Auditory Steady-State Evoked Potentials in Post Traumatic Stress Disorder: Introduction of a Potential Biomarker
Abstract
Objective: The lack of steady-state evoked potential (SSEP) studies on post-traumatic stress disorder (PTSD) has led to undiscovered useful information about the pathophysiology of the disorder. Thus, we explored SSEP patterns in PTSD patients during a stop-signal task to disclose possible impairments in these informative brain potentials.
Method: 25 adult patients with PTSD and 25 healthy adults participated in this research. Subjects were assessed with electroencephalography while the tone signal stimuli at 40 Hz were used to evoke SSEPs and subjects performed a stop-signal task. The amplitude and phase of SSEPs were then computed in different brain regions. The subjects were also evaluated using the Mississippi PTSD questionnaire. Appropriate statistical methods such as repeated measure ANOVA were used to compare the two groups, and the correlation between SSEPs and clinical symptoms was assessed using Pearson correlation analysis.
Results: Patients showed considerably poorer performance in the cognitive task (P < 0.01), accompanied by raised SSEP phase and amplitude in the anterior and midline regions compared to healthy controls (P < 0.05). The Mississippi total score was positively correlated with the SSEP amplitude in the midline region (r = 0.62, P < 0.05). Furthermore, based on ROC analysis, the SSEP amplitude in the midline region provided an excellent AUC value (AUC = 0.850) for distinguishing patients with PTSD from normal subjects.
Conclusion: Current findings suggest that abnormalities in the anterior and midline cortical neural networks are involved in the pathophysiology of PTSD. Importantly, midline abnormalities may provide a clinically-relevant measure for researchers wishing to assess the use of biomarkers for early diagnosis of PTSD as well as to evaluate new therapeutic and management approaches in the treatment of PTSD.
1. Wang C, Rapp P, Darmon D, Trongnetrpunya A, Costanzo ME, Nathan DE, et al. Utility of P300 ERP in monitoring post-trauma mental health: A longitudinal study in military personnel returning from combat deployment. J Psychiatr Res. 2018;101:5-13.
2. Mohammadi MR, Ahmadi N, Khaleghi A, Mostafavi SA, Kamali K, Rahgozar M, et al. Prevalence and Correlates of Psychiatric Disorders in a National Survey of Iranian Children and Adolescents. Iran J Psychiatry. 2019;14(1):1-15.
3. Mohammadi MR, Badrfam R, Khaleghi A, Hooshyari Z, Ahmadi N, Zandifar A. Prevalence, Comorbidity and Predictor of Separation Anxiety Disorder in Children and Adolescents. Psychiatr Q. 2020;91(4):1415-29.
4. Seal KH, Metzler TJ, Gima KS, Bertenthal D, Maguen S, Marmar CR. Trends and risk factors for mental health diagnoses among Iraq and Afghanistan veterans using Department of Veterans Affairs health care, 2002-2008. Am J Public Health. 2009;99(9):1651-8.
5. Ghanbari Z, Moradi MH, Moradi A, Mirzaei J. Resting state functional connectivity in PTSD veterans: an EEG study. J MED BIOL ENG. 2020;40:505-16.
6. McLay RN, Deal WE, Murphy JA, Center KB, Kolkow TT, Grieger TA. On-the-record screenings versus anonymous surveys in reporting PTSD. Am J Psychiatry. 2008;165(6):775-6.
7. Khaleghi A, Mohammadi MR, Shahi K, Nasrabadi AM. Computational Neuroscience Approach to Psychiatry: A Review on Theory-driven Approaches. Clin Psychopharmacol Neurosci. 2022;20(1):26-36.
8. Kunimatsu A, Yasaka K, Akai H, Kunimatsu N, Abe O. MRI findings in posttraumatic stress disorder. J Magn Reson Imaging. 2020;52(2):380-96.
9. Pan X, Kaminga AC, Wen SW, Liu A. Catecholamines in Post-traumatic Stress Disorder: A Systematic Review and Meta-Analysis. Front Mol Neurosci. 2018;11:450.
10. Rasmusson AM, Pineles SL. Neurotransmitter, Peptide, and Steroid Hormone Abnormalities in PTSD: Biological Endophenotypes Relevant to Treatment. Curr Psychiatry Rep. 2018;20(7):52.
11. Laxminarayan S, Wang C, Oyama T, Cashmere JD, Germain A, Reifman J. Identification of Veterans With PTSD Based on EEG Features Collected During Sleep. Front Psychiatry. 2020;11:532623.
12. Hashtjini MM, Jahromi GP, Sadr SS, Khaleghi A, Hatef B, Meftahi GH. Comparison of the effects of deep brain stimulation of the prelimbic cortex and basolateral amygdala for facilitation of extinction process of conditioned fear. Arch Neurosci. 2020;7(4).
13. Mohammadi MR, Khaleghi A, Nasrabadi AM, Rafieivand S, Begol M, Zarafshan H. EEG classification of ADHD and normal children using non-linear features and neural network. Biomedical Engineering Letters. 2016;6:66-73.
14. Khaleghi A, Sheikhani A, Mohammadi MR, Nasrabadi AM, Vand SR, Zarafshan H, et al. EEG classification of adolescents with type I and type II of bipolar disorder. Australas Phys Eng Sci Med. 2015;38(4):551-9.
15. Zarafshan H, Khaleghi A, Mohammadi MR, Moeini M, Malmir N. Electroencephalogram complexity analysis in children with attention-deficit/hyperactivity disorder during a visual cognitive task. J Clin Exp Neuropsychol. 2016;38(3):361-9.
16. Moeini M, Khaleghi A, Mohammadi MR. Characteristics of Alpha Band Frequency in Adolescents with Bipolar II Disorder: A Resting-State QEEG Study. Iran J Psychiatry. 2015;10(1):8-12.
17. Moeini M, Khaleghi A, Amiri N, Niknam Z. Quantitative electroencephalogram (QEEG) Spectrum Analysis of Patients with Schizoaffective Disorder Compared to Normal Subjects. Iran J Psychiatry. 2014;9(4):216-21.
18. Khaleghi A, Sheikhani A, Mohammadi MR, Moti Nasrabadi A. Evaluation of Cerebral Cortex Function in Clients with Bipolar Mood Disorder I (BMD I) Compared With BMD II Using QEEG Analysis. Iran J Psychiatry. 2015;10(2):93-9.
19. Khaleghi A, Birgani PM, Fooladi MF, Mohammadi MR. Applicable features of electroencephalogram for ADHD diagnosis. Research on Biomedical Engineering. 2020;36:1-11.
20. Khaleghi A, Mohammadi MR, Moeini M, Zarafshan H, Fadaei Fooladi M. Abnormalities of Alpha Activity in Frontocentral Region of the Brain as a Biomarker to Diagnose Adolescents With Bipolar Disorder. Clin EEG Neurosci. 2019;50(5):311-8.
21. Newson JJ, Thiagarajan TC. EEG Frequency Bands in Psychiatric Disorders: A Review of Resting State Studies. Front Hum Neurosci. 2018;12:521.
22. Brunner JF, Hansen TI, Olsen A, Skandsen T, Håberg A, Kropotov J. Long-term test-retest reliability of the P3 NoGo wave and two independent components decomposed from the P3 NoGo wave in a visual Go/NoGo task. Int J Psychophysiol. 2013;89(1):106-14.
23. Regier DA, Narrow WE, Clarke DE, Kraemer HC, Kuramoto SJ, Kuhl EA, et al. DSM-5 field trials in the United States and Canada, Part II: test-retest reliability of selected categorical diagnoses. Am J Psychiatry. 2013;170(1):59-70.
24. Sharon O, Nir Y. Attenuated Fast Steady-State Visual Evoked Potentials During Human Sleep. Cereb Cortex. 2018;28(4):1297-311.
25. Vialatte FB, Maurice M, Dauwels J, Cichocki A. Steady-state visually evoked potentials: focus on essential paradigms and future perspectives. Prog Neurobiol. 2010;90(4):418-38.
26. McFadden KL, Steinmetz SE, Carroll AM, Simon ST, Wallace A, Rojas DC. Test-retest reliability of the 40 Hz EEG auditory steady-state response. PLoS One. 2014;9(1):e85748.
27. Chen J, Gong Q, Wu F. Deficits in the 30-Hz auditory steady-state response in patients with major depressive disorder. Neuroreport. 2016;27(15):1147-52.
28. Xiao W, Manyi G, Khaleghi A. Deficits in auditory and visual steady-state responses in adolescents with bipolar disorder. J Psychiatr Res. 2022;151:368-76.
29. Thuné H, Recasens M, Uhlhaas PJ. The 40-Hz Auditory Steady-State Response in Patients With Schizophrenia: A Meta-analysis. JAMA Psychiatry. 2016;73(11):1145-53.
30. Khaleghi A, Zarafshan H, Mohammadi MR. Visual and auditory steady-state responses in attention-deficit/hyperactivity disorder. Eur Arch Psychiatry Clin Neurosci. 2019;269(6):645-55.
31. Edition F. Diagnostic and statistical manual of mental disorders. APA 21, 591–643. 2013.
32. Basharpoor S, Shafiei M, Daneshvar S. The Comparison of Experiential Avoidance, [corrected] Mindfulness and Rumination in Trauma-Exposed Individuals With and Without Posttraumatic Stress Disorder (PTSD) in an Iranian Sample. Arch Psychiatr Nurs. 2015;29(5):279-83.
33. Mostafavi SA, Khaleghi A, Vand SR, Alavi SS, Mohammadi MR. Neuro-cognitive Ramifications of Fasting and Feeding in Obese and Non-obese Cases. Clin Psychopharmacol Neurosci. 2018;16(4):481-8.
34. Camfield DA, Scholey A, Pipingas A, Silberstein R, Kras M, Nolidin K, et al. Steady state visually evoked potential (SSVEP) topography changes associated with cocoa flavanol consumption. Physiol Behav. 2012;105(4):948-57.
35. Kemp AH, Gray MA, Silberstein RB, Armstrong SM, Nathan PJ. Augmentation of serotonin enhances pleasant and suppresses unpleasant cortical electrophysiological responses to visual emotional stimuli in humans. Neuroimage. 2004;22(3):1084-96.
36. Silberstein RB, Nunez PL, Pipingas A, Harris P, Danieli F. Steady state visually evoked potential (SSVEP) topography in a graded working memory task. Int J Psychophysiol. 2001;42(2):219-32.
37. Qureshi SU, Long ME, Bradshaw MR, Pyne JM, Magruder KM, Kimbrell T, et al. Does PTSD impair cognition beyond the effect of trauma? J Neuropsychiatry Clin Neurosci. 2011;23(1):16-28.
38. Lobo I, Portugal LC, Figueira I, Volchan E, David I, Garcia Pereira M, et al. EEG correlates of the severity of posttraumatic stress symptoms: A systematic review of the dimensional PTSD literature. J Affect Disord. 2015;183:210-20.
39. Liberzon I, Sripada CS. The functional neuroanatomy of PTSD: a critical review. Prog Brain Res. 2008;167:151-69.
40. Myers KM, Carlezon WA, Jr., Davis M. Glutamate receptors in extinction and extinction-based therapies for psychiatric illness. Neuropsychopharmacology. 2011;36(1):274-93.
41. Nishi D, Hashimoto K, Noguchi H, Hamazaki K, Hamazaki T, Matsuoka Y. Glutamatergic system abnormalities in posttraumatic stress disorder. Psychopharmacology (Berl). 2015;232(23):4261-8.
42. Bae KY, Kim DW, Im CH, Lee SH. Source imaging of P300 auditory evoked potentials and clinical correlations in patients with posttraumatic stress disorder. Prog Neuropsychopharmacol Biol Psychiatry. 2011;35(8):1908-17.
43. Javanbakht A, Liberzon I, Amirsadri A, Gjini K, Boutros NN. Event-related potential studies of post-traumatic stress disorder: a critical review and synthesis. Biol Mood Anxiety Disord. 2011;1(1):5.
44. Araki T, Kasai K, Yamasue H, Kato N, Kudo N, Ohtani T, et al. Association between lower P300 amplitude and smaller anterior cingulate cortex volume in patients with posttraumatic stress disorder: a study of victims of Tokyo subway sarin attack. Neuroimage. 2005;25(1):43-50.
45. Guild EB, Levine B. Functional Correlates of Midline Brain Volume Loss in Chronic Traumatic Brain Injury. J Int Neuropsychol Soc. 2015;21(8):650-5.
2. Mohammadi MR, Ahmadi N, Khaleghi A, Mostafavi SA, Kamali K, Rahgozar M, et al. Prevalence and Correlates of Psychiatric Disorders in a National Survey of Iranian Children and Adolescents. Iran J Psychiatry. 2019;14(1):1-15.
3. Mohammadi MR, Badrfam R, Khaleghi A, Hooshyari Z, Ahmadi N, Zandifar A. Prevalence, Comorbidity and Predictor of Separation Anxiety Disorder in Children and Adolescents. Psychiatr Q. 2020;91(4):1415-29.
4. Seal KH, Metzler TJ, Gima KS, Bertenthal D, Maguen S, Marmar CR. Trends and risk factors for mental health diagnoses among Iraq and Afghanistan veterans using Department of Veterans Affairs health care, 2002-2008. Am J Public Health. 2009;99(9):1651-8.
5. Ghanbari Z, Moradi MH, Moradi A, Mirzaei J. Resting state functional connectivity in PTSD veterans: an EEG study. J MED BIOL ENG. 2020;40:505-16.
6. McLay RN, Deal WE, Murphy JA, Center KB, Kolkow TT, Grieger TA. On-the-record screenings versus anonymous surveys in reporting PTSD. Am J Psychiatry. 2008;165(6):775-6.
7. Khaleghi A, Mohammadi MR, Shahi K, Nasrabadi AM. Computational Neuroscience Approach to Psychiatry: A Review on Theory-driven Approaches. Clin Psychopharmacol Neurosci. 2022;20(1):26-36.
8. Kunimatsu A, Yasaka K, Akai H, Kunimatsu N, Abe O. MRI findings in posttraumatic stress disorder. J Magn Reson Imaging. 2020;52(2):380-96.
9. Pan X, Kaminga AC, Wen SW, Liu A. Catecholamines in Post-traumatic Stress Disorder: A Systematic Review and Meta-Analysis. Front Mol Neurosci. 2018;11:450.
10. Rasmusson AM, Pineles SL. Neurotransmitter, Peptide, and Steroid Hormone Abnormalities in PTSD: Biological Endophenotypes Relevant to Treatment. Curr Psychiatry Rep. 2018;20(7):52.
11. Laxminarayan S, Wang C, Oyama T, Cashmere JD, Germain A, Reifman J. Identification of Veterans With PTSD Based on EEG Features Collected During Sleep. Front Psychiatry. 2020;11:532623.
12. Hashtjini MM, Jahromi GP, Sadr SS, Khaleghi A, Hatef B, Meftahi GH. Comparison of the effects of deep brain stimulation of the prelimbic cortex and basolateral amygdala for facilitation of extinction process of conditioned fear. Arch Neurosci. 2020;7(4).
13. Mohammadi MR, Khaleghi A, Nasrabadi AM, Rafieivand S, Begol M, Zarafshan H. EEG classification of ADHD and normal children using non-linear features and neural network. Biomedical Engineering Letters. 2016;6:66-73.
14. Khaleghi A, Sheikhani A, Mohammadi MR, Nasrabadi AM, Vand SR, Zarafshan H, et al. EEG classification of adolescents with type I and type II of bipolar disorder. Australas Phys Eng Sci Med. 2015;38(4):551-9.
15. Zarafshan H, Khaleghi A, Mohammadi MR, Moeini M, Malmir N. Electroencephalogram complexity analysis in children with attention-deficit/hyperactivity disorder during a visual cognitive task. J Clin Exp Neuropsychol. 2016;38(3):361-9.
16. Moeini M, Khaleghi A, Mohammadi MR. Characteristics of Alpha Band Frequency in Adolescents with Bipolar II Disorder: A Resting-State QEEG Study. Iran J Psychiatry. 2015;10(1):8-12.
17. Moeini M, Khaleghi A, Amiri N, Niknam Z. Quantitative electroencephalogram (QEEG) Spectrum Analysis of Patients with Schizoaffective Disorder Compared to Normal Subjects. Iran J Psychiatry. 2014;9(4):216-21.
18. Khaleghi A, Sheikhani A, Mohammadi MR, Moti Nasrabadi A. Evaluation of Cerebral Cortex Function in Clients with Bipolar Mood Disorder I (BMD I) Compared With BMD II Using QEEG Analysis. Iran J Psychiatry. 2015;10(2):93-9.
19. Khaleghi A, Birgani PM, Fooladi MF, Mohammadi MR. Applicable features of electroencephalogram for ADHD diagnosis. Research on Biomedical Engineering. 2020;36:1-11.
20. Khaleghi A, Mohammadi MR, Moeini M, Zarafshan H, Fadaei Fooladi M. Abnormalities of Alpha Activity in Frontocentral Region of the Brain as a Biomarker to Diagnose Adolescents With Bipolar Disorder. Clin EEG Neurosci. 2019;50(5):311-8.
21. Newson JJ, Thiagarajan TC. EEG Frequency Bands in Psychiatric Disorders: A Review of Resting State Studies. Front Hum Neurosci. 2018;12:521.
22. Brunner JF, Hansen TI, Olsen A, Skandsen T, Håberg A, Kropotov J. Long-term test-retest reliability of the P3 NoGo wave and two independent components decomposed from the P3 NoGo wave in a visual Go/NoGo task. Int J Psychophysiol. 2013;89(1):106-14.
23. Regier DA, Narrow WE, Clarke DE, Kraemer HC, Kuramoto SJ, Kuhl EA, et al. DSM-5 field trials in the United States and Canada, Part II: test-retest reliability of selected categorical diagnoses. Am J Psychiatry. 2013;170(1):59-70.
24. Sharon O, Nir Y. Attenuated Fast Steady-State Visual Evoked Potentials During Human Sleep. Cereb Cortex. 2018;28(4):1297-311.
25. Vialatte FB, Maurice M, Dauwels J, Cichocki A. Steady-state visually evoked potentials: focus on essential paradigms and future perspectives. Prog Neurobiol. 2010;90(4):418-38.
26. McFadden KL, Steinmetz SE, Carroll AM, Simon ST, Wallace A, Rojas DC. Test-retest reliability of the 40 Hz EEG auditory steady-state response. PLoS One. 2014;9(1):e85748.
27. Chen J, Gong Q, Wu F. Deficits in the 30-Hz auditory steady-state response in patients with major depressive disorder. Neuroreport. 2016;27(15):1147-52.
28. Xiao W, Manyi G, Khaleghi A. Deficits in auditory and visual steady-state responses in adolescents with bipolar disorder. J Psychiatr Res. 2022;151:368-76.
29. Thuné H, Recasens M, Uhlhaas PJ. The 40-Hz Auditory Steady-State Response in Patients With Schizophrenia: A Meta-analysis. JAMA Psychiatry. 2016;73(11):1145-53.
30. Khaleghi A, Zarafshan H, Mohammadi MR. Visual and auditory steady-state responses in attention-deficit/hyperactivity disorder. Eur Arch Psychiatry Clin Neurosci. 2019;269(6):645-55.
31. Edition F. Diagnostic and statistical manual of mental disorders. APA 21, 591–643. 2013.
32. Basharpoor S, Shafiei M, Daneshvar S. The Comparison of Experiential Avoidance, [corrected] Mindfulness and Rumination in Trauma-Exposed Individuals With and Without Posttraumatic Stress Disorder (PTSD) in an Iranian Sample. Arch Psychiatr Nurs. 2015;29(5):279-83.
33. Mostafavi SA, Khaleghi A, Vand SR, Alavi SS, Mohammadi MR. Neuro-cognitive Ramifications of Fasting and Feeding in Obese and Non-obese Cases. Clin Psychopharmacol Neurosci. 2018;16(4):481-8.
34. Camfield DA, Scholey A, Pipingas A, Silberstein R, Kras M, Nolidin K, et al. Steady state visually evoked potential (SSVEP) topography changes associated with cocoa flavanol consumption. Physiol Behav. 2012;105(4):948-57.
35. Kemp AH, Gray MA, Silberstein RB, Armstrong SM, Nathan PJ. Augmentation of serotonin enhances pleasant and suppresses unpleasant cortical electrophysiological responses to visual emotional stimuli in humans. Neuroimage. 2004;22(3):1084-96.
36. Silberstein RB, Nunez PL, Pipingas A, Harris P, Danieli F. Steady state visually evoked potential (SSVEP) topography in a graded working memory task. Int J Psychophysiol. 2001;42(2):219-32.
37. Qureshi SU, Long ME, Bradshaw MR, Pyne JM, Magruder KM, Kimbrell T, et al. Does PTSD impair cognition beyond the effect of trauma? J Neuropsychiatry Clin Neurosci. 2011;23(1):16-28.
38. Lobo I, Portugal LC, Figueira I, Volchan E, David I, Garcia Pereira M, et al. EEG correlates of the severity of posttraumatic stress symptoms: A systematic review of the dimensional PTSD literature. J Affect Disord. 2015;183:210-20.
39. Liberzon I, Sripada CS. The functional neuroanatomy of PTSD: a critical review. Prog Brain Res. 2008;167:151-69.
40. Myers KM, Carlezon WA, Jr., Davis M. Glutamate receptors in extinction and extinction-based therapies for psychiatric illness. Neuropsychopharmacology. 2011;36(1):274-93.
41. Nishi D, Hashimoto K, Noguchi H, Hamazaki K, Hamazaki T, Matsuoka Y. Glutamatergic system abnormalities in posttraumatic stress disorder. Psychopharmacology (Berl). 2015;232(23):4261-8.
42. Bae KY, Kim DW, Im CH, Lee SH. Source imaging of P300 auditory evoked potentials and clinical correlations in patients with posttraumatic stress disorder. Prog Neuropsychopharmacol Biol Psychiatry. 2011;35(8):1908-17.
43. Javanbakht A, Liberzon I, Amirsadri A, Gjini K, Boutros NN. Event-related potential studies of post-traumatic stress disorder: a critical review and synthesis. Biol Mood Anxiety Disord. 2011;1(1):5.
44. Araki T, Kasai K, Yamasue H, Kato N, Kudo N, Ohtani T, et al. Association between lower P300 amplitude and smaller anterior cingulate cortex volume in patients with posttraumatic stress disorder: a study of victims of Tokyo subway sarin attack. Neuroimage. 2005;25(1):43-50.
45. Guild EB, Levine B. Functional Correlates of Midline Brain Volume Loss in Chronic Traumatic Brain Injury. J Int Neuropsychol Soc. 2015;21(8):650-5.
| Files | ||
| Issue | Vol 19 No 2 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijps.v19i2.15110 | |
| Keywords | ||
| Biomarker Electroencephalography Pathophysiology Post-Traumatic Stress Disorder | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Pirzad Jahromi G, Gharaati Sotoudeh H, Mostafaie R, Khaleghi A. Auditory Steady-State Evoked Potentials in Post Traumatic Stress Disorder: Introduction of a Potential Biomarker. Iran J Psychiatry. 2024;19(2):235-243.
