cEc) × 100], and post-error trials [E(post-error) = eEc/(eCc + eEc) × 100]. Repeated measures analysis of variance (ANOVA) was used with an alpha level of .05 for all statistical tests, using the Greenhouse-Geisser epsilon (ε) correction for nonsphericity (Jennings & Wood, 1976) and partial eta-squared ( η2p ) reported as a measure of effect size. Post hoc pairwise analysis was made via a Bonferroni procedure. We conducted a Group (HSSs vs. LSSs) × Sex (male vs. female) × Congruency (incongruent vs. congruent) ANOVA for error rates and RT data separately. Sequential analyses were performed with a Group × Sex × Trial Type (cCc, cCe, cEc, and eCc) ANOVA for RT data, and a Group × Sex × Trial Type (cCc vs. eCc) ANOVA for error rates. The ERN and Pe amplitudes were analyzed separately with two 2 × 2 × 2 × 2 ANOVAs: Group × Sex × Correctness (error vs. correct) × Electrode (ERN: Fz, FCz, and Cz; Pe: Cz, CPz, and Pz). Likewise, The N2 and P3 component analyses were performed separately with two Group × Sex × Congruency × Electrode (N2: Fz, FCz, and Cz; P3: Cz, CPz, and Pz) ANOVAs. The ΔERN and ΔN2 were analyzed separately with a Group × Sex × Electrode (Fz, FCz, and Cz) ANOVA. Furthermore, Pearson’s correlation test was applied to evaluate whether ΔERN/ΔN2 amplitude at FCz or Pe/P3 amplitude at CPz correlated with subscales of sensation seeking as a function of sex. Results Behavioral Data Behavioral data of the two groups as a function of sex are shown in Table 1. The accuracy rates were similar across the two groups, as

827 well as across males and females (Fs < 1). With respect to error rates, there was a significant main effect of congruency, F(1,32) = 147.09, p < .001; η2p = .82 , indicating that more errors were made to incongruent trials than to congruent trials. No other significant effects were observed (Fs < 1). As expected, the RTs for correct responses were shorter on congruent than incongruent trials, leading to a significant congruency main effect, F(1,32) = 285.39, p < .0001, η2p = .90 . No other effects reached significance (ps > .1). For sequential analysis, there was a significant main effect of trial type, F(3,96) = 121.50, p < .0001, ε = .76, η2p = .79 . The group effect is marginally significant, F(1,32) = 3.67, p = .064, η2p = .10 , which was qualified by a significant interaction of Group × Trial Type, F(3,96) = 3.89, p = .020, ε = .76, η2p = .11. Further analyses suggested that RTs were longer for HSSs relative to LSSs on post-error trials (p = .004) and all-correct trials (p = .090), but not on pre-error trials (p = .860) and error trials (p = .443). In addition, RTs were longer on post-error trials than those on all-correct trials, indicating a post-error slowing effect for both groups (ps < .0001). The post-error slowing effect, calculated as RT difference between post-error and all-correct trials, was larger for HSSs (25 ms) than for LSSs (14 ms, p = .033). Moreover, RTs were faster on pre-error trials than those on all-correct trials, indicating a pre-error speed-up effect, which only appeared for HSSs (p < .001) but not for LSSs (p = .180). Neither sex effect nor interactions involving sex were significant (ps > .2). In addition, error rates were similar between all-correct trials (12.0%) and post-error trials (11.4%). Also, no other significant effects reached significance (ps > .1). Electrophysiological Data Response-locked and stimulus-locked ERP component data for HSSs and LSSs as a function of sex are presented in Table 2. Figure 1 shows response-locked waveforms at FCz in response to the error and correct trials. Difference waveforms (error minus correct) and individual data for ΔERN are also presented in Figure 1. ERN. ERP activity elicited by error responses was significantly more negative than that by correct responses, as reflected by a correctness main effect, F(1,32) = 223.50, p < .001, η2p = .88 . There was a significant interaction of Correctness × Electrode, F(2,64) = 37.32, p < .001, ε = .68, η2p = .54 . Post hoc decomposition suggested that ERN for error trials was more negative at FCz relative to Fz (p = .008), whereas ERN for correct trials was more negative at Fz relative to FCz (p < .001), and Cz (p < .001), as well as at FCz relative to Cz (p = .001). There was a significant main effect of group, F(1,32) = 5.90, p = .021, η2p = .16 , with smaller ERN amplitude for HSSs relative to LSSs. This group effect was qualified by a significant interaction of Group × Correctness, F(1,32) = 5.46, p = .026, η2p = .15 . Follow-up analysis revealed that HSSs had reduced ERN amplitude for the error trials as compared to LSSs (p = .007), but no significant group difference was observed on the ERN for the correct trials (p = .211). Critically, the interaction of Group × Correctness was modulated by sex, resulting in a marginally significant three-way interaction of Correctness × Group × Sex, F(1,32) = 3.22, p = .082, η2p = .09 . Further analysis suggested that the reduced ERN for HSSs relative to LSSs on the error trials appeared only for females (p = .002), but not for males (p = .159). The ΔERN was smaller for HSSs as compared to LSSs, F(1,32) = 5.46, p = .026, η2p = .15 . Although there was no signifi-

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Table 2. Mean (± SD) Amplitudes (μV) for the Response-Locked and Stimulus-Locked Event-Related Potential Components Females HSSs ERN for error Fz 3.9 ± 6.1 FCz 2.1 ± 6.7 Cz −0.2 ± 8.3 ERN for correct Fz 9.7 ± 3.8 FCz 11.7 ± 5.2 Cz 12.2 ± 6.1 ΔERN Fz −5.8 ± 4.6 FCz −9.6 ± 4.2 Cz −12.4 ± 4.7 Pe for error Cz 22.3 ± 9.9 CPz 19.8 ± 8.4 Pz 18.6 ± 8.6 Pe for correct Cz 7.3 ± 3.7 CPz 6.2 ± 2.7 Pz 5.1 ± 2.3 N2 for incongruent Fz 7.0 ± 5.7 FCz 8.4 ± 6.9 Cz 8.7 ± 7.6 N2 for congruent Fz 10.1 ± 5.6 FCz 11.9 ± 6.8 Cz 12.3 ± 7.4 ΔN2 Fz −3.1 ± 1.7 FCz −3.5 ± 1.6 Cz −3.5 ± 1.5 P3 for incongruent Cz 8.9 ± 3.8 CPz 8.0 ± 3.3 Pz 7.0 ± 3.2 P3 for congruent Cz 8.7 ± 4.1 CPz 7.3 ± 3.4 Pz 5.9 ± 3.4

Males

LSSs

HSSs

LSSs

−7.8 ± 6.0 −10.2 ± 8.4 −8.1 ± 10.0

−2.3 ± 4.0 −4.7 ± 6.0 −4.7 ± 6.4

−4.9 ± 3.0 −6.8 ± 7.2 −5.0 ± 8.5

4.7 ± 5.0 8.0 ± 5.8 10.4 ± 5.4

7.0 ± 4.2 8.7 ± 5.4 10.1 ± 6.2

5.5 ± 4.0 8.2 ± 5.7 9.7 ± 5.3

−12.5 ± 5.5 −18.2 ± 7.5 −18.4 ± 7.4

−9.3 ± 4.6 −10.5 ± 5.0 −13.3 ± 5.6 −15.0 ± 5.8 −14.8 ± 6.0 −14.7 ± 6.6

18.4 ± 8.7 18.8 ± 7.5 17.8 ± 6.2

19.5 ± 9.3 18.4 ± 8.8 16.4 ± 7.8

20.7 ± 9.9 18.8 ± 8.1 16.5 ± 7.0

3.9 ± 7.7 4.1 ± 6.3 4.0 ± 4.8

6.0 ± 5.3 4.7 ± 4.2 3.0 ± 3.1

4.6 ± 3.0 3.5 ± 2.7 2.7 ± 1.9

1.3 ± 3.5 3.1 ± 4.7 5.8 ± 5.6

2.6 ± 2.1 3.0 ± 3.1 4.7 ± 3.8

4.6 ± 4.0 7.4 ± 5.5 7.9 ± 5.5

5.3 ± 4.0 8.3 ± 5.5 10.7 ± 5.8

4.5 ± 2.5 5.7 ± 3.9 7.7 ± 5.0

7.4 ± 4.7 11.0 ± 5.9 11.9 ± 5.9

−4.0 ± 2.3 −5.3 ± 2.9 −4.9 ± 2.5

−1.9 ± 1.5 −2.7 ± 1.8 −3.0 ± 1.7

−2.7 ± 1.6 −3.6 ± 1.9 −4.0 ± 2.2

5.7 ± 7.4 6.0 ± 6.4 5.6 ± 4.9

7.6 ± 5.8 6.6 ± 4.7 4.8 ± 3.4

6.3 ± 3.8 5.5 ± 3.8 4.3 ± 3.2

4.4 ± 7.7 4.3 ± 6.6 3.9 ± 5.3

6.7 ± 5.2 5.4 ± 4.1 3.6 ± 2.8

5.2 ± 4.0 4.6 ± 3.8 2.8 ± 3.2

Note. HSSs = high sensation seekers; LSSs = low sensation seekers.

cant main effect of sex (F < 0.1), the interaction of Group × Sex was marginally significant, F(1,32) = 3.22, p = .083, η2p = .09 . Further analysis suggested that, whereas the group difference was significant among females (p = .008), no group difference was observed for males (p = .696). Pe. With respect to Pe, there was a significant main effect of correctness, F(1,32) = 121.50, p < .001, η2p = 0.79 , suggesting the mean ERP amplitude between 160 and 300 ms postresponse was more significantly enhanced on error trials than that on correct trials. This mean activity decreased as a gradient from Cz to CPz, and to Pz sites, as indicated by a significant main effect of electrode, F(1,32) = 21.00, p < .001, ε = .61, η2p = .40 . Neither group or sex effect nor interactions related to group or sex were significant (ps > .2). Stimulus-locked ERPs. Only main effects or interactions involving group or sex are reported for stimulus-locked ERPs. For N2 component, neither group nor sex main effect was significant

(Fs < 1). However, there was a significant interaction of Group × Sex, F(1,32) = 5.41, p = .027, η2p = .15 , which was driven by the fact that females relative to males displayed reduced N2 amplitude (more positive) only for HSSs (p = .037) but not for LSSs (p = .273). Importantly, no reliable group effect was obtained for females (p = .104) or males (p = .116). For ΔN2 amplitude, neither group nor sex effect nor interactions related to group or sex were significant (ps > .1). Similarly, no significant effects involving group or sex were found for P3 component (ps > .1). Relationships between ΔERN and subscales of sensation seeking. For males, no significant correlations were detected between ΔERN at FCz and any of subscales of sensation seeking (ps > .4). In contrast, for females, the ΔERN at FCz was significantly correlated with thrill and adventure-seeking scores (r = 0.66, p = .004) and boredom susceptibility scores (r = 0.65, p = .005), as well as marginally significantly correlated with disinhibition scores (r = 0.46, p = .062), but not with experience-seeking scores (r = 0.36, p = .163). The linear correlations of ΔERN at FCz with subscales of sensation seeking are plotted in Figure 2. Pe data from CPz, ΔN2 data from FCz, or P3 data from CPz did not show any significant correlations with subscales of sensation seeking (ps > .1). Discussion The present study examined error processing in sensation seeking. We found that, compared with LSSs, HSSs displayed a reduced ERN component only in response to error trials, which was specific to females but not males. Furthermore, different subdimensions of sensation seeking were related to ERN amplitude differently. Finally, no group differences were found to Pe, N2, and P3 components, as well as behavioral patterns except a larger post-error slowing effect for HSSs relative to LSSs. The novel finding of the present study is that the relationship between sensation seeking and ERN is specific to females, which is demonstrated by group analysis as well as correlation analysis. Given that there is a reliable sex difference in sensation seeking, with men usually scoring higher than women on the sensationseeking scale (Cross, Cyrenne, & Brown, 2013; Zuckerman et al., 1978), HSSs and LSSs in the present study were selected by using the top and bottom quartiles within males and females separately, leading to similar sensation-seeking scores across the sexes. Interestingly, the ERN pattern emerged despite comparable sensationseeking scores as well as similar ERN amplitudes across females and males, indicating somewhat qualitative differences in the underlying mechanisms of sensation seeking between the sexes. Paralleling with this study, one recent study has also found that the relationship between ERN amplitude and worry (i.e., anxious apprehension) is female-specific (Moran, Taylor, & Moser, 2012). In this study, worry is associated with enhanced ERN amplitude in female but not male undergraduates. The ERN amplitude could either be enhanced by internalizing disorders such as anxiety and depression or be attenuated by externalizing problems such as substance use (for a review, see Olvet & Hajcak, 2008). Given that there is a higher prevalence of internalizing behaviors among females such as depression or anxiety (Kessler, Chiu, Demler, Merikangas, & Walters, 2005), it is possible that the sensation-seeking-related deficient ERN is mainly driven by a reduced aversive motivational system in sensation seeking. Actually, early studies have shown that, compared with LSSs, HSSs experience reduced self-reported anxious reactivity to

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Figure 1. Response-locked ERP waveforms at FCz in response to the error (A) and correct (B) trials, as well as the difference waves (error minus correct) (C), for high sensation seekers (HSSs) and low sensation seekers (LSSs) in females and males. Scatter plots for the relationship between sensation-seeking score and ΔERN (error minus correct) amplitude in females and males are also depicted (D).

stress situations (e.g., Blankstein, 1975; Burkhart, Schwarz, & Green, 1978; R. E. Franken et al., 1992), and physiologically anxious reactivity as indexed by affective startle reflex in the face of visual threatening stimuli (Lissek & Powers, 2003) as well as during the anticipation of aversive stimuli (Lissek et al., 2005). More recently, a functional magnetic resonance imaging (fMRI) study has demonstrated that HSSs relative to LSSs show decreased activation to emotionally arousing stimuli in the ACC and anterior medial orbitofrontal cortex (Joseph et al., 2009). Likewise, during a risky decision-making task, whereas HSSs are less sensitive to punishments and tend to exhibit more risky behaviors after prior punishments, LSSs are more sensitive in evaluating different punishment intensities in brain areas including the left superior frontal gyrus, right nucleus accumbens, and left precuneus (Kruschwitz et al., 2012). Moreover, the attenuated ERN in high versus low

sensation seekers is consistent with our previous findings that HSSs compared with LSSs exhibit a decreased N2 component to novel stimuli (Zheng et al., 2010), as well as emotional pictures (Zheng et al., 2011). Overall, these findings are consistent with the view that HSSs might possess a weaker avoidance-withdrawal system than do LSSs (Depue & Collins, 1999; Lang, Shin, & Lee, 2005), whereby individuals with high sensation seeking present a vigilant response to a lesser extent in the face of the commission of an error. Of note, this explanation appears speculative, and awaits further experiment manipulating the affective significance of an error directly (e.g., by reward and/or punishment). The current study failed to replicate a recent investigation by Santesso and Segalowitz (2009), which showed an attenuated ERN in HSSs than LSSs among male adolescents. There are at least two possible interpretations. First, the discrepancy between

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Figure 2. Scatter plots depicting the relationship between the amplitude of ΔERN (error minus correct) and thrill and adventure-seeking score, experience-seeking score, disinhibition score, and boredom susceptibility score, separately for females and males.

this study and Santesso et al.’s findings may reflect age-related differences in ERN amplitude. Specifically, in the study by Santesso and Segalowitz, the participants comprised males aged 18–19 years, a time span during which developmental changes occur rapidly in the ACC (Segalowitz & Dywan, 2009). In contrast, the participants in the present study aged between 23 and 27 years, beyond adolescence. The second possible explanation might be due to a small sample in the current study, which appears to be underpowered to detect the sensation-seeking difference in the ERN. Actually, when closely checking the ERN waveforms depicted in Figure 1, HSSs displayed somewhat smaller ERN amplitude than LSSs in males. Future studies with larger sample size are needed to address the relationship between ERN and sensation seeking in male adults. In the current study, not only was sensation seeking associated with deficient error monitoring, but also different sensationseeking dimensions were related to this process differently. Specifically, whereas neither experience-seeking disinhibition (although marginally significant) dimensions were not associated with ERN component, both the thrill and adventure-seeking and boredom susceptibility dimensions were related to ERN component significantly. Consistent with our findings, it has been pro-

posed theoretically that sensation seeking is a multidimensional rather than a unidimensional trait (Zuckerman, 1994). While most previous studies have not discriminated between various sensationseeking dimensions, our findings indicate possible distinct influences of subdimensions of sensation seeking on error processing, and further studies using a factor analysis approach are needed to address the relationship between the dimensionality of sensation seeking and error processing in detail. As expected, we did not observe a significant effect of sensation seeking on N2, indicating a dissociation between ERN and N2 components in this personality trait. Although the conflict monitoring theory has suggested that the two components probably index a similar role of ACC during the monitoring of response conflict (Yeung et al., 2004), our finding is partially inconsistent with this view, suggesting that these two components might reflect similar but distinct aspects of performance monitoring. Actually, the conflict monitoring theory has viewed both ERN and N2 components as only a cognitive process per se (van Veen & Carter, 2002; Yeung et al., 2004). However, recent ERN studies are being directed toward the emotional appraisal of errors and the influence of affect and motivation on this component (van Noordt & Segalowitz, 2012). As a personality trait, sensation seeking is

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driven mainly by the approach and avoidance motivational systems (Lang et al., 2005; Lissek et al., 2005; Zuckerman, 1994), rather than the “cool” cognitive control system (Castellanos-Ryan, Rubia, & Conrod, 2011). For example, previous studies have demonstrated that both emotional N2 and novelty N2 are reduced for HSSs compared with LSSs, whereas no group difference is found for control-related N2 component, such as the target N2 during a visual oddball task (Zheng et al., 2010). Therefore, it might be reasonable that there is a dissociation between the ERN and N2 components in sensation seeking. Similarly, this dissociation is in line with previous studies investigating individuals with alcoholic consumption (Ridderinkhof et al., 2002), cocaine dependence (I. H. Franken et al., 2007), borderline personality disorder (de Bruijn et al., 2006), high punishment sensitivity (Boksem et al., 2006), or a left ACC lesion (Swick & Turken, 2002). It should be noted that the ERN deficits among HSSs observed here are not a result of poor task performance because of the comparable accuracy levels across HSSs and LSSs. In fact, HSSs displayed a higher level of compensatory post-error slowing as opposed to LSSs. Given that ERN amplitude is shown to be related to post-error adjustment (Debener et al., 2005; Gehring et al., 1993), it is interesting that HSSs with reduced ERN showed a stronger post-error slowing effect. On one hand, recent studies have demonstrated that it is unnecessary that increased post-error slowing indexes a strategic increase in control (Dudschig & Jentzsch, 2009; Notebaert et al., 2009). For instance, post-error slowing could reflect either an orienting response to an unexpected event that is unrelated to error per se (Notebaert et al., 2009), or the shift of attention resulting from a capacity-limited error-monitoring process devoted to strategic control (Dudschig & Jentzsch, 2009). Furthermore, in the current study, there was a feedback following an error trial but no feedback following a correct trial. Therefore, the group difference for the post-error slowing was likely in response to the feedback itself (e.g., attentional capture by feedback stimuli), rather than in response to internal adjustments in control. On the other hand, HSSs displayed a pre-error speed-up

effect, another index of performance adjustment, suggesting that HSSs might lower their response threshold to achieve faster responses. In contrast, this pre-error speeding phenomenon disappeared among LSSs, indicating that LSSs might monitor their performance more closely. In this regard, HSSs relative to LSSs might exert coarser control over their behaviors, rather than monitoring their performance more closely. Moreover, no significant group differences were found to Pe amplitude and P3 amplitude. Although the functional significance of the Pe remains ambiguous, this component is associated with the conscious recognition of an error (Overbeek et al., 2005), and might reflect similar neural and functional processes as the classic P3 does (Ridderinkhof, Ramautar, & Wijnen, 2009). In support of our results, previous ERP studies have demonstrated that there is no relationship between sensation seeking and P3b component (Fjell et al., 2007; Zheng et al., 2010), providing evidence that the response inhibition remains to some extent intact in sensation seeking. Of note, one limitation in the present study is the relatively small sample size for HSSs and LSSs in females and males. However, the modulation of the relationship between ERN and sensation seeking by sex appears robust enough to be detected even with the small sample, as evidenced jointly by group analysis as well as by correlation analysis. Of course, to generalize our results, further studies should be conducted involving a larger number of participants. In summary, our findings demonstrated a sensation-seekingrelated deficiency in error processing with a normal sample. Despite their other intact aspects of performance monitoring, individuals with high sensation seeking exhibit a deficient ERN component to an error event, reflecting their carelessness about the affective significance incurred by the error event. Importantly, the relationship between sensation seeking and deficient ERN is female-specific. Our findings, therefore, highlight the importance of considering sensation seeking as a factor in the study of error processing.

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