DOI QR코드

DOI QR Code

Increased Frontal Gamma and Posterior Delta Powers as Potential Neurophysiological Correlates Differentiating Posttraumatic Stress Disorder from Anxiety Disorders

  • Moon, Sun-Young (Department of Psychiatry, Seoul National University Hospital) ;
  • Choi, Yoo Bin (Department of Psychiatry, Seoul National University Hospital) ;
  • Jung, Hee Kyung (Department of Psychiatry, Seoul National University Hospital) ;
  • Lee, Yoonji Irene (Department of Psychiatry, Seoul National University Hospital) ;
  • Choi, Soo-Hee (Department of Psychiatry, Seoul National University Hospital)
  • Received : 2018.07.06
  • Accepted : 2018.09.30
  • Published : 2018.11.30

Abstract

Objective Posttraumatic stress disorder (PTSD) is distinct from anxiety disorders in its etiology and clinical symptomatology, and was reclassified into trauma- and stressor-related disorders in DSM-5. This study aimed to find neurophysiological correlates differentiating PTSD from anxiety disorders using resting-state quantitative electroencephalography (qEEG). Methods Thirty-six patients with either PTSD or acute stress disorder and 79 patients with anxiety disorder were included in the analysis. qEEG data of absolute and relative powers and patients' medication status on the day of qEEG examination were obtained. Electrodes were grouped into frontal, central, and posterior regions to analyze for regional differences. General linear models were utilized to test for group differences in absolute and relative powers while controlling for medications. Results PTSD patients differed from those with anxiety disorders in overall absolute powers [F(5,327)=2.601, p=0.025]. Specifically, overall absolute delta powers [F(1,331)=4.363, p=0.037], and overall relative gamma powers [F(1,331)=3.965, p=0.047] were increased in PTSD group compared to anxiety disorder group. Post hoc analysis regarding brain regions showed that the increase in absolute delta powers were localized to the posterior region [F(1,107)=4.001, p=0.048]. Additionally, frontal absolute gamma powers [F(1,107)=4.138, p=0.044] were increased in PTSD group compared to anxiety disorder group. Conclusion Our study suggests increased overall absolute delta powers and relative gamma powers as potential markers that could differentiate PTSD from anxiety disorders. Moreover, increased frontal absolute gamma and posterior delta powers might pose as novel markers of PTSD, which may reflect its distinct symptomatology.

Keywords

Acknowledgement

Supported by : National Research Foundation of Korea (NRF)

References

  1. Careaga MBL, Girardi CEN, Suchecki D. Understanding posttraumatic stress disorder through fear conditioning, extinction and reconsolidation. Neurosci Biobehav Rev 2016;71:48-57. https://doi.org/10.1016/j.neubiorev.2016.08.023
  2. Shin LM, Liberzon I. The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 2010;35:169-191. https://doi.org/10.1038/npp.2009.83
  3. American Psychiatric Association. DSM-IV-TR: Diagnostic and Statistical Manual of Mental Disorders, Text Revision. Washington, DC; American Psychiatric Association; 2000.
  4. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders $(DSM-5^{(R)})$. Washington, DC: American Psychiatric Pub; 2013.
  5. Etkin A, Wager TD. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am J Psychiatry 2007;164:1476-1488. https://doi.org/10.1176/appi.ajp.2007.07030504
  6. Milad MR, Quirk GJ. Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 2002;420:70-74. https://doi.org/10.1038/nature01138
  7. Delgado MR, Nearing KI, LeDoux JE, Phelps EA. Neural circuitry underlying the regulation of conditioned fear and its relation to extinction. Neuron 2008;59:829-838. https://doi.org/10.1016/j.neuron.2008.06.029
  8. Urry HL, Van Reekum CM, Johnstone T, Kalin NH, Thurow ME, Schaefer HS, et al. Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. J Neurosci 2006;26:4415-4425. https://doi.org/10.1523/JNEUROSCI.3215-05.2006
  9. Wager TD, Davidson ML, Hughes BL, Lindquist MA, Ochsner KN. Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron 2008;59:1037-1050. https://doi.org/10.1016/j.neuron.2008.09.006
  10. Welborn BL, Papademetris X, Reis DL, Rajeevan N, Bloise SM, Gray JR. Variation in orbitofrontal cortex volume: relation to sex, emotion regulation and affect. Soc Cogn Affect Neurosci 2009;4:328-339. https://doi.org/10.1093/scan/nsp028
  11. Russo SJ, Murrough JW, Han MH, Charney DS, Nestler EJ. Neurobiology of resilience. Nat Neurosci 2012;15:1475-1484. https://doi.org/10.1038/nn.3234
  12. Davidson RJ. Affective style, psychopathology, and resilience: brain mechanisms and plasticity. Am Psychol 2000;55:1196-1214. https://doi.org/10.1037/0003-066X.55.11.1196
  13. Shin LM, Wright CI, Cannistraro PA, Wedig MM, McMullin K, Martis B, et al. A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. Arch Gen Psychiatry 2005;62:273-281. https://doi.org/10.1001/archpsyc.62.3.273
  14. Kim MJ, Chey J, Chung A, Bae S, Khang H, Ham B, et al. Diminished rostral anterior cingulate activity in response to threat-related events in posttraumatic stress disorder. J Psychiatr Res 2008;42:268-277. https://doi.org/10.1016/j.jpsychires.2007.02.003
  15. Admon R, Milad MR, Hendler T. A causal model of post-traumatic stress disorder: disentangling predisposed from acquired neural abnormalities. Trends Cogn Sci 2013;17:337-347. https://doi.org/10.1016/j.tics.2013.05.005
  16. Moscovitch DA, Santesso DL, Miskovic V, McCabe RE, Antony MM, Schmidt LA. Frontal EEG asymmetry and symptom response to cognitive behavioral therapy in patients with social anxiety disorder. Biol Psychol 2011;87:379-385. https://doi.org/10.1016/j.biopsycho.2011.04.009
  17. Knott VJ, Bakish D, Lusk S, Barkely J Perugini M. Quantitative EEG correlates of panic disorder. Psychiatry Res 1996;68:31-39. https://doi.org/10.1016/S0925-4927(96)02962-9
  18. Sachs G, Anderer P, Dantendorfer K, Saletu B. EEG mapping in patients with social phobia. Psychiatry Res 2004;131:237-247. https://doi.org/10.1016/j.pscychresns.2003.08.007
  19. Begic D, Hotujac L, Jokic-Begic N. Electroencephalographic comparison of veterans with combat-related post-traumatic stress disorder and healthy subjects. Int J Psychophysiol 2001;40:167-172. https://doi.org/10.1016/S0167-8760(00)00153-7
  20. Todder D, Levine J, Abujumah A, Mater M, Cohen H, Kaplan Z. The quantitative electroencephalogram and the low-resolution electrical tomographic analysis in posttraumatic stress disorder. Clin EEG Neurosci 2012;43:48-53. https://doi.org/10.1177/1550059411428716
  21. Imperatori C, Farina B, Quintiliani MI, Onofri A, Gattinara PC, Lepore M, et al. Aberrant EEG functional connectivity and EEG power spectra in resting state post-traumatic stress disorder: A sLORETA study. Biol Psychol 2014;102:10-17. https://doi.org/10.1016/j.biopsycho.2014.07.011
  22. Jokic-Begic N, Begic D. Quantitative electroencephalogram (qEEG) in combat veterans with post-traumatic stress disorder (PTSD). Nord J Psychiatry 2003;57:351-355. https://doi.org/10.1080/08039480310002688
  23. Lee S-H, Yoon S, Kim JI, Jin SH, Chung CK. Functional connectivity of resting state EEG and symptom severity in patients with post-traumatic stress disorder. Prog Neuropsychopharmacol Biol Psychiatry 2014;51:51-57. https://doi.org/10.1016/j.pnpbp.2014.01.008
  24. Shim M, Im C, Lee S. Disrupted cortical brain network in post-traumatic stress disorder patients: a resting-state electroencephalographic study. Transl Psychiatry 2017;7:e1231. https://doi.org/10.1038/tp.2017.200
  25. Jang KI, Shim M, Lee SM, Huh HJ, Huh S, Joo JY, et al. Increased beta power in the bereaved families of the S ewol ferry disaster: a paradoxical compensatory phenomenon? A two channel electroencephalography study. Psychiatry Clin Neurosci 2017;71:759-768. https://doi.org/10.1111/pcn.12546
  26. World Health Organization. The ICD-10 Classification of Mental and Behavioural Disorders : Diagnostic Criteria for Research. Geneva; World Health Organization; 1993.
  27. Gardner DM, Murphy AL, O'Donnell H, Centorrino F, Baldessarini RJ. International consensus study of antipsychotic dosing. Am J Psychiatry 2010;167:686-693. https://doi.org/10.1176/appi.ajp.2009.09060802
  28. Ashton CH. Benzodiazepines: How They Work and How to Withdraw. The Ashton Manual. Newcastle: Newcastle University; 2006.
  29. Bollini P, Pampaliona S, Tibaldi G, Kupelnick B, Munizza C. Effectiveness of antidepressants: meta-analysis of dose-effect relationships in randomised clinical trials. Br J Psychiatry 1999;174:297-303. https://doi.org/10.1192/bjp.174.4.297
  30. Nierenberg AA, Greist JH, Mallinckrodt CH, Prakash A, Sambunaris A, Tollefson GD, et al. Duloxetine versus escitalopram and placebo in the treatment of patients with major depressive disorder: onset of antidepressant action, a non-inferiority study. Curr Med Res Opin 2007;23:401-416. https://doi.org/10.1185/030079906X167453
  31. Kim S, Shin JE, Kim MJ, Kwon JS, Choi SH. Correlation between Quantitative Electroencephalogram Findings and Neurocognitive Functions in Patients with Obsessive-Compulsive Disorder and Schizophrenia. Korean J Biol Psychiatry 2016;23:193-198.
  32. Son K, Choi J, Lee J, Park S, Lim J, Lee J, et al. Neurophysiological features of Internet gaming disorder and alcohol use disorder: a restingstate EEG study. Transl Psychiatry 2015;5:e628. https://doi.org/10.1038/tp.2015.124
  33. Sheynin J, Liberzon I. Circuit dysregulation and circuit-based treatments in posttraumatic stress disorder. Neurosci Lett 2017;649:133-138. https://doi.org/10.1016/j.neulet.2016.11.014
  34. Roux F, Uhlhaas PJ. Working memory and neural oscillations: alphagamma versus theta-gamma codes for distinct WM information? Trends Cogn Sci 2014;18:16-25. https://doi.org/10.1016/j.tics.2013.10.010
  35. Phaf RH, Kan KJ. The automaticity of emotional Stroop: A meta-analysis. J Behav Ther Exp Psychiatry 2007;38:184-199. https://doi.org/10.1016/j.jbtep.2006.10.008
  36. Armengol CG, Cavanaugh-Sawan A. Differential Performance of Post-traumatic stress disorder (PTSD), Attention deficit hyperactivity disorder (ADHD), and a Non-Clinical Control Group on Tests of Attention and Inhibition. Rev Esp Neurophysiol 2003;5:65-79.
  37. Brown VM, Morey RA. Neural systems for cognitive and emotional processing in posttraumatic stress disorder. Front Psychol 2012;3:449.
  38. Schweizer S, Dalgleish T. Emotional working memory capacity in posttraumatic stress disorder (PTSD). Behav Res Ther 2011;49:498-504. https://doi.org/10.1016/j.brat.2011.05.007
  39. Shaw ME, Moores KA, Clark RC, McFarlane AC, Strother SC, Bryant RA, et al. Functional connectivity reveals inefficient working memory systems in post-traumatic stress disorder. Psychiatry Res 2009;172: 35-241.
  40. Bremner JD, Narayan M, Staib LH, Southwick SM, McGlashan T, Charney DS. Neural correlates of memories of childhood sexual abuse in women with and without posttraumatic stress disorder. Am J Psychiatry 1999;156:1787-1795.
  41. Bremner JD, Vermetten E, Vythilingam M, Afzal N, Schmahl C, Elzinga B, et al. Neural correlates of the classic color and emotional stroop in women with abuse-related posttraumatic stress disorder. Biol Psychiatry 2004;55:612-620. https://doi.org/10.1016/j.biopsych.2003.10.001
  42. Yin Y, Li L, Jin C, Hu X, Duan L, Eyler LT, et al. Abnormal baseline brain activity in posttraumatic stress disorder: a resting-state functional magnetic resonance imaging study. Neurosci Lett 2011;498:185-189. https://doi.org/10.1016/j.neulet.2011.02.069
  43. Marshall AC, Cooper NR. The association between high levels of cumulative life stress and aberrant resting state EEG dynamics in old age. Biol Psychol 2017;127:64-73. https://doi.org/10.1016/j.biopsycho.2017.05.005
  44. Ansell EB, Rando K, Tuit K, Guarnaccia J, Sinha R. Cumulative adversity and smaller gray matter volume in medial prefrontal, anterior cingulate, and insula regions. Biol Psychiatry 2012;72:57-64. https://doi.org/10.1016/j.biopsych.2011.11.022
  45. Centorrino F, Price BH, Tuttle M, Bahk WM, Hennen J, Albert MJ, et al. EEG abnormalities during treatment with typical and atypical antipsychotics. Am J Psychiatry 2002;159:109-115. https://doi.org/10.1176/appi.ajp.159.1.109
  46. Buchsbaum MS, Hazlett E, Sicotte N, Stein M, Wu J, Zetin M. Topographic EEG changes with benzodiazepine administration in generalized anxiety disorder. Biol Psychiatry 1985;20:837-842.

Cited by

  1. Predicting Symptomatic and Functional Improvements over 1 Year in Patients with First-Episode Psychosis Using Resting-State Electroencephalography vol.16, pp.9, 2018, https://doi.org/10.30773/pi.2019.06.20.1
  2. Two Tell-tale Perspectives of PTSD : Neurobiological Abnormalities and Bayesian Regulatory Network of the Underlying Disorder in a Refugee Context vol.3, pp.3, 2018, https://doi.org/10.1145/3351259
  3. Classifying post-traumatic stress disorder using the magnetoencephalographic connectome and machine learning vol.10, pp.None, 2018, https://doi.org/10.1038/s41598-020-62713-5