Maintaining the clinical relevance of animal models in translational studies of post-traumatic stress disorder

ILAR Journal

Volumn 55, Issue 2, 2014, Pages 233-245

  Cohen, Hagit ^a   Matar, Michael A ^a   Zohar, Joseph ^b  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

Animal model; Anxiety; Behavioral criteria; Post traumatic stress disorder; Translation research

Indexed keywords

ANIMALIA;

BIOLOGICAL MARKER;

ANIMAL; ANIMAL BEHAVIOR; BEHAVIOR; CLASSIFICATION; DISEASE MODEL; HUMAN; INDIVIDUALITY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; STRESS DISORDERS, POST-TRAUMATIC; THEORETICAL MODEL;

ANIMALS; BEHAVIOR, ANIMAL; BEHAVIORAL SYMPTOMS; BIOLOGICAL MARKERS; CLASSIFICATION; DISEASE MODELS, ANIMAL; HUMANS; INDIVIDUALITY; MODELS, THEORETICAL; STRESS DISORDERS, POST-TRAUMATIC;

EID: 84911465835     PISSN: 10842020     EISSN: 19306180     Source Type: Journal    
DOI: 10.1093/ilar/ilu006     Document Type: Article

References (109)

1. Ablin JN, Cohen H, Neumann L, Kaplan Z, Buskila D. 2008. Coping styles in fibromyalgia: effect of co-morbid posttraumatic stress disorder. Rheumatol Int 28:649-56.
2. Adamec R. 1997. Transmitter systems involved in neural plasticity underlying increased anxiety and defense-implications for understanding anxiety following traumatic stress. Neurosci Biobehav Rev 21:755-65.
3. Adamec R, Head D, Blundell J, Burton P, Berton O. 2006a. Lasting anxiogenic effects of feline predator stress in mice: sex differences in vulnerability to stress and predicting severity of anxiogenic response from the stress experience. Physiol Behav 88:12-29. Epub 2006 Apr 19.
4. Adamec R, Holmes A, Blundell J. 2008. Vulnerability to lasting anxiogenic effects of brief exposure to predator stimuli: Sex, serotonin and other factors-Relevance to PTSD. Neurosci Biobehav Rev 32:1287-1292.
5. Adamec R, Muir C, Grimes M, Pearcey K. 2007. Involvement of noradrenergic and corticoid receptors in the consolidation of the lasting anxiogenic effects of predator stress. Behav Brain Res 179:192-207. Epub 2007 Feb 6.
6. Adamec R, Strasser K, Blundell J, Burton P, McKay DW. 2006b. Protein synthesis and the mechanisms of lasting change in anxiety induced by severe stress. Behav Brain Res 167:270-86.
7. Adamec RE, Blundell J, Burton P. 2006c. Relationship of the predatory attack experience to neural plasticity, pCREB expression and neuroendocrine response. Neurosci Biobehav Rev 30:356-75. Epub 2005 Aug 22.
8. Adamec RE, Shallow T. 1993. Lasting effects on rodent anxiety of a single exp+sure to a cat. Physiol Behav 54:101-9.
9. Akirav I, Maroun M. 2007. The role of the medial prefrontal cortex-amygdala circuit in stress effects on the extinction of fear. Neural Plast:30873.
10. American Psychiatric Association. 1994. Diagnostic and Statistical Manual of Mental Disorders.Washington, DC: American Psychiatric Association.
11. American Psychiatric Association. 2013. Diagnostic and statistical manual of mental disorders. 5th ed. Washington, DC.
12. Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS. 2005. The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev 29:1123-44. Epub 2005 Aug 8.
13. Belzung C, Le Pape G. 1994. Comparison of different behavioral test situations used in psychopharmacology for measurement of anxiety. Physiol Behav 56:623-628.
14. Belzung C, Lemoine M. 2011. Criteria of validity for animal models of psychiatric disorders: focus on anxiety disorders and depression. Biol Mood Anxiety Disord 1:9.
15. Blanchard DC, Griebel G, Blanchard RJ. 2003. Conditioning and residual emotionality effects of predator stimuli: some reflections on stress and emotion. Prog Neuropsychopharmacol Biol Psychiatry 27(8):1177-1185.
16. Blanchard RJ, Blanchard DC, Rodgers J,Weiss SM. 1990. The characterization and modelling of antipredator defensive behavior. Neurosci Biobehav Rev 14:463-72.
17. Blanchard RJ, Griebel G, Henrie JA, Blanchard DC. 1997. Differentiation of anxiolytic and panicolytic drugs by effects on rat and mouse defense test batteries. Neurosci Biobehav Rev 21:783-9.
18. Blanchard RJ, Nikulina JN, Sakai RR, McKittrick C, McEwen B, Blanchard DC. 1998. Behavioral and endocrine change following chronic predatory stress. Physiol Behav 63:561-9.
19. Blechert J, Michael T, Vriends N, Margraf J, Wilhelm FH. 2007. Fear conditioning in posttraumatic stress disorder: evidence for delayed extinction of autonomic, experiential, and behavioural responses. Behav Res Ther 45(9):2019-33.
20. Blundell J, Adamec R, Burton P. 2005. Role of NMDA receptors in the syndrome of behavioral changes produced by predator stress. Physiol Behav. 86(1-2):233-43.
21. Born J, Rasch B, Gais S. 2006. Sleep to remember. Neuroscientist 12:410-424.
22. Borsboom D. 2008. Psychometric perspectives on diagnostic systems. J Clin Psych 64:1089-1108.
23. Bouton ME. 2004. Context and behavioral processes in extinction. Learn Mem 11:485-94.
24. Breslau N, Davis GC, Andreski P, Peterson E. 1991. Traumatic events and posttraumatic stress disorder in an urban population of young adults. Arch Gen Psychiatry 48:216-22.
25. Breslau N, Davis GC, Andreski P, Peterson EL, Schultz LR. 1997. Sex differences in posttraumatic stress disorder. Arch Gen Psychiatry 54:1044-8.
26. 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 55:626-32.
27. Bryant RA. 2006. Recovery after the tsunami: timeline for rehabilitation. J Clin Psychiatry 67:50-5.
28. Cahill L, Alkire MT. 2003. Epinephrine enhancement of human memory consolidation: Interaction with arousal at encoding. Neurobiol Learn Mem 79:194-198.
29. Cahill L, Babinsky R, Markowitsch HJ, McGaugh JL. 1995. The amygdala and emotional memory. Nature 377:295-296.
30. Cahill L, Prins B, Weber M, McGaugh JL. 1994. Beta-adrenergic activation and memory for emotional events. Nature 371:702-704.
31. Clinchy M, Schulkin J, Zanette LY, Sheriff MJ, McGowan PO, Boonstra R. 2011. The Neurological ecology of fear: Insights Neuroscientists and ecologists have to offer one another. Front Behav Neurosci 4:21.
32. Cohen H, Benjamin J, Kaplan Z, Kotler M. 2000. Administration of highdose ketoconazole, an inhibitor of steroid synthesis, prevents posttraumatic anxiety in an animal model. Eur Neuropsychopharmacol 10:429-435.
33. Cohen H, Friedberg S, Michael M, Kotler M, Zeev K. 1996. Interaction of CCK-4 induced anxiety and post-cat exposure anxiety in rats. Depress Anxiety 4:144-5.
34. Cohen H, Joseph Z, Matar M. 2003. The relevance of differential response to trauma in an animal model of post-traumatic stress disorder. Biol Psychiatry 53:463-473.
35. Cohen H, Kaplan Z, Koresh O, Matar MA, Geva AB, Zohar J. 2011. Early post-stressor intervention with propranolol is ineffective in preventing posttraumatic stress responses in an animal model for PTSD. Eur Neuropsychopharmacol 21:230-40.
36. Cohen H, Kaplan Z, Kotler M. 1999. CCK-antagonists in a rat exposed to acute stress: implication for anxiety associated with post-traumatic stress disorder. Depress Anxiety 10:8-17.
37. Cohen H, Kaplan Z, Matar M, Loewenthal U, Kozlovsky N, Zohar J. 2006. Anisomycin, a protein synthesis inhibitor, disrupts traumatic memory consolidation and attenuates post traumatic stress response in rats. Biol Psychiatry 60:767-776.
38. Cohen H, Kaplan Z, Matar MA, Loewenthal U, Zohar J, Richter-Levin G. 2007a. Long-lasting behavioral effects of juvenile trauma in an animal model of PTSD associated with a failure of the autonomic nervous system to recover. Eur Neuropsychopharmacol 17:464-677.
39. Cohen H, Kozlovsky N, Savion N, Matar MA, Loewenthal U, Loewenthal N, Zohar J, Kaplan Z. 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.
40. Cohen H, Maayan R, Touati-Werner D, Kaplan Z, Matar M, Loewenthal U, Kozlovsky N, Weizman R. 2007b. Decreased circulatory levels of neuroactive steroids in behaviorally more extremely affected rats subsequent to exposure to a potentially traumatic experience. Int J Neuropsychopharmacol 10:203-209.
41. Cohen H, Matar M, Buskila D, Kaplan Z, J Z. 2008. Early post-stressor intervention with high dose corticosterone attenuates post traumatic stress response in an animal model of PTSD. Biol Psych 15:708-717.
42. Cohen H, Matar MA, Joseph Z. 2013. Animal models of post-traumatic stress disorder. Curr Protoc Neurosci Chapter 9:Unit 9 45.
43. Cohen H, Matar MA, Richter-Levin G, Zohar J. 2006b. The contribution of an animal model toward uncovering biological risk factors for PTSD. Ann N YAcad Sci. 1071:335-350.
44. Cohen H, Ziv Y, Cardon M, Kaplan Z, Matar MA, Gidron Y, Schwartz M, Kipnis J. 2006c. Maladaptation to mental stress mitigated by the adaptive immune system via depletion of naturally occurring regulatory CD4 +CD25+ cells. J Neurobiol 66:552-563.
45. Cohen H, Zohar J. 2004. Animal models of post traumatic stress disorder: The use of cut off behavioral criteria. The Annals New-York Academy of Sciences 1032:167-178.
46. Cohen H, Zohar J, Matar MA, Kaplan Z, Geva AB. 2005. Unsupervised fuzzy clustering analysis supports behavioral cutoff criteria in an animal model of posttraumatic stress disorder. Biol Psychiatry 58:640-650.
47. Cohen H, Zohar J, Matar MA, Zeev K, Loewenthal U, Richter-Levin G. 2004. Setting apart the affected: the use of behavioral criteria in animal models of post traumatic stress disorder. Neuropsychopharmacology 29:1962-1970.
48. Cohen S, Kozlovsky N, Matar MA, Kaplan Z, Zohar J, Cohen H. 2012. Postexposure sleep deprivation facilitates correctly timed interactions between glucocorticoid and adrenergic systems, which attenuate traumatic stress responses. Neuropsychopharmacology 37:2388-404.
49. Davidson JR. 2006. Pharmacologic treatment of acute and chronic stress following trauma: 2006. J Clin Psychiatry 67:34-9.
50. De Bellis MD, Keshavan MS, Shifflett H, Iyengar S, Beers SR, Hall J, Moritz G. 2002. Brain structures in pediatric maltreatment-related posttraumatic stress disorder: a sociodemographically matched study. Biol Psychiatry 52:1066-78.
51. Diamond DM, Campbell AM, Park CR, Woodson JC, Conrad CD, Bachstetter AD, Mervis RF. 2006. Influence of predator stress on the consolidation versus retrieval of long-term spatial memory and hippocampal spinogenesis. Hippocampus 16:571-6.
52. Ehlers A, Clark DM. 2000. A cognitive model of posttraumatic stress disorder. Behav Res Ther. 38(4):319-45.
53. Endres T, Apfelbach R, Fendt M. 2005. Behavioral changes induced in rats by exposure to trimethylthiazoline, a component of fox odor. Behav Neurosci 119:1004-10.
54. Etkin A, Wager TD. 2007. Functional Neuroimaging of anxiety: A metaanalysis of emotional processing in PTSD, Social anxiety disorder, and specific phobia. Am J Psychiatry 164:1476-88.
55. Fairbank JA, Schlenger WE, Saigh PA, Davidson JRT. 1995. An Epidemiologic profile of post-traumatic stress disorder: Prevalence, comorbidity, and risk factors. In: M.J F, D.S C, A.Y D, editors. Neurobiological and clinical Consequences of Stress: From Normal Adaptation to PTSD. Philadelphia: Lippincott-Raven. p. 415-427.
56. File SE, Zangrossi H Jr, Sanders FL, Mabbutt PS. 1993. Dissociation between behavioral and corticosterone responses on repeated exposures to cat odor. Physiol Behav 54:1109-1111.
57. Foa EB, Kozak MJ. 1986. Emotional processing of fear: Exposure to corrective information. Psychol Bull 99:20-35.
58. Foa EB, Stein DJ, McFarlane AC. 2006. Symptomatology and psychopathology of mental health problems after disaster. J Clin Psychiatry 67:15-25.
59. Gais S, Born J. 2004. Declarative memory consolidation: Mechanisms acting during human sleep. Learn Mem 11:679-685.
60. Griebel G, Blanchard DC, Jung A, Lee JC, Masuda CK, Blanchard RJ. 1995. Further evidence that the mouse defense test battery is useful for screening anxiolytic and panicolytic drugs: effects of acute and chronic treatment with alprazolam. Neuropharmacology 34:1625-33.
61. Hagewoud R, Whitcomb SN, Heeringa AN, Havekes R, Koolhaas JM, Meerlo P. 2010. A time for learning and a time for sleep: the effect of sleep deprivation on contextual fear conditioning at different times of the day. Sleep 33:1315-22.
62. Helzer J, Robins L, McEvoy L. 1987. Post-traumatic stress disorder in the general population. Findings of the epidemiologic catchment area survey. N Engl J Med 317:1630-1634.
63. Hurlemann R, Hawellek B, Matusch A, Kolsch H, Wollersen H, Madea B, et al. 2005. Noradrenergic modulation of emotion-induced forgetting and remembering. Journal of Neuroscience 25:6343-6349.
64. Kessler RC, Sonnega A, Bromet E, Hughes M, Nelson CB. 1995. Posttraumatic stress disorder in the national comorbidity survey. Arch Gen Psychiatry 52:1048-60.
65. Knox D, George SA, Fitzpatrick CJ, Rabinak CA, Maren S, Liberzon I. 2012a. Single prolonged stress disrupts retention of extinguished fear in rats. Learn Mem 19:43-9.
66. Knox D, Nault T, Henderson C, Liberzon I. 2012b. Glucocorticoid receptors and extinction retention deficits in the single prolonged stress model. Neuroscience 223:163-73.
67. Kozlovsky N, Matar MA, Kaplan Z, Kotler M, Zohar J, Cohen H. 2007. The immediate early gene Arc is associated with behavioral resilience to stress exposure in an animal model of posttraumatic stress disorder. Eur Neuropsychopharmacol 18:107-116.
68. Kozlovsky N, Matar MA, Kaplan Z, Kotler M, Zohar J, Cohen H. 2007. Long-term down-regulation of BDNF mRNA in rat hippocampal CA1 subregion correlates with PTSD-like behavioural stress response. Int J Neuropsychopharmacol :1-18.
69. 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 posttraumatic stress disorder. European Neuropsychopharmacology 19:759-771.
70. Le Merrer J, Becker JA, Befort K, Kieffer BL. 2009. Reward processing by the opioid system in the brain. Physiol Rev 89:1379-412.
71. LeDoux J. 1996. Emotional networks and motor control: a fearful view. Prog Brain Res 107:437-46.
72. LeDoux JE. 2000. Emotion circuits in the brain. Annu Rev Neurosci 23:155-84.
73. Lewitus GM, Cohen H, Schwartz M. 2008. Reducing post-traumatic anxiety by immunization. Brain Behav Immun 22:1108-14.
74. Liberzon I, KrstovM, Young EA. 1997. Stress-restress: effects on ACTH and fast feedback. Psychoneuroendocrinology 22:443-53.
75. Liberzon I, Sripada CS. 2008. The functional neuroanatomy of PTSD: a critical review. Prog Brain Res 167:151-69.
76. Maquet P. 2000. Sleep on it!. Nat Neurosci 3:1235-6.
77. Maquet P. 2001. The role of sleep in learning and memory. Science 294:1048-1052.
78. Maquet P. 2001. The role of sleep in learning and memory. Science 294:1048-52.
79. Maren S. 2001. Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24:897-931.
80. Maren S, Chang CH. 2006. Recent fear is resistant to extinction. Proc Natl Acad Sci U S A. 103:18020-5. Epub 2006 Nov 7.
81. Matar MA, Cohen H, Kaplan Z, Zohar J. 2006. The effect of early poststressor intervention with sertraline on behavioral responses in an animal model of post-traumatic stress disorder. Neuropsychopharmacology 31:2610-8.
82. Matar MA, Zohar J, Kaplan Z, Cohen H. 2009. Alprazolam treatment immediately after stress exposure interferes with the normal HPA-stress response and increases vulnerability to subsequent stress in an animal model of PTSD. Eur Neuropsychopharmacol 19:283-95.
83. Mazor A, Matar M, Kozlovsky N, Zohar J, Kaplan Z, Cohen H. 2009. Gender-related qualitative differences in baseline and post stress anxiety responses are not reflected in the incidence of criterion-based PTSD-like behavior patterns. The World Journal of Biological Psychiatry. 10:856-869.
84. McEwen BS. 2002. The neurobiology and neuroendocrinology of stress. Implications for post-traumatic stress disorder from a basic science perspective. Psychiatr Clin North Am 25:469-494.
85. Milad MR, Rauch SL, Pitman RK, Quirk GJ. 2006. Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biol Psychol 73:61-71. Epub 2006 Feb 13.
86. Myers KM, Davis M. 2002. Behavioral and neural analysis of extinction. Neuron 36:567-584.
87. Nutt D, Davidson J. 2000. Post-Traumatic Stress Disorder Diagnosis, Management and Treatment. London: Taylor & Francis.
88. Peigneux P, Laureys S, Delbeuck X, Maquet P. 2001. Sleeping brain, learning brain. The role of sleep for memory systems. Neuroreport 12:A111-24.
89. Pitman RK, Rasmusson AM, Koenen KC, Shin LM, Orr SP, GilbertsonMW, Milad MR, Liberzon I. 2012. Biological studies of post-traumatic stress disorder. Nat Rev Neurosci 13:769-87.
90. Rauch SL, Shin LM, Phelps EA. 2006. Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research-past, present, and future. Biol Psychiatry 60:376-82.
91. Resick PA, Bovin MJ, Calloway AL, Dick AM, King MW, Mitchell KS, Suvak MK, Wells SY, Stirman SW, Wolf EJ. 2012. A critical evaluation of the complex PTSD literature: implications for DSM-5. J Trauma Stress 25:241-51.
92. Resnick H, Yehuda R, Pitman R, Foy D. 1995. Effect of previous trauma on acute plasma cortisol level following rape. Am J Psychiatry 152:1675-1677.
93. Roseboom PH, Nanda SA, Bakshi VP, Trentani A, Newman SM, Kalin NH. 2007. Predator threat induces behavioral inhibition, pituitary-adrenal activation and changes in amygdala CRF-binding protein gene expression. Psychoneuroendocrinology 32:44-55. Epub 2006 Nov 20.
94. Schelling G, Kilger E, Roozendaal B, de Quervain DJ, Briegel J, Dagge A, Rothenhausler HB, Krauseneck T, Nollert G, Kapfhammer HP. 2004. Stress doses of hydrocortisone, traumatic memories, and symptoms of posttraumatic stress disorder in patients after cardiac surgery: a randomized study. Biol Psychiatry 55:627-33.
95. Shalev AY. 2002. Acute stress reactions in adults. Biol Psychiatry 51:532-43.
96. Shore J, Vollmer W, Tatum E. 1989. Community patterns of posttraumatic stress disorders. J Nerv Ment Dis 177:681-685.
97. Solomon Z, Shklar R, Mikulincer M. 2005. Frontline treatment of combat stress reaction: a 20-year longitudinal evaluation study. Am J Psychiatry 162:2309-2314.
98. Stickgold R. 2005. Sleep-dependent memory consolidation. Nature 437:1272-1278.
99. Sullivan M, Gratton A. 1998. Relationships between stress-induced increases in medial prefrontal cortical dopamine and plasma corticosterone levels in rats: role of cerebral laterality. Neuroscience 83:81-91.
100. Szapiro G, Vianna M, McGaugh J, Medina J, Izquierdo I. 2003. The role of NMDA glutamate receptors, PKA, MAPK, and CAMKII in the hippocampus in extinction of conditioned fear. Hippocampus 13:53-58.
101. 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 29:1157-67. Epub 2005 Aug 10.
102. van Stegeren AH, Everaerd W, Cahill L, McGaugh JL. 1998. Memory for emotional events: Differential effects of centrally versus peripherally acting beta-blocking agents. Psychopharmacology (Berlin) 138:305-310.
103. Wagner U, Hallschmid M, Rasch B, Born J. 2006. Brief sleep after learning keeps emotional memories alive for years. Biol Psychiatry 60:788-90.
104. Walker MP, Stickgold R. 2006. Sleep, memory, and plasticity. Annu Rev Psychol 57:139-66.
105. Willner P, Mitchell PJ. 2002. The validity of animal models of predisposition to depression. Behav Pharmacol 13:169-88.
106. 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 26:1110-7.
107. Yehuda R, LeDoux J. 2007. Response variation following trauma: a translational neuroscience approach to understanding PTSD. Neuron 56:19-32.
108. Zimmerman G, Shaltiel G, Barbash S, Cohen J, Gasho CJ, Shenhar-Tsarfaty S, Shalev H,Berliner SA, Shelef I, ShohamS, et al. 2013. Post-traumatic anxiety associates with failure of the innate immune receptor TLR9 to evade the pro-inflammatory NFkappaB pathway. Transl Psychiatry 2:e78.
109. Zohar J, Yahalom H, Kozlovsky N, Cwikel-Hamzany S, Matar MA, Kaplan Z, Yehuda R, Cohen H. 2011. High dose hydrocortisone immediately after trauma may alter the trajectory of PTSD: interplay between clinical and animal studies. Eur Neuropsychopharmacol 21:796-809.