This is the first fMRI study to characterize the neurobiological profile of emotional arousal and reactivity in sensation seeking. Previous research has shown that HSSs, compared with LSSs, show greater reactivity to intense stimuli (Smith et al., 1990
; Zuckerman, 2005
) and weaker avoidance responses to stressors (Lissek et al., 2005
; Roberti, 2004
). Such outcomes may be understood within a framework in which HSSs tend to have overactive approach systems and dampened avoidance systems (A. Lang et al., 2005
). The present findings are consistent with this framework in that fMRI responses to high-arousal stimuli were stronger in HSSs than in LSSs in brain regions associated with arousal and reinforcement, including the insula and posterior medial OFC. In contrast, HSSs did not activate regions involved in emotional regulation, behavioral monitoring, and decision making (e.g., anterior cingulate and anterior medial OFC) as strongly or as early as LSSs did. Moreover, HSSs were not as sensitive to the valence of the stimuli as were LSSs. The propensity for arousal in HSSs may override the valence or content of the arousing material. These differences between the sensation-seeking groups may reflect a stronger arousal focus in HSSs and a stronger valence focus in LSSs (Feldman, 1995
). The present study not only has outlined a core network of brain regions involved in emotional reactivity and regulation, but also has demonstrated that these components are differentially modulated by sensation seeking and related personality dimensions.
HSSs strongly activated brain regions involved in reinforcement (posterior medial OFC) and arousal (right anterior insula). In response to high-arousal stimuli, HSSs activated the posterior medial OFC more strongly than did LSSs, but the Arousal × Sensation Seeking interaction was only marginally significant. This region is often associated with the presentation of primary reinforcers, such as taste and pain, regardless of their reward value (Kringelbach & Rolls, 2004
). The right anterior insula was also more strongly activated in HSSs than in LSSs for high-arousal stimuli. Strong neurobiological and neuroanatomical evidence supports the view that the right anterior insula may be a somatic marker for arousal and sympathetic stress responses (Craig, 2005
; Critchley, Melmed, Featherstone, Mathias, & Dolan, 2002
; Paulus et al., 2003
; Zuckerman, 2005
). In addition, the insula responds to pictures of appetizing food (Simmons, Martin, & Barsalou, 2005
), is activated during sexual arousal (Stoleru et al., 1999
), and may be involved in addictive cravings and urges (Naqvi, Rudrauf, Damasio, & Bechara, 2007
); these findings suggest an association with appetitive behavior. In the present study, peak activation in the right insula occurred fairly early (around 2.5 s after image presentation; see ), and this early latency is consistent with the proposal that the insula may provide a direct and somewhat immediate representation of autonomic states.
Other neuroimaging studies have implicated right insula activity as related to the personality traits of reward or novelty seeking (Suhara et al., 2001
) and neuroticism (Paulus et al., 2003
). Activation in this region may be related to individual differences in part by reflecting sympathetic states that differ as a function of personality (e.g., Paulus et al., 2003
). The present findings indicate that sensation seeking is the primary personality dimension predicting activation in this region because correlations with the convergent measure of sensation seeking were very strong, and no other personality variables predicted activation in this region when level of sensation seeking was controlled.
Compared with HSSs, LSSs more strongly activated brain regions associated with emotional regulation—the anterior cingulate and anterior medial OFC. The anterior cingulate may be involved in top-down, or intentional, modulation of intense emotional states (Matthews, Paulus, Simmons, Nelesen, & Dimsdale, 2004
; Ochsner et al., 2004
). In addition, the regulatory role of the rostral anterior cingulate cortex in affective behavior may depend on an interaction between incentive conditions and personality traits (Cunningham et al., 2005
). Interestingly, in the present study, the fMRI response of the left anterior cingulate to high-arousal images was earlier in LSSs than in HSSs. This result suggests that this particular brain region may be engaged more readily in LSSs in the face of intense arousal. Because activation in the anterior cingulate was also negatively correlated with urgency, this region was engaged less strongly in impulsive sensation-seeking individuals than in individuals with low urgency scores. In contrast, HSSs engaged the right anterior insula more strongly in the face of intense arousal. Consequently, the anterior cingulate may be an important part of emotional regulation of somatic responses that are processed in the insula (Craig, 2005
). This interpretation is also consistent with the negative correlation found between activation in the left anterior cingulate cortex and scores on urgency, a personality dimension believed to relate to emotional dyscontrol (Whiteside & Lynam, 2003
Recall that LSSs also activated the anterior medial OFC more strongly than did HSSs. The peak response for LSSs occurred earlier and was more robust than the peak response for HSSs. Damage to the medial OFC leads to profound deficits in emotional decision making (Bechara, Damasio, & Damasio, 2000
). In addition, Kringelbach and Rolls (2004)
suggested that activation in anterior medial OFC could represent the availability of information on reinforcers to conscious processing. Other recent neuroimaging studies have reported that the anterior medial OFC region is activated in conscious processing of emotions (Takahishi et al., 2004
) and emotional suppression (Ohira et al., 2006
), and is related to self-consciousness as a personality trait (Eisenberger et al., 2005
). The role of the anterior medial OFC in conscious processing of emotions and in emotional decision making suggests that it may play a role in emotional regulation. In the present study, activation in this region, as in the anterior cingulate, was negatively associated with urgency. Again, this association may implicate this region in emotional regulation and control.
In conclusion, HSSs and LSSs showed clear differences in brain response to high-arousal stimuli. The brain regions activated more strongly by HSSs are often associated with autonomic arousal. In contrast, the brain regions activated more strongly and more readily by LSSs are associated with emotional regulation and showed negative correlations with urgency, a personality dimension associated with emotional dysregulation. LSSs were also more sensitive to valence of the stimuli than were HSSs. Given that sensation seeking, as originally described by Zuckerman (1994)
, is composed of two distinct dimensions—one involving the degree of activation-approach and the other involving a lack of inhibition—future research should attempt to separate these aspects. Nevertheless, the present results may help to elucidate the processes by which sensation seeking leads to various negative behavioral outcomes, including substance use, risky sex, and antisocial behavior. Individuals high in sensation seeking not only are strongly activated by exciting, thrilling, and potentially dangerous activities, but also may be less likely than other people to inhibit or appropriately regulate that activation.