Right anterior cingulate cortical volume covaries with respiratory sinus arrhythmia magnitude in combat veterans

Journal of Rehabilitation Research and Development

Volumn 45, Issue 3, 2008, Pages 451-464

  Woodward, Steven H ^a   Kaloupek, Danny G ^b,c   Schaer, Marie ^d,e   Martinez, Christelle ^d   Eliez, Stephan ^d  

^a VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^b VA BOSTON HEALTHCARE SYSTEM   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF GENEVA   (Switzerland)

^e EPFL   (Switzerland)

Author keywords

Autonomic denervation; Cardiac chronotropy; Gyrus cinguli; Heart rate variability; Insular cortex; Magnetic resonance imaging; Posttraumatic; Respiratory sinus arrhythmia; Stress disorders; Vagotomy

Indexed keywords

AUTONOMIC DENERVATION; CARDIAC CHRONOTROPY; GYRUS CINGULI; HEART RATE VARIABILITY; INSULAR CORTEX; POSTTRAUMATIC; RESPIRATORY SINUS ARRHYTHMIA; STRESS DISORDERS; VAGOTOMY;

HEART VALVE PROSTHESES; MAGNETIC RESONANCE IMAGING;

MAGNETIC RESONANCE;

ADULT; ARTICLE; BRAIN SIZE; CINGULATE GYRUS; CONTROLLED STUDY; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; REST; RIGHT HEMISPHERE; SINUS ARRHYTHMIA; SURVIVOR; VETERAN; AMYGDALOID NUCLEUS; AUTONOMIC NERVOUS SYSTEM; HISTOLOGY; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PSYCHOMETRY; WAR;

AMYGDALA; ARRHYTHMIA, SINUS; AUTONOMIC NERVOUS SYSTEM; GULF WAR; GYRUS CINGULI; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; PSYCHOMETRICS; VETERANS; VIETNAM CONFLICT; WAR;

EID: 63249104998     PISSN: 07487711     EISSN: 07487711     Source Type: Journal    
DOI: 10.1682/JRRD.2007.06.0082     Document Type: Article

References (70)

1. Dobbs D, Wilson WP. Observations on persistence of war neurosis. Dis Nerv Syst. 1960;21:686-691
2. Keane TM, Kolb LC, Kaloupek DG, Orr SP, Blanchard EB, Thomas RG, Hsieh FY, Lavori PW. Utility of psychophysiological measurement in the diagnosis of posttraumatic stress disorder: results from a Department of Veterans Affairs Cooperative Study. J Consult Clin Psychol. 1998; 66(6):914-923
3. Shalev AY, Sahar T, Freedman S, Peri T, Glick N, Brandes D, Orr SP, Pitman RK. A prospective study of heart rate response following trauma and the subsequent development of posttraumatic stress disorder. Arch Gen Psychiatry. 1998; 55(6):553-559
4. Orr SP, Metzger LJ, Lasko NB, Macklin ML, Hu FB, Shalev AY, Pitman RK; Harvard/Veterans Affairs Post-traumatic Stress Disorder Twin Study Investigators. Physiologic responses to sudden, loud tones in monozygotic twins discordant for combat exposure: association with posttraumatic stress disorder. Arch Gen Psychiatry 2003;60(3):283-288
5. Griffin MG, Resick PA, Mechanic MB. Objective assessment of peritraumatic dissociation: psychophysiological indicators. Am J Psychiatry. 1997;154(8):1081-1088
6. Cohen H, Benjamin J, Geva AB, Matar MA, Kaplan Z, Kotler M. Autonomic dysregulation in panic disorder and in post-traumatic stress disorder: application of power spectrum analysis of heart rate variability at rest and in response to recollection of trauma or panic attacks. Psychiatry Res. 2000;96(1):1-13.
7. Sahar T, Shalev AY, Porges SW. Vagal modulation of responses to mental challenge in posttraumatic stress disorder. Biol Psychiatry. 2001;49(7):637-643
8. Hopper JW, Spinazzola J, Simpson WB, Van der Kolk BA. Preliminary evidence of parasympathetic influence on basal heart rate in posttraumatic stress disorder. J Psychosom Res. 2006;60(1):83-90.
9. Bremner JD, Randall P, Scott TM, Bronen RA, Seibyl JP, Southwick SM, Delaney RC, McCarthy G, Charney DS, Innis RB. MRI-based measurement of hippocampal volume in patients with combat-related posttraumatic stress disorder. Am J Psychiatry. 1995;152(7):973-981
10. Gurvits TV, Shenton ME, Hokama H, Ohta H, Lasko NB, Gilbertson MW, Orr SP, Kikinis R, Jolesz FA, McCarley RW, Pitman RK. Magnetic resonance imaging study of hippocampal volume in chronic, combat-related posttraumatic stress disorder. Biol Psychiatry. 1996;40(11):1091-1099 [PMID: 8931911] (Pubitemid 26400873)
11. Stein MB, Koverola C, Hanna C, Torchia MG, McClarty B. Hippocampal volume in women victimized by childhood sexual abuse. Psychol Med. 1997;27(4):951-959
12. Villarreal G, Hamilton DA, Petropoulos H, Driscoll I, Rowland LM, Griego JA, Kodituwakku PW, Hart BL, Escalona R, Brooks WM. Reduced hippocampal volume and total white matter volume in posttraumatic stress disorder. Biol Psychiatry. 2002;52(2):119-125
13. Gilbertson MW, Shenton ME, Ciszewski A, Kasai K, Lasko NB, Orr SP, Pitman RK. Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nat Neurosci. 2002;5(11):1242-1247
14. Lindauer RJ, Vlieger EJ, Jalink M, Olff M, Carlier IV, Majoie CB, den Heeten GJ, Gersons BP. Smaller hippocampal volume in Dutch police officers with posttraumatic stress disorder. Biol Psychiatry. 2004;56(5):356-363
15. Woodward SH, Kaloupek DG, Streeter CC, Kimble MO, Reiss AL, Eliez S, Wald LL, Renshaw PF, Frederick BB, Lane B, Sheikh JI, Stegman WK, Kutter CJ, Stewart LP, Prestel RS, Arsenault NJ. Hippocampal volume, PTSD, and alcoholism in combat veterans. Am J Psychiatry. 2006; 163(4):674-681
16. Rauch SL, Shin LM, Segal E, Pitman RK, Carson MA, McMullin K, Whalen PJ, Makris N. Selectively reduced regional cortical volumes in post-traumatic stress disorder. Neuroreport. 2003;14(7):913-916
17. Woodward SH, Kaloupek DG, Streeter CC, Martinez C, Schaer M, Eliez S. Decreased anterior cingulate volume in combat-related PTSD. Biol Psychiatry. 2006;59(7):582-587
18. Kitayama N, Quinn S, Bremner JD. Smaller volume of anterior cingulate cortex in abuse-related posttraumatic stress disorder. J Affect Disord. 2006;90(2-3):171-174
19. Yamasue H, Kasai K, Iwanami A, Ohtani T, Yamada H, Abe O, Kuroki N, Fukuda R, Tochigi M, Furukawa S, Sadamatsu M, Sasaki T, Aoki S, Ohtomo K, Asukai N, Kato N. Voxelbased analysis of MRI reveals anterior cingulate gray-matter volume reduction in posttraumatic stress disorder due to terrorism. Proc Natl Acad Sci U S A. 2003; 100(15):9039-9043
20. Chen S, Xia W, Li L, Liu J, He Z, Zhang Z, Yan L, Zhang J, Hu D. Gray matter density reduction in the insula in fire survivors with posttraumatic stress disorder: a voxel-based morphometric study. Psychiatry Res. 2006;146(1):65-72.
21. Mahmutyazicioglu K, Konuk N, Ozdemir H, Atasoy N, Atik L, Gundogdu S. Evaluation of the hippocampus and the anterior cingulate gyrus by proton MR spectroscopy in patients with post-traumatic stress disorder. Diagn Interv Radiol. 2005;11(3):125-129
22. De Bellis MD, Keshavan MS, Spencer S, Hall J. N-Acetylaspartate concentration in the anterior cingulate of maltreated children and adolescents with PTSD. Am J Psychiatry. 2000; 157(7):1175-1177
23. Kasai K, Yamasue H, Gilbertson MW, Shenton ME, Rauch SL, Pitman RK. Evidence for acquired pregenual anterior cingulate gray matter loss from a twin study of combatrelated posttraumatic stress disorder. Biol Psychiatry. 2008; 63(6):550-556
24. Shin LM, McNally RJ, Kosslyn SM, Thompson WL, Rauch SL, Alpert NM, Metzger LJ, Lasko NB, Orr SP, Pitman RK. Regional cerebral blood flow during script-driven imagery in childhood sexual abuse-related PTSD: a PET investigation. Am J Psychiatry. 1999;156(4):575-584
25. Bremner JD, Staib LH, Kaloupek D, Southwick SM, Soufer R, Charney DS. Neural correlates of exposure to traumatic pictures and sound in Vietnam combat veterans with and without posttraumatic stress disorder: a positron emission tomography study. Biol Psychiatry. 1999;45(7): 806-816
26. Shin LM, Whalen PJ, Pitman RK, Bush G, Macklin ML, Lasko NB, Orr SP, McInerney SC, Rauch SL. An fMRI study of anterior cingulate function in posttraumatic stress disorder. Biol Psychiatry. 2001;50(12):932-942
27. Lanius RA, Williamson PC, Hopper J, Densmore M, Boksman K, Gupta MA, Neufeld RW, Gati JS, Menon RS. Recall of emotional states in posttraumatic stress disorder: an fMRI investigation. Biol Psychiatry. 2003;53(3):204-210
28. Liberzon I, Britton JC, Phan KL. Neural correlates of traumatic recall in posttraumatic stress disorder. Stress. 2003; 6(3):151-156
29. Bremner JD, Vythilingam M, Vermetten E, Southwick SM, McGlashan T, Staib LH, Soufer R, Charney DS. Neural correlates of declarative memory for emotionally valenced words in women with posttraumatic stress disorder related to early childhood sexual abuse. Biol Psychiatry. 2003; 53(10):879-889
30. Yang P, Wu MT, Hsu CC, Ker JH. Evidence of early neurobiological alternations in adolescents with posttraumatic stress disorder: A functional MRI study. Neurosci Lett. 2004; 370(1):13-18. [PMID: 15489009] (Pubitemid 39369848)
31. Shin LM, Wright CI, Cannistraro PA, Wedig MM, McMullin K, Martis B, Macklin ML, Lasko NB, Cavanagh SR, Krangel TS, Orr SP, Pitman RK, Whalen PJ, Rauch SL. 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(3):273-281
32. Card JP, Rinaman L, Lynn RB, Lee BH, Meade RP, Miselis RR, Enquist LW. Pseudorabies virus infection of the rat central nervous system: ultrastructural characterization of viral replication, transport, and pathogenesis. J Neurosci. 1993; 13(6):2515-2539
33. Ter Horst GJ, Postema F. Forebrain parasympathetic control of heart activity: retrograde transneuronal viral labeling in rats. Am J Physiol. 1997;273(6 Pt 2):H2926-30.
34. Benarroch EE. The central autonomic network: functional organization, dysfunction, and perspective. Mayo Clin Proc. 1993;68(10):988-1001.
35. Neafsey EJ. Prefrontal cortical control of the autonomic nervous system: anatomical and physiological observations. Prog Brain Res. 1990;85:147-166
36. Critchley HD, Corfield DR, Chandler MP, Mathias CJ, Dolan RJ. Cerebral correlates of autonomic cardiovascular arousal: a functional neuroimaging investigation in humans. J Physiol. 2000;523 Pt 1:259-270
37. Gianaros PJ, Derbyshire SW, May JC, Siegle GJ, Gamalo MA, Jennings JR. Anterior cingulate activity correlates with blood pressure during stress. Psychophysiology. 2005;42(6): 627-635
38. Gianaros PJ, Jennings JR, Sheu LK, Derbyshire SW, Matthews KA. Heightened functional neural activation to psychological stress covaries with exaggerated blood pressure reactivity. Hypertension. 2007;49(1):134-140
39. Critchley HD, Rotshtein P, Nagai Y, O'Doherty J, Mathias CJ, Dolan RJ. Activity in the human brain predicting differential heart rate responses to emotional facial expressions. Neuroimage. 2005;24(3):751-762
40. Gianaros PJ, Van Der Veen FM, Jennings JR. Regional cerebral blood flow correlates with heart period and highfrequency heart period variability during working-memory tasks: implications for the cortical and subcortical regulation of cardiac autonomic activity. Psychophysiology. 2004; 41(4):521-530
41. Berntson GG, Bigger JT Jr, Eckberg DL, Grossman P, Kaufmann PG, Malik M, Nagaraja HN, Porges SW, Saul JP, Stone PH, Van Der Molen MW. Heart rate variability: origins, methods, and interpretive caveats. Psychophysiology. 1997;34(6):623-648
42. Critchley HD, Mathias CJ, Josephs O, O'Doherty J, Zanini S, Dewar BK, Cipolotti L, Shallice T, Dolan RJ. Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. Brain. 2003;126(Pt 10):2139-2152
43. Stein PK, Freedland KE, Skala JA, Carney RM, Davila- Roman V, Rich MW, Kleiger RE. Heart rate variability is independent of age, gender, and race in congestive heart failure with a recent acute exacerbation. Am J Cardiol. 1997;79(4):511-512
44. Thayer JF, Lane RD. The role of vagal function in the risk for cardiovascular disease and mortality. Biol Psychol. 2007; 74(2):224-242
45. Masi CM, Hawkley LC, Rickett EM, Cacioppo JT. Respiratory sinus arrhythmia and diseases of aging: obesity, diabetes mellitus, and hypertension. Biol Psychol. 2007;74(2):212-223
46. Norman SB, Means-Christensen AJ, Craske MG, Sherbourne CD, Roy-Byrne PP, Stein MB. Associations between psychological trauma and physical illness in primary care. J Trauma Stress. 2006;19(4):461-470
47. Violanti JM, Fekedulegn D, Hartley TA, Andrew ME, Charles LE, Mnatsakanova A, Burchfiel CM. Police trauma and cardiovascular disease: association between PTSD symptoms and metabolic syndrome. Int J Emerg Ment Health. 2006;8(4):227-237
48. Kubzansky LD, Koenen KC, Spiro A 3rd, Vokonas PS, Sparrow D. Prospective study of posttraumatic stress disorder symptoms and coronary heart disease in the Normative Aging Study. Arch Gen Psychiatry. 2007;64(1):109-116
49. Scheeringa MS, Zeanah CH, Myers L, Putnam F. Heart period and variability findings in preschool children with posttraumatic stress symptoms. Biol Psychiatry. 2004;55(7): 685-691
50. Cohen H, Kotler M, Matar MA, Kaplan Z, Miodownik H, Cassuto Y. Power spectral analysis of heart rate variability in posttraumatic stress disorder patients. Biol Psychiatry. 1997;41(5):627-629
51. McEwen BS, Magarinos AM. Stress effects on morphology and function of the hippocampus. Ann N Y Acad Sci. 1997;821:271-284
52. Blake DD, Weathers FW, Nagy LM, Kaloupek DG, Charney DS, Keane TM. Clinician-administered PTSD scale for DSM-IV: Current and lifetime version. Boston (MA): Behavioral Science Division, Boston VA Medical Center/Neurosciences Division,West Haven VA Medical Center; 1997.
53. First MB, Spitzer RL, Gibbon M, Williams JB. Structured clinical interview for the DSM-IV Axis-I disorders. New York (NY): Biometrics Research Department, New York State Psychiatric Institute; 1997.
54. Psychological Corporation. WAIS-III: Administration and scoring manual. 3rd ed. San Antonio (TX): Harcourt Brace; 1997.
55. Keane TM, Fairbank JA, Caddell JM, Zimering RT, Taylor KL, Mora CA. Clinical evaluation of a measure to assess combat exposure. Psychol Assess. 1989;1(1):53-55.
56. Keane TM, Caddell JM, Taylor KL. Mississippi Scale for Combat-Related Posttraumatic Stress Disorder: three studies in reliability and validity. J Consult Clin Psychol. 1988; 56(1):85-90.
57. Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J. An inventory for measuring depression. Arch Gen Psychiatry. 1961;4:561-571
58. Berntson GG, Stowell JR. ECG artifacts and heart period variability: Don't miss a beat! Psychophysiology. 1998; 35(1):127-132
59. Reiss AL, Hennessey JG, Rubin M, Beach L, Abrams MT, Warsofsky IS, Liu AM, Links JM. Reliability and validity of an algorithm for fuzzy tissue segmentation of MRI. J Comput Assist Tomogr. 1998;22(3):471-479
60. Kates WR, Warsofsky IS, Patwardhan A, Abrams MT, Liu AM, Naidu S, Kaufmann WE, Reiss AL. Automated Talairach atlas-based parcellation and measurement of cerebral lobes in children. Psychiatry Res. 1999;91(1):11-30.
61. Talairach J, Tournoux P. Co-planar stereotaxic atlas of the human brain: 3-Dimensional proportional system: An approach to cerebral imaging. New York (NY): Thieme Medical Publishers; 1988.
62. Huster RJ, Westerhausen R, Kreuder F, Schweiger E, Wittling W. Morphologic asymmetry of the human anterior cingulate cortex. Neuroimage. 2007;34(3):888-895
63. Paus T, Tomaiuolo F, Otaky N, MacDonald D, Petrides M, Atlas J, Morris R, Evans AC. Human cingulate and paracingulate sulci: pattern, variability, asymmetry, and probabilistic map. Cereb Cortex. 1996;6(2):207-214
64. Fornito A, Whittle S, Wood SJ, Velakoulis D, Pantelis C, Yucel M. The influence of sulcal variability on morphometry of the human anterior cingulate and paracingulate cortex. Neuroimage. 2006;33(3):843-854
65. Rauch SL, Shin LM, Phelps EA. Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research-Past, present, and future. Biol Psychiatry. 2006;60(4):376-382
66. Samuelson KW, Neylan TC, Metzler TJ, Lenoci M, Rothlind J, Henn-Haase C, Choucroun G, Weiner MW, Marmar CR. Neuropsychological functioning in posttraumatic stress disorder and alcohol abuse. Neuropsychology. 2006;20(6): 716-726
67. Woodward SH, Kaloupek DG, Streeter CC, Kimble MO, Reiss AL, Eliez S, Wald LL, Renshaw PF, Frederick BB, Lane B, Sheikh JI, Stegman WK, Kutter CJ, Stewart LP, Prestel RS, Arsenault NJ. Brain, skull, and cerebrospinal fluid volumes in adult posttraumatic stress disorder. J Trauma Stress. 2007;20(5):763-774
68. De Meersman RE, Stein PK. Vagal modulation and aging. Biol Psychol. 2007;74(2):165-173
69. Critchley HD, Good CD, Ashburner J, Frackowiak RS, Mathias CJ, Dolan RJ. Changes in cerebral morphology consequent to peripheral autonomic denervation. Neuroimage. 2003;18(4):908-916
70. Golding LA, Myers CR, Sinning WE, editors. Y's way to physical fitness: The complete guide to fitness testing and instruction. 3rd ed. Chicago (IL): Human Kinetics Publishers; 1989.