Neural representation of anxiety and personality during exposure to anxiety‐provoking and neutral scenes from scary movies

Some people search for intense sensations such as being scared by frightening movies while others do not. The brain mechanisms underlying such inter‐individual differences are not clear. Testing theoretical models, we investigated neural correlates of anxiety and the personality trait sensation seeking in 40 subjects who watched threatening and neutral scenes from scary movies during functional magnetic resonance imaging. Threat versus neutral scenes induced increased activation in anterior cingulate cortex, insula, thalamus, and visual areas. Movie‐induced anxiety correlated positively with activation in dorsomedial prefrontal cortex, indicating a role for this area in the subjective experience of being scared. Sensation seeking‐scores correlated positively with brain activation to threat versus neutral scenes in visual areas and in thalamus and anterior insula, i.e. regions involved in the induction and representation of arousal states. For the insula and thalamus, these outcomes were partly due to an inverse relation between sensation seeking scores and brain activation during neutral film clips. These results support models predicting cerebral hypoactivation in high sensation seekers during neutral stimulation, which may be compensated by more intense sensations such as watching scary movies. Hum Brain Mapp, 2010. © 2009 Wiley‐Liss, Inc.

[1]  Sven Joubert,et al.  Areas of brain activation in males and females during viewing of erotic film excerpts , 2002, Human brain mapping.

[2]  A. Loewy,et al.  Brainstem projections to midline and intralaminar thalamic nuclei of the rat , 2002, The Journal of comparative neurology.

[3]  A. Damasio,et al.  Consciousness and the brainstem , 2001, Cognition.

[4]  Thomas Straube,et al.  Effects of cognitive-behavioral therapy on brain activation in specific phobia , 2006, NeuroImage.

[5]  Patrizia Baraldi,et al.  Functional activity mapping of the mesial hemispheric wall during anticipation of pain , 2003, NeuroImage.

[6]  T. Shallice,et al.  Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. , 2003, Brain : a journal of neurology.

[7]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[8]  J. Duncan,et al.  Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli , 2004, Nature Neuroscience.

[9]  U. Hegerl,et al.  Sensory cortical processing and the biological basis of personality , 1995, Biological Psychiatry.

[10]  M. Paulus,et al.  An Insular View of Anxiety , 2006, Biological Psychiatry.

[11]  Thomas Weiss,et al.  Time course of amygdala activation during aversive conditioning depends on attention , 2007, NeuroImage.

[12]  André Beauducel,et al.  Psychometrische Eigenschaften und Normen einer deutschsprachigen Fassung der Sensation Seeking-Skalen, Form V , 2003 .

[13]  M. Zuckerman,et al.  The psychophysiology of sensation seeking. , 1990, Journal of personality.

[14]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[15]  S. Paradiso,et al.  Emotional activation of limbic circuitry in elderly normal subjects in a PET study. , 1997, The American journal of psychiatry.

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

[17]  Raymond J. Dolan,et al.  Levels of appraisal: A medial prefrontal role in high-level appraisal of emotional material , 2006, NeuroImage.

[18]  R Turner,et al.  Optimized EPI for fMRI studies of the orbitofrontal cortex , 2003, NeuroImage.

[19]  M. Erb,et al.  Brain activity underlying emotional valence and arousal: A response‐related fMRI study , 2004, Human brain mapping.

[20]  Thomas Straube,et al.  Effect of task conditions on brain responses to threatening faces in social phobics: An event-related functional magnetic resonance imaging study , 2004, Biological Psychiatry.

[21]  M. Witter,et al.  The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness , 2002, Brain Research Reviews.

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

[23]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[24]  R. Stark,et al.  Influences of disgust sensitivity on hemodynamic responses towards a disgust-inducing film clip. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[25]  André Beauducel,et al.  Sensation Seeking and Affective Disorders: Characteristics in the Intensity Dependence of Acoustic Evoked Potentials , 2000, Neuropsychobiology.

[26]  M. Zuckerman Sensation Seeking : Beyond the Optimal Level of Arousal , 1979 .

[27]  Karl J. Friston,et al.  Neuroanatomical correlates of externally and internally generated human emotion. , 1997, The American journal of psychiatry.

[28]  M. Zuckerman,et al.  Sensation seeking and music preferences , 1986 .

[29]  Johannes Hewig,et al.  A revised film set for the induction of basic emotions. , 2005 .

[30]  M. Zuckerman,et al.  Personality and risk-taking: common biosocial factors. , 2000, Journal of personality.

[31]  Geraint Rees,et al.  The cognitive neuroscience of consciousness , 2010, Cognitive neuroscience.

[32]  G. Sparks Developing a Scale to Assess Cognitive Responses to Frightening Films , 1986 .

[33]  M. Raichle,et al.  Emotion-induced changes in human medial prefrontal cortex: II. During anticipatory anxiety. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Thomas Weiss,et al.  Dynamic activation of the anterior cingulate cortex during anticipatory anxiety , 2009, NeuroImage.

[35]  M. Zuckerman Item revisions in the Sensation Seeking Scale Form V (SSS-V) , 1996 .

[36]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Michael D. Slater,et al.  Alienation, Aggression, and Sensation Seeking as Predictors of Adolescent Use of Violent Film, Computer, and Website Content , 2003 .

[38]  R. Lane,et al.  Neural Correlates of Levels of Emotional Awareness: Evidence of an Interaction between Emotion and Attention in the Anterior Cingulate Cortex , 1998, Journal of Cognitive Neuroscience.

[39]  Thomas Straube,et al.  Waiting for spiders: Brain activation during anticipatory anxiety in spider phobics , 2007, NeuroImage.

[40]  H. Critchley,et al.  Fear Conditioning in Humans The Influence of Awareness and Autonomic Arousal on Functional Neuroanatomy , 2002, Neuron.

[41]  E. Rolls,et al.  Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices. , 2003, Brain : a journal of neurology.

[42]  H. Critchley The human cortex responds to an interoceptive challenge. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Gary H. Glover,et al.  The neural bases of amusement and sadness: A comparison of block contrast and subject-specific emotion intensity regression approaches , 2005, NeuroImage.

[44]  J. Siegel Augmenting and Reducing of Visual Evoked Potentials in High- and Low-Sensation Seeking Humans, Cats, and Rats , 1997, Behavior genetics.

[45]  Thomas Straube,et al.  Neural Mechanisms of Automatic and Direct Processing of Phobogenic Stimuli in Specific Phobia , 2006, Biological Psychiatry.

[46]  Ron Tamborini,et al.  Preference for Graphic Horror Featuring Male versus Female Victimization: Personality and Past Film Viewing Experiences. , 1987 .

[47]  Gregor Hasler,et al.  Cerebral Blood Flow in Immediate and Sustained Anxiety , 2007, The Journal of Neuroscience.

[48]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.