Sex commonalities and differences in the relationship between resilient personality and the intrinsic connectivity of the salience and default mode networks

Increased resilience is associated with better health outcomes and reduced morbidity in response to injury and homeostatic perturbations. Proper functioning of the salience network (SN) and modulation of the default mode network (DMN) by SN may play a role in adaptively responding to stress. Here, we demonstrate that resilient personality in healthy subjects is associated with SN and DMN connectivity patterns and that these patterns are influenced by sex. While connectivity of SN with several brain regions including right anterior insula was significantly associated with resilient personality in both men and women, results suggest that increased functional integration of anterior DMN preferentially benefits women while increased functional integration of posterior DMN preferentially benefits men in terms of resilience. These findings may relate to previous demonstrations that men and women engage different information processing and behavioral strategies to achieve resilience and highlight the importance of considering sex in resilience research.

[1]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[2]  J. Pekar,et al.  On the relationship between seed‐based and ICA‐based measures of functional connectivity , 2011, Magnetic resonance in medicine.

[3]  G. Glover,et al.  Resting-State Functional Connectivity in Major Depression: Abnormally Increased Contributions from Subgenual Cingulate Cortex and Thalamus , 2007, Biological Psychiatry.

[4]  O. Blanke,et al.  The Out-of-Body Experience: Disturbed Self-Processing at the Temporo-Parietal Junction , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[5]  Jessica A. Turner,et al.  Behavioral Interpretations of Intrinsic Connectivity Networks , 2011, Journal of Cognitive Neuroscience.

[6]  M. Hoptman,et al.  Functional connectivity in apathy of late-life depression: a preliminary study. , 2013, Journal of affective disorders.

[7]  G. Windle,et al.  A methodological review of resilience measurement scales , 2011, Health and quality of life outcomes.

[8]  Y. Hamama-Raz.  Does psychological adjustment of melanoma survivors differs between genders? , 2012, Psycho-oncology.

[9]  L. Ferrucci,et al.  Personality and metabolic syndrome , 2010, AGE.

[10]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[11]  Antao Chen,et al.  Gender differences in behavioral inhibitory control: ERP evidence from a two-choice oddball task. , 2008, Psychophysiology.

[12]  S. Rombouts,et al.  Resting-state functional connectivity abnormalities in limbic and salience networks in social anxiety disorder without comorbidity , 2013, European Neuropsychopharmacology.

[13]  Jennifer H. Pfeifer,et al.  How and where: Theory-of-mind in the brain , 2014, Developmental Cognitive Neuroscience.

[14]  O. Sporns,et al.  The economy of brain network organization , 2012, Nature Reviews Neuroscience.

[15]  E. Maguire.  The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings. , 2001, Scandinavian journal of psychology.

[16]  J. Berry,et al.  Resilient, Undercontrolled, and Overcontrolled Personality Prototypes Among Persons With Spinal Cord Injury , 2007, Journal of personality assessment.

[17]  Marion Trousselard,et al.  Relationship between emotional experience and resilience: An fMRI study in fire-fighters , 2013, Neuropsychologia.

[18]  Aapo Hyvärinen,et al.  Validating the independent components of neuroimaging time series via clustering and visualization , 2004, NeuroImage.

[19]  John M. Pearson,et al.  Posterior cingulate cortex: adapting behavior to a changing world , 2011, Trends in Cognitive Sciences.

[20]  Sheldon Cohen,et al.  Psychological stress and disease. , 2007, JAMA.

[21]  Robert Leech,et al.  Salience network integrity predicts default mode network function after traumatic brain injury , 2012, Proceedings of the National Academy of Sciences.

[22]  B. Bunting,et al.  Associations between obesity (BMI and waist circumference) and socio-demographic factors, physical activity, dietary habits, life events, resilience, mood, perceived stress and hopelessness in healthy older Europeans , 2012, BMC Public Health.

[23]  Tracy Yuen,et al.  A systematic review of resilience in the physically ill. , 2011, Psychosomatics.

[24]  S. Southwick,et al.  The Science of Resilience: Implications for the Prevention and Treatment of Depression , 2012, Science.

[25]  O. Hjemdal,et al.  Resilience is a good predictor of hopelessness even after accounting for stressful life events, mood and personality (NEO-PI-R). , 2012, Scandinavian journal of psychology.

[26]  J. Gray,et al.  Testing Predictions From Personality Neuroscience , 2010, Psychological science.

[27]  Bruce S. McEwen,et al.  Psychobiological allostasis: resistance, resilience and vulnerability , 2011, Trends in Cognitive Sciences.

[28]  Tetsuya Iidaka,et al.  Imaging brain and immune association accompanying cognitive appraisal of an acute stressor , 2008, NeuroImage.

[29]  O. Blanke.  Multisensory brain mechanisms of bodily self-consciousness , 2012, Nature Reviews Neuroscience.

[30]  Xin Wang,et al.  Neural Dysregulation in Posttraumatic Stress Disorder: Evidence for Disrupted Equilibrium Between Salience and Default Mode Brain Networks , 2012, Psychosomatic medicine.

[31]  Yasumasa Okamoto,et al.  Personality traits and the amplitude of spontaneous low-frequency oscillations during resting state , 2011, Neuroscience Letters.

[32]  G. Hazlett,et al.  Reward circuitry in resilience to severe trauma: An fMRI investigation of resilient special forces soldiers , 2009, Psychiatry Research: Neuroimaging.

[33]  R. Saxe,et al.  What gets the attention of the temporo-parietal junction? An fMRI investigation of attention and theory of mind , 2010, Neuropsychologia.

[34]  M. Diehl,et al.  Age and sex differences in strategies of coping and defense across the life span. , 1996, Psychology and aging.

[35]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[36]  S. Debener,et al.  Default-mode brain dysfunction in mental disorders: A systematic review , 2009, Neuroscience & Biobehavioral Reviews.

[37]  T. Egner,et al.  Emotional processing in anterior cingulate and medial prefrontal cortex , 2011, Trends in Cognitive Sciences.

[38]  Marcus E. Raichle,et al.  The Restless Brain , 2011, Brain Connect..

[39]  Rebecca Elliott,et al.  Neuronal correlates of theory of mind and empathy: A functional magnetic resonance imaging study in a nonverbal task , 2006, NeuroImage.

[40]  Murray B Stein,et al.  Relationship of resilience to personality, coping, and psychiatric symptoms in young adults. , 2006, Behaviour research and therapy.

[41]  Michael L Platt,et al.  Allocentric Spatial Referencing of Neuronal Activity in Macaque Posterior Cingulate Cortex , 2006, The Journal of Neuroscience.

[42]  Anthony Randal McIntosh,et al.  Tracing the route to path analysis in neuroimaging , 2012, NeuroImage.

[43]  Terrence J. Sejnowski,et al.  The “independent components” of natural scenes are edge filters , 1997, Vision Research.

[44]  Anthony Randal McIntosh,et al.  Contexts and catalysts , 2007, Neuroinformatics.

[45]  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.

[46]  R. Maddock.  The retrosplenial cortex and emotion: new insights from functional neuroimaging of the human brain , 1999, Trends in Neurosciences.

[47]  A. Mackey,et al.  Resting-State fMRI , 2014, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[48]  D. Sharp,et al.  Fractionating the Default Mode Network: Distinct Contributions of the Ventral and Dorsal Posterior Cingulate Cortex to Cognitive Control , 2011, The Journal of Neuroscience.

[49]  M. Buonocore,et al.  Remembering familiar people: the posterior cingulate cortex and autobiographical memory retrieval , 2001, Neuroscience.

[50]  M. Buonocore,et al.  Posterior cingulate cortex activation by emotional words: fMRI evidence from a valence decision task , 2003, Human brain mapping.

[51]  Marte Swart,et al.  Altered resting state connectivity of the default mode network in alexithymia. , 2012, Social cognitive and affective neuroscience.

[52]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[53]  Kristl Vonck,et al.  Functional connectivity of dissociation in patients with psychogenic non-epileptic seizures , 2011, Journal of Neurology, Neurosurgery & Psychiatry.

[54]  Angela D. Friederici,et al.  Sex differences in the preattentive processing of vocal emotional expressions , 2005, Neuroreport.

[55]  Larry Cahill,et al.  Sex‐Related Influences on the Neurobiology of Emotionally Influenced Memory , 2003, Annals of the New York Academy of Sciences.

[56]  Rafael Malach,et al.  Deconstructing the default: Cortical subdivision of the default mode/intrinsic system during self‐related processing , 2014, Human brain mapping.

[57]  G. Northoff,et al.  Distinction between Externally vs. Internally Guided Decision-Making: Operational Differences, Meta-Analytical Comparisons and Their Theoretical Implications , 2012, Front. Neurosci..

[58]  Timothy E. Ham,et al.  Cognitive Control and the Salience Network: An Investigation of Error Processing and Effective Connectivity , 2013, The Journal of Neuroscience.

[59]  Tor D Wager,et al.  The neural correlates of trait resilience when anticipating and recovering from threat. , 2008, Social cognitive and affective neuroscience.

[60]  Werner Strik,et al.  The effect of appraisal level on processing of emotional prosody in meaningless speech , 2008, NeuroImage.

[61]  Florin Dolcos,et al.  Sex differences in the response to emotional distraction: an event-related fMRI investigation , 2013, Cognitive, affective & behavioral neuroscience.

[62]  Anthony Randal McIntosh,et al.  Partial least squares analysis of neuroimaging data: applications and advances , 2004, NeuroImage.

[63]  Jack Block,et al.  IQ and ego-resiliency: conceptual and empirical connections and separateness. , 1996 .

[64]  D. Sharp,et al.  The role of the posterior cingulate cortex in cognition and disease. , 2014, Brain : a journal of neurology.

[65]  John A Updegraff,et al.  Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. , 2000, Psychological review.

[66]  H. Wagner,et al.  Protective factors and risk modification of violence in Iraq and Afghanistan War veterans. , 2012, The Journal of clinical psychiatry.

[67]  D. Sheehan,et al.  The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. , 1998, The Journal of clinical psychiatry.

[68]  R. Buckner,et al.  Functional-Anatomic Fractionation of the Brain's Default Network , 2010, Neuron.

[69]  Lisa A. Kort-Butler.  Coping Styles and Sex Differences in Depressive Symptoms and Delinquent Behavior , 2009, Journal of youth and adolescence.

[70]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[71]  Yufeng Zang,et al.  DPARSF: A MATLAB Toolbox for “Pipeline” Data Analysis of Resting-State fMRI , 2010 .

[72]  R. Lanius,et al.  Neural correlates and predictive power of trait resilience in an acutely traumatized sample: a pilot investigation. , 2012, The Journal of clinical psychiatry.

[73]  P. Costa,et al.  The revised NEO personality inventory (NEO-PI-R) , 2008 .

[74]  Bernd Foerster,et al.  Police officers under attack: resilience implications of an fMRI study. , 2011, Journal of psychiatric research.

[75]  Alan C. Evans,et al.  Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. , 1993, Journal of neurophysiology.

[76]  E. Nestler,et al.  Neurobiology of resilience , 2011, Nature Neuroscience.

[77]  Simon B Eickhoff,et al.  Investigating the Functional Heterogeneity of the Default Mode Network Using Coordinate-Based Meta-Analytic Modeling , 2009, The Journal of Neuroscience.