Animal models of post-traumatic stress disorder and recent neurobiological insights

Behavioural Pharmacology

Volumn 25, Issue 5-6, 2014, Pages 398-409

  Whitaker, Annie M ^a   Gilpin, Nicholas W ^a   Edwards, Scott ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

alcohol use disorder; animal model; individual differences; neurobiology; post traumatic stress disorder

Indexed keywords

ALCOHOL USE DISORDER; AMYGDALOID NUCLEUS; ANIMAL HOUSING; AROUSAL; ARTICLE; AVOIDANCE BEHAVIOR; COMORBIDITY; CONCEPTUAL FRAMEWORK; ENDOPHENOTYPE; FEAR; IMMOBILIZATION STRESS; MENTAL STRESS; NERVE CONDUCTION; NEUROBIOLOGY; NONHUMAN; ODOR; POSTTRAUMATIC STRESS DISORDER; PREDATOR; PREFRONTAL CORTEX; SOCIAL STRESS; ANIMAL; BRAIN; DISEASE MODEL; HUMAN; PATHOPHYSIOLOGY;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; HUMANS; STRESS DISORDERS, POST-TRAUMATIC;

EID: 84906056888     PISSN: 09558810     EISSN: 14735849     Source Type: Journal    
DOI: 10.1097/FBP.0000000000000069     Document Type: Article

References (151)

1. Aisa B, Tordera R, Lasheras B, Del Río J, Ramírez MJ (2007). Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 32:256-266.
2. Andrews B, Brewin CR, Rose S (2003). Gender, social support, and PTSD in victims of violent crime. J Trauma Stress 16:421-427.
3. Armario A, Vallàs A, Dal-Zotto S, Márquez C, Belda X (2004). A single exposure to severe stressors causes long-Term desensitisation of the physiological response to the homotypic stressor. Stress 7:157-172.
4. Arnsten AF (2009). Stress signalling pathways that impair prefrontal cortex structure and function. Nat Rev Neurosci 10:410-422.
5. Belda X, Rotllant D, Fuentes S, Delgado R, Nadal R, Armario A (2008). Exposure to severe stressors causes long-lasting dysregulation of resting and stressinduced activation of the hypothalamic-pituitary-Adrenal axis. Ann N Y Acad Sci 1148:165-173.
6. Besnard A, Bouveyron N, Kappes V, Pascoli V, Pagàs C, Heck N, et al. (2011). Alterations of molecular and behavioral responses to cocaine by selective inhibition of Elk-1 phosphorylation. J Neurosci 31:14296-14307.
7. Blanco C, Xu Y, Brady K, Pérez-Fuentes G, Okuda M, Wang S (2013). Comorbidity of posttraumatic stress disorder with alcohol dependence among US adults: Results from National Epidemiological Survey on Alcohol and Related Conditions. Drug Alcohol Depend 132:630-638.
8. Breslau N, Kessler RC, Chilcoat HD, Schultz LR, Davis GC, Andreski P (1998). Trauma and posttraumatic stress disorder in the community: The 1996 Detroit Area Survey of Trauma. Arch Gen Psychiatry 55:626-632.
9. Butler TR, Ariwodola OJ, Weiner JL (2014). The impact of social isolation on HPA axis function, anxiety-like behaviors, and ethanol drinking. Front Integr Neurosci 7:102.
10. Chester JA, Barrenha GD, Hughes ML, Keuneke KJ (2008). Age-And sexdependent effects of footshock stress on subsequent alcohol drinking and acoustic startle behavior in mice selectively bred for high-Alcohol preference. Alcohol Clin Exp Res 32:1782-1794.
11. Cloitre M, Stolbach BC, Herman JL, van der Kolk B, Pynoos R,Wang J, Petkova E (2009). A developmental approach to complex PTSD: Childhood and adult cumulative trauma as predictors of symptom complexity. J Trauma Stress 22:399-408.
12. Cohen H, Zohar J (2004). An animal model of posttraumatic stress disorder: The use of cut-off behavioral criteria. Ann N Y Acad Sci 1032:167-178.
13. Cohen H, Zohar J, Matar M (2003). The relevance of differential response to trauma in an animal model of posttraumatic stress disorder. Biol Psychiatry 53:463-473.
14. Cohen H, Matar MA, Richter-Levin G, Zohar J (2006). The contribution of an animal model toward uncovering biological risk factors for PTSD. Ann N Y Acad Sci 1071:335-350.
15. Cohen H, Zohar J, Gidron Y, Matar MA, Belkind D, Loewenthal U, et al. (2006). Blunted HPA axis response to stress influences susceptibility to posttraumatic stress response in rats. Biol Psychiatry 59:1208-1218.
16. Cohen H, Kozlovsky N, Savion N, Matar MA, Loewenthal U, Loewenthal N, et al. (2009). An association between stress-induced disruption of the hypothalamic-pituitary-Adrenal axis and disordered glucose metabolism in an animal model of post-Traumatic stress disorder. J Neuroendocrinol 21:898-909.
17. Cohen H, Kaplan Z, Koresh O, Matar MA, Geva AB, Zohar J (2011). Early poststressor intervention with propranolol is ineffective in preventing posttraumatic stress responses in an animal model for PTSD. Eur Neuropsychopharmacol 21:230-240.
18. Cook CJ (2002). Glucocorticoid feedback increases the sensitivity of the limbic system to stress. Physiol Behav 75:455-464.
19. Corley MJ, Caruso MJ, Takahashi LK (2012). Stress-induced enhancement of fear conditioning and sensitization facilitates extinction-resistant and habituationresistant fear behaviors in a novel animal model of posttraumatic stress disorder. Physiol Behav 105:408-416.
20. Crews FT, Zou J, Qin L (2011). Induction of innate immune genes in brain create the neurobiology of addiction. Brain Behav Immun 25 (Suppl 1):S4-S12.
21. Croft AP, Brooks SP, Cole J, Little HJ (2005). Social defeat increases alcohol preference of C57BL/10 strain mice; effect prevented by a CCKB antagonist. Psychopharmacology (Berl) 183:163-170.
22. Daniels WM, Pietersen CY, Carstens ME, Stein DJ (2004). Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metab Brain Dis 19:3-14.
23. Daoura L, Haaker J, Nylander I (2011). Early environmental factors differentially affect voluntary ethanol consumption in adolescent and adult male rats. Alcohol Clin Exp Res 35:506-515.
24. Daskalakis NP, Lehrner A, Yehuda R (2013). Endocrine aspects of posttraumatic stress disorder and implications for diagnosis and treatment. Endocrinol Metab Clin North Am 42:503-513.
25. Daskalakis NP, Yehuda R, Diamond DM (2013). Animal models in translational studies of PTSD. Psychoneuroendocrinology 38:1895-1911.
26. Davis S, Laroche S (2006). Mitogen-Activated protein kinase/extracellular regulated kinase signalling and memory stabilization: A review. Genes Brain Behav 5 (Suppl 2):61-72.
27. Daviu N, Fuentes S, Nadal R, Armario A (2010). A single footshock causes longlasting hypoactivity in unknown environments that is dependent on the development of contextual fear conditioning. Neurobiol Learn Mem 94:183-190.
28. De Jongh R, Geyer MA, Olivier B, Groenink L (2005). The effects of sex and neonatal maternal separation on fear-potentiated and light-enhanced startle. Behav Brain Res 161:190-196.
29. Dina OA, Khasar SG, Alessandri-Haber N, Green PG, Messing RO, Levine JD (2008). Alcohol-induced stress in painful alcoholic neuropathy. Eur J Neurosci 27:83-92.
30. DSM-5 (2013). American psychiatric association: Diagnostic and statistical manual of mental disorders. 5th ed. Arlington, VA: American Psychiatric Association.
31. Edwards S, Vendruscolo LF, Schlosburg JE, Misra KK, Wee S, Park PE, et al. (2012). Development of mechanical hypersensitivity in rats during heroin and ethanol dependence: Alleviation by CRF1 receptor antagonism CRF(1) receptor antagonism. Neuropharmacology 62:1142-1151.
32. Edwards S, Baynes BB, Carmichael CY, Zamora-Martinez ER, Barrus M, Koob GF, Gilpin NW (2013). Traumatic stress reactivity promotes excessive alcohol drinking and alters the balance of prefrontal cortex-Amygdala activity. Transl Psychiatry 3:e296.
33. Egli M, Koob GF, Edwards S (2012). Alcohol dependence as a chronic pain disorder. Neurosci Biobehav Rev 36:2179-2192.
34. Engdahl B, Dikel TN, Eberly R, Blank A Jr (1998). Comorbidity and course of psychiatric disorders in a community sample of former prisoners of war. Am J Psychiatry 155:1740-1745.
35. Fasano S, D'Antoni A, Orban PC, Valjent E, Putignano E, Vara H, et al. (2009). Ras-guanine nucleotide-releasing factor 1 (Ras-GRF1) controls activation of extracellular signal-regulated kinase (ERK) signaling in the striatum and longterm behavioral responses to cocaine. Biol Psychiatry 66:758-768.
36. Freund J, Brandmaier AM, Lewejohann L, Kirste I, Kritzler M, Krüger A, et al. (2013). Emergence of individuality in genetically identical mice. Science 340:756-759.
37. Fu Y, Neugebauer V (2008). Differential mechanisms of CRF1 and CRF2 receptor functions in the amygdala in pain-related synaptic facilitation and behavior. J Neurosci 28:3861-3876.
38. Fu Y, Han J, Ishola T, Scerbo M, Adwanikar H, Ramsey C, Neugebauer V (2008). PKA and ERK, but not PKC, in the amygdala contribute to pain-related synaptic plasticity and behavior. Mol Pain 4:26.
39. Gameiro GH, Gameiro PH, Andrade Ada S, Pereira LF, Arthuri MT, Marcondes FK, Veiga MC (2006). Nociception-And anxiety-like behavior in rats submitted to different periods of restraint stress. Physiol Behav 87:643-649.
40. García-Sáinz JA, Vázquez-Prado J, Villalobos-Molina R (1999). Alpha 1-Adrenoceptors: Subtypes, signaling, and roles in health and disease. Arch Med Res 30:449-458.
41. Gehlert DR, Cippitelli A, Thorsell A, Le AD, Hipskind PA, Hamdouchi C, et al. (2007). 3-(4-Chloro-2-morpholin-4-yl-Thiazol-5-yl)-8-(1-ethylpropyl)-2,6- dimethyl-imidazo [1,2-b]pyridazine: A novel brain-penetrant, orally available corticotropin-releasing factor receptor 1 antagonist with efficacy in animal models of alcoholism. J Neurosci 27:2718-2726.
42. George O, Koob GF (2010). Individual differences in prefrontal cortex function and the transition from drug use to drug dependence. Neurosci Biobehav Rev 35:232-247.
43. George O, Sanders C, Freiling J, Grigoryan E, Vu S, Allen CD, et al. (2012). Recruitment of medial prefrontal cortex neurons during alcohol withdrawal predicts cognitive impairment and excessive alcohol drinking. Proc Natl Acad Sci USA 109:18156-18161.
44. Gilboa A, Shalev AY, Laor L, Lester H, Louzoun Y, Chisin R, Bonne O (2004). Functional connectivity of the prefrontal cortex and the amygdala in posttraumatic stress disorder. Biol Psychiatry 55:263-272.
45. Gilpin NW, Koob GF (2008). Neurobiology of alcohol dependence: Focus on motivational mechanisms. Alcohol Res Health 31:185-195.
46. Gilpin NW, Koob GF (2010). Effects of β-Adrenoceptor antagonists on alcohol drinking by alcohol-dependent rats. Psychopharmacology (Berl) 212:431-439.
47. Gilpin NW, Roberto M (2012). Neuropeptide modulation of central amygdala neuroplasticity is a key mediator of alcohol dependence. Neurosci Biobehav Rev 36:873-888.
48. Gilpin NW, Richardson HN, Koob GF (2008). Effects of CRF1-receptor and opioid-receptor antagonists on dependence-induced increases in alcohol drinking by alcohol-preferring (P) rats. Alcohol Clin Exp Res 32:1535-1542.
49. Gomez JL, Lewis MJ, Luine VN (2012). The interaction of chronic restraint stress and voluntary alcohol intake: Effects on spatial memory in male rats. Alcohol 46:499-504.
50. Grissom NM, Bhatnagar S (2011). The basolateral amygdala regulates adaptation to stress via β-Adrenergic receptor-mediated reductions in phosphorylated extracellular signal-regulated kinase. Neuroscience 178:108-122.
51. Herman JP, McKlveen JM, Solomon MB, Carvalho-Netto E, Myers B (2012). Neural regulation of the stress response: Glucocorticoid feedback mechanisms. Braz J Med Biol Res 45:292-298.
52. Hermans EJ, Battaglia FP, Atsak P, de Voogd LD, Fernández G, Roozendaal B (2014). How the amygdala affects emotional memory by altering brain network properties. Neurobiol Learn Mem 112C:2-16.
53. Hill MN, Carrier EJ, McLaughlin RJ, Morrish AC, Meier SE, Hillard CJ, Gorzalka BB (2008). Regional alterations in the endocannabinoid system in an animal model of depression: Effects of concurrent antidepressant treatment. J Neurochem 106:2322-2336.
54. Hill MN, Bierer LM, Makotkine I, Golier JA, Galea S, McEwen BS, et al. (2013). Reductions in circulating endocannabinoid levels in individuals with posttraumatic stress disorder following exposure to the World Trade Center attacks. Psychoneuroendocrinology 38:2952-2961.
55. Holloway-Erickson CM, McReynolds JR, McIntyre CK (2012). Memory-enhancing intra-basolateral amygdala infusions of clenbuterol increase Arc and CaMKIIa protein expression in the rostral anterior cingulate cortex. Front Behav Neurosci 6:17.
56. Holmes A, Singewald N (2013). Individual differences in recovery from traumatic fear. Trends Neurosci 36:23-31.
57. Holmes A, Fitzgerald PJ, MacPherson KP, DeBrouse L, Colacicco G, Flynn SM, et al. (2012). Chronic alcohol remodels prefrontal neurons and disrupts NMDAR-mediated fear extinction encoding. Nat Neurosci 15:1359-1361.
58. Imanaka A, Morinobu S, Toki S, Yamawaki S (2006). Importance of early environment in the development of post-Traumatic stress disorder-like behaviors. Behav Brain Res 173:129-137.
59. Iwamoto Y, Morinobu S, Takahashi T, Yamawaki S (2007). Single prolonged stress increases contextual freezing and the expression of glycine transporter 1 and vesicle-Associated membrane protein 2 mRNA in the hippocampus of rats. Prog Neuropsychopharmacol Biol Psychiatry 31:642-651.
60. Jaworski JN, Francis DD, Brommer CL, Morgan ET, Kuhar MJ (2005). Effects of early maternal separation on ethanol intake, GABA receptors and metabolizing enzymes in adult rats. Psychopharmacology (Berl) 181:8-15.
61. Ji G, Neugebauer V (2012). Modulation of medial prefrontal cortical activity using in vivo recordings and optogenetics. Mol Brain 5:36.
62. Ji G, Fu Y, Ruppert KA, Neugebauer V (2007). Pain-related anxiety-like behavior requires CRF1 receptors in the amygdala. Mol Pain 3:13.
63. Johansen JP, Cain CK, Ostroff LE, LeDoux JE (2011). Molecular mechanisms of fear learning and memory. Cell 147:509-524.
64. Kalinichev M, Easterling KW, Plotsky PM, Holtzman SG (2002). Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long-Evans rats. Pharmacol Biochem Behav 73:131-140.
65. Keen-Rhinehart E, Michopoulos V, Toufexis DJ, Martin EI, Nair H, Ressler KJ, et al. (2009). Continuous expression of corticotropin-releasing factor in the central nucleus of the amygdala emulates the dysregulation of the stress and reproductive axes. Mol Psychiatry 14:37-50.
66. Kessler RC (2000). Posttraumatic stress disorder: The burden to the individual and to society. J Clin Psychiatry 61 (Suppl 5):4-12, Discussion 13-14.
67. Kessler RC, Sonnega A, Bromet E, Hughes M, Nelson CB (1995). Posttraumatic stress disorder in the National Comorbidity Survey. Arch Gen Psychiatry 52:1048-1060.
68. Khan S, Liberzon I (2004). Topiramate attenuates exaggerated acoustic startle in an animal model of PTSD. Psychopharmacology (Berl) 172:225-229.
69. Kim A, Zamora-Martinez ER, Edwards S, Mandyam CD (2014). Structural reorganization of pyramidal neurons in the medial prefrontal cortex of alcohol dependent rats is associated with altered glial plasticity. Brain Struct Funct [Epub ahead of print].
70. Knox D, George SA, Fitzpatrick CJ, Rabinak CA, Maren S, Liberzon I (2012). Single prolonged stress disrupts retention of extinguished fear in rats. Learn Mem 19:43-49.
71. Koenigs M, Grafman J (2009). Posttraumatic stress disorder: The role of medial prefrontal cortex and amygdala. Neuroscientist 15:540-548.
72. Kolber BJ, Roberts MS, Howell MP, Wozniak DF, Sands MS, Muglia LJ (2008). Central amygdala glucocorticoid receptor action promotes fear-Associated CRH activation and conditioning. Proc Natl Acad Sci USA 105:12004-12009.
73. Koob GF, Le Moal M (2008). Addiction and the brain antireward system. Annu Rev Psychol 59:29-53.
74. Koolhaas JM, Bartolomucci A, Buwalda B, de Boer SF, Flügge G, Korte SM, et al. (2011). Stress revisited: A critical evaluation of the stress concept. Neurosci Biobehav Rev 35:1291-1301.
75. Kozlovsky N, Matar MA, Kaplan Z, Zohar J, Cohen H (2009). A distinct pattern of intracellular glucocorticoid-related responses is associated with extreme behavioral response to stress in an animal model of post-Traumatic stress disorder. Eur Neuropsychopharmacol 19:759-771.
76. Krishnan V, Nestler EJ (2011). Animal models of depression: Molecular perspectives. Curr Top Behav Neurosci 7:121-147.
77. Krishnan V, Han MH, Graham DL, Berton O, Renthal W, Russo SJ, et al. (2007). Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131:391-404.
78. Krystal JH, Neumeister A (2009). Noradrenergic and serotonergic mechanisms in the neurobiology of posttraumatic stress disorder and resilience. Brain Res 1293:13-23.
79. Kvetnansky R, Mikulaj L (1970). Adrenal and urinary catecholamines in rats during adaptation to repeated immobilization stress. Endocrinology 87:738-743.
80. Liberzon I, Krstov M, Young EA (1997). Stress-restress: Effects on ACTH and fast feedback. Psychoneuroendocrinology 22:443-453.
81. Liberzon I, López JF, Flagel SB, Vázquez DM, Young EA (1999). Differential regulation of hippocampal glucocorticoid receptors mRNA and fast feedback: Relevance to post-Traumatic stress disorder. J Neuroendocrinol 11:11-17.
82. Logrip ML, Zorrilla EP (2012). Stress history increases alcohol intake in relapse: Relation to phosphodiesterase 10A. Addict Biol 17:920-933.
83. Logrip ML, Zorrilla EP, Koob GF (2012). Stress modulation of drug self-Administration: Implications for addiction comorbidity with post-Traumatic stress disorder. Neuropharmacology 62:552-564.
84. Lopez MF, Doremus-Fitzwater TL, Becker HC (2011). Chronic social isolation and chronic variable stress during early development induce later elevated ethanol intake in adult C57BL/6J mice. Alcohol 45:355-364.
85. Louvart H, Maccari S, Ducrocq F, Thomas P, Darnaudéry M (2005). Long-Term behavioural alterations in female rats after a single intense footshock followed by situational reminders. Psychoneuroendocrinology 30:316-324.
86. Louvart H, Maccari S, Lesage J, Léonhardt M, Dickes-Coopman A, Darnaudéry M (2006). Effects of a single footshock followed by situational reminders on HPA axis and behaviour in the aversive context in male and female rats. Psychoneuroendocrinology 31:92-99.
87. Mackenzie L, Nalivaiko E, Beig MI, Day TA, Walker FR (2010). Ability of predator odour exposure to elicit conditioned versus sensitised post traumatic stress disorder-like behaviours, and forebrain deltaFosB expression, in rats. Neuroscience 169:733-742.
88. Mahan AL, Ressler KJ (2012). Fear conditioning, synaptic plasticity and the amygdala: Implications for posttraumatic stress disorder. Trends Neurosci 35:24-35.
89. Maren S, Phan KL, Liberzon I (2013). The contextual brain: Implications for fear conditioning, extinction and psychopathology. Nat Rev Neurosci 14:417-428.
90. McClung CA, Ulery PG, Perrotti LI, Zachariou V, Berton O, Nestler EJ (2004). DeltaFosB: A molecular switch for long-Term adaptation in the brain. Brain Res Mol Brain Res 132:146-154.
91. McEwen BS (2007). Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiol Rev 87:873-904.
92. Meng QY, Chen XN, Tong DL, Zhou JN (2011). Stress and glucocorticoids regulated corticotropin releasing factor in rat prefrontal cortex. Mol Cell Endocrinol 342:54-63.
93. Meyer EM, Long V, Fanselow MS, Spigelman I (2013). Stress increases voluntary alcohol intake, but does not alter established drinking habits in a rat model of posttraumatic stress disorder. Alcohol Clin Exp Res 37:566-574.
94. Moeller-Bertram T, Keltner J, Strigo IA (2012). Pain and post traumatic stress disorder-review of clinical and experimental evidence. Neuropharmacology 62:586-597.
95. Moore NL, Gauchan S, Genovese RF (2012). Differential severity of anxiogenic effects resulting from a brief swim or underwater trauma in adolescent male rats. Pharmacol Biochem Behav 102:264-268.
96. Myers-Schulz B, Koenigs M (2012). Functional anatomy of ventromedial prefrontal cortex: Implications for mood and anxiety disorders. Mol Psychiatry 17:132-141.
97. Neumann ID, Wegener G, Homberg JR, Cohen H, Slattery DA, Zohar J, et al. (2011). Animal models of depression and anxiety: What do they tell us about human condition? Prog Neuropsychopharmacol Biol Psychiatry 35:1357-1375.
98. Olson VG, Rockett HR, Reh RK, Redila VA, Tran PM, Venkov HA, et al. (2011). The role of norepinephrine in differential response to stress in an animal model of posttraumatic stress disorder. Biol Psychiatry 70:441-448.
99. Oreland S, Raudkivi K, Oreland L, Harro J, Arborelius L, Nylander I (2011). Ethanol-induced effects on the dopamine and serotonin systems in adult Wistar rats are dependent on early-life experiences. Brain Res 1405:57-68.
100. Pape HC, Pare D (2010). Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol Rev 90:419-463.
101. Park CR, Campbell AM, Diamond DM (2001). Chronic psychosocial stress impairs learning and memory and increases sensitivity to yohimbine in adult rats. Biol Psychiatry 50:994-1004.
102. Perrin M, Vandeleur CL, Castelao E, Rothen S, Glaus J, Vollenweider P, Preisig M (2014). Determinants of the development of post-Traumatic stress disorder, in the general population. Soc Psychiatry Psychiatr Epidemiol 49:447-457.
103. Pibiri F, Nelson M, Guidotti A, Costa E, Pinna G (2008). Decreased corticolimbic allopregnanolone expression during social isolation enhances contextual fear: A model relevant for posttraumatic stress disorder. Proc Natl Acad Sci USA 105:5567-5572.
104. Pigott TA (1999). Gender differences in the epidemiology and treatment of anxiety disorders. J Clin Psychiatry 60 (Suppl 18):4-15.
105. Pigott TA (2003). Anxiety disorders in women. Psychiatr Clin North Am 26:621-672, vi-vii.
106. Pihoker C, Owens MJ, Kuhn CM, Schanberg SM, Nemeroff CB (1993). Maternal separation in neonatal rats elicits activation of the hypothalamic-pituitary- Adrenocortical axis: A putative role for corticotropinreleasing factor. Psychoneuroendocrinology 18:485-493.
107. Pijlman FT, Herremans AH, van de Kieft J, Kruse CG, van Ree JM (2003). Behavioural changes after different stress paradigms: Prepulse inhibition increased after physical, but not emotional stress. Eur Neuropsychopharmacol 13:369-380.
108. Pijlman FT, Wolterink G, Van Ree JM (2003). Physical and emotional stress have differential effects on preference for saccharine and open field behaviour in rats. Behav Brain Res 139:131-138.
109. Pynoos RS, Ritzmann RF, Steinberg AM, Goenjian A, Prisecaru I (1996). A behavioral animal model of posttraumatic stress disorder featuring repeated exposure to situational reminders. Biol Psychiatry 39:129-134.
110. Radley JJ, Arias CM, Sawchenko PE (2006). Regional differentiation of the medial prefrontal cortex in regulating adaptive responses to acute emotional stress. J Neurosci 26:12967-12976.
111. Raskind MA, Peskind ER, Kanter ED, Petrie EC, Radant A, Thompson CE, et al. (2003). Reduction of nightmares and other PTSD symptoms in combat veterans by prazosin: A placebo-controlled study. Am J Psychiatry 160:371-373.
112. Rau V, Fanselow MS (2009). Exposure to a stressor produces a long lasting enhancement of fear learning in rats. Stress 12:125-133.
113. Rau V, DeCola JP, Fanselow MS (2005). Stress-induced enhancement of fear learning: An animal model of posttraumatic stress disorder. Neurosci Biobehav Rev 29:1207-1223.
114. Rauch SL, van der Kolk BA, Fisler RE, Alpert NM, Orr SP, Savage CR, et al. (1996). A symptom provocation study of posttraumatic stress disorder using positron emission tomography and script-driven imagery. Arch Gen Psychiatry 53:380-387.
115. Rauch SL, Whalen PJ, Shin LM, McInerney SC, Macklin ML, Lasko NB, et al. (2000). Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: A functional MRI study. Biol Psychiatry 47:769-776.
116. Reul JM (2014). Making memories of stressful events: A journey along epigenetic, gene transcription, and signaling pathways. Front Psychiatry 5:5.
117. Richardson HN, Zhao Y, Fekete EM, Funk CK, Wirsching P, Janda KD, et al. (2008). MPZP: A novel small molecule corticotropin-releasing factor type 1 receptor (CRF1) antagonist. Pharmacol Biochem Behav 88:497-510.
118. Richter-Levin G (1998). Acute and long-Term behavioral correlates of underwater trauma-potential relevance to stress and post-stress syndromes. Psychiatry Res 79:73-83.
119. Ritov G, Richter-Levin G (2014). Water associated zero maze: A novel rat test for long term traumatic re-experiencing. Front Behav Neurosci 8:1.
120. Ritov G, Ardi Z, Richter-Levin G (2014). Differential activation of amygdala, dorsal and ventral hippocampus following an exposure to a reminder of underwater trauma. Front Behav Neurosci 8:18.
121. Rodrigues SM, LeDoux JE, Sapolsky RM (2009). The influence of stress hormones on fear circuitry. Annu Rev Neurosci 32:289-313.
122. Rudy JW, Huff NC, Matus-Amat P (2004). Understanding contextual fear conditioning: Insights from a two-process model. Neurosci Biobehav Rev 28:675-685.
123. Russo SJ, Murrough JW, Han MH, Charney DS, Nestler EJ (2012). Neurobiology of resilience. Nat Neurosci 15:1475-1484.
124. Saavedra-Rodríguez L, Feig LA (2013). Chronic social instability induces anxiety and defective social interactions across generations. Biol Psychiatry 73:44-53.
125. Servatius RJ, Ottenweller JE, Natelson BH (1995). Delayed startle sensitization distinguishes rats exposed to one or three stress sessions: Further evidence toward an animal model of PTSD. Biol Psychiatry 38:539-546.
126. Shepard JD, Barron KW, Myers DA (2000). Corticosterone delivery to the amygdala increases corticotropin-releasing factor mRNA in the central amygdaloid nucleus and anxiety-like behavior. Brain Res 861:288-295.
127. Silberman Y, Ariwodola OJ, Weiner JL (2012). β1-Adrenoceptor activation is required for ethanol enhancement of lateral paracapsular GABAergic synapses in the rat basolateral amygdala. J Pharmacol Exp Ther 343:451-459.
128. Sparta DR, Jennings JH, Ung RL, Stuber GD (2013). Optogenetic strategies to investigate neural circuitry engaged by stress. Behav Brain Res 255:19-25.
129. Ströhle A, Scheel M, Modell S, Holsboer F (2008). Blunted ACTH response to dexamethasone suppression-CRH stimulation in posttraumatic stress disorder. J Psychiatr Res 42:1185-1188.
130. Sweatt JD (2001). The neuronal MAP kinase cascade: A biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 76:1-10.
131. Takahashi LK, Nakashima BR, Hong H, Watanabe K (2005). The smell of danger: A behavioral and neural analysis of predator odor-induced fear. Neurosci Biobehav Rev 29:1157-1167.
132. Tipps ME, Raybuck JD, Lattal KM (2014). Substance abuse, memory, and posttraumatic stress disorder. Neurobiol Learn Mem 112C:87-100.
133. Tulogdi A, Sörös P, Tóth M, Nagy R, Biró L, Aliczki M, et al. (2012). Temporal changes in c-Fos activation patterns induced by conditioned fear. Brain Res Bull 88:359-370.
134. Vallàs A, Martí O, Armario A (2006). Long-Term effects of a single exposure to immobilization: A c-fos mRNA study of the response to the homotypic stressor in the rat brain. J Neurobiol 66:591-602.
135. Van Dijken HH, Van der Heyden JA, Mos J, Tilders FJ (1992). Inescapable footshocks induce progressive and long-lasting behavioural changes in male rats. Physiol Behav 51:787-794.
136. Vanhoose AM, Emery M, Jimenez L, Winder DG (2002). ERK activation by G-protein-coupled receptors in mouse brain is receptor identity-specific. J Biol Chem 277:9049-9053.
137. Vendruscolo LF, Barbier E, Schlosburg JE, Misra KK, Whitfield TW Jr, Logrip ML, et al. (2012). Corticosteroid-dependent plasticity mediates compulsive alcohol drinking in rats. J Neurosci 32:7563-7571.
138. Vertes RP (2004). Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32-58.
139. Von Frijtag JC, Reijmers LG, Van der Harst JE, Leus IE, Van den Bos R, Spruijt BM (2000). Defeat followed by individual housing results in long-Term impaired reward-And cognition-related behaviours in rats. Behav Brain Res 117:137-146.
140. Walker BM, Rasmussen DD, Raskind MA, Koob GF (2008). alpha1-noradrenergic receptor antagonism blocks dependence-induced increases in responding for ethanol. Alcohol 42:91-97.
141. Wang W, Liu Y, Zheng H, Wang HN, Jin X, Chen YC, et al. (2008). A modified single-prolonged stress model for post-Traumatic stress disorder. Neurosci Lett 441:237-241.
142. Warren BL, Vialou VF, Iñiguez SD, Alcantara LF, Wright KN, Feng J, et al. (2013). Neurobiological sequelae of witnessing stressful events in adult mice. Biol Psychiatry 73:7-14.
143. Yamamoto S, Morinobu S, Takei S, Fuchikami M, Matsuki A, Yamawaki S, Liberzon I (2009). Single prolonged stress: Toward an animal model of posttraumatic stress disorder. Depress Anxiety 26:1110-1117.
144. Yang R, Daigle BJ Jr, Muhie SY, Hammamieh R, Jett M, Petzold L, Doyle FJ 3rd (2013). Core modular blood and brain biomarkers in social defeat mouse model for post traumatic stress disorder. BMC Syst Biol 7:80.
145. Yang X, Wang S, Rice KC, Munro CA, Wand GS (2008). Restraint stress and ethanol consumption in two mouse strains. Alcohol Clin Exp Res 32:840-852.
146. Yehuda R (2005). Neuroendocrine aspects of PTSD. Handb Exp Pharmacol 169:371-403.
147. Yehuda R, Antelman SM (1993). Criteria for rationally evaluating animal models of posttraumatic stress disorder. Biol Psychiatry 33:479-486.
148. Yehuda R, LeDoux J (2007). Response variation following trauma: A translational neuroscience approach to understanding PTSD. Neuron 56:19-32.
149. Zoladz PR, Diamond DM (2013). Current status on behavioral and biological markers of PTSD: A search for clarity in a conflicting literature. Neurosci Biobehav Rev 37:860-895.
150. Zoladz PR, Conrad CD, Fleshner M, Diamond DM (2008). Acute episodes of predator exposure in conjunction with chronic social instability as an animal model of post-Traumatic stress disorder. Stress 11:259-281.
151. Zoladz PR, Fleshner M, Diamond DM (2012). Psychosocial animal model of PTSD produces a long-lasting traumatic memory, an increase in general anxiety and PTSD-like glucocorticoid abnormalities. Psychoneuroendocrinology 37:1531-1545.