Neural Correlates of Emotional Reactivity in Sensation Seeking

High sensation seeking has been linked to increased risk for drug abuse and other negative behavioral outcomes. This study explored the neurobiological basis of this personality trait using functional magnetic resonance imaging (fMRI). High sensation seekers (HSSs) and low sensation seekers (LSSs) viewed high- and low-arousal pictures. Comparison of the groups revealed that HSSs showed stronger fMRI responses to high-arousal stimuli in brain regions associated with arousal and reinforcement (right insula, posterior medial orbitofrontal cortex), whereas LSSs showed greater activation and earlier onset of fMRI responses to high-arousal stimuli in regions involved in emotional regulation (anterior medial orbitofrontal cortex, anterior cingulate). Furthermore, fMRI response in anterior medial orbitofrontal cortex and anterior cingulate was negatively correlated with urgency. Finally, LSSs showed greater sensitivity to the valence of the stimuli than did HSSs. These distinct neurobiological profiles suggest that HSSs exhibit neural responses consistent with an overactive approach system, whereas LSSs exhibit responses consistent with a stronger inhibitory system.

[1]  Kevin N. Ochsner,et al.  For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion , 2004, NeuroImage.

[2]  Jack L. Lancaster,et al.  Clustered pixels analysis for functional MRI activation studies of the human brain , 1995 .

[3]  P T Fox,et al.  A Highly Accurate Method of Localizing Regions of Neuronal Activation in the Human Brain with Positron Emission Tomography , 1989, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[4]  M. Zuckerman,et al.  Sensation seeking and arousal systems , 1983 .

[5]  Jonathan W. Roberti,et al.  A review of behavioral and biological correlates of sensation seeking , 2004 .

[6]  M. Bradley,et al.  Emotional arousal and activation of the visual cortex: an fMRI analysis. , 1998, Psychophysiology.

[7]  Annie Lang,et al.  Sensation Seeking, Motivation, and Substance Use: A Dual System Approach , 2005 .

[8]  Hans J. Eysenck,et al.  Manual of the Eysenck personality questionnaire , 1975 .

[9]  Tetsuya Matsuda,et al.  Brain activation associated with evaluative processes of guilt and embarrassment: an fMRI study , 2004, NeuroImage.

[10]  A. Damasio,et al.  Emotion, decision making and the orbitofrontal cortex. , 2000, Cerebral cortex.

[11]  A. Craig Forebrain emotional asymmetry: a neuroanatomical basis? , 2005, Trends in Cognitive Sciences.

[12]  W. K. Simmons,et al.  Pictures of appetizing foods activate gustatory cortices for taste and reward. , 2005, Cerebral cortex.

[13]  M. Bradley,et al.  Emotion and motivation I: defensive and appetitive reactions in picture processing. , 2001, Emotion.

[14]  M. Zuckerman Behavioral Expressions and Biosocial Bases of Sensation Seeking , 1994 .

[15]  Martin P Paulus,et al.  Functional subdivisions within anterior cingulate cortex and their relationship to autonomic nervous system function , 2004, NeuroImage.

[16]  M. Zuckerman Psychobiology of Personality: Subject Index , 2005 .

[17]  H. Damasio,et al.  Damage to the Insula Disrupts Addiction to Cigarette Smoking , 2007, Science.

[18]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[19]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[20]  S. Whiteside,et al.  Understanding the role of impulsivity and externalizing psychopathology in alcohol abuse: application of the UPPS impulsive behavior scale. , 2003, Experimental and clinical psychopharmacology.

[21]  M. Bardo,et al.  Psychobiology of novelty seeking and drug seeking behavior , 1996, Behavioural Brain Research.

[22]  W. Perlstein,et al.  Sensation-seeking: electrodermal and behavioral effects of stimulus content and intensity. , 1990, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[23]  R. C. Oldfield THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[24]  L. Feldman Valence Focus and Arousal Focus: Individual Differences in the Structure of Affective Experience , 1995 .

[25]  Matthew D. Lieberman,et al.  Personality from a controlled processing perspective: An fMRI study of neuroticism, extraversion, and self-consciousness , 2005, Cognitive, Affective, & Behavioral Neuroscience.

[26]  E. Rolls,et al.  The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology , 2004, Progress in Neurobiology.

[27]  Yoshiro Okubo,et al.  Dopamine D2 Receptors in the Insular Cortex and the Personality Trait of Novelty Seeking , 2001, NeuroImage.

[28]  S. Srivastava,et al.  The Big Five Trait taxonomy: History, measurement, and theoretical perspectives. , 1999 .

[29]  Hugo D. Critchley,et al.  Volitional Control of Autonomic Arousal: A Functional Magnetic Resonance Study , 2002, NeuroImage.

[30]  William A. Cunningham,et al.  Neural correlates of evaluation associated with promotion and prevention regulatory focus , 2005, Cognitive, affective & behavioral neuroscience.

[31]  Henrik Walter,et al.  Prediction error as a linear function of reward probability is coded in human nucleus accumbens , 2006, NeuroImage.

[32]  S. Whiteside,et al.  The Five Factor Model and impulsivity: using a structural model of personality to understand impulsivity , 2001 .

[33]  Atsushi Sato,et al.  Association of neural and physiological responses during voluntary emotion suppression , 2006, NeuroImage.

[34]  M. Zuckerman,et al.  A comparison of three structural models for personality: the big three , 1993 .

[35]  J. Decety,et al.  Neuroanatomical Correlates of Visually Evoked Sexual Arousal in Human Males , 1999, Archives of sexual behavior.

[36]  M. Bradley,et al.  Brain potentials in affective picture processing: covariation with autonomic arousal and affective report , 2000, Biological Psychology.

[37]  R. Depue,et al.  Neurobiology of the structure of personality: Dopamine, facilitation of incentive motivation, and extraversion , 1999, Behavioral and Brain Sciences.

[38]  Corianne Rogalsky,et al.  Increased activation in the right insula during risk-taking decision making is related to harm avoidance and neuroticism , 2003, NeuroImage.

[39]  P. Lang,et al.  International Affective Picture System (IAPS): Instruction Manual and Affective Ratings (Tech. Rep. No. A-4) , 1999 .

[40]  R. Hoyle,et al.  Reliability and validity of a brief measure of sensation seeking , 2002 .

[41]  S. Guze Psychobiology of Personality , 1992 .

[42]  Daniel S Pine,et al.  Sensation seeking and the aversive motivational system. , 2005, Emotion.