Brain, body, and cognition: Neural, physiological and self-report correlates of phobic and normative fear

The phobic fear response appears to resemble an intense form of normal threat responding that can be induced in a nonthreatening situation. However, normative and phobic fear are rarely contrasted directly, thus the degree to which these two types of fear elicit similar neural and bodily responses is not well understood. To examine biological correlates of normal and phobic fear, 21 snake phobic and 21 nonphobic controls saw videos of slithering snakes, attacking snakes and fish in an event-related fMRI design. Simultaneous eletrodermal, pupillary, and self-reported affective responses were collected. Nonphobic fear activated a network of threat-responsive brain regions and involved pupillary dilation, electrodermal response and self-reported affect selective to the attacking snakes. Phobic fear recruited a large array of brain regions including those active in normal fear plus additional structures and also engendered increased pupil dilation, electrodermal and self-reported responses that were greater to any snake versus fish. Importantly, phobics showed greater between- and within-subject concordance among neural, electrodermal, pupillary, and subjective report measures. These results suggest phobic responses recruit overlapping but more strongly activated and more extensive networks of brain activity as compared to normative fear, and are characterized by greater concordance among neural activation, peripheral physiology and self-report. It is yet unclear whether concordance is unique to psychopathology, or rather simply an indicator of the intense fear seen in the phobic response, but these results underscore the importance of synchrony between brain, body, and cognition during the phobic reaction.

[1]  D. M. Klieger The Snake Anxiety Questionnaire as a Measure of Ophidophobia , 1987 .

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

[3]  Desynchrony of fear in phobic exposure , 2010, Journal of psychopharmacology.

[4]  Bertram Walter,et al.  Hemodynamic brain correlates of disgust and fear ratings , 2007, NeuroImage.

[5]  D. Weinberger,et al.  Neocortical modulation of the amygdala response to fearful stimuli , 2003, Biological Psychiatry.

[6]  David Matsumoto,et al.  Evidence for universality in phenomenological emotion response system coherence. , 2007, Emotion.

[7]  S. Mineka,et al.  Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. , 2001, Psychological review.

[8]  B. Cuthbert,et al.  Fear and the startle reflex: blink modulation and autonomic response patterns in animal and mutilation fearful subjects. , 1997, Psychophysiology.

[9]  H. Lachnit,et al.  Tracking stimulus processing in Pavlovian pupillary conditioning. , 2006, Psychophysiology.

[10]  Neil Roberts,et al.  Role for human posterior parietal cortex in visual processing of aversive objects in peripersonal space. , 2006, Journal of neurophysiology.

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

[12]  B. Teachman,et al.  Age differences in anxious responding: older and calmer, unless the trigger is physical. , 2009, Psychology and aging.

[13]  Kevin M. Connolly,et al.  Domain-specific and generalized disgust sensitivity in blood-injection-injury phobia: the application of behavioral approach/avoidance tasks. , 2002, Journal of anxiety disorders.

[14]  Fred J Helmstetter,et al.  Neural Substrates Mediating Human Delay and Trace Fear Conditioning , 2004, The Journal of Neuroscience.

[15]  J. Gross,et al.  The Neural Bases of Emotion Regulation: Reappraisal and Suppression of Negative Emotion , 2008, Biological Psychiatry.

[16]  J. S. Mizes,et al.  Patterns of distorted cognitions in phobic disorders: An investigation of clinically severe simple phobics, social phobics, and agoraphobics , 1987, Cognitive Therapy and Research.

[17]  G Sartory,et al.  An investigation of the relation between reported fear and heart rate. , 1977, Behaviour research and therapy.

[18]  H. Merckelbach,et al.  Self-Reported Automaticity and Irrationality in Spider Phobia , 2000, Psychological reports.

[19]  Johanne Lévesque,et al.  “Change the mind and you change the brain”: effects of cognitive-behavioral therapy on the neural correlates of spider phobia , 2003, NeuroImage.

[20]  A. Arntz,et al.  Negative beliefs of spider phobics: A psychometric evaluation of the spider phobia beliefs questionnaire , 1993 .

[21]  G. Rizzolatti,et al.  Both of Us Disgusted in My Insula The Common Neural Basis of Seeing and Feeling Disgust , 2003, Neuron.

[22]  Wolfgang Ambach,et al.  Weaving the (neuronal) web: Fear learning in spider phobia , 2011, NeuroImage.

[23]  J. Davidson Contesting stigma and contested emotions: personal experience and public perception of specific phobias. , 2005, Social science & medicine.

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

[25]  P. D. de Jong,et al.  Disgust and disgust sensitivity in spider phobia: facial EMG in response to spider and oral disgust imagery. , 2002, Journal of anxiety disorders.

[26]  Andreas Keil,et al.  Cortical activation during Pavlovian fear conditioning depends on heart rate response patterns: an MEG study. , 2005, Brain research. Cognitive brain research.

[27]  P. Ekman,et al.  What the face reveals : basic and applied studies of spontaneous expression using the facial action coding system (FACS) , 2005 .

[28]  Axel Schäfer,et al.  Emotion regulation in spider phobia: role of the medial prefrontal cortex. , 2009, Social cognitive and affective neuroscience.

[29]  Jeffrey B. Henriques,et al.  While a phobic waits: regional brain electrical and autonomic activity in social phobics during anticipation of public speaking , 2000, Biological Psychiatry.

[30]  J. Gross,et al.  The tie that binds? Coherence among emotion experience, behavior, and physiology. , 2005, Emotion.

[31]  J. Fernández-Dols,et al.  Are Spontaneous Expressions and Emotions Linked? an Experimental Test of Coherence , 1997 .

[32]  M. Kindt,et al.  Phobia-related cognitive bias for pictorial and linguistic stimuli. , 1997, Journal of abnormal psychology.

[33]  Mats Fredrikson,et al.  Disentangling the web of fear: Amygdala reactivity and functional connectivity in spider and snake phobia , 2009, Psychiatry Research: Neuroimaging.

[34]  Peter J. Lang,et al.  Parallel amygdala and inferotemporal activation reflect emotional intensity and fear relevance , 2005, NeuroImage.

[35]  M. Thase,et al.  Pupillary assessment and computational modeling of the Stroop task in depression. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[37]  Alessandro Angrilli,et al.  Blood phobia and spider phobia: two specific phobias with different autonomic cardiac modulations , 2002, Biological Psychology.

[38]  E. Gordon,et al.  BOLD, sweat and fears: fMRI and skin conductance distinguish facial fear signals , 2005, Neuroreport.

[39]  P. Girardi,et al.  Functional neuroimaging in specific phobia , 2012, Psychiatry Research: Neuroimaging.

[40]  Paul Wright,et al.  Dissociated responses in the amygdala and orbitofrontal cortex to bottom–up and top–down components of emotional evaluation , 2008, NeuroImage.

[41]  Daniel B. Rowe,et al.  An evaluation of thresholding techniques in fMRI analysis , 2004, NeuroImage.

[42]  Dan J Stein,et al.  Meta‐analysis of functional brain imaging in specific phobia , 2013, Psychiatry and clinical neurosciences.

[43]  P. Ekman,et al.  Coherence between expressive and experiential systems in emotion , 1994 .

[44]  Axel Schäfer,et al.  Symptom provocation and reduction in patients suffering from spider phobia , 2007, European Archives of Psychiatry and Clinical Neuroscience.

[45]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[46]  J. Gross,et al.  Emotional suppression: physiology, self-report, and expressive behavior. , 1993, Journal of personality and social psychology.

[47]  A. Ohman,et al.  Emotion drives attention: detecting the snake in the grass. , 2001, Journal of experimental psychology. General.

[48]  D. Hope,et al.  Gender, gender roles, and anxiety: perceived confirmability of self report, behavioral avoidance, and physiological reactivity. , 2012, Journal of anxiety disorders.

[49]  Joseph E LeDoux,et al.  Extinction Learning in Humans Role of the Amygdala and vmPFC , 2004, Neuron.

[50]  Jane F. Banfield,et al.  Medial prefrontal activity predicts memory for self. , 2004, Cerebral cortex.

[51]  S. Rauch,et al.  Recall of Fear Extinction in Humans Activates the Ventromedial Prefrontal Cortex and Hippocampus in Concert , 2007, Biological Psychiatry.