Differential Brain Activation to Angry Faces by Elite Warfighters: Neural Processing Evidence for Enhanced Threat Detection

Background Little is known about the neural basis of elite performers and their optimal performance in extreme environments. The purpose of this study was to examine brain processing differences between elite warfighters and comparison subjects in brain structures that are important for emotion processing and interoception. Methodology/Principal Findings Navy Sea, Air, and Land Forces (SEALs) while off duty (n = 11) were compared with n = 23 healthy male volunteers while performing a simple emotion face-processing task during functional magnetic resonance imaging. Irrespective of the target emotion, elite warfighters relative to comparison subjects showed relatively greater right-sided insula, but attenuated left-sided insula, activation. Navy SEALs showed selectively greater activation to angry target faces relative to fearful or happy target faces bilaterally in the insula. This was not accounted for by contrasting positive versus negative emotions. Finally, these individuals also showed slower response latencies to fearful and happy target faces than did comparison subjects. Conclusions/Significance These findings support the hypothesis that elite warfighters deploy greater processing resources toward potential threat-related facial expressions and reduced processing resources to non-threat-related facial expressions. Moreover, rather than expending more effort in general, elite warfighters show more focused neural and performance tuning. In other words, greater neural processing resources are directed toward threat stimuli and processing resources are conserved when facing a nonthreat stimulus situation.

[1]  M. Kringelbach.  The human orbitofrontal cortex: linking reward to hedonic experience , 2005, Nature Reviews Neuroscience.

[2]  S. Shipp.  The importance of being agranular: a comparative account of visual and motor cortex , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[3]  Paul W. Davenport,et al.  Cortical and subcortical central neural pathways in respiratory sensations , 2009, Respiratory Physiology & Neurobiology.

[4]  Karl F. Van Orden,et al.  A neuroscience approach to optimizing brain resources for human performance in extreme environments , 2009, Neuroscience & Biobehavioral Reviews.

[5]  M. Stein,et al.  Randomized Placebo-Controlled Trial of a Selective Serotonin Reuptake Inhibitor in the Treatment of Nondepressed Tinnitus Subjects , 2005, Psychosomatic medicine.

[6]  A B Vallbo,et al.  Receptive field characteristics of tactile units with myelinated afferents in hairy skin of human subjects. , 1995, The Journal of physiology.

[7]  E. Stein,et al.  Right hemispheric dominance of inhibitory control: an event-related functional MRI study. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Y. Lamarre,et al.  Unmyelinated tactile afferents signal touch and project to insular cortex , 2002, Nature Neuroscience.

[9]  David Borsook,et al.  Noxious hot and cold stimulation produce common patterns of brain activation in humans: a functional magnetic resonance imaging study , 2000, Neuroscience Letters.

[10]  Murray B. Stein,et al.  Intolerance of uncertainty correlates with insula activation during affective ambiguity , 2008, Neuroscience Letters.

[11]  L. F. Barrett,et al.  Handbook of Emotions , 1993 .

[12]  S. Quartz,et al.  Human Insula Activation Reflects Risk Prediction Errors As Well As Risk , 2008, The Journal of Neuroscience.

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

[14]  R. Turner,et al.  Characterizing Evoked Hemodynamics with fMRI , 1995, NeuroImage.

[15]  Hugo D. Critchley,et al.  Interoceptive Basis to Craving , 2007, Neuron.

[16]  A. Craig,et al.  Interoception and Emotion : a Neuroanatomical Perspective , 2007 .

[17]  M. Egan,et al.  Serotonin Transporter Genetic Variation and the Response of the Human Amygdala , 2002, Science.

[18]  Hugo D. Critchley,et al.  Psychophysiology of neural, cognitive and affective integration: fMRI and autonomic indicants , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[19]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[20]  Stuart D. Rosen,et al.  Breathlessness in humans activates insular cortex , 2000, Neuroreport.

[21]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

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

[23]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[24]  K. Luan Phan,et al.  Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging , 2003, NeuroImage.

[25]  Raymond J. Dolan,et al.  Anterior cingulate activity during error and autonomic response , 2005, NeuroImage.

[26]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

[27]  Katerina Hnatkova,et al.  Mental stress and sudden cardiac death: asymmetric midbrain activity as a linking mechanism. , 2004, Brain : a journal of neurology.

[28]  D. S. Zahm,et al.  Specificity in the Projections of Prefrontal and Insular Cortex to Ventral Striatopallidum and the Extended Amygdala , 2005, The Journal of Neuroscience.

[29]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[30]  R. Davidson,et al.  The functional neuroanatomy of emotion and affective style , 1999, Trends in Cognitive Sciences.

[31]  A. Craig.  A new view of pain as a homeostatic emotion , 2003, Trends in Neurosciences.

[32]  R. Dolan,et al.  Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans , 2006, Nature.

[33]  Martin P Paulus,et al.  Decision-Making Dysfunctions in Psychiatry—Altered Homeostatic Processing? , 2007, Science.

[34]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[35]  J. Fudge,et al.  Insular and gustatory inputs to the caudal ventral striatum in primates , 2005, The Journal of comparative neurology.

[36]  Matthew D. Lieberman,et al.  Does Rejection Hurt? An fMRI Study of Social Exclusion , 2003, Science.

[37]  Michael F Egan,et al.  A susceptibility gene for affective disorders and the response of the human amygdala. , 2005, Archives of general psychiatry.

[38]  R. LaMotte,et al.  Peripheral neural mechanisms of cutaneous hyperalgesia following mild injury by heat , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  A. Simmons,et al.  Anticipation of emotionally aversive visual stimuli activates right insula , 2004, Neuroreport.

[40]  Richard Hoffman,et al.  Predictors of Success in Basic Underwater Demolition/SEAL (BUD/S) Training - Part 1: What Do We Know and Where Do We Go From Here? , 2006 .

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

[42]  Mark S. Cohen,et al.  Parametric Analysis of fMRI Data Using Linear Systems Methods , 1997, NeuroImage.

[43]  Justin S. Feinstein,et al.  Dose-dependent decrease of activation in bilateral amygdala and insula by lorazepam during emotion processing. , 2005, Archives of general psychiatry.

[44]  B. Shukitt-Hale,et al.  Effects of caffeine, sleep loss, and stress on cognitive performance and mood during U.S. Navy SEAL training , 2002, Psychopharmacology.

[45]  Hermann O. Handwerker,et al.  Specific C-Receptors for Itch in Human Skin , 1997, The Journal of Neuroscience.

[46]  H. Critchley,et al.  Neural systems supporting interoceptive awareness , 2004, Nature Neuroscience.

[47]  M. J. Norušis,et al.  SPSS base system user's guide , 1990 .

[48]  William F. Eddyy,et al.  Improved image registration by using fourier interpolation , 1996, Magnetic resonance in medicine.

[49]  Rita Z. Goldstein,et al.  Role of the anterior cingulate and medial orbitofrontal cortex in processing drug cues in cocaine addiction , 2007, Neuroscience.

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

[51]  D. Bowsher,et al.  Clinical and instrumental evaluation of sensory function before and after percutaneous anterolateral cordotomy at cervical level in man , 1990, Pain.

[52]  Gregory McCarthy,et al.  Dynamic and strategic aspects of executive processing , 2004, Brain Research.

[53]  Vladimir Coric,et al.  Relation between cardiac vagal tone and performance in male military personnel exposed to high stress: three prospective studies. , 2007, Psychophysiology.

[54]  Timothy E. J. Behrens,et al.  Choice, uncertainty and value in prefrontal and cingulate cortex , 2008, Nature Neuroscience.

[55]  A R Damasio,et al.  Descartes' error and the future of human life. , 1994, Scientific American.

[56]  Murray B. Stein,et al.  Anticipation of Aversive Visual Stimuli Is Associated With Increased Insula Activation in Anxiety-Prone Subjects , 2006, Biological Psychiatry.

[57]  Tom Johnstone,et al.  Stability of amygdala BOLD response to fearful faces over multiple scan sessions , 2005, NeuroImage.

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

[59]  E. Rolls.  The functions of the orbitofrontal cortex , 1999, Brain and Cognition.

[60]  L. Jasmin,et al.  Rostral agranular insular cortex and pain areas of the central nervous system: A tract‐tracing study in the rat , 2004, The Journal of comparative neurology.

[61]  J. R. Augustine.  Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.

[62]  M. Bushnell,et al.  The thermal grill illusion: unmasking the burn of cold pain. , 1994, Science.

[63]  Qasim Aziz,et al.  Brain response to visceral aversive conditioning: a functional magnetic resonance imaging study. , 2005, Gastroenterology.

[64]  George Mendelson,et al.  Book Reviews , 1995 .

[65]  J R Augustine,et al.  The insular lobe in primates including humans. , 1985, Neurological research.

[66]  E. Perl,et al.  Unmyelinated afferent fibers are not only for pain anymore , 2003, The Journal of comparative neurology.

[67]  Suzanne N. Haber,et al.  Insular Cortical Projections to Functional Regions of the Striatum Correlate with Cortical Cytoarchitectonic Organization in the Primate , 1997, The Journal of Neuroscience.

[68]  Dieter Vaitl,et al.  Interoception , 1996, Biological Psychology.

[69]  A. Dickinson,et al.  Neuronal coding of prediction errors. , 2000, Annual review of neuroscience.

[70]  C. Feinle.  Role of intestinal chemoreception in the induction of gastrointestinal sensations. , 1998, DTW. Deutsche tierarztliche Wochenschrift.