Biological Psychology 107 (2015) 44–51

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Diminished P300 to physical risk in sensation seeking Ya Zheng a , Fei Tan a , Jing Xu b,∗ , Yi Chang b , Yuanyuan Zhang c , Huijuan Shen a a

Department of Psychology, Dalian Medical University, Dalian 116044, China Department of Neurology and Psychiatry, First Affiliated Hospital, Dalian Medical University, Dalian 116011, China c School of Public Health, Dalian Medical University, Dalian 116044, China b

a r t i c l e

i n f o

Article history: Received 1 October 2014 Accepted 2 March 2015 Available online 9 March 2015 Keywords: Sensation seeking Emotional arousal Event-related potentials P300

a b s t r a c t Zuckerman’s theory proposes individual differences in optimal arousal and arousability level as the root of the sensation-seeking trait. The current study addressed how sensation seeking influences responses to emotional arousal at the electrophysiological level during a passive viewing task and at the psychometrical level during a self-assessment task. Electrophysiologically, high sensation seekers (HSSs) compared to low sensation seekers (LSSs) exhibited a reduced P300 for high-arousing stimuli (adventure and surreal pictures), but not for low-arousing stimuli (leisure and neutral pictures). Psychometrically, HSSs displayed a higher preference for adventure and surreal pictures whereas LSSs showed a higher preference for leisure pictures. Instead of supporting the optimal arousal hypothesis, these findings suggest that sensation seeking is associated with diminished P300 to physical risk, which may be driven by a hypoactive avoidance system in sensation seeking. © 2015 Elsevier B.V. All rights reserved.

1. Introduction As a personality trait characterized by a strong desire for varied, novel, complex, and intense stimulation and a willingness to take risks for such experience (Zuckerman, 1994), sensation seeking has been viewed as a potential endophenotype of various risktaking behaviors (Benjamin, Ebstein, & Belmaker, 2001; Gottesman & Gould, 2003). High sensation seekers (HSSs), as compared to low sensation seekers (LSSs), are more likely to engage in reckless driving (Jonah, 1997), physical risk sports (Ruedl, Abart, Ledochowski, Burtscher, & Kopp, 2012), substance abuse (Bardo et al., 2007), excessive gambling (Harris, Newby, & Klein, 2013), risky sexual activities (Hoyle, Fejfar, & Miller, 2000), aggressive and unsocialized behaviors (Wilson & Scarpa, 2011), and even suicide behavior (Ortin, Lake, Kleinman, & Gould, 2012). Behavioral differences between HSSs and LSSs may be attributed to an underlying dimension of arousal. The arousal concept was first proposed by Eysenck and aligned with his theory of extraversion (Eysenck, 1967). Eysenck asserted that extroverts have a higher optimal level of stimulation or arousal than introverts, as evidenced by the fact of a reduced sensitivity to physical stimulation in extroverts compared to introverts (De Pascalis, 2004; Matthews & Gilliland, 1999). Similarly, Zuckerman (1969) postulated that HSSs, as compared to LSSs, are below an optimal level of arousal and

∗ Corresponding author. Tel.: +86 411 83635963x7257. E-mail address: xujing [email protected] (J. Xu). http://dx.doi.org/10.1016/j.biopsycho.2015.03.003 0301-0511/© 2015 Elsevier B.V. All rights reserved.

thus need more novel and intense forms of sensation to reach and maintain a higher optimal level of arousal. Such a view affords the hypothesis of lower tonic or phasic arousal levels or both in HSSs compared to LSSs, which however, in contrast to the extraversion theory, has received little empirical support. Later, Zuckerman (1984) emphasized the sensation-seeking theory based on an optimal level of catecholamine system activity such that HSSs relative to LSSs have more excitable autonomic nervous systems and central nervous systems. In support of this hypothesis, numerous studies have found that HSSs exhibit increased event-related potential responses as a function of increasing intensity of sensory stimulus, whereas LSSs display an opposite pattern (Brocke, Beauducel, John, Debener, & Heilemann, 2000; Hegerl, Gallinat, & Mrowinski, 1995; Zuckerman, Murtaugh, & Siegel, 1974). Given that emotional stimuli provide a reliable source of arousal, it is of importance to investigate emotional arousal in sensation seeking. Ample research has demonstrated a close relationship between sensation seeking and emotional activity. At the psychometrical level, HSSs compared to LSSs show a stronger preference for negative stimuli (Rawlings, 2003; Zaleski, 1984) and lower sensitivity to disgust video (Dvorak, Simons, & Wray, 2011). At the autonomic level, HSSs give greater skin conductance responses to violent and sexual stimuli compared to LSSs (Smith, Davidson, Perlstein, & Gonzalez, 1990; Smith, Davidson, Smith, Goldstein, & Perlstein, 1989; Smith, Perlstein, Davidson, & Michael, 1986). However, HSSs versus LSSs exhibit no startle potentiation in the face of threatening stimuli (Lissek & Powers, 2003) and weaker fear-potentiated startle during the anticipation of aversive stimuli

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(Lissek et al., 2005). At the neural level, HSSs show greater activation to emotionally arousing stimuli in the right insula and posterior medial orbitofrontal cortex, whereas LSSs exhibit greater activation in the anterior medial orbitofrontal cortex and anterior cingulate (Joseph, Liu, Jiang, Lynam, & Kelly, 2009). However, sensation seeking is negatively correlated with brain activation in the thalamus and insula to neutral movie clips, but not to threat clips (Straube et al., 2010). Additionally, HSSs compared to LSSs display a reduced N2 component but an enhanced P300 component in the frontal areas for emotional stimuli (Zheng et al., 2011). A limitation of previous research is that most have focused on the dimension of emotional valence. On the contrary, there is a surprising scarceness of research addressing the relationship between emotional arousal and sensation seeking systematically. It is well-known that all emotional events are rooted in motivational states and can be organized by the defensive motivational system (linked to negative affect) and the appetitive motivational system (linked to positive affect). As another dominant dimension of emotion, arousal reflects the intensity that is mobilized by either motivational system (Lang, Bradley, & Cuthbert, 1997). A multitude of research has demonstrated that whereas the behavioral activation system (BAS) is associated with the positive-approach emotion, the behavioral inhibition system (BIS) is associated with the negative-avoidance emotion (Balconi, Falbo, & Conte, 2012; Pascalis, Strippoli, Riccardi, & Vergari, 2004; De Pascalis, Varriale, & D’Antuono, 2010; Simon et al., 2010). As a BAS-related dimension, sensation seeking would be theoretically related to enhanced sensitivity and responsiveness to stimuli with positive valence. Therefore, the present study aimed to address systematically the issue between sensation seeking and emotionally positive arousal. Event-related potential (ERP) technique provides unique insights into the neural dynamics of emotional processing (e.g., emotional valence and arousal), from the early attention allocation to the late cognitive appraisal (Hajcak, Weinberg, MacNamara, & Foti, 2012; Olofsson, Nordin, Sequeira, & Polich, 2008). Although early ERP components (e.g., 300 ms); that is, the P300 and late positive potential (LPP). The P300 is a parietally maximal positive deflection that peaks between 300 and 400 ms post stimulus onset (Sutton, Braren, Zubin, & John, 1965). Following the P300, the LPP is a slow, sustained positivity with a centroparietal distribution beginning around 400 ms (Cuthbert, Schupp, Bradley, Birbaumer, & Lang, 2000). Despite the similar onset latency of the P300 and LPP, there is emerging evidence that the P300 reflects the initial allocation of attentional resources based on motivational significance, whereas the LPP indexes more elaborated processing related to stimulus significance (Hajcak et al., 2012; Schupp, Flaisch, Stockburger, & Junghofer, 2006). For instance, the LPP, unlike the P300, is uniquely associated with memory encoding and storage (Dolcos & Cabeza, 2002), cognitive reappraisal (Hajcak & Nieuwenhuis, 2006), and behavioral interference (Weinberg & Hajcak, 2011). The present study was to investigate the relationship between sensation seeking and emotional stimuli varying along the arousal dimension at the electrophysiological level and the psychometrical level. Because sensation seeking would be theoretically related to enhanced sensitivity to stimuli with positive valence, we employed positive stimuli of varying arousal (low, medium, and high) with neutral stimuli serving as the baseline condition. Moreover, because stimulus relevance is one of the important factors to maximize sensation-seeking group differences (Smith et al., 1990, 1989, 1986), we employed the stimuli presumably associated with the sensation-seeking trait. During the ERP task, HSSs and LSSs passively viewed neutral pictures and positive pictures of

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varying arousal. Later, they rated each picture on the level of valence, arousal, and approach/avoidance tendency in a selfassessment task. We predicted that both the P300 and LPP would increase as a function of arousal level. Based on the previous observation of more excitable central nervous systems for HSSs, we predicted that psychometrically HSSs would display a greater preference for high-arousing pictures whereas LSSs would exhibit a higher preference for low-arousing pictures. Importantly, the ERP arousal effect would be modulated by sensation seeking such that HSSs compared to LSSs would display an enhanced P300 and LPP, especially for the high-arousing pictures. 2. Methods 2.1. Participants Participants were recruited on the basis of their scores on the Chinese version of the Sensation Seeking Scale Form V (SSS-V; Wang et al., 2000; Zuckerman, Eysenck, & Eysenck, 1978). The SSS-V was administered initially in a large sample (N = 250, 162 females and 88 males) in introductory psychology courses at the Dalian Medical University (Fall 2013). Responders in the top quartile of the distribution were assigned to high sensation-seeking group whereas those in the bottom quartile to low sensation-seeking group. Given the gender imbalance in the sample, the selection criterion was applied separately to the males and females. Additional recruitment criteria included: (1) aged 18–25 years, (2) normal or correct-to-normal visual acuity, (3) right-handed as determined by self-report, (4) no current substance use, (5) free from any neurological or psychological disorders. Thus, the final sample was composed of 16 HSSs (8 females and 8 males) and 16 LSSs (8 females and 8 males). As expected, HSSs and LSSs differed significantly on the overall sensation-seeking score (p < .0001) but did not differ by age, gender, and educational level (ps > .5; Table 1). This study was approved by a local ethical committee in accordance with the 1964 Declaration of Helsinki. Informed consent was obtained from each participant before the experiment. 2.2. Stimuli The stimulus selection consisted of three steps. First, a preliminary collection was performed from the International Affective Picture System (Lang, Bradley, & Cuthbert, 2005), the Chinese Affective Picture System (Bai, Ma, Huang, & Luo, 2005), and other various sources on the Internet, resulting in a total of 1670 pictures (408 adventure, 544 surreal, 512 leisure, and 206 neutral pictures). As specific picture content appears to affect the electrophysiological activity (Briggs & Martin, 2009; Weinberg & Hajcak, 2010), the adventure, surreal, and leisure pictures were carefully selected on the basis of the items in the SSS-V to keep the content of each category homogeneous. The adventure pictures depicted people’s adventure activities such as parachuting, base jumping, and Table 1 Sample characteristics and accepted ERP trials (M ± SD). HSSs (N = 16)

LSSs (N = 16)

Gender (M/F) Age (years) Sensation seeking score

8/8 22.94 ± 1.06 26.56 ± 4.05

8/8 22.50 ± .63 7.44 ± 1.37

Accepted ERP trials Adventure Surreal Leisure Neutral

47 ± 2.34 46 ± 2.38 45 ± 3.08 46 ± 2.62

46 ± 2.63 46 ± 3.10 47 ± 2.75 46 ± 3.31

Note: HSSs, high sensation seekers; LSSs, low sensation seekers.

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Fig. 1. Rating data of 34 people for neutral, leisure, surreal, and adventure pictures (A), ERP component data ((B) P300, (C) late positive potential) and rating data ((D) valence, (E) arousal, and (F) approach/avoidance) as a function of category for high sensation seekers (HSSs) and low sensation seekers (LSSs). Standard errors are also shown.

hang-gliding; the surreal pictures depicted people’s activities that were ambiguous, incongruous, or unfamiliar (Furnham & Avison, 1997); the leisure pictures depicted people’s leisure activities such as fishing, doing yoga, and playing chess. The neural pictures depicted people’s daily activities such as washing, taking the elevator, and answering telephone. Second, 360 pictures (90 each category) were selected by the first and second authors from the 1670 pictures on the basis of having a figure-ground composition with people and excluding content associated with violence and sex. Thirty-four undergraduates (17 females and 17 males) then gave their valence, arousal, and approach/avoidance ratings for each picture via a computerized version of the self-assessment manikin (Bradley & Lang, 1994). Following the methodology of Briggs and Martin (2009), the approach/avoidance appraisal instructed the participants to think of themselves in relation to each picture and to rate the degree to which they would desire to be or avoid being the person in the image. Third, a final set of stimuli, including 25 adventure, 25 surreal, 25 leisure, and 25 neutral pictures, was selected for the current ERP experiment on basis of their arousal and valence ratings of the 360 pictures, in order to vary systematically arousal level while match valence level for the adventure (high-arousing), surreal (medium-arousing), and leisure (low-arousing) pictures. Fig. 1A shows the rating data for each of the four picture categories that varied in valence, arousal, and approach/avoidance (a 9-point scale). Emotional valence varied as a function of picture category, F(3, 72) = 45.06, p < .00001, p 2 = .65. Adventure, surreal, and leisure pictures were rated as more pleasant compared to neutral pictures (ps < .00001), but did not differ from each other (ps > .95). Likewise, emotional arousal varied as a function of picture category, F(3, 72) = 374.17, p < .000001, p 2 = .94. Adventure pictures were rated as more emotionally arousing compared to surreal, leisure, and neutral pictures (ps < .001), followed by surreal (compared to leisure and neutral pictures, ps < .001) and leisure (compared to neutral pictures, p < .001) pictures. For approach/avoidance ratings, the main effect of category was significant, F(3, 72) = 27.75, p < .001, p 2 = .54. People tended to approach leisure pictures than the other categories (ps < .05), followed by adventure and surreal pictures (compared to neutral pictures, ps < .001) with no significant difference between adventure and surreal pictures (p > .95).

2.3. Procedure Subsequent to electrode application, participants were seated in a reclining chair in a sound-attenuated and dimly lit chamber. The participants were then instructed that a series of pictures would be displayed and that they should pay close attention to the content of each picture during each presentation, keeping their eyes comfortably focused on the center of a cathode ray tube (CRT) monitor. The total 100 pictures were delivered randomly and, thereafter, were presented randomly again to yield 50 trials for each category. Each picture was displayed in color at the center of the monitor with a light gray background and viewed from a distance of approximately 75 cm, subtending a visual angle of 7.27◦ horizontally and 6.06◦ vertically. Each trial began with a 1000-ms fixation cross in the center of the screen. A picture then was presented for 1500 ms, followed by an inter-trial interval of 1000 ms. The entire experimental task comprised of 200 trails with breaks after every 40 trials. A brief training block was provided prior to the formal experiment to accommodate the participants to the task. The training block adopted six pictures that were not included in the formal experiment. Following the completion of electroencephalographic acquisition, the 100 pictures were presented again and participants were asked to rate each picture on the level of valence, arousal, and approach/avoidance tendency, using the computerized modification of the self-assessment manikin described above. 2.4. Data recording and analysis The electroencephalogram (EEG) was recorded from a set of 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), which were equipped in an elastic cap based on the extended 10/20 system. The signals were recorded using a left mastoid reference electrode, and then re-referenced offline to the average of the left and right mastoids (Luck, 2014). The electrooculogram (EOG) generated from eye movements and eye blinks was recorded via two pairs of additional tin electrodes: horizontal EOG was measured via one pair of electrodes placed above and below the

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Fig. 2. ERPs for neutral, leisure, surreal, and adventure pictures over parietal regions (averaged across P3, Pz, and Pz sites), where shaded areas depict the P300 time window. The topographic maps (300–400 ms) of the P300 are also presented.

left eye; vertical EOG was measured via the other pair of electrodes located approximately 1 cm outside the outer edge of both eyes. The EEG and EOG were amplified via a NeuroScan NuAmps amplifier and digitized with a band-pass of .1–100 Hz and a sampling rate of 500 Hz. Electrode impedance was kept below 5 K throughout the experiment. The EEG data were preprocessed and analyzed using Matlab 2012b (MathWorks, US) and EEGLAB toolbox (Delorme & Makeig, 2004). Continuous EEG data were low-pass filtered at 20 Hz with a linear digital finite impulse response filter (designed using FWTGEN V3.8, Cook & Miller, 1992) and then were screened manually for artifacts (e.g., spikes, drifts, and nonbiological signals). Following which EEG data was epoched beginning 200 ms prior to the picture onset and continuing for 1200 ms with the activity from −200 to 0 ms serving as the baseline. The epoched data for each participant were subjected to an infomax independent component analysis (runica) (Delorme & Makeig, 2004; Jung et al., 2001) and blink components were manually selected and removed. In all dataset, the blink components had a large EOG channel contribution and a frontal scalp distribution. For the resulting data, epoches belonging to the same picture category were averaged together for each participant. Preliminary analysis on the number of the accepted ERP trials (Table 1) revealed no significant group or picture category effect (ps > .3). Statistical analyses were performed by averaging a cluster of electrodes over the regions where each ERP component exhibited its maximal amplitude (Luck, 2014). The P300 was scored as the mean activity over parietal electrode sites (P3, Pz, and P4) in the time interval from 300 to 400 ms following the picture onset. The LPP was measured as the mean activity over centroparietal electrode sites (CP3, CPz, and CP4) in the time window of 500–1000 ms following the picture onset. All the ERP data were analyzed in separate mixed-model analysis of variance (ANOVA), using group (HSSs vs. LSSs) as a between-subjects factor and category (adventure, surreal, leisure, and neutral) as a within-subjects factor. Greenhouse–Geisser epsilon correction was applied for

non-sphericity when necessary (Jennings & Wood, 1976). The partial eta-squared (p 2 ) was reported as a measure of the proportion between the variance explained by one experimental factor and the total variance. Post-hoc pairwise comparisons were performed by using a t-test procedure with the Bonferroni correction. 3. Results 3.1. Electrophysiological data Fig. 2 depicts the grand-average ERPs over parietal electrode sites and topographic maps (300–400 ms) of the P300 in response to each picture category. Grand-average ERPs over centroparietal electrode sites and topographic maps (500–1000 ms) of the LPP for each picture category are presented in Fig. 3. 3.1.1. P300 As shown in Fig. 2, the P300 peaks between 300 and 400 ms and is maximal over the parietal sites. The overall amplitude of the P300 differed as a function of category, F(3, 90) = 24.33, p < .00001, p 2 = .45. The P300 was larger for adventure (p < .0001), surreal (p < .0001), and leisure (p < .001) pictures than that for neutral pictures. In addition, adventure pictures elicited a larger P300 compared to leisure pictures (p = .022). Likewise, the P300 varied as a function of group, F(1, 30) = 5.78, p = .023, p 2 = .16, such that HSSs had significantly reduced P300 compared to LSSs. Importantly, there was a significant interaction between category and group, F(3, 90) = 3.10, p = .041, p 2 = .09. Post-hoc comparison (Fig. 1B) showed that the group effect was significant for adventure (p = .024) and surreal (p = .011) pictures, but not for leisure (p = .063) and neutral pictures (p = .065). For HSSs, the P300 was significantly larger for adventure (p = .016) and leisure (p = .007) pictures compared to neutral pictures. For LSSs, the P300 was larger for adventure (p < .0001), surreal (p < .001), and leisure (p < .0001) pictures compared to neutral pictures, with no significant differences between adventure, surreal, and leisure pictures (ps > .5).

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Fig. 3. ERPs for neutral, leisure, surreal, and adventure pictures over centroparietal regions (averaged across CP3, CPz, and CP4 sites), where shaded areas depicted the LPP time window. The topographic maps (500–1000 ms) of the LPP are also presented.

3.1.2. LPP As shown in Fig. 3, the LPP is maximal over the centroparietal electrode sites. Like P300, the overall amplitude of the LPP differed as a function of category, F(3, 90) = 26.90, p < .000001, p 2 = .47. The LPP was significantly enhanced in response to adventure and surreal pictures compared to leisure (ps < .005) and neutral (ps < .00001) pictures, but did not differ between adventure and surreal pictures (p > .95). In addition, the LPP was significantly larger for leisure compared to neutral pictures (p < .001). The amplitude of the LPP did not vary as a function of group (Fig. 1C), F(1, 30) = .04, p = .853, p 2 = .01. Likewise, there was no significant interaction between category and group, F(3, 90) = 1.93, p = .143, p 2 = .06. 3.1.3. Repetition effect In the ERP experiment, since each picture was presented twice and since sensation seeking is associated with fast habituation (Zuckerman, 1990), it is possible that HSSs found the task boring because not novel and, after initial reactivity to the images, stopped to pay attention to the pictures. Thus, faster habituation in HSSs might be a confounding variable that affected the P300 and LPP results in sensation seeking. To clarify the effect of repetition on the ERP findings, we conducted a Group × Category × Repetition (first vs. second) ANOVA separately for the P300 and LPP components. For both the two components, although repetition seemed to enhance the amplitudes for the P300, F(1, 30) = 3.97, p = .056, p 2 = .12, and for the LPP, F(1, 30) = 3.59, p = .068, p 2 = .11, it did not interact with group (ps > .1). Therefore, the P300 and LPP results were not affected by the repetition of picture.

3.2. Self-reported data Fig. 1D–F presents the self-report ratings of valence, arousal, and approach/avoidance for each of the four picture categories as a function of sensation seeking.

3.2.1. Valence ratings There was no group difference for valence ratings, F(1, 30) = .30, p = .590, p 2 = .01. The main effect of category was significant, F(3, 90) = 25.67, p < .001, p 2 = .46, which was qualified by a significant interaction between category and group, F(3, 90) = 7.89, p = .001, p 2 = .21. Post-hoc comparison indicated that HSSs reported higher valence experience to adventure, surreal, and leisure pictures compared to neutral pictures (ps < .001), as well as higher valence experience to surreal compared to leisure pictures (p = .027) with no other differences obtained (ps > .05). By contrast, LSSs reported higher valence experience to leisure (p < .001) and surreal (p = .002) pictures compared to neutral pictures with no other differences obtained (ps > .05). 3.2.2. Arousal ratings There was no group difference for arousal ratings, F(1, 30) = .1, p = .985, p 2 = .01. There were significant effects for category, F(3, 90) = 56.09, p < .00001, p 2 = .65) and for the interaction of category and group, F(3, 90) = 6.41, p = .004, p 2 = .18. HSSs reported higher arousal experience to adventure pictures compared to the other three categories (ps < .003), followed by surreal pictures (compared to leisure and neutral pictures, ps < .001) and leisure pictures (compared to neutral pictures, p = .003). In contrast, LSSs reported higher arousal experience to adventure pictures compared to leisure and neutral pictures (ps < .05) with no difference between adventure and surreal pictures (p = .734), and higher arousal experience to both surreal and leisure pictures compared to neutral pictures (ps < .004) with no difference between surreal and leisure pictures (p = .173). 3.2.3. Approach/avoidance ratings The main effect of group was marginally significant, F(1, 30) = 3.31, p = .079, p 2 = .10. There were significant effects for category, F(3, 90) = 19.58, p < .00001, p 2 = .40, and for the category × group interaction, F(3, 90) = 17.93, p < .00001, p 2 = .37. HSSs reported higher on the level of approach to adventure pictures

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compared to leisure and neutral pictures (ps < .05) but no difference between adventure and surreal pictures (p = .358), and higher to surreal and leisure pictures compared to neutral pictures (ps < .001). In contrast, LSSs reported higher on the level of approach to leisure pictures compared to adventure and neutral pictures (ps < .001) and higher to surreal compared to adventure pictures (p = .007) with no other differences obtained (ps > .10).

4. Discussion The current study examined the cognitive processing of emotionally arousing pictures (i.e., adventure, surreal, and leisure pictures) in sensation seeking as indexed by the P300 and LPP components. The emotionally arousing pictures varied as a function of arousal ratings while were relatively well matched on valence ratings. Importantly, they were created on the basis of the items in the sensation-seeking scale. Specifically, adventure and surreal pictures depicted activities preferred by HSSs, whereas leisure pictures depicted activities preferred by LSSs. Emotional arousal has been shown to primarily modulate the P300 and LPP components in previous research (Olofsson et al., 2008). Although both the P300 and LPP have been linked to motivational attention, recent evidence has emphasized their distinct functional significances (Foti, Hajcak, & Dien, 2009; Weinberg & Hajcak, 2011). Whereas the P300 reflects the initial allocation of attentional resources, the LPP indexes more elaborated processing such as memory encoding and storage, cognitive reappraisal, and behavioral interference (Hajcak et al., 2012). Consistent with previous research (e.g., Cuthbert et al., 2000; Schupp et al., 2000), the P300 and LPP elicited by emotionally arousing pictures were larger than those elicited by neutral pictures. Moreover, both the P300 and LPP varied as a function of arousal level (Hajcak et al., 2012; Olofsson et al., 2008). Specifically, adventure pictures elicited a larger LPP compared to leisure and neutral pictures, which is in line with previous studies (Kuhr, Schomberg, Gruber, & Quirin, 2013; van Lankveld & Smulders, 2008) but at variance with other research observing that the LPP to sport stimuli was not different from (Briggs & Martin, 2009), or even smaller than (Weinberg & Hajcak, 2010), neutral stimuli. However, it should be noted that adventure stimuli employed in the current experiment consisted of various extreme sport pictures, which appear to signal some degrees of danger. In contrast, the sport stimuli adopted in previous research included not only extreme sport pictures, but also daily sport pictures depicting running, even people’s congratulations (Briggs & Martin, 2009; Weinberg & Hajcak, 2010), which may dilute the LPP amplitude. Moreover, surreal pictures elicited a comparable P300, but a larger LPP compared to leisure pictures. This finding suggests that although surreal and leisure pictures attracted comparable attentional resources at the P300 stage (300–400 ms), more deliberative cognitive process came into play at the LPP stage (500–1000 ms) such that the finer-gained distinction between surreal and leisure pictures occurred (Foti et al., 2009; Weinberg & Hajcak, 2010). In terms of the relationship between ERP amplitudes and arousal ratings, there were some similarities and discrepancies as observed in previous research (Cuthbert et al., 2000; Weinberg & Hajcak, 2010). For example, adventure stimuli were rated as the most arousing and also elicited the largest P300 and LPP, whereas neutral stimuli were rated the least arousing and also resulted in the smallest P300 and LPP. However, we failed to observe other corresponding between the self-report ratings of arousal and the P300 or LPP. These discrepancies can be understandable given that arousal is not a simple universal construct (Zuckerman & Como, 1983). Indeed, recent evidence has demonstrated the P300 and LPP differences between different picture categories despite their similar

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self-reported ratings of arousal (Briggs & Martin, 2009; Weinberg & Hajcak, 2010). As expected, at the psychometrical level, although adventure, surreal, and leisure pictures were relatively well matched on the valence ratings of a pretest run, HSSs rated both adventure and surreal pictures more pleasantly compared to neutral pictures, whereas LSSs gave higher pleasant ratings both to leisure and surreal pictures compared to neutral pictures. Similarly, HSSs displayed the highest approach level to adventure and surreal stimuli, whereas LSSs showed the highest approach level to leisure stimuli. These patterns are consistent with the behavioral preferences observed in the real world: HSSs tend to approach novel and intense stimuli to maintain his/her arousal level at a higher optimal level, whereas LSSs tend to keep themselves away from danger and prefer weak or familiar stimuli (Zuckerman, 1994). Our findings therefore indicate that the stimuli employed here capture the sensationseeking trait to some extent and thus, in conjunction with previous findings (Furnham & Avison, 1997; Rawlings, 2003), validate the sensation-seeking scale at the psychometrical level. Since previous research has indicated more excitable central nervous systems for HSSs (Zuckerman, 1984), it follows that sensation seeking should correlate with enhanced ERP responses to stimuli with highly emotional arousal (Zuckerman, 1984). Surprisingly, HSSs relative to LSSs exhibited a reduced P300 for high-arousing (adventure) and medium-arousing (surreal) stimuli, but not for low-arousing (leisure and neutral) stimuli. As the P300 is thought to reflect the allocation of attentional resources based on the motivational significance of a stimulus (Nieuwenhuis, AstonJones, & Cohen, 2005), our finding indicates that HSSs relative to LSSs might direct less attentional resources to high-arousing stimuli. In this regard, the P300 finding fails to support the hypothesis of more excitable central nervous systems in sensation seeking (Zuckerman, 1984). On the contrary, this finding provides some support for the optimal arousal hypothesis. According to this hypothesis (Zuckerman, 1969), HSSs need more novel and intense sensation to reach and maintain a higher optimal level compared to LSSs. Therefore, a level of stimulation preferred by LSSs may fail to reach the optimal level of stimulation for HSSs. Accordingly, HSSs compared to LSSs displayed reduced neural responses to emotional stimuli with high arousal. However, this still is unsatisfied in that there were no group differences for low-arousing stimuli. Besides the optimal level of arousal hypothesis, we propose that the P300 findings may be interpreted by a reduced sensitivity to risk in sensation seeking, which is driven by a hypoactive avoidance system. Previous studies have demonstrated that for individuals with high sensation seeking, the rewards of the varied, novel, complex, and intense sensations outweigh the negative consequences of engaging in sensation-seeking behaviors, as an expression of a hyperactive approach system in sensation seeking (Joseph et al., 2009; Zuckerman, 1990, 1994). However, recent data are more supportive of a hypoactive avoidance system in sensation seeking (Kruschwitz, Simmons, Flagan, & Paulus, 2012; Lissek et al., 2005; Zheng, Sheng, Xu, & Zhang, 2014). For example, HSSs compared to LSSs show a reduced negative bias (Zheng et al., 2011), a blunted response to error (Santesso & Segalowitz, 2009; Zheng et al., 2014), an insensitivity to punishment when performing a risky decision-making (Kruschwitz et al., 2012), and diminished physiologically anxious responses in the face of threatening stimuli (Lissek & Powers, 2003) and during the anticipation of aversive stimuli (Lissek et al., 2005). Moreover, when looking at the valence rating data (Fig. 1D), it is clear that HSSs gave higher valence ratings for high-arousing versus low-arousing stimuli, whereas LSSs gave higher valence ratings to low-arousing versus high-arousing stimuli. In conjunction with these findings, our results suggest that sensation seeking may be associated with a decreased sensitivity

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to risk, which seems to be driven by a hypoactive avoidance system rather than a hyperactive approach system. An interesting finding in the present study is that there were discrepancies between the ERP findings and rating data in sensation seeking. For example, whereas HSSs compared to LSSs subjectively reported experiencing higher approach levels to high-arousing stimuli, objective measures, like the P300 and LPP, did not reflect these group differences. The inconsistency between the electrophysiological and psychometrical measurements was also reported in previous studies (e.g., Horan, Wynn, Kring, Simons, & Green, 2010; Weinberg & Hajcak, 2010). One possibility is associated with the ERP task adopted in the current study, which is a passive viewing task without any explicit emotional processing. In contrast, the rating data were obtained by requiring participants to explicitly rate their valence, arousal, and approach/avoidance. Thus, the preference for high-arousing stimuli among HSSs, as reflected in the rating data, may be evident at the level of response output. One possible limitation of this study is related to the stimulus selection. Due to the limited range of adventure and surreal stimuli in existing picture systems such as the International Affective Picture System, we created many of our pictures in-house. Although we carefully performed a pretest run with 34 undergraduates, it is still possible that our results are somewhat specific to these stimuli. Therefore, this work requires replication using a similar stimulus set. To summarize, our results demonstrated that sensation seeking is associated with a diminished P300 to high-arousing stimuli that may incur physical risk, despite a preference for these stimuli. Future research should focus on other types of risk that associated with sensation seeking such as social risk (e.g., sexual promiscuity), financial risk (e.g., excessive gambling), and legal risk (e.g., getting arrested and put in jail), in order to understand the neurobiological basis of sensation seeking and thus optimize prevention programs targeting for sensation-seeking behaviors (Everett & Palmgreen, 1995; Perry et al., 2011). Acknowledgements This work was supported by the Construction Project of Key Medical Specialty, Liaoning Province, China. The authors have declared that no competing interests exist. The authors thank Dr. John Allen for providing a MATLAB script to process the EEG data. References Bai, L., Ma, H., Huang, Y. X., & Luo, Y. J. (2005). The development of native Chinese affective picture system: A pretest in 46 college students. Chinese Mental Health Journal, 19(11), 719–722. Balconi, M., Falbo, L., & Conte, V. A. (2012). BIS and BAS correlates with psychophysiological and cortical response systems during aversive and appetitive emotional stimuli processing. Motivation and Emotion, 36(2), 218–231. http://dx.doi.org/10.1007/s11031-011-9244-7 Bardo, M. T., Williams, Y., Dwoskin, L. P., Moynahan, S. E., Perry, I. B., & Martin, C. A. (2007). The sensation seeking trait and substance use: Research findings and clinical implications. Current Psychiatry Reviews, 3(1), 3–13. http://dx.doi.org/10.2174/157340007779815682 Benjamin, J., Ebstein, R. P., & Belmaker, R. H. (2001). Genes for human personality traits: Endophenotypes of psychiatric disorders? World Journal of Biological Psychiatry, 2(2), 54–57. http://dx.doi.org/10.3109/15622970109027494 Bradley, M. M., & Lang, P. J. (1994). Measuring emotion: The self-assessment manikin and the semantic differential. Journal of Behavior Therapy and Experimental Psychiatry, 25(1), 49–59. http://dx.doi.org/10.1016/0005-7916(94)90063-9 Briggs, K. E., & Martin, F. H. (2009). Affective picture processing and motivational relevance: Arousal and valence effects on ERPs in an oddball task. International Journal of Psychophysiology, 72(3), 299–306. http://dx.doi.org/ 10.1016/j.ijpsycho.2009.01.009 Brocke, B., Beauducel, A., John, R., Debener, S., & Heilemann, H. (2000). Sensation seeking and affective disorders: Characteristics in the intensity dependence of acoustic evoked potentials. Neuropsychobiology, 41(1), 24–30, 26629. Cook, E. W., III, & Miller, G. A. (1992). Digital filtering: Background and tutorial for psychophysiologists. Psychophysiology, 29(3), 350–367. http://dx.doi.org/ 10.1111/j. 1469-8986.1992.tb01709.x

Cuthbert, B. N., Schupp, H. T., Bradley, M. M., Birbaumer, N., & Lang, P. J. (2000). Brain potentials in affective picture processing: Covariation with autonomic arousal and affective report. Biological Psychology, 52(2), 95–111. http://dx.doi.org/10.1016/S0301-0511(99)00044-7 De Pascalis, V. (2004). On the psychophysiology of extraversion. In R. M. Stelmack (Ed.), On the psychobiology of personality: Essays in honor of Marvin Zuckerman (pp. 295–327). Amsterdam: Elsevier. De Pascalis, V., Strippoli, E., Riccardi, P., & Vergari, F. (2004). Personality, eventrelated potential (ERP) and heart rate (HR) in emotional word processing. Personality and Individual Differences, 36(4), 873–891. http://dx.doi.org/ 10.1016/S0191-8869(03)00159-4 De Pascalis, V., Varriale, V., & D’Antuono, L. (2010). Event-related components of the punishment and reward sensitivity. Clinical Neurophysiology, 121(1), 60–76. http://dx.doi.org/10.1016/j.clinph.2009.10.004 Delorme, A., & Makeig, S. (2004). EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods, 134(1), 9–21. http://dx.doi.org/ 10.1016/j.jneumeth.2003.10.009 Dolcos, F., & Cabeza, R. (2002). Event-related potentials of emotional memory: Encoding pleasant, unpleasant, and neutral pictures. Cognitive, Affective and Behavioral Neuroscience, 2(3), 252–263. http://dx.doi.org/10.3758/CABN.2.3.252 Dvorak, R. D., Simons, J. S., & Wray, T. B. (2011). Poor control strengthens the association between sensation seeking and disgust reactions. Journal of Individual Differences, 32(4), 219–224. http://dx.doi.org/10.1027/1614-0001/A000054 Everett, M. W., & Palmgreen, P. (1995). Influences of sensation seeking, message sensation value, and program context on effectiveness of anticocaine public service announcements. Health Communication, 7(3), 225–248. http://dx.doi.org/10.1207/s15327027hc0703 3 Eysenck, H. J. (1967). The biological basis of personality. Springfield, IL: Thomas. Foti, D., Hajcak, G., & Dien, J. (2009). Differentiating neural responses to emotional pictures: Evidence from temporal-spatial PCA. Psychophysiology, 46(3), 521–530. http://dx.doi.org/10.1111/j. 1469-8986.2009.00796.x Furnham, A., & Avison, M. (1997). Personality and preference for surreal paintings. Personality and Individual Differences, 23(6), 923–935. http://dx.doi.org/ 10.1016/S0191-8869(97)00131-1 Gottesman, I. I., & Gould, T. D. (2003). The endophenotype concept in psychiatry: Etymology and strategic intentions. The American Journal of Psychiatry, 160(4), 636–645. http://dx.doi.org/10.1176/appi.ajp.160.4.636 Hajcak, G., & Nieuwenhuis, S. (2006). Reappraisal modulates the electrocortical response to unpleasant pictures. Cognitive, Affective and Behavioral Neuroscience, 6(4), 291–297. Hajcak, G., Weinberg, A., MacNamara, A., & Foti, D. (2012). ERPs and the study of emotion. In S. J. Luck, & E. S. Kappenman (Eds.), The oxford handbook of event-related potential components (pp. 441–474). New York, NY, USA: Oxford University Press. Harris, N., Newby, J., & Klein, R. G. (2013). Competitiveness facets and sensation seeking as predictors of problem gambling among a sample of University Student Gamblers. Journal of Gambling Studies, http://dx.doi.org/ 10.1007/s10899-013-9431-4 Hegerl, U., Gallinat, J., & Mrowinski, D. (1995). Sensory cortical processing and the biological basis of personality. Biological Psychiatry, 37(7), 467–472. http://dx.doi.org/10.1016/0006-3223(94)00177-5 Horan, W. P., Wynn, J. K., Kring, A. M., Simons, R. F., & Green, M. F. (2010). Electrophysiological correlates of emotional responding in schizophrenia. Journal of Abnormal Psychology, 119(1), 18–30. http://dx.doi.org/10.1037/a0017510 Hoyle, R. H., Fejfar, M. C., & Miller, J. D. (2000). Personality and sexual risk taking: A quantitative review. Journal of Personality, 68(6), 1203–1231. http://dx.doi.org/10.1111/1467-6494.00132 Jennings, J. R., & Wood, C. C. (1976). The ␧-adjustment procedure for repeated-measures analyses of variance. Psychophysiology, 13(3), 277–278. http://dx.doi.org/10.1111/j. 1469-8986.1976.tb00116.x Jonah, B. A. (1997). Sensation seeking and risky driving: A review and synthesis of the literature. Accident Analysis and Prevention, 29(5), 651–665. http://dx.doi.org/10.1016/S0001-4575(97)00017-1 Joseph, J. E., Liu, X., Jiang, Y., Lynam, D., & Kelly, T. H. (2009). Neural correlates of emotional reactivity in sensation seeking. Psychological Science, 20(2), 215–223. http://dx.doi.org/10.1111/j. 1467-9280.2009.02283.x Jung, T. P., Makeig, S., Westerfield, M., Townsend, J., Courchesne, E., & Sejnowski, T. J. (2001). Analysis and visualization of single-trial event-related potentials. Human Brain Mapping, 14(3), 166–185. http://dx.doi.org/10.1002/hbm.1050 Kruschwitz, J. D., Simmons, A. N., Flagan, T., & Paulus, M. P. (2012). Nothing to lose: Processing blindness to potential losses drives thrill and adventure seekers. NeuroImage, 59(3), 2850–2859. http://dx.doi.org/10.1016/ j.neuroimage.2011.09.048 Kuhr, B., Schomberg, J., Gruber, T., & Quirin, M. (2013). Beyond pleasure and arousal: Appetitive erotic stimuli modulate electrophysiological brain correlates of early attentional processing. NeuroReport, 24(5), 246–250. http://dx.doi.org/10.1097/WNR.0b013e32835f4eba Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (1997). Motivated attention: Affect, activation, and action. In P. J. Lang, R. F. Simons, & M. T. Balaban (Eds.), Attention and orienting: Sensory and motivational processes (pp. 97–135). Hillsdale, NJ: Erlbaum. Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (2005). International affective picture system (IAPS): Affective ratings of pictures and instruction manual (Tech. Rep. No. A-6). Gainesville, FL: University of Florida. Lissek, S., Baas, J. M., Pine, D. S., Orme, K., Dvir, S., Rosenberger, E., et al. (2005). Sensation seeking and the aversive motivational system. Emotion, 5(4), 396–407. http://dx.doi.org/10.1037/1528-3542.5.4.396

Y. Zheng et al. / Biological Psychology 107 (2015) 44–51 Lissek, S., & Powers, A. S. (2003). Sensation seeking and startle modulation by physically threatening images. Biological Psychology, 63(2), 179–197. http://dx.doi.org/10.1016/S0301-0511(03)00053-X Luck, S. J. (2014). An introduction to the event-related potential technique (2nd ed.). Cambridge, MA: MIT Press. Matthews, G., & Gilliland, K. (1999). The personality theories of H. J. Eysenck and J. A. Gray: A comparative review. Personality and Individual Differences, 26(4), 583–626, 10.1016/S0191-8869(98)00158-5. Nieuwenhuis, S., Aston-Jones, G., & Cohen, J. D. (2005). Decision making, the P3, and the locus coeruleus-norepinephrine system. Psychological Bulletin, 131(4), 510–532. http://dx.doi.org/10.1037/0033-2909.131.4.510 Olofsson, J. K., Nordin, S., Sequeira, H., & Polich, J. (2008). Affective picture processing: An integrative review of ERP findings. Biological Psychology, 77(3), 247–265. http://dx.doi.org/10.1016/j.biopsycho.2007.11.006 Ortin, A., Lake, A. M., Kleinman, M., & Gould, M. S. (2012). Sensation seeking as risk factor for suicidal ideation and suicide attempts in adolescence. Journal of Affective Disorders, 143(1–3), 214–222. http://dx.doi.org/10.1016/j.jad.2012.05.058 Perry, J. L., Joseph, J. E., Jiang, Y., Zimmerman, R. S., Kelly, T. H., Darna, M., et al. (2011). Prefrontal cortex and drug abuse vulnerability: Translation to prevention and treatment interventions. Brain Research Reviews, 65(2), 124–149. http://dx.doi.org/10.1016/j.brainresrev.2010.09.001 Rawlings, D. (2003). Personality correlates of liking for ‘unpleasant’ paintings and photographs. Personality and Individual Differences, 34(3), 395–410. http://dx.doi.org/10.1016/s0191-8869(02)00062-4 Ruedl, G., Abart, M., Ledochowski, L., Burtscher, M., & Kopp, M. (2012). Self reported risk taking and risk compensation in skiers and snowboarders are associated with sensation seeking. Accident Analysis and Prevention, 48, 292–296. http://dx.doi.org/10.1016/j.aap.2012.01.031 Santesso, D. L., & Segalowitz, S. J. (2009). The error-related negativity is related to risk taking and empathy in young men. Psychophysiology, 46(1), 143–152. http://dx.doi.org/10.1111/j. 1469-8986.2008.00714.x Schupp, H. T., Cuthbert, B. N., Bradley, M. M., Cacioppo, J. T., Ito, T., & Lang, P. J. (2000). Affective picture processing: The late positive potential is modulated by motivational relevance. Psychophysiology, 37(2), 257–261. http://dx.doi.org/10.1017/S0048577200001530 Schupp, H. T., Flaisch, T., Stockburger, J., & Junghofer, M. (2006). Emotion and attention: Event-related brain potential studies. Progress in Brain Research, 156, 31–51. http://dx.doi.org/10.1016/S0079-6123(06)56002-9 Simon, J. J., Walther, S., Fiebach, C. J., Friederich, H. C., Stippich, C., Weisbrod, M., et al. (2010). Neural reward processing is modulated by approachand avoidance-related personality traits. NeuroImage, 49(2), 1868–1874. http://dx.doi.org/10.1016/j.neuroimage.2009.09.016 Smith, B. D., Davidson, R. A., Perlstein, W., & Gonzalez, F. (1990). Sensationseeking: Electrodermal and behavioral effects of stimulus content and intensity. International Journal of Psychophysiology, 9(2), 179–188. http://dx.doi.org/10.1016/0167-8760(90)90072-L Smith, B. D., Davidson, R. A., Smith, D. L., Goldstein, H., & Perlstein, W. (1989). Sensation seeking and arousal: Effects of strong stimulation of electrodermal activation and memory task performance. Personality and Individual Differences, 10(6), 671–679. http://dx.doi.org/10.1016/0191-8869(89)90226-2 Smith, B. D., Perlstein, W. M., Davidson, R. A., & Michael, K. (1986). Sensation seeking: Differential effects of relevant, novel stimulation on

51

electrodermal activity. Personality and Individual Differences, 7(4), 445–452. http://dx.doi.org/10.1016/0191-8869(86)90122-4 Straube, T., Preissler, S., Lipka, J., Hewig, J., Mentzel, H. J., & Miltner, W. H. R. (2010). Neural representation of anxiety and personality during exposure to anxietyprovoking and neutral scenes from scary movies. Human Brain Mapping, 31(1), 36–47. http://dx.doi.org/10.1002/hbm.20843 Sutton, S., Braren, M., Zubin, J., & John, E. R. (1965). Evoked-potential correlates of stimulus uncertainty. Science, 150(3700), 1187–1188. http://dx.doi.org/ 10.1126/science.150.3700.1187 van Lankveld, J. J., & Smulders, F. T. (2008). The effect of visual sexual content on the event-related potential. Biological Psychology, 79(2), 200–208. http://dx.doi.org/10.1016/j.biopsycho.2008.04.016 Wang, W., Wu, Y. X., Peng, Z. G., Lu, S. W., Yu, L., Wang, G. P., et al. (2000). Test of sensation seeking in a Chinese sample. Personality and Individual Differences, 28(1), 169–179. http://dx.doi.org/10.1016/S0191-8869(99)00092-6 Weinberg, A., & Hajcak, G. (2010). Beyond good and evil: The time-course of neural activity elicited by specific picture content. Emotion, 10(6), 767–782. http://dx.doi.org/10.1037/a0020242 Weinberg, A., & Hajcak, G. (2011). The late positive potential predicts subsequent interference with target processing. Journal of Cognitive Neuroscience, 23(10), 2994–3007. http://dx.doi.org/10.1162/jocn.2011.21630 Wilson, L. C., & Scarpa, A. (2011). The link between sensation seeking and aggression: A meta-analytic review. Aggressive Behavior, 37(1), 81–90. http://dx.doi.org/ 10.1002/ab.20369 Zaleski, Z. (1984). Sensation-seeking and preference for emotional visual stimuli. Personality and Individual Differences, 5(5), 609–611. http://dx.doi.org/ 10.1016/0191-8869(84)90040-0 Zheng, Y., Sheng, W., Xu, J., & Zhang, Y. (2014). Sensation seeking and error processing. Psychophysiology, 51(9), 824–833. http://dx.doi.org/ 10.1111/psyp.12240 Zheng, Y., Xu, J., Jia, H., Tan, F., Chang, Y., Zhou, L., et al. (2011). Electrophysiological correlates of emotional processing in sensation seeking. Biological Psychology, 88(1), 41–50. http://dx.doi.org/10.1016/j.biopsycho.2011.06.006 Zuckerman, M. (1969). Theoretical formulations: I. In J. P. Zubek (Ed.), Sensory deprivation: Fifteen years of research (pp. 407–432). New York, NY: AppletonCentury-Crofts. Zuckerman, M. (1984). Sensation seeking—A comparative approach to a human trait. Behavioral and Brain Sciences, 7(3), 413–434. http://dx.doi.org/ 10.1017/S0140525X00018938 Zuckerman, M. (1990). The psychophysiology of sensation seeking. Journal of Personality, 58(1), 313–345. http://dx.doi.org/10.1111/j. 1467-6494.1990.tb00918.x Zuckerman, M. (1994). Behavioral expressions and biosocial bases of sensation seeking. New York, NY: Cambridge University Press. Zuckerman, M., & Como, P. (1983). Sensation seeking and arousal systems. Personality and Individual Differences, 4(4), 381–386. http://dx.doi.org/ 10.1016/0191-8869(83)90003-x Zuckerman, M., Eysenck, S., & Eysenck, H. J. (1978). Sensation seeking in England and America: Cross-cultural, age, and sex comparisons. Journal of Consulting and Clinical Psychology, 46(1), 139–149. http://dx.doi.org/10.1037/0022-006X.46.1.139 Zuckerman, M., Murtaugh, T., & Siegel, J. (1974). Sensation seeking and cortical augmenting-reducing. Psychophysiology, 11(5), 535–542. http://dx.doi.org/ 10.1111/j. 1469-8986.1974.tb01109.x