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Dynamic Neural Activity During Stress Signals Resilient Coping Dynamic neural activity during stress signals resilient coping Rajita Sinhaa,b,c,d,1, Cheryl M. Lacadiee, R. Todd Constablee, and Dongju Seoa,b aYale Stress Center, Yale University School of Medicine, New Haven, CT 06519; bDepartment of Psychiatry, Yale University School of Medicine, New Haven, CT 06511; cDepartment of Neuroscience, Yale University School of Medicine, New Haven, CT 06520; dChild Study Center, Yale University School of Medicine, New Haven, CT 06519; and eRadiology and Biomedical Imaging, Yale University School of Medicine, New Haven, CT 06520 Edited by Bruce S. McEwen, The Rockefeller University, New York, NY, and approved June 9, 2016 (received for review January 21, 2016) Active coping underlies a healthy stress response, but neural pro- Growing basic science research suggests that there is an evo- cesses supporting such resilient coping are not well-known. Using a lutionary bias toward reduced prefrontal executive control dur- brief, sustained exposure paradigm contrasting highly stressful, ing high stress to promote short-term stress-related habitual threatening, and violent stimuli versus nonaversive neutral visual behavioral responses for survival (8–11). A host of human stimuli in a functional magnetic resonance imaging (fMRI) study, functional neuroimaging and behavioral laboratory studies doc- we show significant subjective, physiologic, and endocrine increases ument decreased prefrontal activity and reduced executive and temporally related dynamically distinct patterns of neural acti- function during stress (9, 12, 13) and increased activation in the vation in brain circuits underlying the stress response. First, stress- limbic-striatal network associated with high emotional and be- specific sustained increases in the amygdala, striatum, hypothalamus, havioral reactivity in healthy and patient samples (13–17). midbrain, right insula, and right dorsolateral prefrontal cortex (DLPFC) Nonetheless, humans often face high levels of stress, trauma, and regions supported the stress processing and reactivity circuit. Sec- aggression in daily life, but they also show a remarkable ability to ond, dynamic neural activation during stress versus neutral runs, adapt and reduce stress levels and actively cope and persist in the showing early increases followed by later reduced activation in face of such unpredictable and uncontrollable events, which has the ventrolateral prefrontal cortex (VLPFC), dorsal anterior cingulate led to an increasing focus on identifying brain responses to stress cortex (dACC), left DLPFC, hippocampus, and left insula, suggested a and stress resilience mechanisms that may drive individual dif- stress adaptation response network. Finally, dynamic stress-specific ferences in stress coping and stress-related negative sequelae (11, mobilization of the ventromedial prefrontal cortex (VmPFC), marked by initial hypoactivity followed by increased VmPFC activation, 18, 19). Although previous neuroimaging research has documented pointed to the VmPFC as a key locus of the emotional and behav- ioral control network. Consistent with this finding, greater neural increased brain limbic-striatal activation during stress, with evi- flexibility signals in the VmPFC during stress correlated with active dence of reduced ventromedial prefrontal cortex (VmPFC) or coping ratings whereas lower dynamic activity in the VmPFC also dorsolateral prefrontal cortex (DLPFC) response, these func- predicted a higher level of maladaptive coping behaviors in real life, tional responses may represent an initial and early neural stress including binge alcohol intake, emotional eating, and frequency of response as shown by research using event-related presentation arguments and fights. These findings demonstrate acute functional of aversive images or very brief block presentation of movie clips neuroplasticity during stress, with distinct and separable brain net- or trauma/stress imagery to assess neural stress responses (14, 17, works that underlie critical components of the stress response, and a 20). Thus, few studies have focused on the acute temporal dy- specific role for VmPFC neuroflexibility in stress-resilient coping. namics of the limbic-striatal responses and the prefrontal cortical responses to stress or how the brain may dynamically adapt to functional neuroimaging | stress | resilience coping | binge alcohol intake | reduce and respond to acute stress in the moment. For example, emotional eating Significance npredictable and uncontrollable events are highly common in Udaily life, and our cognitive and behavioral coping responses We live in a time of increasing terror, stress, and trauma, and yet are central to determining the long-term negative or positive effects humans show a remarkable ability to cope under high stress of stress on health. Consider the following example. You are in the states. How the brain supports such active resilient coping is not underground on your way to give a critical presentation at a large well-understood. Findings showed high stress levels are ac- meeting and the train stops. There is no information on what has companied by dynamic brain signals in circuits representing the happened and the phone signal is down. We almost instantaneously stress reaction, adaptation, and behavioral control responses. In addition, a ventromedial prefrontal cortical region showed ini- begin to consider options of what to do: Perhaps seek out someone tial decreases in brain activation, but then mobilized with in- in authority or, alternatively, quickly without much thought push creased activation, and this dynamic change was correlated with alarm buttons to get out. Active coping (involving strategies such as active coping. Conversely, individuals who failed to show such altering perception via appraisal strategies, reframing or reasoning, “neuroflexibility” in this specific ventromedial prefrontal region exercising cognitive and behavioral control, and problem solving reported higher maladaptive coping behaviors. Findings suggest during stress) signals resilience and regulates stress to promote that strategies to promote such neuroflexibility under stress adaptive behaviors and positive health outcomes (1–3). On the may increase stress resilience in humans. COGNITIVE SCIENCES other hand, extensive research documents that poor emotional and PSYCHOLOGICAL AND behavioral coping (using avoidance, suppression, rumination, and Author contributions: R.S., R.T.C., and D.S. designed research; R.S., C.M.L., and D.S. per- formed research; C.M.L. and D.S. analyzed data; R.S. wrote the paper; R.T.C. provided habitual motivation during stress) is associated with a number of neuroimaging parameters and support; and D.S. generated all data for figures and tables. – maladaptive health behaviors and poor health outcomes (3 7). The authors declare no conflict of interest. Despite this evidence, the specific neural components of the stress This article is a PNAS Direct Submission. response that may underlie acute stress reactivity, adaptation, and 1To whom correspondence should be addressed. Email: [email protected]. active coping that support stress resilience mechanisms in humans This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. NEUROSCIENCE are not well-understood. 1073/pnas.1600965113/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1600965113 PNAS | August 2, 2016 | vol. 113 | no. 31 | 8837–8842 Downloaded by guest on September 29, 2021 ’ Stress response during stress will be associated with a subject sreportsof A Stress + Stress Stress + image _ _ _ _ image images Ratings emotional and behavioral coping. Study (per Run) Design Neutral Neutral Neutral Neutral _ _ _ _ + image image Ratings + image (per Run) Results (run1- run6) _ _ Thirty community young adult participants (mean age 25.7 (8.61) y 3 min. _ _ _ _ _ _ _ 6 _min. _ _ _ _ _ _ _ 4 min. Cort. Cort. Cort. with no history of physical or mental health disorders participated B Baseline Provocation Recovery Stress Reponse in a multimethod functional magnetic resonance imaging (fMRI) i) Stress Stress ii) Arousal iii) Heart Rate iv) Cortisol scan involving a brief and passive sustained provocation procedure 8 8 Neutral * * to assess separable and distinct temporally related neural pro- *** *** 0.2 0.2 6 6 0.1 cesses involved in the stress response and in active coping. The 0.1 4 4 0.0 fMRI paradigm involved brief successive exposure to a block of 0.0 -0.1 highly aversive images of terror, violence, mutilation, fear, disgust, 2 2 -0.2 -0.1 and desperation that were compared with a no-stress, neutral 0 0 -0.3 Change from Baseline (Z) Change from Baseline (Z) Neutral Stress Neutral Stress control block involving nonaversive neutral images [all pictures Early Mid Late Early Mid Late from the International Affective Picture System (28)]; each image Fig. 1. Study design and subjective, physiologic, and neuroendocrine stress of the stress/neutral block was presented for 5 s per image with a response. (A) A sample experimental successive run block made up of three 1-s interstimulus interval (ISI), over six successive runs of 60 s each baseline gray fixation runs, followed by six stress/neutral provocation runs (10 images per run) making up each of the stress and neutral and a 4-min recovery period to constitute each of the stress and neutral run blocks to provoke sustained unpredictable emotional stress versus blocks. (B) Significantly increased subjective stress and arousal ratings (visual analog 1–9 scale; P < 0.0001
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