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Altered Cortico-Limbic Functional Connectivity During an Empathy Task in Subjects with Post-Traumatic Stress Disorder

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Abstract

Empathy is a multidimensional construct consisting of cognitive (inferring mental states) and emotional (empathic concern) components. Emotional empathy is severely impaired in individuals affected by Post-Traumatic Stress Disorder (PTSD). Here, we investigated the neural correlates of such an emotional empathy dysfunction to shed light on the neural circuitry responsible for the social and emotional dysfunction in PTSD. We asked a group of PTSD and a group of healthy controls to solve a Multifaceted Empathy Test, measuring both cognitive and emotional empathy, and investigated the functional connectivity of the cortical areas involved in solving the test. The results revealed that, in healthy individuals, increased neural activity in the frontal cortex modulates activity in the insula while subjects perform the emotional empathy task; whereas, in individuals affected by PTSD, increased activity in limbic regions such the insula and the amygdala modulates activity in the frontal cortex while performing the emotional empathy task. These findings suggest that the lack of cortical top-down control of the frontal cortex on the limbic system in PTSD during empathic processing may explain the emotional and social difficulties experienced by individuals suffering from PTSD.

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References

  • American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders: DSM-V, 5 the dn. Arlington: AmericanPsychiatric Publishing.

    Book  Google Scholar 

  • Bandelow, B., Koch, M., Zimmermann, P., Biesold, K. H., Wedekind, D., & Falkai, P. (2012). Post-traumatic stress disorder (PTSD) in the German Armed Forces: a retrospective study in inpatients of a German army hospital. European Archives of Psychiatry and Clinical Neuroscience, 262(6), 459–467.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bernhardt, B. C., & Singer, T. (2012). The neural basis of empathy. Annual Review of Neuroscience, 35, 1–2.

    Article  PubMed  Google Scholar 

  • Carr, L., Iacoboni, M., Dubeau, M. C., Mazziotta, J. C., & Lenzi, G. L. (2003). Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas. Proceedings of the National Academy of Sciences of the United States of America, 100, 5497–5502.

    Article  PubMed  PubMed Central  Google Scholar 

  • Catani, C., Adenauer, H., Keil, J., Aichinger, H., & Neuner, F. (2009). Pattern of cortical activation during processing of aversive stimuli in traumatized survivors of war and torture. European Archives of Psychiatry and Clinical Neuroscience, 259(6), 340–351.

    Article  PubMed  Google Scholar 

  • Cloitre, M., Koenen, K. C., Cohen, L. R., & Han, H. (2002). Skills training in affective and interpersonal regulation followed by exposure: a phase-based treatment for PTSD related to childhood abuse. Journal of Consulting and Clinical Psychology, 70(5), 1067–1074.

    Article  PubMed  Google Scholar 

  • Collingridge, G.L., Peineau, S., Howland, J.G., & Wang, Y.T. (2010). Long-term depression in the CNS. Nature Reviews Neuroscience, 11(7), 459–473. Review.

  • Craig, A. D. (2005). Forebrain emotional asymmetry: a neuroanatomical basis? Trends in Cognitive Sciences, 9, 566–571.

    Article  PubMed  Google Scholar 

  • Decety, J., & Meyer, M. (2008). From emotion resonance to empathic understanding: a social developmental neuroscience account. Development and Psychopathology, 20(4), 1053–1080.

    Article  PubMed  Google Scholar 

  • Duerden, E. G., Arsalidou, M., Lee, M., & Taylor, M. J. (2013). Lateralization of affective processing in the insula. NeuroImage, 78, 159–175.

    Article  PubMed  Google Scholar 

  • Dziobek, I., Rogers, K., Fleck, S., Bahnemann, M., Heekeren, H. R., Wolf, O. T., et al. (2008). Dissociation of cognitive and emotional empathy in adults with Asperger syndrome using the Multifaceted Empathy Test (MET). Journal of Autism and Developmental Disorders, 38(3), 464–473.

    Article  PubMed  Google Scholar 

  • Dziobek, I., Preissler, S., Grozdanovic, Z., Heuser, I., Heekeren, H. R., & Roepke, S. (2011). Neuronal correlates of altered empathy and social cognition in borderline personality disorder. NeuroImage, 57(2), 539–548.

    Article  PubMed  Google Scholar 

  • Etkin, A., & Wager, T. D. (2007). Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry, 164(10), 1476–1488.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fonzo, G. A., Simmons, A. N., Thorp, S. R., Norman, S. B., Paulus, M. P., & Stein, M. B. (2010). Exaggerated and disconnected insular-amygdalar blood oxygenation level-dependent response to threat-related emotional faces in women with intimate-partner violence posttraumatic stress disorder. Biological Psychiatry, 68(5), 433–441.

    Article  PubMed  PubMed Central  Google Scholar 

  • Friston, K. J., Williams, S., Howard, R., Frackowiak, R. S. J., & Turner, R. J. (1996). Movement related effects in fmri time series. Magnetic Resonance in Medicine, 35(3), 346–355.

    Article  PubMed  Google Scholar 

  • Gallese, V. (2007). Before and below ‘theory of mind’: embodied simulation and the neural correlates of social cognition. Philosophical Transactions of the Royal Society, B: Biological Sciences, 362(1480), 659–669.

    Article  PubMed Central  Google Scholar 

  • Gilboa, A., Shalev, A. Y., Laor, L., Lester, H., Louzoun, Y., Chisin, R., et al. (2004). Functional connectivity of the prefrontal cortex and the amygdala in posttraumatic stress disorder. Biological Psychiatry, 55(3), 263–272.

    Article  PubMed  Google Scholar 

  • Goebel, R., Roebroeck, A., Kim, D. S., & Formisano, E. (2003). Investigating directed cortical interactions in time-resolved fMRI data using vector auto regressive modeling and Granger causality map**. Magnetic Resonance in Medicine, 21(10), 1251–1261.

    Google Scholar 

  • Hooker, C. I., Verosky, S. C., Germine, L. T., Knight, R. T., & D’Esposito, M. (2010). Neural activity during social signal perception correlates with self-reported empathy. Brain Research, 1308, 100–113.

    Article  PubMed  Google Scholar 

  • Hopper, J. W., Frewen, P. A., van der Kolk, B. A., & Lanius, R. A. (2007). Neural correlates of reexperiencing, avoidance, and dissociation in PTSD: symptom dimensions and emotion dysregulation in responses to script-driven trauma imagery. Journal of Traumatic Stress, 20(5), 713–725.

    Article  PubMed  Google Scholar 

  • Keightley, M. L., Winocur, G., Graham, S. J., Mayberg, H. S., Hevenor, S. J., & Grady, C. L. (2003). An fMRI study investigating cognitive modulation of brain regions associated with emotional processing of visual stimuli. Neuropsychology, 41(5), 585–596.

    Article  Google Scholar 

  • Liberzon, I., & Sripada, C. S. (2008). The functional neuroanatomy of PTSD: a critical review. Progress in Brain Research, 167, 151–169. Review.

    Article  PubMed  Google Scholar 

  • Long, H., Liu, B., Hou, B., Wang, C., Li, J., Qin, W., et al. (2013). The long rather than the short allele of 5-HTTLPR predisposes Han Chinese to anxiety and reduced connectivity between prefrontal cortex and amygdala. Neuroscience Bulletin, 29(1), 4–15. doi:10.1007/s12264-013-1299-x.

    Article  PubMed  Google Scholar 

  • Lui, S., Huang, X., Chen, L., Tang, H., Zhang, T., Li, X., et al. (2009). High-field MRI reveals an acute impact on brain function in survivors of the magnitude 8.0 earthquake in china. Proceedings of the National Academy of Sciences of the United States of America, 106(36), 15412–15417.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mazza, M., Giusti, L., Albanese, A., Mariano, M., Pino, M. C., & Roncone, R. (2012a). Social cognition disorders in military police officers affected by posttraumatic stress disorder after the attack of An-Nasiriyah in Iraq 2006. Psychiatry Research, 198(2), 248–252.

    Article  PubMed  Google Scholar 

  • Mazza, M., Catalucci, A., Mariano, M., Pino, M. C., Tripaldi, S., Roncone, R., et al. (2012b). Neural correlates of automatic perceptual sensitivity to facial affect in posttraumatic stress disorder subjects who survived L’Aquila eartquake of April 6, 2009. Brain Imaging and Behavior, 6(3), 374–386.

    Article  PubMed  Google Scholar 

  • Mazza, M., Tempesta, D., Pino, M. C., Catalucci, A., Gallucci, M., & Ferrara, M. (2013). Regional cerebral changes and functional connectivity during the observation of negative emotional stimuli in subjects with post-traumatic stress disorder. European Archives of Psychiatry and Clinical Neuroscience, 263(7), 575–583.

    Article  PubMed  Google Scholar 

  • Mazza, M., Tempesta, D., Pino, M. C., Nigri, A., Catalucci, A., Guadagni, V., et al. (2015). Neural activity related to cognitive and emotional empathy in post-traumatic stress disorder. Behavioural Brain Research, 282, 37–45.

    Article  PubMed  Google Scholar 

  • Nietlisbach, G., Maercker, A., Rössler, W., & Haker, H. (2010). Are empathic abilities impaired in posttraumatic stress disorder? Psychological Reports, 106(3), 832–844.

    Article  PubMed  Google Scholar 

  • Oppenheimer, S. M., Gelb, A., Girvin, J. P., & Hachinski, V. C. (1992). cardiovascular effects of human insular cortex stimulation. Neurology, 42, 1727–1732.

    Article  PubMed  Google Scholar 

  • Rauch, S. A., Shin, L. M., & Phelps, E. (2006). Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research—past, present, and future. Biological Psychiatry, 60(4), 376–382.

    Article  PubMed  Google Scholar 

  • Roebroeck, A., Formisano, E., & Goebel, R. (2005). Map** directed influence over the brain using Granger causality and fMRI. NeuroImage, 25(1), 230–242.

    Article  PubMed  Google Scholar 

  • Sadeh, N., Spielberg, J. M., Warren, S. L., Miller, G. A., & Heller, W. (2014). Aberrant neural connectivity during emotional processing associated with posttraumatic stress. Clinical Psychological Science, 2(6), 748–755.

    Article  PubMed  PubMed Central  Google Scholar 

  • Seitz, R. J., Schäfer, R., Scherfeld, D., Friederichs, S., Popp, K., Wittsack, H. J., et al. (2008). Valuating other people’s emotional face expression: a combined functional magnetic resonance imaging and electroencephalography study. Neuroscience, 152, 713–722.

    Article  PubMed  Google Scholar 

  • Seth, A. K., Chorley, P., & Barnett, L. C. (2013). Granger causality analysis of fMRI BOLD signals is invariant to hemodynamic convolution but not downsampling. NeuroImage, 65, 540–555.

    Article  PubMed  Google Scholar 

  • Shamay-Tsoory, S. G. (2011). The neural bases for empathy. The Neuroscientist, 17(1), 18–24.

    Article  PubMed  Google Scholar 

  • Shin, L. M., Rauch, S. L., & Pitman, R. K. (2006). Amygdala, medial prefrontal cortex, and hippocampal function in PTSD. Annals of the New York Academy of Sciences, 1071, 67–79.

    Article  PubMed  Google Scholar 

  • Simmons, A. N., Matthews, S. C., Strigo, I. A., Baker, D. G., Donovan, H. K., Motezadi, A., et al. (2011). Altered amygdala activation during face processing in Iraqi and Afghanistani war veterans. Biology of Mood & Anxiety Disorders, 1(1), 6.

    Article  Google Scholar 

  • Singer, T. (2006). The neuronal basis and ontogeny of empathy and mind reading: review of literature and implications for future research. Neuroscience & Biobehavioral Reviews, 30(6), 855–863.

    Article  Google Scholar 

  • Smith, S. M., Miller, K. L., Salimi-Khorshidi, G., Webster, M., Beckmann, C. F., Nichols, T. E., et al. (2011). Network modelling methods for fMRI. NeuroImage, 54(2), 875–891.

    Article  PubMed  Google Scholar 

  • Stevens, J. S., Jovanovic, T., Fani, N., Ely, T. D., Glover, E. M., Bradley, B., et al. (2013). Disrupted amygdala-prefrontal functional connectivity in civilian women with posttraumatic stress disorder. Journal of Psychiatric Research, 47(10), 1469–1478.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Professor Vidotto of the University of Padua for allow-ing us to use Brain Voyager QX 2.8 for data analysis.

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Correspondence to Maria Chiara Pino.

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Maria Chiara Pino, Daniela Tempesta, Alessia Catalucci, Monica Anselmi, Anna Nigri, Giuseppe Iaria, Michele Ferrara, and Monica Mazza declare no competing financial interests or potential conflicts of interest.

Experiment Participants

The study was conducted at the San Salvatore Hospital of L’Aquila, according to the principlesestablished by the Declaration of Helsinki. Ethical approval was obtained by the hospital’s Ethics Committee (ASL1 Avezzano-Sulmona-L’Aquila). Informed consent was obtained from all participants beforeinvestigation.

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In memoriam Massimo Gallucci

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Pino, M.C., Tempesta, D., Catalucci, A. et al. Altered Cortico-Limbic Functional Connectivity During an Empathy Task in Subjects with Post-Traumatic Stress Disorder. J Psychopathol Behav Assess 38, 398–405 (2016). https://doi.org/10.1007/s10862-016-9538-x

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