The neural correlates of trait resilience when anticipating and recovering from threat.

A facet of emotional resilience critical for adapting to adversity is flexible use of emotional resources. We hypothesized that in threatening situations, this emotional flexibility enables resilient people to use emotional resources during appropriately emotional events, and conserve emotional resources during innocuous events. We tested this hypothesis using functional magnetic resonance imaging in a repeated recovery from threat task with low- and high-trait resilient individuals (LowR and HighR, respectively, as measured by ER89). In an event-related design, 13 HighR and 13 LowR participants viewed 'threat' cues, which signaled either an aversive or neutral picture with equal probabilities, or 'nonthreat' cues, which signaled a neutral picture. Results show that when under threat, LowR individuals exhibited prolonged activation in the anterior insula to both the aversive and neutral pictures, whereas HighR individuals exhibited insula activation only to the aversive pictures. These data provide neural evidence that in threatening situations, resilient people flexibly and appropriately adjust the level of emotional resources needed to meet the demands of the situation.

[1]  W. Goodman,et al.  Disgust and the insula: fMRI responses to pictures of mutilation and contamination , 2004, Neuroreport.

[2]  Sam J. Maglio,et al.  Emotional category data on images from the international affective picture system , 2005, Behavior research methods.

[3]  K. Yau,et al.  Interoception: the sense of the physiological condition of the body , 2003, Current Opinion in Neurobiology.

[4]  S. Rauch,et al.  Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge , 1998, The Journal of Neuroscience.

[5]  B. Fredrickson,et al.  Resilient individuals use positive emotions to bounce back from negative emotional experiences. , 2004, Journal of personality and social psychology.

[6]  R. Dolan,et al.  A Functional Anatomy of Anticipatory Anxiety , 1999, NeuroImage.

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

[8]  Joseph J. Paton,et al.  The primate amygdala represents the positive and negative value of visual stimuli during learning , 2006, Nature.

[9]  Jesper Andersson,et al.  Predictability modulates the affective and sensory-discriminative neural processing of pain , 2006, NeuroImage.

[10]  John D E Gabrieli,et al.  Amygdala Response to Happy Faces as a Function of Extraversion , 2002, Science.

[11]  J. Moskowitz,et al.  Positive affect and the other side of coping. , 2000, The American psychologist.

[12]  C. Carter,et al.  Outcome representations, counterfactual comparisons and the human orbitofrontal cortex: implications for neuroimaging studies of decision-making. , 2005, Brain research. Cognitive brain research.

[13]  C S Bergeman,et al.  Psychological resilience, positive emotions, and successful adaptation to stress in later life. , 2006, Journal of personality and social psychology.

[14]  Lutz Jäncke,et al.  Neural correlates of a ‘pessimistic’ attitude when anticipating events of unknown emotional valence , 2007, NeuroImage.

[15]  Christian E. Waugh,et al.  Adapting to life's slings and arrows: Individual differences in resilience when recovering from an anticipated threat. , 2008, Journal of research in personality.

[16]  M. Posner.  The Brain and Emotion , 1999, Nature Medicine.

[17]  Matthew L. Davidson,et al.  The neuroimaging of emotion. , 2008 .

[18]  Richard J. Davidson,et al.  Brain mechanisms of expectation associated with insula and amygdala response to aversive taste: Implications for placebo , 2006, Brain, Behavior, and Immunity.

[19]  L. Becerra,et al.  Neural circuitry underlying pain modulation: expectation, hypnosis, placebo , 2003, Trends in Cognitive Sciences.

[20]  Christian E. Waugh,et al.  What good are positive emotions in crises? A prospective study of resilience and emotions following the terrorist attacks on the United States on September 11th, 2001. , 2003, Journal of personality and social psychology.

[21]  Wang Zhan,et al.  Simultaneous perfusion and BOLD imaging using reverse spiral scanning at 3T: Characterization of functional contrast and susceptibility artifacts , 2002, Magnetic resonance in medicine.

[22]  E. Rolls,et al.  Abstract reward and punishment representations in the human orbitofrontal cortex , 2001, Nature Neuroscience.

[23]  Matthew T. Kaufman,et al.  Distributed Neural Representation of Expected Value , 2005, The Journal of Neuroscience.

[24]  Karl J. Friston,et al.  Opponent appetitive-aversive neural processes underlie predictive learning of pain relief , 2005, Nature Neuroscience.

[25]  Thomas M. Moerland,et al.  Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation , 2005, NeuroImage.

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

[27]  J. Turner.  Human Emotions: A Sociological Theory , 2007 .

[28]  Ravi S. Menon,et al.  Dissociating pain from its anticipation in the human brain. , 1999, Science.

[29]  Richard J. Davidson,et al.  Functional neuroanatomy of aversion and its anticipation , 2006, NeuroImage.

[30]  Joseph E LeDoux,et al.  Contributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior , 2005, Neuron.

[31]  D. R. Lehman,et al.  Resilience to loss and chronic grief: a prospective study from preloss to 18-months postloss. , 2002, Journal of personality and social psychology.

[32]  Michael Angstadt,et al.  Beyond threat: Amygdala reactivity across multiple expressions of facial affect , 2006, NeuroImage.

[33]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[34]  P. Costa,et al.  Normal Personality Assessment in Clinical Practice: The NEO Personality Inventory. , 1992 .

[35]  Danielle S. Bassett,et al.  A validated network of effective amygdala connectivity , 2007, NeuroImage.

[36]  J. O'Doherty,et al.  Empathy for Pain Involves the Affective but not Sensory Components of Pain , 2004, Science.

[37]  P. Bandettini,et al.  Understanding neural system dynamics through task modulation and measurement of functional MRI amplitude, latency, and width , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[38]  J. Block,et al.  IQ and ego-resiliency: conceptual and empirical connections and separateness. , 1996, Journal of personality and social psychology.

[39]  K. Luan Phan,et al.  Subjective rating of emotionally salient stimuli modulates neural activity , 2003, NeuroImage.

[40]  Andrew Ortony,et al.  The complexity of intensity: Issues concerning the structure of emotion intensity , 1992 .

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

[42]  Matthew C. Keller,et al.  Increased sensitivity in neuroimaging analyses using robust regression , 2005, NeuroImage.

[43]  A. Lüthi,et al.  Processing of Temporal Unpredictability in Human and Animal Amygdala , 2007, The Journal of Neuroscience.

[44]  Kristopher J Preacher,et al.  Use of the extreme groups approach: a critical reexamination and new recommendations. , 2005, Psychological methods.

[45]  G. Glover.  Deconvolution of Impulse Response in Event-Related BOLD fMRI1 , 1999, NeuroImage.

[46]  Matthew D. Lieberman,et al.  Neural bases of moderation of cortisol stress responses by psychosocial resources. , 2008, Journal of personality and social psychology.

[47]  D. Charney,et al.  Psychobiological mechanisms of resilience and vulnerability: implications for successful adaptation to extreme stress. , 2004, The American journal of psychiatry.

[48]  P. Lang.  International Affective Picture System (IAPS) : Technical Manual and Affective Ratings , 1995 .

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

[50]  J. Cohen,et al.  Spiral K‐space MR imaging of cortical activation , 1995, Journal of magnetic resonance imaging : JMRI.

[51]  J. Kagan,et al.  The value of extreme groups. , 1998 .

[52]  S. Petersen,et al.  Characterizing the Hemodynamic Response: Effects of Presentation Rate, Sampling Procedure, and the Possibility of Ordering Brain Activity Based on Relative Timing , 2000, NeuroImage.

[53]  H. Critchley.  Neural mechanisms of autonomic, affective, and cognitive integration , 2005, The Journal of comparative neurology.

[54]  M. Mikulincer,et al.  Does hardiness contribute to mental health during a stressful real-life situation? The roles of appraisal and coping. , 1995, Journal of personality and social psychology.

[55]  Lars R. Bergman,et al.  Methods and models for studying the individual. , 1998 .

[56]  J. Block,et al.  The Role of Ego-Control and Ego-Resiliency in the Organization of Behavior , 1980 .

[57]  C. Carver,et al.  Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: The BIS/BAS Scales , 1994 .

[58]  G. Pagnoni,et al.  Does Anticipation of Pain Affect Cortical Nociceptive Systems? , 2002, The Journal of Neuroscience.

[59]  M. Phillips,et al.  A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder , 2008, Molecular Psychiatry.

[60]  M. Thase,et al.  Can’t shake that feeling: event-related fMRI assessment of sustained amygdala activity in response to emotional information in depressed individuals , 2002, Biological Psychiatry.

[61]  Edward E. Smith,et al.  Altering expectancy dampens neural response to aversive taste in primary taste cortex , 2006, Nature Neuroscience.

[62]  D. Perrett,et al.  A specific neural substrate for perceiving facial expressions of disgust , 1997, Nature.

[63]  Christian E. Waugh,et al.  What good are positive emotions in crises? A prospective study of resilience and emotions following the terrorist attacks on the United States on September 11th, 2001. , 2003, Journal of personality and social psychology.

[64]  Michael W. Bridges,et al.  Distinguishing optimism from neuroticism (and trait anxiety, self-mastery, and self-esteem): a reevaluation of the Life Orientation Test. , 1994, Journal of personality and social psychology.

[65]  H. Critchley,et al.  Neural Activity in the Human Brain Relating to Uncertainty and Arousal during Anticipation , 2001, Neuron.

[66]  S. Paradiso.  The Emotional Brain: The Mysterious Underpinnings of Emotional Life , 1998 .

[67]  Christian E. Waugh,et al.  PERSONALITY PROCESSES AND INDIVIDUAL DIFFERENCES What Good Are Positive Emotions in Crises ? A Prospective Study of Resilience and Emotions Following the Terrorist Attacks on the United States on September 11 th , 2001 , 2003 .

[68]  R. Cabeza,et al.  Remembering one year later: role of the amygdala and the medial temporal lobe memory system in retrieving emotional memories. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[69]  R. Larsen,et al.  The Satisfaction with Life Scale , 1985, Journal of personality assessment.

[70]  M. Lindquist,et al.  Validity and power in hemodynamic response modeling: A comparison study and a new approach , 2007, Human brain mapping.