Translationally relevant modeling of PTSD in rodents

Cell and Tissue Research

Volumn 354, Issue 1, 2013, Pages 127-139

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

^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

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOSTERONE; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; NEUROMODULIN; PLACEBO; SERTRALINE; SYNAPTOPHYSIN; TYROSINE KINASE RECEPTOR;

ACUTE STRESS DISORDER; BEHAVIORAL SCIENCE; COMORBIDITY; CONDITIONING; DIAGNOSTIC TEST; DISEASE CLASSIFICATION; DISEASE MODEL; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG MEGADOSE; EXPERIMENTAL MODEL; EXPOSURE; FEAR; GENETIC PREDISPOSITION; HABITUATION; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LOW DRUG DOSE; MEMORY CONSOLIDATION; MENTAL STRESS; METABOLIC DISORDER; NEUROBIOLOGY; NONHUMAN; PHYSIOLOGICAL STRESS; POSTTRAUMATIC STRESS DISORDER; PREDATOR; PREVALENCE; PRIORITY JOURNAL; PSYCHOTRAUMA; REINFORCEMENT; REVIEW; RODENT; SCORING SYSTEM; STARTLE REFLEX; STIMULUS RESPONSE; TIME; TRANSLATIONAL RESEARCH; VALIDITY; ANIMAL; MOUSE; RAT; STRESS DISORDERS, POST-TRAUMATIC;

ANIMALIA; RODENTIA;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; MICE; RATS; RODENTIA; STRESS DISORDERS, POST-TRAUMATIC; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84885670049     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-013-1687-6     Document Type: Review

References (87)

1. Adamec R (1997) Transmitter systems involved in neural plasticity underlying increased anxiety and defense-implications for understanding anxiety following traumatic stress. Neurosci Biobehav Rev 21:755-765 (Pubitemid 27524770)
2. Adamec RE, Shallow T (1993) Lasting effects on rodent anxiety of a single exposure to a cat. Physiol Behav 54:101-109 (Pubitemid 23172429)
3. Adamec R, Kent P, Anisman H, Shallow T, Merali Z (1998) Neural plasticity, neuropeptides and anxiety in animals-implications for understanding and treating affective disorder following traumatic stress in humans. Neurosci Biobehav Rev 23:301-318 (Pubitemid 29011633)
4. 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 (Pubitemid 43795970)
5. 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 167:270-286 (Pubitemid 43099789)
6. Adamec RE, Blundell J, Burton P (2006c) Relationship of the predatory attack experience to neural plasticity, pCREB expression and neuroendocrine response. Neurosci Biobehav Rev 30:356-375 (Pubitemid 43230168)
7. 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 (Pubitemid 46497456)
8. Akirav I, Maroun M (2007) The role of the medial prefrontal cortex-amygdala circuit in stress effects on the extinction of fear. Neural Plast 2007:30873 (Pubitemid 351210896)
9. American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders, 4th edn. American Psychiatric Association, Washington, DC
10. 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 29:1123-1144 (Pubitemid 41446891)
11. Blanchard RJ, Blanchard DC (1990) Anti-predator defense as models of fear and anxiety. In: Blanchard RJ, Parmigiani S (eds) Brain. Harwood Academic, London
12. Blanchard RJ, Blanchard DC, Rodgers J, Weiss SM (1990) The characterization and modelling of antipredator defensive behavior. Neurosci Biobehav Rev 14:463-472
13. Blanchard RJ, Shepherd JK, Rodgers RJ, Magee L, Blanchard DC (1993) Attenuation of antipredator defensive behavior in rats following chronic treatment with imipramine. Psychopharmacology 110:245-253 (Pubitemid 23029458)
14. Blanchard RJ, Nikulina JN, Sakai RR, McKittrick C, McEwen B, Blanchard DC (1998) Behavioral and endocrine change following chronic predatory stress. Physiol Behav 63:561-569 (Pubitemid 28119190)
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 27:1177-1185 (Pubitemid 37501024)
16. 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 45:2019-2033 (Pubitemid 47210952)
17. Blundell J, Adamec R, Burton P (2005) Role of NMDA receptors in the syndrome of behavioral changes produced by predator stress. Physiol Behav 86:233-243 (Pubitemid 41316627)
18. Borsboom D (2008) Psychometric perspectives on diagnostic systems. J Clin Psychol 64:1089-1108
19. Bouton ME (2004) Context and behavioral processes in extinction. Learn Mem 11:485-494 (Pubitemid 39299694)
20. Bremner JD, Licinio J, Darnell A, Krystal JH, Owens MJ, Southwick SM et al (1997) Elevated CSF corticotropin-releasing factor concentrations in posttraumatic stress disorder. Am J Psychiatry 154:624-629 (Pubitemid 27197594)
21. 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 48:216-222
22. 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 (Pubitemid 28340351)
23. Broekman BF, Olff M, Boer F (2007) The genetic background to PTSD. Neurosci Biobehav Rev 31:348-362 (Pubitemid 46241450)
24. Cabib S, Orsini C, Le Moal M, Piazza P (2000) Abolition and reversal of strain differences in behavioral responses to drugs of abuse after a brief experience. Science 289:463-465 (Pubitemid 30490460)
25. Cabib S, Puglisi-Allegra S, Ventura R (2002) The contribution of comparative studies in inbred strains of mice to the understanding of the hyperactive phenotype. Behav Brain Res 13:103-109 (Pubitemid 34195327)
26. Caspi A, Moffitt T (2006) Gene-environment interactions in psychiatry: joining forces with neuroscience. Nat Rev Neurosci 7:583-590 (Pubitemid 43995433)
27. 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
28. Cohen H, Zohar J (2004) Animal models of post traumatic stress disorder: the use of cut off behavioral criteria. Ann N Y Acad Sci 1032:167-178 (Pubitemid 40298469)
29. 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 4:144-145 (Pubitemid 27237378)
30. 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 (Pubitemid 29404544)
31. Cohen H, Benjamin J, Kaplan Z, Kotler M (2000) Administration of high-dose ketoconazole, an inhibitor of steroid synthesis, prevents posttraumatic anxiety in an animal model. Eur Neuropsychopharmacol 10:429-435
32. 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 (Pubitemid 36331885)
33. 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 (Pubitemid 39486547)
34. 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 (Pubitemid 41565579)
35. Cohen H, Matar MA, Richter-Levin G, Zohar J (2006a) The contribution of an animal model toward uncovering biological risk factors for PTSD. Ann N Y Acad Sci 1071:335-350 (Pubitemid 44126740)
36. Cohen H, Ziv Y, Cardon M, Kaplan Z, Matar MA, Gidron Y et al (2006b) Maladaptation to mental stress mitigated by the adaptive immune system via depletion of naturally occurring regulatory CD4+CD25+ cells. J Neurobiol 66:552-563
37. Cohen H, Zohar J, Gidron Y, Matar AM, Belkind D, Loewenthal U et al (2006c) Blunted HPA axis response to stress influences susceptibility to posttraumatic stress response in rats. Biol Psychiatry 15:1208-1218
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 (Pubitemid 46497658)
39. Cohen H, Maayan R, Touati-Werner D, Kaplan Z, Matar MA, Loewenthal U et al (2007b) Decreased circulatory levels of neuroactive steroids in behaviourally more extremely affected rats subsequent to exposure to a potentially traumatic experience. Int J Neuropsychopharmacol 10:203-209
40. Cohen H, Geva AB, Matar MA, Zohar J, Kaplan Z (2008a) Post-traumatic stress behavioural responses in inbred mouse strains: can genetic predisposition explain phenotypic vulnerability? Int J Neuropsychopharmacol 11:331-349 (Pubitemid 351482499)
41. Cohen H, Matar MA, Buskila D, Kaplan Z, Zohar J (2008b) Early post-stressor intervention with high-dose corticosterone attenuates posttraumatic stress response in an animal model of posttraumatic stress disorder. Biol Psychiatry 64:708-717
42. 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
43. 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 52:1066-1078 (Pubitemid 35379964)
44. Delahanty D, Raimonde A, Spoonster E (2000) Initial posttraumatic urinary cortisol levels predict subsequent PTSD symptoms in motor vehicle accident victims. Biol Psychiatry 48:940-947
45. 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 16:571-576 (Pubitemid 44405259)
46. Dunsmoor JE, Bandettini PA, Knight DC (2007) Neural correlates of unconditioned response diminution during Pavlovian conditioning. Neuroimage 40:811-817
47. Endres T, Apfelbach R, Fendt M (2005) Behavioral changes induced in rats by exposure to trimethylthiazoline, a component of fox odor. Behav Neurosci 119:1004-1010 (Pubitemid 41377251)
48. Etkin A, Wager TD (2007) Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am J Psychiatry 164:1476-1488 (Pubitemid 350069724)
49. File SE (1993) The interplay of learning and anxiety in the elevated plus-maze. Behav Brain Res 58:199-202 (Pubitemid 24024058)
50. 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 (Pubitemid 23343130)
51. Foa EB, Kozak MJ (1986) Emotional processing of fear: exposure to corrective information. Psychol Bull 99:20-35
52. 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 34:1625-1633 (Pubitemid 26006359)
53. 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 19:43-49
54. Knox D, Nault T, Henderson C, Liberzon I (2012b) Glucocorticoid receptors and extinction retention deficits in the single prolonged stress model. Neuroscience 223:163-173
55. 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 10:741-758 (Pubitemid 350035829)
56. Kozlovsky N, Matar MA, Kaplan Z, Kotler M, Zohar J, Cohen H (2008) 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
57. 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
58. Le Merrer J, Becker JA, Befort K, Kieffer BL (2009) Reward processing by the opioid system in the brain. Physiol Rev 89:1379-1412
59. LeDoux J (1996) Emotional networks and motor control: a fearful view. Prog Brain Res 107:437-446
60. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155-184 (Pubitemid 30350041)
61. Lewitus GM, Cohen H, Schwartz M (2008) Reducing post-traumatic anxiety by immunization. Brain Behav Immun 22:1108-1114
62. Liberzon I, Sripada CS (2008) The functional neuroanatomy of PTSD: a critical review. Prog Brain Res 167:151-169
63. Liberzon I, Krstov M, Young EA (1997) Stress-restress: effects on ACTH and fast feedback. Psychoneuroendocrinology 22:443-453 (Pubitemid 27431506)
64. Maren S (2001) Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24:897-931 (Pubitemid 32695248)
65. Maren S, Chang CH (2006) Recent fear is resistant to extinction. Proc Natl Acad Sci U S A 103:18020-18025 (Pubitemid 44852278)
66. Mason JW, Giller EL, Kosten TR, Ostroff RB, Podd L (1986) Urinary free-cortisol levels in posttraumatic stress disorder patients. J Nerv Ment Dis 174:145-149 (Pubitemid 16117404)
67. 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 31:2610-2618 (Pubitemid 44764158)
68. 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. World J Biol Psychiatry 10:856-869
69. 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
70. Moffitt T, Caspi A, Rutter M (2006) Measured gene-environment interactions in psychopathology. Perspect Psychol Sci 1:5-27
71. Myers KM, Davis M (2002) Behavioral and neural analysis of extinction. Neuron 36:567-584 (Pubitemid 35346753)
72. Nutt D, Davidson J (2000) Post-traumatic stress disorder diagnosis, management and treatment. Taylor & Francis, London
73. Pitman R, Orr S (1990) Twenty-four hour urinary cortisol and catecholamine excretion in combat-related posttraumatic stress disorder. Biol Psychiatry 27:245-247 (Pubitemid 20033772)
74. Pitman RK, Rasmusson AM, Koenen KC, Shin LM, Orr SP, Gilbertson MW et al (2012) Biological studies of post-traumatic stress disorder. Nat Rev Neurosci 13:769-787
75. Rasmusson AM, Lipschitz DS, Wang S, Hu S, Vojvoda D, Bremner JD et al (2001) Increased pituitary and adrenal reactivity in premenopausal women with posttraumatic stress disorder. Biol Psychiatry 50:965-977 (Pubitemid 34066489)
76. Rauch SL, Shin LM, Phelps EA (2006) Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research-past, present, and future. Biol Psychiatry 60:376-382 (Pubitemid 44215857)
77. Resick PA, Bovin MJ, Calloway AL, Dick AM, King MW, Mitchell KS et al (2012) A critical evaluation of the complex PTSD literature: implications for DSM-5. J Trauma Stress 25:241-251
78. 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
79. 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 (Pubitemid 44959459)
80. Schelling G, Kilger E, Roozendaal B, de Quervain DJ, Briegel J, Dagge A et al (2004) Stress doses of hydrocortisone, traumatic memories, and symptoms of posttraumatic stress disorder in patients after cardiac surgery: a randomized study. Biol Psychiatry 55:627-633 (Pubitemid 38315037)
81. 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 (Pubitemid 28068040)
82. 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 (Pubitemid 41446893)
83. 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
84. Yehuda R (2005) Neuroendocrine aspects of PTSD. Handb Exp Pharmacol 169:371-403
85. Yehuda R, LeDoux J (2007) Response variation following trauma: a translational neuroscience approach to understanding PTSD. Neuron 56:19-32 (Pubitemid 47484180)
86. Yehuda R, Morris A, Labinsky E, Zemelman S, Schmeidler J (2007) Ten-year follow-up study of cortisol levels in aging holocaust survivors with and without PTSD. J Trauma Stress 20:757-761 (Pubitemid 350144883)
87. Zohar J, Yahalom H, Kozlovsky N, Cwikel-Hamzany S, Matar MA, Kaplan Z et al (2011) High dose hydrocortisone immediately after trauma may alter the trajectory of PTSD: interplay between clinical and animal studies. Eur Neuropsychopharmacol 21:796-809