Unique insula subregion resting-state functional connectivity with amygdala complexes in posttraumatic stress disorder and its dissociative subtype

Psychiatry Research - Neuroimaging

Volumn 250, Issue , 2016, Pages 61-72

  Nicholson, Andrew A ^a   Sapru, Iman ^a   Densmore, Maria ^b   Frewen, Paul A ^a   Neufeld, Richard W J ^a   Théberge, Jean ^a,b,c   McKinnon, Margaret C ^d,e   Lanius, Ruth A ^a,b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^c ST JOSEPH S HEALTH CENTRE   (Canada)

^d MCMASTER UNIVERSITY   (Canada)

^e MCMASTER UNIVERSITY   (Canada)

Author keywords

Basolateral amygdala; fMRI; Insular cortex; PTSD

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ANTERIOR INSULA; ARTICLE; BASOLATERAL AMYGDALA; CONTROLLED STUDY; DEPERSONALIZATION; DEREALIZATION SYMPTOM; DISSOCIATIVE DISORDER; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HEMISPHERE; HUMAN; MAJOR CLINICAL STUDY; MALE; POSTERIOR INSULA; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; RESTING STATE NETWORK; AMYGDALA; AROUSAL; BRAIN CORTEX; DIAGNOSTIC IMAGING; EMOTION; MIDDLE AGED; NERVE CELL NETWORK; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; PSYCHOLOGY; REST;

ADULT; AMYGDALA; AROUSAL; CEREBRAL CORTEX; DISSOCIATIVE DISORDERS; EMOTIONS; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NERVE NET; NEURAL PATHWAYS; REST; STRESS DISORDERS, POST-TRAUMATIC;

EID: 84961918629     PISSN: 09254927     EISSN: 18727506     Source Type: Journal    
DOI: 10.1016/j.pscychresns.2016.02.002     Document Type: Article

References (55)

1. Aghajani M., Veer I.M., van Hoof M.J., Rombouts S.A.R.B., van der Wee N.J., Vermeiren R.R.J.M. Abnormal functional architecture of amygdala-centered networks in adolescent posttraumatic stress disorder. Hum. Brain Mapp 2016, 10.1002/hbm.23093.
2. Aupperle R.L., Melrose A.J., Stein M.B., Paulus M.P. Executive function and PTSD: Disengaging from trauma. Neuropharmacology 2012, 62:686-694.
3. Baur V., Hänggi J., Langer N., Jäncke L. Resting-state functional and structural connectivity within an insula-amygdala route specifically index state and trait anxiety. Biol. Psychiatry 2013, 73:85-92.
4. Beck A.T., Guth D., Steer R.A., Ball R. Screening for major depression disorders in medical inpatients with the beck depression inventory for primary care. Behav. Res. Ther. 1997, 35:785-791.
5. Bernstein D.P., Stein J.A., Newcomb M.D., Walker E., Pogge D., Ahluvalia T., Stokes J., Handelsman L., Medrano M., Desmond D., Zule W. Development and validation of a brief screening version of the Childhood Truama Questionnaire. Child Abuse Negl. 2003, 27:169-190.
6. Birn R.M., Murphy K., Handwerker D.A., Bandettini P.A. fMRI in the presence of task-correlated breathing variations. Neuroimage 2009, 47:1092-1104.
7. Blake D.D., Weathers F.W., Nagy L.M., Kaloupek D.G., Gusman F.D., Charney D.S., Keane T.M. The development of a clinician-administered PTSD scale. J. Trauma. Stress. 1995, 8:75-90.
8. Briere J., Weathers F.W., Runtz M. Is dissociation a multidimensional construct? Data from the multiscale dissociation inventory. J. Trauma. Stress. 2005, 18:221-231.
9. Brown V.M., LaBar K.S., Haswell C.C., Gold A.L., Mid-Atlantic MIRECC Workgroup, McCarthy G., Morey R.A. Altered resting-state functional connectivity of basolateral and centromedial amygdala complexes in posttraumatic stress disorder. Neuropsychopharmacology 2014, 36:361-369.
10. Carrion V.G., Garrett A., Menon V., Weems C.F., Reiss A.L. Posttraumatic stress symptoms and brain function during a response-inhibition task: an fMRI study in youth. Depression Anxiety 2008, 25:514-526.
11. Cauda F., D'Agata F., Sacco K., Duca S., Geminiani G., Vercelli A. Functional connectivity of the insula in the resting brain. Neuroimage 2011, 55:8-23.
12. Cisler J.M., Steele J.S., Lenow J.K., Smitherman S., Everett B., Messias E., Kilts C.D. Functional reorganization of neural networks during repeated exposure to the traumatic memory in posttraumatic stress disorder: An exploratory fMRI study. J. Psychiatr. Res. 2014, 48:47-55.
13. Cloutman L.L., Binney R.J., Drakesmith M., Parker G.J.M., Lambon Ralph M.A. The variation of function across the human insula mirrors its patterns of structural connectivity: evidence from in vivo probabilistic tractography. NeuroImage 2012, 59:3514-3521.
14. Cordes D., Haughton V.M., Arfanakis K., Carew J.D., Turski P.A., Moritz C.H., Quigley M.A., Meyerand M.E. Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. AJNR Am. J. Neuroradiol. 2001, 22:1326-1333.
15. Craig A.D.B. How do you feel-now? The anterior insula and human awareness. Nat. Rev. Neurosci. 2009, 10:59-70.
16. Craig A.D.B. Significance of the insula for the evolution of human awareness of feelings from the body. Ann. N. Y. Acad. Sci. 2011, 1225:72-82.
17. Critchley H.D., Wiens S., Rotshtein P., Ohman A., Dolan R.J. Neural systems supporting interoceptive awareness. Nat. Neurosci. 2004, 7:189-195.
18. Deen B., Pitskel N.B., Pelphrey K.A. Three systems of insular functional connectivity identified with cluster analysis. Cereb. Cortex 2011, 21:1498-1506.
19. Eickhoff S.B., Stephan K.E., Mohlberg H., Grefkes C., Fink G.R., Amunts K., Zilles K. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 2005, 25:1325-1335.
20. Etkin A., Wager T.D. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am. J. Psychiatry 2007, 165:1476-1488.
21. First M.B. User's guide for the structured clinical interview for DSM-IV axis I disorders SCID-I: Clinician version 1997, American Psychiatric Press, Washington DC.
22. Fonzo G.A., Simmons A.N., Thorp S.R., Norman S.B., Paulus M.P., Stein M.B. Exaggerated and disconnected insular-amygdalar blood oxygenation level-dependent response to threat-related emotional faces in women with intimate-partner violence posttraumatic stress disorder. Biol. Psychiatry 2010, 68:433-441.
23. Gasquoine P.G. Contributions of the insula to cognition and emotion. Neuropsychol. Rev. 2014, 24:77-87.
24. Hopper J.W., Frewen P.A., van der Kolk B.A., Lanius R.A. Neural correlates of reexperiencing, avoidance, and dissociation in PTSD: symptom dimensions and emotion dysregulation in responses to script-driven trauma imagery. J. Trauma. Stress. 2007, 20:713-725.
25. Ichesco E., Schmidt-Wilcke T., Bhavsar R., Clauw D.J., Peltier S.J., Kim J.N., Vitaly H., Johnson P., Kairys A.E., Williams D.A., Harris R.E. Altered resting state connectivity of the insular cortex in individuals with fibromyalgia. J. Pain 2014, 15:815-882.
26. Jovanovic T., Ressler K.J. How the neurocircuitry and genetics of fear inhibition may inform our understanding of PTSD. Am. J. Psychiatry 2010, 167:648-662.
27. Kurth F., Zilles K., Fox P.T., Laird A.R., Eickhoff S.B. A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct. Funct. 2010, 214:519-534.
28. Lancaster J.L., Woldorff M.G., Parsons L.M., Liotti M., Freitas C.S., Rainey L., Kochunov P.V., Nickerson D., Mikiten S.A., Fox P.T. Automated Talairach Atlas labels for functional brain mapping. Hum. Brain Mapp. 2000, 10:120-131.
29. Lanius R.A., Brand B., Vermetten E., Frewen P.A., Spiegel D. The dissociative subtype of posttraumatic stress disorder: rationale, clinical and neurobiological evidence, and implications. Depression Anxiety 2012, 29:701-708.
30. Lanius R.A., Frewen P.A., Tursich M., Jetly R., Mckinnon M.C. Restoring large-scale brain networks in PTSD and related disorders: a proposal for neuroscientifically-informed treatment interventions. Eur. J. Psychotraumatol. 2015, 1:1-12.
31. Lanius R.A., Vermetten R., Loewenstein R.J., Brand B., Christian S., Bremner J.D., Spiegel D. Emotion modulation in PTSD: clinical and neurobiological evidence for a dissociative subtype. Am. J. Psychiatry 2010, 167:640-647.
32. Lanius R.A., Williamson P.C., Bluhm R.L., Densmore M., Boksman K., Neufeld R.W.J., Gati J.S., Menon R.S. Functional connectivity of dissociative responses in posttraumatic stress disorder: a functional magnetic resonance imaging investigation. Biol. Psychiatry 2005, 57:873-884.
33. Maldjian J.A., Laurienti P.J., Burdette J.B., Kraft R.A. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 2003, 19:1233-1239.
34. Mazza M., Tempesta D., Pino M.C., Catalucci A., Gallucci M., Ferrara M. Regional cerebral changes and functional connectivity during the observation of negative emotional stimuli in subjects with post-traumatic stress disorder. Eur. Arch. Psychiatry Clin. Neurosci. 2013, 263:575-583.
35. Meier L., Friedrich H., Federspiel A., Jann K., Morishima Y., Landis B.N., Wiest R., Strik R., Dierks T. Rivalry of homeostatic and sensory-evoked emotions: Dehydration attenuates olfactory disgust and its neural correlates. NeuroImage 2015, 114:120-127.
36. Menon V., Uddin L.Q. Saliency, switching, attention and control: a network model of insula function. Brain Struct. Funct. 2010, 214:655-667.
37. Mickleborough M.J.S., Daniels J.K., Coupland N.J., Kao R., Williamson P.C., Lanius U.F., Hegadoren K., Schore A., Densmore M., Stevens T., Lanius R.A. Effects of trauma-related cues on pain processing in posttraumatic stress disorder: an fMRI investigation. J. Psychiatry Neurosci. 2011, 36:6-14.
38. Nicholson A.A., Densmore M., Frewen P., Théberge J., Neufeld R.W.J., McKinnon M.C., Lanius R.A. The dissociative subtype of posttraumatic stress disorder: unique basolateral and centromedial amygdala complex connectivity. Neuropsychopharmacology 2015, 40(10):2317-2326. 10.1038/npp.2015.79.
39. Paulus M.P., Stein M.B. An insular view of anxiety. Biol. Psychiatry 2006, 60:383-387.
40. Pitman R.K., Rasmusson A.M., Koenen K.C., Shin L.M., Orr S.P., Gilbertson M.W., Milad M.R., Liberzon I. Biological studies of post-traumatic stress disorder. Nat. Rev. Neurosci. 2012, 13:769-787.
41. Qin L., Wang Z., Sun Y., Wan J., Su S., Zhou Y., Xu J. A preliminary study of alterations in default network connectivity in post-traumatic stress disorder patients following recent trauma. Brain Res. 2012, 1484:50-56.
42. Rosso I.M., Weiner M.R., Crowley D.J., Silveri M.M., Rauch S.L., Jensen J.E. Insula and anterior cingulate GABA levels in posttraumatic stress disorder: preliminary findings using magnetic resonance spectroscopy. Depression Anxiety 2014, 31:115-123.
43. Seeley W.W., Menon V., Schatzberg A.F., Keller J., Glover G.H., Kenna H., Reiss A.L., Greicius M.D. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 2007, 27:2349-2356.
44. Shin L.M., Liberzon I. The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 2010, 35:169-191.
45. Simmons A., Strigo I.A., Matthews S.C., Paulus M.P., Stein M.B. Initial evidence of a failure to activate right anterior insula during affective set shifting in posttraumatic stress disorder. Psychosom. Med. 2009, 71:373-377.
46. Sripada R.K., Garfinkel S.N., Liberzon I. Avoidant symptoms in PTSD predict fear circuit activation during multimodal fear extinction. Front. Hum. Neurosci. 2013, 7:672.
47. Sripada R.K., King A.P., Garfinkel S.N., Wang X., Sripada C.S., Welsh R.C., Liberzon I. Altered resting-state amygdala functional connectivity in men with posttraumatic stress disorder. J. Psychiatry Neurosci. 2012, 37:241-249.
48. Sripada R.K., King A.P., Welsh R.C., Garfinkel S.N., Wang X., Sripada C.S., Liberzon I. Neural dysregulation in posttraumatic stress disorder: evidence for disrupted equilibrium between salience and default mode brain networks. Psychosom. Med. 2012, 911:904-911.
49. Stein D.J., Koenen K.C., Friedman M.J., Hill E., McLaughlin K.A., Petukhova M., Ruscio A.M., Shahly V., Spiegel D., Borges G., Bunting B., Caldas-de-Almeida J.M., Girolamo G., Demyttenaere K., Florescu S., Haro J.M., Karam E.G., Kovess-Masfety V., Lee S., Matschinger H., Mladenova M., Posada-Villa J., Tachimori H., Viana M.C., Kessler R.C. Dissociation in posttraumatic stress disorder: evidence from the world mental health surveys. Biol. Psychiatry 2013, 73:302-312.
50. Steuwe C., Lanius R.A., Frewen P.A. Evidence for a dissociative subtype of PTSD by latent profile and confirmatory factor analyses in a civilian sample. Depression Anxiety 2012, 29:689-700.
51. Stevens J.S., Jovanovic T., Fani N., Ely T.D., Glover E.M., Bradley B., Ressler K.J. Disrupted amygdala-prefrontal functional connectivity in civilian women with posttraumatic stress disorder. J. Psychiatr. Res. 2013, 47:1469-1478.
52. Taylor K.S., Seminowicz D.A., Davis K.D. Two systems of resting state connectivity between the insula and cingulate cortex. Hum. Brain Mapp. 2009, 30:2731-2745.
53. Weston C.S.E. Posttraumatic stress disorder: a theoretical model of the hyperarousal subtype. Front. Psychiatry 2014, 5:1-20.
54. Wolf E.J., Miller M., Rearon A.F., Rybchenko K.A., Castillo D., Freund R. Latent class analysis of dissociation and PTSD: evidence for a dissociative subtype. Arch. Gen. Psychiatry 2012, 69:698-705.
55. Young K.D., Zotev V., Phillips R., Misaki M., Yuan H., Drevets W.C., Bodurka J. Real-time fMRI neurofeedback training of amygdala activity in patients with major depressive disorder. PLoS One 2014, 9:1-13.