The neurobiological basis of anxiety and fear: Circuits, mechanisms, and neurochemical interactions (Part II)

Neuroscientist

Volumn 4, Issue 2, 1998, Pages 122-132

  Charney, Dennis S ^a   Grillon, Christian C G ^a   Bremner, J Douglas ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Corticotropin releasing hormone; Cortisol; Norepinephrine; Panic disorder; PTSD; Stress

Indexed keywords

AMYGDALOID NUCLEUS; ANXIETY NEUROSIS; BEHAVIOR; BRAIN REGION; CONDITIONING; FEAR; HIPPOCAMPUS; HUMAN; LOCUS CERULEUS; NEUROBIOLOGY; NEUROCHEMISTRY; PANIC; PATHOPHYSIOLOGY; POSTTRAUMATIC STRESS DISORDER; REINFORCEMENT; REVIEW; STRESS;

EID: 0031954427     PISSN: 10738584     EISSN: None     Source Type: Journal    
DOI: 10.1177/107385849800400208     Document Type: Review

References (129)

1. McGaugh JL. Involvement of hormonal and neuromodulatory systems in the regulation of memory storage. Annu Rev Neurosci 1989;2:255-287.
2. McGaugh JL. Significance and remembrance: The role of neuromodulatory systems. Psychol Sci 1990;1:15-25.
3. Gold PE, vanBuskirk RB. Effects of alpha- and beta-adrenergic receptor antagonists on posttrial epinephrine modulation of memory: Relationship to posttraining brain norepinephrine concentrations. Behav Biol 1978;24:1168-1184.
4. Introini-Collison IB, McGaugh JL. Epinephrine modulates long-term retention of an aversively motivated discrimination task. Behav Neural Biol 1986;45:358-365.
5. Roozendaal B, McGaugh JL. Basolateral amygdala lesions block the memory enhancing effects of glucocorticoid administration in the dorsal hippocampus (abstract). Neurosci Abstr 1996;22: 1869.
6. Devanges V, Sara SJ. Memory retrieval enhancement by locus coeruleus stimulation: Evidence for mediation by β-receptors. Behav Brain Res 1991;43:93-97.
7. 2 antagonist, facilitates memory retrieval in the rat. Behav Neural Biol 1989;51:401-411.
8. Roozendaal B, Carmi O, McGaugh JL. Adrenocortical suppression of the memory enhancing effects of amphetamine and epinephrine. Proc Natl Acad Sci U S A 1996;93:1429-1433.
9. Quirarte GL, Roozendaal B, McGaugh JL. Glucocorticoid induced memory modulation depends upon noradrenergic neurotransmission in the basolateral nucleus of the amygdala (abstract). Neurosci Abstr 1996;22:2869.
10. Southwick SM, Krystal JH, Morgan CA, et al. Abnormal noradrenergic function in post traumatic stress disorder. Arch Gen Psychiatr 1993;50:266-274.
11. Cahill L, Prins B, Weber M, McGaugh JL. β-Adrenergic activation and memory for emotional events. Nature 1994;371:702-704.
12. Nakane H, Shimizu H, Hori T. Stress induced NE increase in the rat prefrontal cortex measured by microdialysis. Am J Physiol 1994;167:R1559-R1560.
13. Redmond DE Jr. Studies of the nucleus locus coeruleus in monkeys and hypotheses for neuropsychopharmacology. In: Meltzer HY, editor. Psychopharmacology: the third generation of progress. New York: Raven; 1987. p. 967-975.
14. Abercrombie ED, Jacobs BL. Single-unit response of noradrenergic neurons in the locus coeruleus of freely moving cats. I: Acutely presented stressful and nonstressful stimuli. J Neurosci 1987;7:2837-2843.
15. Foote SL, Bloom FE, Aston-Jones G. Nucleus locus coeruleus: New evidence for anatomical and physiological specificity. Physiol Rev 1983;63:844-914.
16. Levine ES, Litto WJ, Jacobs BL. Activity of cat locus coeruleus noradrenergic neurons during the defense reaction. Brain Res 1990;531:189-195.
17. Simson PE, Weiss JM. Altered activity of the locus coeruleus in an animal model of depression. Neuropsychopharmacology 1988;1:287-295.
18. Simson PE, Weiss JM. Responsiveness of locus coeruleus neurons to excitatory stimulation is uniquely regulated by alpha-2 receptors. Psychopharmacol Bull 1988;24:349-354.
19. Torda T, Kvetnansky R, Petrikova M. Effect of repeated immobilization stress on rat central and peripheral adrenoceptors. In: Usdin E, Kvetnansky R, Axelrod J, editors. Stress: the role of catecholamines and other neurotransmitters. New York: Gordon & Breach; 1984. p. 691-701.
20. Nisenbaum LK, Abercrombie ED. Presynaptic alterations associated with enhancement of evoked release and synthesis of NE in hippocampus of chemically cold stressed rats. Brain Res 1993; 608:280-287.
21. 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 Psychiatr 1984;41:751-763.
22. Charney DS, Woods SW, Goodman WK, Heninger GR. Neurobiological mechanisms of panic anxiety: Biochemical and behavioral correlates of yohimbine-induced panic attacks. Am J Psychiatr 1987;144:1030-1036.
23. Green BL, Grace MC, Lindy JP, Gleser GC, Leonard A. Risk factors for PTSD and other diagnoses in a general sample of Vietnam veterans. Am J Psychiatr 1990;147:729-733.
24. Shirao I, Tsuda A, Yoshisshige I, et al. Effect of acute ethanol administration on noradrenaline metabolism in brain regions of stressed and nonstressed rats. Pharmacol Biochem Behav 1988; 30:769-773.
25. Tanaka M, Kohnoy, Tsuda A, et al. Differential effects of morphine on noradrenaline release in brain regions of stressed and non-stressed rats. Brain Res 1983;275:105-115.
26. Ida Y, Tanaka M, Tsuda A, Tsujimaru S, Nagasaki N. Attenuating effect of diazepam on stress-induced increases in noradrenaline turnover in specific brain regions of rats: Antagonism by Ro 15-1788. Life Sci 1985;37:2491-2498.
27. Malloy PF, Fairbank JA, Keane TM. Validation of a multimethod assessment of post-traumatic stress disorders in Vietnam veterans. J Consul Clin Psychol 1983;51:488-494.
28. Pitman RK, Orr SP, Forgue DF, deJong JB, Claiborn JM. Psychophysiologic assessment of post-traumatic stress disorder in Vietnam combat veterans. Arch Gen Psychiatr 1987;44:970-975.
29. McFall MF, Murburg MM, Ko GM, Veith RC. Autonomic responses to stress in Vietnam veterans with post traumatic stress disorder. Biol Psychol 1990;27:1165-1175.
30. Aston-Jones G, Shipley MT, Chouvet G, et al. Afferent regulation of locus coeruleus neurons: Anatomy, physiology and pharmacology. Prog Brain Res 1991;88:47-75.
31. Krystal JH, Kosten TR, Perry BD, Southwick S, Mason JW, Giller EL. Neurobiological aspects of PTSD: Review of clinical and preclinical studies. Behav Ther 1989;20:177-198.
32. 2 adrenergic binding sites in posttraumatic stress disorder. Am J Psychiatr 1987;144:1511-1512.
33. Southwick SM, Krystal JH, Bremner JD, et al. Noradrenergic and serotonergic function in posttraumatic stress disorder. Arch Gen Psychiatr 1997;54:749-758.
34. Bremner JD, Innis RB, Ng CK, et al. PET Measurement of central metabolic correlates of yohimbine administration in posttraumatic stress disorder. Arch Gen Psychiatr 1997;54:246-254.
35. Gurguis GN, Uhde TW. Plasma MHPG and growth hormone responses to yohimbine in panic disorder patients and normal controls. Psychoneuroendocrinology 1990;15:217-224.
36. Charney DS, Woods SW, Krystal JH, Nagy LM, Heninger GR. Noradrenergic neuronal dysregulation in panic disorder: The effects of intravenous yohimbine and clonidine in panic disorder patients. Acta Psychiatr Scand 1992;86:273-282.
37. Uhde TW, Murray MB, Vittone BJ, et al. Behavioral and physiological effects of short-term and long-term administration of clonidine in panic disorder. Arch Gen Psychiatr 1989;46:170-177.
38. 2-adrenoceptor sensitivity in panic disorder. Arch Gen Psychiatr 1989;46:165-169.
39. Coplan JD, Pine D, Papp L, et al. Uncoupling of the noradrenergic-hypothalamic-pituitary adrenal axis in panic disorder. Neuropsychopharmacology 1995;13:65-73.
40. Chalmers DT, Lovenberg TW, Grigoriadis DE, Behan DP, DeSanza EB. Corticotropin-releasing factor receptors: From molecular biology to drug design. Trends Pharmacol Sci 1996;17: 166-172.
41. Chappell PB, Smith MA, Kitts CD, et al. Alterations in corticotropin-releasing factor-like immunoreactivity in discrete rat brain regions after acute and chronic stress. J Neurosci 1986;6: 2908-2914.
42. Swanson LW, Sawchenko PE. Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Ann Rev Neuro 1983;6:269-234.
43. Heilig M, Koob GF, Ekman R, Britton KT. Corticotropin-releasing factor and neuropeptide Y: Role in emotional integration. Trends Neuro Sci 1994;17:80-85.
44. Liang KC, Melia KR, Miserendino MJD, Falls WA, Campeau S, Davis M. Corticotropin-releasing factor: Long-lasting facilitation of the acoustic startle reflex. J Neurosci 1992;12:2303-2312.
45. Swerdlow NR, Geyer MA, Vale WW, Koob GF. Cortico-releasing factor potentiates acoustic startle response in rats: Blockade by chlordiazepide. Psychopharmacol 1986;88:147-152.
46. Swerdlow NR, Britton KT, Koob GF. Potentiation of acoustic startle by cortico-releasing factor (CRF) and by fear are both reversed by alpha-helical CRF(9-41). Neuropsychopharmacol 1989;2:285-292.
47. Berridge CW, Dunn AJ. A Corticotropin-releasing factor antagonist reverses the stress-induced changes of exploratory behavior in mice. Horm Behav 1987;21:393-401.
48. Skutella T, Montkowski A, Stohr T, et al. CRH antisense oligodeoxynucleotide treatment attenuates social defeat anxiety in rats. Mol Cell Neurobiol 1994;14:579-588.
49. Pich EM, Lorang M, Yeganeh M, et al. Increase of extracellular corticotropin-releasing factor-like immunoreactivity levels in the amygdala of awake rats during restraint stress and ethanol withdrawal as measured by microdialysis. J Neurosci 1995;15:5439-5447.
50. Liang K, Lee E. Intra-amygdala injections of corticotropin releasing factor facilitate inhibitory avoidance learning and reduce exploratory behavior in rats. Psychopharmacology (Berl) 1988; 96:232-236.
51. Liebsch G, Landgraf P, Gerstberger R, et al. Chronic infusion of a CRF1 receptor antisense oligodeoxynucleotide into the central nucleus of the amygdala reduced anxiety in socially defeated rats. Regul Peptides 1995;59:229-239.
52. Henke PG. The bed nucleus of the stria terminalis and immobilization stress: Unit activity, escape behavior, and gastric pathology in rats. Behav Brain Res 1984;11:35-45.
53. Casada JH, Dafny N. Evidence for two different afferent pathways carrying stress-related information (noxious and amygdala stimulation) to the bed nucleus of the stria terminalis. Brain Res 1992;579:93-98.
54. Sawchenko PE, Swanson LW. The organization of forebrain afferents to the paraventricular and supraoptic nuclei of the rat. J Comp Neurol 1983;218:121-144.
55. Lee Y, Davis M. The role of the bed nucleus of the stria terminalis in CRH enhanced startle: An animal model of anxiety (abstract). Neurosci Abstr 1996;22:465.
56. Valentino RJ, Foote SL, Page ME. The locus coeruleus as a site for integrating corticotropin-releasing factor and noradrenergic mediation of the stress response. Ann NY Acad Sci 1993;697: 173-188.
57. Weiss J, Stout J, Aaron M, Owens M, Nemeroff C. Experimental studies of depression and anxiety: Role of locus coeruleus and corticotropin-releasing factor. Brain Res Bull 1995;35:561-572.
58. Butler P, Weiss J, Stout J, Nemeroff C. Corticotropin-releasing factor produces fear-enhancing and behavioral activating effects following infusion into the locus coeruleus. J Neurosci 1990;10: 176-183.
59. Smagin GN, Swiergiel AH, Dunn AJ. Corticotropin-releasing factor administered into the locus coeruleus, but not the parabrachial nucleus, stimulates norepinephrine release in the prefrontal cortex. Brain Res Bull 1995;36:71-76.
60. Valentino R, Foote S. Corticotropin-releasing hormone increases tonic but not sensory-evoked activity of noradrenergic locus coeruleus neurons in unanesthetized rats. J Neurosci 1988;8:1016-1025.
61. Page ME, Abercrombie ED. Analysis of discharge. characteristics of locus coeruleus, neurons during activation by diverse neurochemical inputs (abstract). Neurosci Abstr 1996;22:600.
62. Curtis AL, Florin-Lechner SM, Pavcovich LA, Valentino RJ. CRF microinfusion into the LC: Effects on discharge rate, cortical NE levels and cortical EEG activity (abstract). Neurosci Abstr 1996;22:1554.
63. Smagin GN, Zhou J, Harris RPS, Ryan DH. CRF antagonist infused into the LC attenuates immobilization stress induced increase of NE in the prefrontal cortex (abstract). Neurosci Abstr 1996;22:464.
64. McEwen BS, DeKloet ER, Rostene W. Adrenal steroid receptors and actions in the nervous system. Physiol Rev 1986;66:1121-1188.
65. Sapolsky RM, Plotsky PM. Hypercortisolism and its possible neural bases. Biol Psychiatr 1990;27:937-952.
66. Song L-N. Stress-induced changes in glucorticoid receptors: molecular mechanisms and clinical implications. Mol Cell Endocrinol 1991;80:C171-C174.
67. Sapolsky R, Krey L, McEwen BS. Glucorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc Natl Acad Sci U S A 1984;81:6174-6178.
68. Sapolsky R, Krey L, McEwen BS. Stress downregulates corticosterone receptors in a site specific manner in the brain. Endocrinology 1984;114:287-293.
69. Kant GJ, Eggleston T, Landman-Roberts L, Kenion CC, Driver GC, Meyerhoff JL. Habituation to repeated stress in stressor specific. Pharmacol Biochem Behav 1985;22:631-634.
70. Kant GJ, Leu JR, Anderson SM, Mougey EH. Effects of chronic stress on plasma corticosterone, ACTH and prolactin. Physiol Behav 1987;40:775-779.
71. Irwin J, Ahluwalia P, Zacharko RM, Anisman H. Central norepinephrine and plasma corticosterone following acute and chronic stressors: Influence of social isolation and handling. Pharmacol Biochem Behav 1986;24:1151-1154.
72. Hennessy MB, Levine S. Sensitive pituitary-adrenal responsiveness to varying intensities of psychological stimulation. Physiol Behav 1978;21:295-297.
73. Armario A, Restrepo C, Castellanos JM, Baslasch J. Dissociation between adrenocorticotropin and corticosterone responses to restraint stress after previous exposure to stress. Life Sci 1985;37: 2085-2092.
74. Gamallo A, Villanna A, Trandro G, Fraile A. Stress adaptation and adrenal activity in isolated and crowded rat. Physiol Behav 1989;26:829-841.
75. Ottenweller AT, Natelson BH, Pitman DL, Drestal SD. Adrenocortical and behavioral responses to repeated stressors: Toward an animal model of chronic stress and stress-related mental illness. Biol Behav 1986;36:217-221.
76. Caggiula AR, Antelman SM, Aul E, Knopf S, Edwards DJ. Prior stress attenuates the analgesic response but sensitizes the corticosterone and cortical dopamine responses to stress 10 days later. Psychopharmacology 1989;99:233-237.
77. Yehuda R, Giller EL, Southwick SM, Lawry MT, Mason JW. Hypothalamic-pituitary-adrenal dysfunction in post traumatic stress disorder. Biol Psychiatr 1991;30:1031-1048.
78. Pacak K, Palkovits M, Kvetnansky R, et al. Catecholamine inhibition by hypercortisolemic on the PVN of conscious rats. Endocrinology 1995;136:4814-4819.
79. Pacak K, Palkovits M, Kopin IJ, Goldstein DJ. Stress induced NE release in the hypothalamic PVN and pituitary-adrenal and sympathodrenal activity: In vivo microdialysis studies. Frontiers Neuroendocrinol 1995;16:89-150.
80. Vetrugno GC, Lachuer J, Perego C, Miranda E, DeSimons MG, Tappaz M. Lack of glucocorticoids sustains the stress induced release of noradrenaline in the anterior hypothalamus. Neuroendocrinology 1993;57:835-842.
81. Kvetnansky R. Fukuhara K, Pacak K, Cizza G, Goldstein DJ, Kopin IJ. Endogenous GC restrain catecholamine synthesis and release at rest and during immobilization stress in rats. Endocrinology 1993;133:1411-1419.
82. Pacak K, Kvetnansky R, Palkovits M, et al. Adrenalectory augments in vivo release of NE in the PVN during stress. Endocrinology 1993;133:1404-1410.
83. Komesaroff PA, Funder JW. Differential glucocorticoid effects on catecholamine responses to stress. Am J Physiol 1994;266: E118-E128.
84. Pacak K, Armando I, Komoly S. Hypercortisolemia inhibits yohimbine-induced release of norepinephrine in the posterolateral hypothalamus. Endocrinology 1991;131:1369-1376.
85. Lenders JWM, Golczynska A, Goldstein DS. Glucocorticoids, sympathetic activity and presynaptic alpha-2 adrenoceptor function in humans. J Clin Endocrinol Metab 1995;80:1804-1808.
86. Bremner JD, Licinio J, Darnell A, et al. Elevated CSF corticotropin releasing factor concentrations in PTSD. Am J Psychiatr 1997;154:624-629.
87. Smith MA, Davidson J, Ritchie JC, et al. The corticotropin-releasing hormone test in patients with PTSD. Biol Psychiatr 1989; 26:349-355.
88. Yehuda R, Giller EL, Levengood RA, Southwick SM, Siever LJ. Hypothalamic-pituitary-adrenal functioning in PTSD. In: Friedman MJ, Charney DS, Deutch AY, editors. Neurobiological and clinical consequences of stress. Philadelphia: Lippincott-Raven; 1995. p. 351-365.
89. Jolkkonen J, Lepola V, Bissette G, Nemeroff C, Riekkinen P. CSF corticotropin-releasing factor is not affected in panic disorder. Biol Psychiatr 1993;33:136-138.
90. Roy-Byrne PP, Uhde TW, Post RM, Gallucci W, Chrousos GP, Gold PW. The corticotropin-releasing hormone stimulation test in patients with panic disorder. Am J Psychiatr 1986:143:896-899.
91. Holsboer F, vonBardeleben U, Buller R, Heuser I, Steiger A. Stimulation response to corticotropin-releasing hormone (CRH) in patients with depression, alcoholism and panic disorder. Horm Metab Res 1987;16(suppl):80-88.
92. Brambilla F, Bellodi L, Perna G, et al. Psychoimmunoendocrine aspects of panic disorder. Neuropsychobiology 1992:26:12-22.
93. Rapaport MH, Risch SC, Golshan S, Gillin JC. Neuroendocrine effects of ovine corticotropin-releasing hormone in panic disorder patients. Biol Psychiatr 1989;26:344-348.
94. Coryell W, Noyes R. HPA axis disturbance and treatment outcome in panic disorder. Biol Psychiatr 1988;24:762-766.
95. Kathol RG, Anton R, Noyes R, Lopez AL, Reich JH. Relationship of urinary free cortisol levels in patients with panic disorder to symptoms of depression and agoraphobia. Psychiatr Res 1988; 24:211-221.
96. Uhde T, Joffe RT, Jimerson DC, Post RM. Normal urinary free cortisol and plasma MHPG in panic disorder: clinical and theoretical implications. Biol Psychiatr 1988;23:575-585.
97. Goldstein S, Halbreich U, Asnis G, Endicott J, Alvir J. The hypothalamic-pituitary-adrenal system in panic disorder. Am J Psychiatr 1987;144:1320-1323.
98. Abelson JL, Curtis GC. Hypothalamic pituitary adrenal axis activity in panic disorder. Arch Gen Psychiatr 1996;53:323-331.
99. Ladd CO, Owens MJ, Nemeroff CB. Persistent changes in CRF neuronal systems produced by maternal separation. Endocrinology 1996;137:1212-1218.
100. Plotsky PM, Meaney MJ. Early postnatal experience alters hypothalamic corticotropin releasing factor in RNA, median eminence CRF content and stress-induced release in adult rats. Mol Brain Res 1993;18:195-200.
101. Rosenblum LA, Coplan JD, Friedman S, Bassof T, Gorman JM, Andrews MW. Adverse early experience affect noradrenergic and serotonergic functioning in adult primates. Biol Psychiatr 1994;35:221-227.
102. Coplan JD, Andreas MW, Rosenblum LA, et al. Persistent elevations of CSF CRF in adult nonhuman primates exposed to early life stressors: Implications for the pathophysiology of mood and anxiety disorders. Proc Nat Acad Sci U S A 1996;93:1619-1623.
103. Bremner JD, Southwick SM, Johnson DR, Yehuda R, Charney DS. Childhood physical abuse in combat-related posttraumatic stress disorder. Am J Psychiatr 1993;150:235-239.
104. Perry BD. Neurobiological sequelae of childhood trauma: PTSD in children. In: Murburg MM, editor. Catecholamine function in posttraumatic stress disorder: emerging concepts. Washington (DC): American Psychiatric Press; 1994. p. 233-256.
105. Lemieux AM, Coe CL. Abuse-related posttraumatic stress disorder: Evidence for chronic neuroendocrine activation in women. Psychosom Med 1995;57:105-115.
106. Debellis D, Lefter L, Trickett PK, Putnam FW. Urinary catecholamine excretion in sexually abused girls. J Amer Acad Child Adolescent Psychiatr 1995;33:320-327.
107. Vidu V, Sharma S, Plotsky P, Meaney MJ. The hypothalamic pituitary-adrenal system response to stress in handled and non-handled rats; differences in stress induced plasma ACTH secretion are not dependent upon corticosterone levels. J Neurosci 1993;13:1097-1105.
108. Caldji C, Sharma S, Plotsky PM, Meaney MJ. Postnatal handling/maternal separation alters responses to novelty stress, open field exploration and central benzodiazepine receptor levels in adult rats (abstract). Neurosci Abstr 1996;22:1341.
109. Uno H, Tarara E, Else JG, Suleman MA, Sapolsky RM. Hippocampal damage associated with prolonged and fatal stress in primates. J Neurosci 1989;9:1705-1711.
110. Sapolsky RM, Uno H, Rebert CS, Finch CE. Hippocampal damage associated with prolonged glucocorticoid exposure in primates. J Neurosci 1990;10:2897-2902.
111. Lawrence MS, Sapolsky RM. Glucorticoids accelerate ATP loss following metabolic insults in cultured hippocampal neurons. Brain Res 1994:646:303-306.
112. Virgin CE, Taryn PTH, Packan DR. Glucocorticoids inhibit glucose transport and glutamate uptake in hippocampal astrocytes: Implications for glucocorticoid neurotoxicity. J Neurochem 1991;57:1422-1428.
113. Magarinos AM, McEwen BS. Stress induced atrophy of apical dendrites of hippocampal CA3C neurons: Involvement of GC secretion and excitatory amino acid receptors. Neuroscience 1995;69:89-98.
114. Magarinos AM, McEwen BS. Stress induced atrophy of apical dendrites of hippocampal CA3C neurons comparison of stressors. Neuroscience 1995;69:83-88.
115. Stein-Behrens BA, Lin WJ, Sapolsky RM. Physiological elevations of glucocorticoids potentiate glutamate accumulation in the hippocampus. J Neurochem 1994;63:596-602.
116. Magarinos AM, Verdugo JM, McEwen BS. Chronic restraint stress causes ultrastructural changes in rat mossy fiber terminals (abstract). Neuroscience Abstr 1996;22:1196.
117. Stein B, Sapolsky RM. Chemical adrenalectomy reduces hippocampal damage induced by kainic acid. Brain Res 1988;473: 175-181.
118. Meaney M, Aitken D, Bhatnager S, van Berkel C, Sapolsky R. Effect of neonatal handling on age-related impairments associated with the hippocampus. Science 1988;239:766-769.
119. Arbel I, Kadar T, Silberman M, Levy A. The effects of long-term corticosterone administration on hippocampal morphology and cognitive performance of middle-aged rats. Brain Res 1994; 657:227-235.
120. Luine V, Villages M, Martinex C, McEwen BS. Repeated stress causes reversible impairments of spatial memory performance. Brain Res 1994;639:167-170.
121. Uno H, Lohmiller L, Thieme C, et al. Brain damage induced by prenatal exposure to dexamethasone in fetal rhesus macaques I hippocampus. Dev Brain Res 1990;53:157-167.
122. Bremner JD, Randall P, Scott TM, et al. MRI-based measurement of hippoampal volume in combat related posttraumatic stress disorder. Am J Psychiatr 1995;152:973-981.
123. Bremner JD, Randall P, Vermetten E, et al. Magnetic resonance imaging-based measurement of hippocampal volume in posttraumatic stress disorder related to childhood physical and sexual abuse-A preliminary report. Biol Psychiatr 1997;41:23-32.
124. Gurvits TV, Shenton ME, Hokama H, et al. Magnetic resonance imaging study of hippocampal volume in chronic, combat-related posttraumatic stress disorder. Biol Psychiatr 1996;40:1091-1099.
125. Sutker PB, Winstead DK, Galina ZH, Allain AN. Cognitive deficits and psychopathology among former prisoners of war and combat veterans of the Korean conflict. Am J Psychiatr 1991; 148:67-72.
126. Bremner JD, Scott TM, Delaney RC, Charney DS. Deficits in short-term memory in post-traumatic stress disorder. Am J Psychiatr 1993;150:1015-1019.
127. Uddo M, Vasterling JT, Brailey K, Sutker PB. Memory and attention in posttraumatic stress disorder. J Psychopath Behav Assess 1993;15:43-52.
128. Yehuda R, Keefer RSE, Harvey PD. Learning and memory in combat veterans with posttraumatic stress disorder. Am J Psychiatr 1995;152:137-139.
129. Bremner JD, Randall PR, Capelli S, Scott T, McCarthy G, Charney DS. Deficits in short-term memory in adult survivors of childhood abuse. Psychiatr Res 1995;59:97-107.