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Abnormal Noradrenergic Function in Posttraumatic Stress Disorder

Abnormal Noradrenergic Function in Posttraumatic Stress Disorder Abstract • To evaluate possible abnormal noradrenergic neuronal regulation in patients with posttraumatic stress disorder (PTSD), the behavioral, biochemical, and cardiovascular effects of intravenous yohimbine hydrochloride (0.4 mg/kg) were determined in 18 healthy male subjects and 20 male patients with PTSD. A subgroup of patients with PTSD were observed to experience yohimbine-induced panic attacks (70% [14/20]) and flashbacks (40% [8/20]), and they had larger yohimbine-induced increases in plasma 3-methoxy-4-hydroxyphenylglycol levels, sitting systolic blood pressure, and heart rate than those in healthy subjects. In addition, in the patients with PTSD, yohimbine induced significant increases in core PTSD symptoms, such as intrusive traumatic thoughts, emotional numbing, and grief. These data were consistent with a large body of preclinical data that indicated that uncontrollable stress produces substantial increases in noradrenergic neuronal function. We discuss the implications of these abnormalities in noradrenergic functional regulation in relation to the long-term neurobiological sequelae of severe uncontrollable stress and the pathophysiological relationship between PTSD and other anxiety disorders, such as panic disorder. References 1. Kulka RA, Schlenger WE, Fairbank JA, Hough RL, Jordan BK, Marmar CR, Weiss DS. Trauma and the Vietnam War Generation . New York, NY: Brunner/Mazel Inc; 1990. 2. Browne A, Finkelhor D. Impact of child sexual abuse: a review of the research . Psychol Bull . 1986:99:66-77.Crossref 3. Glavin GB. Stress and brain noradrenaline: a review . Behav Neurosci Rev . 1985;9:233-243.Crossref 4. Tsuda A, Tanaka M. Differential changes in noradrenaline turnover in specific regions of rat brain produced by controllable and uncontrollable shocks . Behav Neurosci . 1985;99:802-817.Crossref 5. Simson PE, Weiss JM. Altered activity of the locus coeruleus in an animal model of depression . Neuropsychopharmacology . 1988;1:287-295. 6. Simson PE, Weiss JM. Responsiveness of locus coereuleus neurons to excitatory stimulation is uniquely regulated by alpha-2 receptors . Psychopharmacol Bull . 1988;24:349-354. 7. Kosten TR, Mason JW, Giller EL. Sustained urinary norepinephrine and epinephrine elevation in posttraumatic stress disorder . Psychoneuroendocrinology . 1987;12:13-20.Crossref 8. Yehuda R, Southwick SM, Giller EL. Urinary catecholamine excretion and severity of PTSD symptoms in Vietnam combat veterans . Nerv Ment Dis . 1992;180:321-325.Crossref 9. Perry BD, Giller EL, Southwick SM. Altered platelet alpha2-adrenergic binding sites in posttraumatic stress disorder . Am J Psychiatry . 1987;144: 1511-1512. 10. Lerer B, Ebstein RP, Shestatsky M, Shemesh Z, Greenberg D. Cyclic AMP signal transduction in posttraumatic stress disorder . Am J Psychiatry . 1987;144:1324-1327. 11. Kolb LC, Burris BC, Griffiths S. Propranolol and clonidine in the treatment of post traumatic stress disorders of war . In: van der Kolk BA, ed. PostTraumatic Stress Disorder: Psychological and Biological Sequelae . Washington, DC: American Psychiatric Press Inc; 1984:98-105. 12. Kinzie JD, Leung P. Clonidine in Cambodian patients with post traumatic stress disorder . J Nerv Ment Dis . 1989;177:546-550.Crossref 13. Orr SP. Psychophysiologic studies of post traumatic stress disorder . In: Giller EL, ed. Biological Assessment and Treatment of Post Traumatic Stress Disorder . Washington, DC: American Psychiatric Press Inc; 1990:75-90. 14. Blanchard EB, Kolb LC, Pallmeyer TP, Gerardi RJ. A psychophysiological study of posttraumatic stress disorder in Vietnam veterans . Psychiatr Q . 1982;54:220-229.Crossref 15. Blanchard EB, Kolb LC, Gerardi RJ, Ryan P, Pallmeyer TP. Cardiac response to relevant stimuli as an adjunctive tool for diagnosing post-traumatic stress disorder in Vietnam veterans . Behav Ther . 1986;17:592-606.Crossref 16. Malloy PF, Fairbank JA, Keane TM. Validation of a multimethod assessment of posttraumatic stress disorders in Vietnam veterans . J Consult Clin Psychol . 1983;51:488-494.Crossref 17. Kolb LC. The post traumatic stress disorders of combat: a subgroup with a conditioned emotional response . Mil Med . 1984;149:237-243. 18. Pallmeyer TP, Blanchard EB, Kolb LC. The psychophysiology of combat-induced posttraumatic stress disorder in Vietnam veterans . Behav Res Ther . 1986;24:645-652.Crossref 19. Pitman RK, Orr SP, Forgue DF, deJong JB, Claiborn JM. Psychophysiologic assessment of post-traumatic stress disorder in Vietnam combat veterans . Arch Gen Psychiatry . 1987;44:970-975.Crossref 20. Charney DS, Heninger GR, Breier A. Noradrenergic function in panic anxiety: effects of yohimbine in healthy subjects and patients with agoraphobia and panic disorder . Arch Gen Psychiatry . 1984;41:751-763.Crossref 21. Charney DS, Woods SW, Goodman WK, Heninger GR. Neurobiological mechanisms of panic anxiety: biochemical and behavioral correlates of yohimbine-induced panic attacks . Am J Psychiatry . 1987;144:1030-1036. 22. Gurguis GNM, Uhde TW. Plasma 3-methoxy-4- hydroxyphenylethylene glycol (MHPG) and growth hormone responses to yohimbine in panic disorder patients and normal controls . Psychoneuroendocrinology . 1990;15:217-224.Crossref 23. 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;56:85-90.Crossref 24. Dekirmenjian H, Maas JW. MHPG in plasma . Clin Chim Acta . 1974; 52:203-208.Crossref 25. Mass JW, Hattox SE, Roth RH. The determination of a brain arteriovenous difference for 3-methoxy-4-hydroxyphenylethyleneglycol (MHPG) . Brain Res . 1976;118:167-174.Crossref 26. Kopin IJ, Gordon EK, Jimerson DC, Polinsky RJ. Relation between plasma and cerebrospinal fluid levels of 3-methoxy-4-hydroxy-phenylglycol . Science . 1983;219:73-75.Crossref 27. Scatton B, Zirkivic B, Devek J. Antidopamine properties of yohimbine . J Pharmacol Exp Ther . 1980;215:494-499. 28. Peskind ER, Veith RC, Dorsa DM, Gumbrecht G, Raskind MA. Yohimbine increases cerebrospinal fluid and plasma norepinephrine but not arginine vasopressin in humans . Neuroendocrinology . 1989;50:286-291.Crossref 29. Rudolph CD, Kaplan SI, Ganong WF. Sites at which clonidine acts to affect blood pressure and the secretion of renin, growth hormone and ACTH . Neuroendocrinology . 1980;31:121-128.Crossref 30. Reid IA, Ahn JN, Trinh T, et al. Mechanism of suppression of vasopressin and adrenocorticotropic hormone secretion by clonidine in anesthetized dogs . I Pharmacol Exp Ther . 1984;229:1-8. 31. Shimizu K. Effect of α1- and -adrenoceptor agonists and antagonists on ACTH secretion in intact and in hypothalamic dealerenated rats . Jpn J Pharmacol . 1984;36:23-33.Crossref 32. Kobinger W. α-Adrenoceptors in cardiovascular regulation . In:Ziegler MG, Lake CR, eds. Norepinephrine . Baltimore, Md: Williams & Wilkins; 1984:307-326. 33. Tung CS, Onnora CO, Robertson D, et al. Hypertensive effect of yohimbine following selective injection into the nucleus tractus solitarii of normotensive rats . Brain Res . 1983;227:193-195.Crossref 34. Bosquet P, Schwartz J. Alpha-adrenergic drugs: pharmacological tools for the study of the central vasomotor control . Biochem Pharmacol . 1983;32:1439-1465. 35. Glazer WM, Charney DS, Heninger GR. Noradrenergic function in schizophrenia . Arch Gen Psychiatry . 1987;44:898-904.Crossref 36. Heninger GR, Charney DS, Price LH. α2-Adrenergic receptor sensitivity in depression: the plasma MHPG, behavioral, and cardiovascular responses to yohimbine . Arch Gen Psychiatry . 1988;45:718-726.Crossref 37. Charney DS, Woods SW, Heninger GR. Noradrenergic function in generalized anxiety disorder: effects of yohimbine in healthy subjects and patients with generalized anxiety disorder . Psychol Res . 1989;27:173-182.Crossref 38. Rasmussen SA, Goodman WK, Woods SW, Heninger GR, Charney DS. Effects of yohimbine in obsessive-compulsive disorder . Psychopharmacology (Berl) . 1987;93:308-313.Crossref 39. Rainey JM, Aleen A, Ortiz A, Yeragami V, Pohl R, Bereliou R. A laboratory procedure for the induction of flashbacks . Am J Psychiatry . 1987; 144:1317-1319. 40. Fyer AJ, Liebowitz MR, Gorman JM, Davies SO, Klein DF. Lactate vulnerability of remitted panic patients . Psychiatry Res . 1985;14:143-148.Crossref 41. Liebowitz MR, Fyer AJ, Gorman JM, Dillon D, Appleby I, Levy G, Anderson S, Levitt M, Palij M, Davies SO, Klein DF. Lactate provocation of panic attacks, I: clinical and behavioral findings . Arch Gen Psychiatry . 1984;41:764-770.Crossref 42. Liebowitz MR, Gorman JM, Fyer AJ, Levitt M, Dillon D, Levy G, Appleby I, Anderson S, Palij M, Davies SO, Klein DF. Lactate provocation of panic attacks, II: biochemical and physiological findings . Arch Gen Psychiatry . 1985;42:709-719.Crossref 43. Rainey JM, Frohman CE, Warner K, Bates S, Pohl R, Yeragani V. Panic anxiety and lactate metabolism . Psychopharmacol Bull . 1985;21:434-437. 44. Crowe RR. The genetics of panic disorder and agoraphobia . Psychiatr Dev . 1985;2:171-186. 45. Nagy L, Marikangas K, Southwick S, Docherty N, Dan E, Harkness L, Charney D. Family relationship between panic and PTSD. In: Program and abstracts of the 144th Annual Meeting of the American Psychiatric Association; May 11-16, 1991; New Orleans, La. Abstract NR182. 46. McGaugh JL. Involvement of hormonal and neuromodulatory systems in the regulation of memory storage . Annu Rev Neurosci . 1989;2:255-287.Crossref 47. McGaugh JL. Significance and remembrance: the role of neuromodulatory systems . Psychol Sci . 1990;1:15-25.Crossref 48. Pitman RK. Post-traumatic stress disorder, hormones, and memory . Biol Psychiatry . 1989;26:221-223.Crossref 49. Squire LR. Mechanisms of memory . Science . 1986;232:1612-1619.Crossref 50. Cassens G, Kuruc A, Roffman M, Orsulak P, Schildkraut JJ. Alterations in brain norepinephrine metabolism and behavior induced by environmental stimuli previously paired with inescapable shock . Behav Brain Res . 1981;2:387-407.Crossref 51. Rasmussen K, Marilak DA, Jacobs BL. Single unit activity of the locus coeruleus in the freely moving cat, I: during naturalistic behaviors and in response to simple and complex stimuli . Brain Res . 1986;371:324-334.Crossref 52. Litz BT, Keane TM. Information processing in anxiety disorders: application to the understanding of post-traumatic stress disorder . Clin Psy- chol Rev . 1989;9:243-257.Crossref 53. McNally RJ, Luedke DL, Besyner JK, Peterson RA, Bohm K, Lips OJ. Sensitivity to stress relevant stimuli in post traumatic stress disorder . J Anxiety Dis . 1987;1:105-116.Crossref 54. VanDyke C, Zilberg NJ, MacKinnon JA. Post traumatic stress disorder: a thirty year delay in a World War II veteran . Am J Psychiatry . 1985;142: 1070-1073. 55. Solomen Z, Garb K, Bleich A, Grupper D. Reactivation of combatrelated post traumatic stress disorder . Am J Psychiatry . 1987;144:51-55. 56. Anisman H, Sklar LS. Catecholamine depletion upon reexposure to stress: mediation of the escape deficits produced by inescapable shock . J Comp Psychol . 1978;93:610-625.Crossref 57. Irwin J, Ahluwalia P, Anisman H. Sensitization of norepinephrine activity following acute and chronic footshock . Brain Res . 1986;379:98-103.Crossref 58. Nisenbaum LK, Zigmund MJ, Sved AF, Abercrombie ED. Prior exposure to chronic stress results in enhanced synthesis and release of hippocampal norepinephrine in response to a novel stressor . J Neurosci . 1991;11: 1478-1484. 59. Krystal JH, Kosten TR, Perry BD, Southwick S, Mason JW, Giller EL Jr. Neurobiological aspects of PTSD: review of clinical and preclinical studies . Behav Ther . 1989;20:177-198.Crossref 60. Dunn AJ, Berridge CW. Corticotropin-releasing factor administration elicits a stresslike activation of cerebral catecholaminergic systems . Pharmacol Biochem Behav . 1987;27:685-691.Crossref 61. Valentino RJ, Foote SL. Corticotropin-releasing hormone increases tonic but not sensory-evoked activity of noradrenergic locus coeruleus neurons in unanesthetized rats . J Neurosci . 1988;8:1016-1025. 62. Chappell PB, Smith MA, Kilts CD, Bissette G, Ritchie J, Anderson C, Nemeroff CB. Alterations in corticotropin-releasing factor-like immunoreactivity in discrete rat brain regions after acute and chronic stress . J Neurosci . 1990;6:2908-2914. 63. Butler PD, Weiss JM, Stout JC, Nemeroff CB. Corticotropin-releasing factor produces fear-enhancing and behavioral activating effects following infusion into the locus coeruleus . J Neurosci . 1990;10:176-183. 64. Redmond DE Jr. Studies of the nucleus locus coeruleus in monkeys and hypotheses for neuropsychopharmacology . In: Meltzer HY, ed: Psychopharmacology: The Third Generation of Progress . New York, NY: Raven Press; 1987:967-975. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Archives of General Psychiatry American Medical Association

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References (73)

Publisher
American Medical Association
Copyright
Copyright © 1993 American Medical Association. All Rights Reserved.
ISSN
0003-990X
eISSN
1598-3636
DOI
10.1001/archpsyc.1993.01820160036003
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Abstract

Abstract • To evaluate possible abnormal noradrenergic neuronal regulation in patients with posttraumatic stress disorder (PTSD), the behavioral, biochemical, and cardiovascular effects of intravenous yohimbine hydrochloride (0.4 mg/kg) were determined in 18 healthy male subjects and 20 male patients with PTSD. A subgroup of patients with PTSD were observed to experience yohimbine-induced panic attacks (70% [14/20]) and flashbacks (40% [8/20]), and they had larger yohimbine-induced increases in plasma 3-methoxy-4-hydroxyphenylglycol levels, sitting systolic blood pressure, and heart rate than those in healthy subjects. In addition, in the patients with PTSD, yohimbine induced significant increases in core PTSD symptoms, such as intrusive traumatic thoughts, emotional numbing, and grief. These data were consistent with a large body of preclinical data that indicated that uncontrollable stress produces substantial increases in noradrenergic neuronal function. We discuss the implications of these abnormalities in noradrenergic functional regulation in relation to the long-term neurobiological sequelae of severe uncontrollable stress and the pathophysiological relationship between PTSD and other anxiety disorders, such as panic disorder. References 1. Kulka RA, Schlenger WE, Fairbank JA, Hough RL, Jordan BK, Marmar CR, Weiss DS. Trauma and the Vietnam War Generation . New York, NY: Brunner/Mazel Inc; 1990. 2. Browne A, Finkelhor D. Impact of child sexual abuse: a review of the research . Psychol Bull . 1986:99:66-77.Crossref 3. Glavin GB. Stress and brain noradrenaline: a review . Behav Neurosci Rev . 1985;9:233-243.Crossref 4. Tsuda A, Tanaka M. Differential changes in noradrenaline turnover in specific regions of rat brain produced by controllable and uncontrollable shocks . Behav Neurosci . 1985;99:802-817.Crossref 5. Simson PE, Weiss JM. Altered activity of the locus coeruleus in an animal model of depression . Neuropsychopharmacology . 1988;1:287-295. 6. Simson PE, Weiss JM. Responsiveness of locus coereuleus neurons to excitatory stimulation is uniquely regulated by alpha-2 receptors . Psychopharmacol Bull . 1988;24:349-354. 7. Kosten TR, Mason JW, Giller EL. Sustained urinary norepinephrine and epinephrine elevation in posttraumatic stress disorder . Psychoneuroendocrinology . 1987;12:13-20.Crossref 8. Yehuda R, Southwick SM, Giller EL. Urinary catecholamine excretion and severity of PTSD symptoms in Vietnam combat veterans . Nerv Ment Dis . 1992;180:321-325.Crossref 9. Perry BD, Giller EL, Southwick SM. Altered platelet alpha2-adrenergic binding sites in posttraumatic stress disorder . Am J Psychiatry . 1987;144: 1511-1512. 10. Lerer B, Ebstein RP, Shestatsky M, Shemesh Z, Greenberg D. Cyclic AMP signal transduction in posttraumatic stress disorder . Am J Psychiatry . 1987;144:1324-1327. 11. Kolb LC, Burris BC, Griffiths S. Propranolol and clonidine in the treatment of post traumatic stress disorders of war . In: van der Kolk BA, ed. PostTraumatic Stress Disorder: Psychological and Biological Sequelae . Washington, DC: American Psychiatric Press Inc; 1984:98-105. 12. Kinzie JD, Leung P. Clonidine in Cambodian patients with post traumatic stress disorder . J Nerv Ment Dis . 1989;177:546-550.Crossref 13. Orr SP. Psychophysiologic studies of post traumatic stress disorder . In: Giller EL, ed. Biological Assessment and Treatment of Post Traumatic Stress Disorder . Washington, DC: American Psychiatric Press Inc; 1990:75-90. 14. Blanchard EB, Kolb LC, Pallmeyer TP, Gerardi RJ. A psychophysiological study of posttraumatic stress disorder in Vietnam veterans . Psychiatr Q . 1982;54:220-229.Crossref 15. Blanchard EB, Kolb LC, Gerardi RJ, Ryan P, Pallmeyer TP. Cardiac response to relevant stimuli as an adjunctive tool for diagnosing post-traumatic stress disorder in Vietnam veterans . Behav Ther . 1986;17:592-606.Crossref 16. Malloy PF, Fairbank JA, Keane TM. Validation of a multimethod assessment of posttraumatic stress disorders in Vietnam veterans . J Consult Clin Psychol . 1983;51:488-494.Crossref 17. Kolb LC. The post traumatic stress disorders of combat: a subgroup with a conditioned emotional response . Mil Med . 1984;149:237-243. 18. Pallmeyer TP, Blanchard EB, Kolb LC. The psychophysiology of combat-induced posttraumatic stress disorder in Vietnam veterans . Behav Res Ther . 1986;24:645-652.Crossref 19. Pitman RK, Orr SP, Forgue DF, deJong JB, Claiborn JM. Psychophysiologic assessment of post-traumatic stress disorder in Vietnam combat veterans . Arch Gen Psychiatry . 1987;44:970-975.Crossref 20. Charney DS, Heninger GR, Breier A. Noradrenergic function in panic anxiety: effects of yohimbine in healthy subjects and patients with agoraphobia and panic disorder . Arch Gen Psychiatry . 1984;41:751-763.Crossref 21. Charney DS, Woods SW, Goodman WK, Heninger GR. Neurobiological mechanisms of panic anxiety: biochemical and behavioral correlates of yohimbine-induced panic attacks . Am J Psychiatry . 1987;144:1030-1036. 22. Gurguis GNM, Uhde TW. Plasma 3-methoxy-4- hydroxyphenylethylene glycol (MHPG) and growth hormone responses to yohimbine in panic disorder patients and normal controls . Psychoneuroendocrinology . 1990;15:217-224.Crossref 23. 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;56:85-90.Crossref 24. Dekirmenjian H, Maas JW. MHPG in plasma . Clin Chim Acta . 1974; 52:203-208.Crossref 25. Mass JW, Hattox SE, Roth RH. The determination of a brain arteriovenous difference for 3-methoxy-4-hydroxyphenylethyleneglycol (MHPG) . Brain Res . 1976;118:167-174.Crossref 26. Kopin IJ, Gordon EK, Jimerson DC, Polinsky RJ. Relation between plasma and cerebrospinal fluid levels of 3-methoxy-4-hydroxy-phenylglycol . Science . 1983;219:73-75.Crossref 27. Scatton B, Zirkivic B, Devek J. Antidopamine properties of yohimbine . J Pharmacol Exp Ther . 1980;215:494-499. 28. Peskind ER, Veith RC, Dorsa DM, Gumbrecht G, Raskind MA. Yohimbine increases cerebrospinal fluid and plasma norepinephrine but not arginine vasopressin in humans . Neuroendocrinology . 1989;50:286-291.Crossref 29. Rudolph CD, Kaplan SI, Ganong WF. Sites at which clonidine acts to affect blood pressure and the secretion of renin, growth hormone and ACTH . Neuroendocrinology . 1980;31:121-128.Crossref 30. Reid IA, Ahn JN, Trinh T, et al. Mechanism of suppression of vasopressin and adrenocorticotropic hormone secretion by clonidine in anesthetized dogs . I Pharmacol Exp Ther . 1984;229:1-8. 31. Shimizu K. Effect of α1- and -adrenoceptor agonists and antagonists on ACTH secretion in intact and in hypothalamic dealerenated rats . Jpn J Pharmacol . 1984;36:23-33.Crossref 32. Kobinger W. α-Adrenoceptors in cardiovascular regulation . In:Ziegler MG, Lake CR, eds. Norepinephrine . Baltimore, Md: Williams & Wilkins; 1984:307-326. 33. Tung CS, Onnora CO, Robertson D, et al. Hypertensive effect of yohimbine following selective injection into the nucleus tractus solitarii of normotensive rats . Brain Res . 1983;227:193-195.Crossref 34. Bosquet P, Schwartz J. Alpha-adrenergic drugs: pharmacological tools for the study of the central vasomotor control . Biochem Pharmacol . 1983;32:1439-1465. 35. Glazer WM, Charney DS, Heninger GR. Noradrenergic function in schizophrenia . Arch Gen Psychiatry . 1987;44:898-904.Crossref 36. Heninger GR, Charney DS, Price LH. α2-Adrenergic receptor sensitivity in depression: the plasma MHPG, behavioral, and cardiovascular responses to yohimbine . Arch Gen Psychiatry . 1988;45:718-726.Crossref 37. Charney DS, Woods SW, Heninger GR. Noradrenergic function in generalized anxiety disorder: effects of yohimbine in healthy subjects and patients with generalized anxiety disorder . Psychol Res . 1989;27:173-182.Crossref 38. Rasmussen SA, Goodman WK, Woods SW, Heninger GR, Charney DS. Effects of yohimbine in obsessive-compulsive disorder . Psychopharmacology (Berl) . 1987;93:308-313.Crossref 39. Rainey JM, Aleen A, Ortiz A, Yeragami V, Pohl R, Bereliou R. A laboratory procedure for the induction of flashbacks . Am J Psychiatry . 1987; 144:1317-1319. 40. Fyer AJ, Liebowitz MR, Gorman JM, Davies SO, Klein DF. Lactate vulnerability of remitted panic patients . Psychiatry Res . 1985;14:143-148.Crossref 41. Liebowitz MR, Fyer AJ, Gorman JM, Dillon D, Appleby I, Levy G, Anderson S, Levitt M, Palij M, Davies SO, Klein DF. Lactate provocation of panic attacks, I: clinical and behavioral findings . Arch Gen Psychiatry . 1984;41:764-770.Crossref 42. Liebowitz MR, Gorman JM, Fyer AJ, Levitt M, Dillon D, Levy G, Appleby I, Anderson S, Palij M, Davies SO, Klein DF. Lactate provocation of panic attacks, II: biochemical and physiological findings . Arch Gen Psychiatry . 1985;42:709-719.Crossref 43. Rainey JM, Frohman CE, Warner K, Bates S, Pohl R, Yeragani V. Panic anxiety and lactate metabolism . Psychopharmacol Bull . 1985;21:434-437. 44. Crowe RR. The genetics of panic disorder and agoraphobia . Psychiatr Dev . 1985;2:171-186. 45. Nagy L, Marikangas K, Southwick S, Docherty N, Dan E, Harkness L, Charney D. Family relationship between panic and PTSD. In: Program and abstracts of the 144th Annual Meeting of the American Psychiatric Association; May 11-16, 1991; New Orleans, La. Abstract NR182. 46. McGaugh JL. Involvement of hormonal and neuromodulatory systems in the regulation of memory storage . Annu Rev Neurosci . 1989;2:255-287.Crossref 47. McGaugh JL. Significance and remembrance: the role of neuromodulatory systems . Psychol Sci . 1990;1:15-25.Crossref 48. Pitman RK. Post-traumatic stress disorder, hormones, and memory . Biol Psychiatry . 1989;26:221-223.Crossref 49. Squire LR. Mechanisms of memory . Science . 1986;232:1612-1619.Crossref 50. Cassens G, Kuruc A, Roffman M, Orsulak P, Schildkraut JJ. Alterations in brain norepinephrine metabolism and behavior induced by environmental stimuli previously paired with inescapable shock . Behav Brain Res . 1981;2:387-407.Crossref 51. Rasmussen K, Marilak DA, Jacobs BL. Single unit activity of the locus coeruleus in the freely moving cat, I: during naturalistic behaviors and in response to simple and complex stimuli . Brain Res . 1986;371:324-334.Crossref 52. Litz BT, Keane TM. Information processing in anxiety disorders: application to the understanding of post-traumatic stress disorder . Clin Psy- chol Rev . 1989;9:243-257.Crossref 53. McNally RJ, Luedke DL, Besyner JK, Peterson RA, Bohm K, Lips OJ. Sensitivity to stress relevant stimuli in post traumatic stress disorder . J Anxiety Dis . 1987;1:105-116.Crossref 54. VanDyke C, Zilberg NJ, MacKinnon JA. Post traumatic stress disorder: a thirty year delay in a World War II veteran . Am J Psychiatry . 1985;142: 1070-1073. 55. Solomen Z, Garb K, Bleich A, Grupper D. Reactivation of combatrelated post traumatic stress disorder . Am J Psychiatry . 1987;144:51-55. 56. Anisman H, Sklar LS. Catecholamine depletion upon reexposure to stress: mediation of the escape deficits produced by inescapable shock . J Comp Psychol . 1978;93:610-625.Crossref 57. Irwin J, Ahluwalia P, Anisman H. Sensitization of norepinephrine activity following acute and chronic footshock . Brain Res . 1986;379:98-103.Crossref 58. Nisenbaum LK, Zigmund MJ, Sved AF, Abercrombie ED. Prior exposure to chronic stress results in enhanced synthesis and release of hippocampal norepinephrine in response to a novel stressor . J Neurosci . 1991;11: 1478-1484. 59. Krystal JH, Kosten TR, Perry BD, Southwick S, Mason JW, Giller EL Jr. Neurobiological aspects of PTSD: review of clinical and preclinical studies . Behav Ther . 1989;20:177-198.Crossref 60. Dunn AJ, Berridge CW. Corticotropin-releasing factor administration elicits a stresslike activation of cerebral catecholaminergic systems . Pharmacol Biochem Behav . 1987;27:685-691.Crossref 61. Valentino RJ, Foote SL. Corticotropin-releasing hormone increases tonic but not sensory-evoked activity of noradrenergic locus coeruleus neurons in unanesthetized rats . J Neurosci . 1988;8:1016-1025. 62. Chappell PB, Smith MA, Kilts CD, Bissette G, Ritchie J, Anderson C, Nemeroff CB. Alterations in corticotropin-releasing factor-like immunoreactivity in discrete rat brain regions after acute and chronic stress . J Neurosci . 1990;6:2908-2914. 63. Butler PD, Weiss JM, Stout JC, Nemeroff CB. Corticotropin-releasing factor produces fear-enhancing and behavioral activating effects following infusion into the locus coeruleus . J Neurosci . 1990;10:176-183. 64. Redmond DE Jr. Studies of the nucleus locus coeruleus in monkeys and hypotheses for neuropsychopharmacology . In: Meltzer HY, ed: Psychopharmacology: The Third Generation of Progress . New York, NY: Raven Press; 1987:967-975.

Journal

Archives of General PsychiatryAmerican Medical Association

Published: Apr 1, 1993

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