Witnessing traumatic events causes severe behavioral impairments in rats

International Journal of Neuropsychopharmacology

Volumn 755, Issue , 2014, Pages

  Patki, Gaurav ^a   Solanki, Naimesh ^a   Salim, Samina ^a  

^a UNIVERSITY OF HOUSTON   (United States)

Author keywords

depression and anxiety; PTSD; stress; trauma; witness

Indexed keywords

CORTICOSTERONE;

ACCLIMATIZATION; AGGRESSION; ANHEDONIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BEHAVIOR DISORDER; BLOOD SAMPLING; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; ELEVATED PLUS MAZE TEST; LONG EVANS RAT; LONG TERM MEMORY; MALE; MEMORY DISORDER; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; RAT; SOCIAL INTERACTION; SOCIAL SUPPORT; SPRAGUE DAWLEY RAT; ANIMAL; ANIMAL HOUSING; BLOOD; DISEASE MODEL; PATHOLOGY; PATHOPHYSIOLOGY; PSYCHOLOGY; SOCIAL BEHAVIOR; SOCIAL DOMINANCE; VISION;

ANIMALS; ANXIETY; CORTICOSTERONE; DEPRESSION; DISEASE MODELS, ANIMAL; DOMINANCE-SUBORDINATION; HOUSING, ANIMAL; MALE; MEMORY DISORDERS; RATS, LONG-EVANS; RATS, SPRAGUE-DAWLEY; SOCIAL BEHAVIOR; STRESS DISORDERS, POST-TRAUMATIC; VISUAL PERCEPTION;

EID: 84939418143     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145714000923     Document Type: Article

References (89)

1. Aleisa AM, Helal G, Alhaider IA, Alzoubi KH, Srivareerat M, Tran TT, Al-Rejaie SS, Alkadhi KA (2011) Acute nicotine treatment prevents REM sleep deprivation-induced learning and memory impairment in rat. Hippocampus 21:899-909.
2. Alhaider IA, Aleisa AM, Tran TT, Alkadhi KA (2010a) Caffeine prevents sleep loss-induced deficits in long-term potentiation and related signaling molecules in the dentate gyrus. Eur J Neurosci 31:1368-1376.
3. Alhaider IA, Aleisa AM, Tran TT, Alzoubi KH, Alkadhi KA (2010b) Chronic caffeine treatment prevents sleep deprivation-induced impairment of cognitive function and synaptic plasticity. Sleep 33:437-444.
4. th ed. Washington, DC: American Psychiatric Association.
5. Andrews B, Brewin CR, Rose S (2003) Gender, social support, and PTSD in victims of violent crime. J Trauma Stress 16:421-427.
6. Atsak P, Orre M, Bakker P, Cerliani L, Roozendaal B, Gazzola V, Moita M, Keysers C (2011) Experience modulates vicarious freezing in rats: a model for empathy. PLoS ONE 6:e21855.
7. Barnett SA (1958) Physiological effects of social stress in wild rats. I. The adrenal cortex. J Psychosom Res 3:1-11.
8. Barrot M, Olivier JD, Perrotti LI, DiLeone RJ, Berton O, Eisch AJ, Impey S, Storm DR, Neve RL, Yin JC, Zachariou V, Nestler EJ (2002) CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc Natl Acad Sci U S A 99:11435-11440.
9. Beck CT (2011) Secondary traumatic stress in nurses: a systematic review. Arch Psychiatr Nurs 25:1-10.
10. Berlin I, Givry-Steiner L, Lecrubier Y, Puech AJ (1998) Measures of anhedonia and hedonic responses to sucrose in depressive and schizophrenic patients in comparison with healthy subjects. Eur Psychiatry 13:303-309.
11. Bert B, Fink H, Huston JP, Voits M (2002) Fischer 344 and wistar rats differ in anxiety and habituation but not in water maze performance. Neurobiol Learn Mem 78:11-22.
12. Berton O, Aguerre S, Sarrieau A, Mormede P, Chaouloff F (1998) Differential effects of social stress on central serotonergic activity and emotional reactivity in Lewis and spontaneously hypertensive rats. Neuroscience 82:147-159.
13. Bhatnagar S, Vining C (2003) Facilitation of hypothalamic-pituitary-adrenal responses to novel stress following repeated social stress using the resident/intruder paradigm. Horm Behav 43:158-165.
14. Bhatnagar S, Vining C, Iyer V, Kinni V (2006) Changes in hypothalamic-pituitary-adrenal function, body temperature, body weight and food intake with repeated social stress exposure in rats. J Neuroendocrinol 18:13-24.
15. Bjorkqvist K (2001) Social defeat as a stressor in humans. Physiol Behav 73:435-442.
16. Blake DD, Cook JD, Keane TM (1992) Post-traumatic stress disorder and coping in veterans who are seeking medical treatment. J Clin Psychol 48:695-704.
17. Blanchard DC, Spencer RL, Weiss SM, Blanchard RJ, McEwen B, Sakai RR (1995) Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates. Psychoneuroendocrinology 20:117-134.
18. Bolanos CA, Barrot M, Berton O, Wallace-Black D, Nestler EJ (2003) Methylphenidate treatment during pre- and periadolescence alters behavioral responses to emotional stimuli at adulthood. Biol Psychiatry 54:1317-1329.
19. Bredy TW, Barad M (2009) Social modulation of associative fear learning by pheromone communication. Learn Mem 16:12-18.
20. Brewin CR, Andrews B, Valentine JD (2000) Meta-analysis of risk factors for posttraumatic stress disorder in trauma-exposed adults. J Consult Clin Psychol 68:748-766.
21. Calvo N, Cecchi M, Kabbaj M, Watson SJ, Akil H (2011) Differential effects of social defeat in rats with high and low locomotor response to novelty. Neuroscience 183:81-89.
22. Carlier P, Jamon M (2006) Observational learning in C57BL/6j mice. Behav Brain Res 174:125-131.
23. Church RM (1959) Emotional reactions of rats to the pain of others. J Comp Physiol Psychol 52:132-134.
24. Clapp JD, Gayle Beck J (2009) Understanding the relationship between PTSD and social support: the role of negative network orientation. Behav Res Ther 47:237-244.
25. Cougle JR, Resnick H, Kilpatrick DG (2009) Does prior exposure to interpersonal violence increase risk of PTSD following subsequent exposure? Behav Res Ther 47:1012-1017.
26. de Jong JG, van der Vegt BJ, Buwalda B, Koolhaas JM (2005) Social environment determines the long-term effects of social defeat. Physiol Behav 84:87-95.
27. Figley CR (1995) Compassion Fatigue: Coping with secondary traumatic stress disorder in those who treat the traumatized.
28. Fitzsimons JT (1978) Angiotensin, thirst, and sodium appetite: retrospect and prospect. Fed Proc 37:2669-2675.
29. Galef BG Jr., Giraldeau LA (2001) Social influences on foraging in vertebrates: causal mechanisms and adaptive functions. Anim Behav 61:3-15.
30. Golden SA, Covington HE III, Berton O, Russo SJ (2011) A standardized protocol for repeated social defeat stress in mice. Nat Protoc 6:1183-1191.
31. Greenleaf JE (1992) Problem: thirst, drinking behavior, and involuntary dehydration. Med Sci Sports Exerc 24:645-656.
32. Guzman YF, Tronson NC, Guedea A, Huh KH, Gao C, Radulovic J (2009) Social modeling of conditioned fear in mice by non-fearful conspecifics. Behav Brain Res 201:173-178.
33. Hadfield MG (1983) Dopamine: mesocortical vs. nigrostriatal uptake in isolated fighting mice and controls. Behav Brain Res 7:269-281.
34. Herman JP, Cullinan WE (1997) Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20:78-84.
35. Heyes CM (1994) Social learning in animals: categories and mechanisms. Biol Rev Camb Philos Soc 69:207-231.
36. Imbe H, Murakami S, Okamoto K, Iwai-Liao Y, Senba E (2004) The effects of acute and chronic restraint stress on activation of ERK in the rostral ventromedial medulla and locus coeruleus. Pain 112:361-371.
37. Iniguez SD, Warren BL, Bolanos-Guzman CA (2010) Short- and long-term functional consequences of fluoxetine exposure during adolescence in male rats. Biol Psychiatry 67:1057-1066.
38. Jeon D, Kim S, Chetana M, Jo D, Ruley HE, Lin SY, Rabah D, Kinet JP, Shin HS (2010) Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC. Nat Neurosci 13:482-488.
39. Kaneyuki H, Yokoo H, Tsuda A, Yoshida M, Mizuki Y, Yamada M, Tanaka M (1991) Psychological stress increases dopamine turnover selectively in mesoprefrontal dopamine neurons of rats: reversal by diazepam. Brain Res 557:154-161.
40. 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.
41. 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.
42. Kim EJ, Kim ES, Covey E, Kim JJ (2010) Social transmission of fear in rats: the role of 22-kHz ultrasonic distress vocalization. PLoS ONE 5:e15077.
43. Kioukia-Fougia N, Antoniou K, Bekris S, Liapi C, Christofidis I, Papadopoulou-Daifoti Z (2002) The effects of stress exposure on the hypothalamic-pituitary-adrenal axis, thymus, thyroid hormones and glucose levels. Prog Neuropsychopharmacol Biol Psychiatry 26:823-830.
44. Kiyokawa Y, Kikusui T, Takeuchi Y, Mori Y (2004) Partner's stress status influences social buffering effects in rats. Behav Neurosci 118:798-804.
45. Knapska E, Mikosz M, Werka T, Maren S (2010) Social modulation of learning in rats. Learn Mem 17:35-42.
46. Koolhaas JM, De Boer SF, De Rutter AJ, Meerlo P, Sgoifo A (1997) Social stress in rats and mice. Acta Physiol Scand Suppl 640:69-72.
47. Korz V, Frey JU (2005) Bidirectional modulation of hippocampal long-term potentiation under stress and no-stress conditions in basolateral amygdala-lesioned and intact rats. J Neurosci 25:7393-7400.
48. Langford DJ, Crager SE, Shehzad Z, Smith SB, Sotocinal SG, Levenstadt JS, Chanda ML, Levitin DJ, Mogil JS (2006) Social modulation of pain as evidence for empathy in mice. Science 312:1967-1970.
49. Lehmann ML, Herkenham M (2011) Environmental enrichment confers stress resiliency to social defeat through an infralimbic cortex-dependent neuroanatomical pathway. J Neurosci 31:6159-6173.
50. Liebschutz J, Saitz R, Brower V, Keane TM, Lloyd-Travaglini C, Averbuch T, Samet JH (2007) PTSD in urban primary care: high prevalence and low physician recognition. J Gen Intern Med 22:719-726.
51. Maercker A, Horn AB (2013) A socio-interpersonal perspective on PTSD: the case for environments and interpersonal processes. Clin Psychol Psychother 20:465-481.
52. Martinez M, Phillips PJ, Herbert J (1998) Adaptation in patterns of c-fos expression in the brain associated with exposure to either single or repeated social stress in male rats. Eur J Neurosci 10:20-33.
53. McCann IL, Pearlman LA (1990) Vicarious traumatization: a framework for understanding the psychological effects of working with victims. J Trauma Stress 3:131-149.
54. McKittrick CR, Blanchard DC, Blanchard RJ, McEwen BS, Sakai RR (1995) Serotonin receptor binding in a colony model of chronic social stress. Biol Psychiatry 37:383-393.
55. Miczek KA (1979) A new test for aggression in rats without aversive stimulation: differential effects of d-amphetamine and cocaine. Psychopharmacology (Berl) 60:253-259.
56. Molteni R, Lipska BK, Weinberger DR, Racagni G, Riva MA (2001) Developmental and stress-related changes of neurotrophic factor gene expression in an animal model of schizophrenia. Mol Psychiatry 6:285-292.
57. Nocjar C, Zhang J, Feng P, Panksepp J (2012) The social defeat animal model of depression shows diminished levels of orexin in mesocortical regions of the dopamine system, and of dynorphin and orexin in the hypothalamus. Neuroscience 218:138-153.
58. Owens GP, Baker DG, Kasckow J, Ciesla JA, Mohamed S (2005) Review of assessment and treatment of PTSD among elderly American armed forces veterans. Int J Geriatr Psychiatry 20:1118-1130.
59. Ozer EJ, Best SR, Lipsey TL, Weiss DS (2003) Predictors of posttraumatic stress disorder and symptoms in adults: a meta-analysis. Psychol Bull 129:52-73.
60. Panksepp JB, Lahvis GP (2011) Rodent empathy and affective neuroscience. Neurosci Biobehav Rev 35:1864-1875.
61. Papp M, Willner P, Muscat R (1991) An animal model of anhedonia: attenuation of sucrose consumption and place preference conditioning by chronic unpredictable mild stress. Psychopharmacology (Berl) 104:255-259.
62. Patki G, Solanki N, Allam F, Salim S (2013) Depression and anxiety-like behavior as well as memory impairment is associated with increased oxidative stress in a rat model of social defeat. Brain Res 1539:73-86.
63. Patki G, Li L, Allam F, Solanki N, Dao AT, Alkadhi K, Salim S (2014a) Moderate treadmill exercise rescues anxiety and depression-like behavior as well as memory impairment in a rat model of posttraumatic stress disorder. Physiol Behav 130C:47-53.
64. Patki G, Solanki N, Ansari A, Allam F, Atrooz F, Jannise B, Maturi J, Salim S (2014b) Novel mechanistic insights into treadmill exercise based rescue of social defeat-induced anxiety -like behavior and learning-memory impairment in rats. Physiol Behav 130:135-144.
65. Preston SD, de Waal FB (2002) Empathy: its ultimate and proximate bases. Behav Brain Sci 25:1-20, discussion 20-71.
66. Reeves RR, Parker JD, Konkle-Parker DJ (2005) War-related mental health problems of today's veterans: new clinical awareness. J Psychosoc Nurs Ment Health Serv 43:18-28.
67. Rice GE, Gainer P (1962) 'Altruism' in the albino rat. J Comp Physiol Psychol 55:123-125.
68. Rohde P (2001) The relevance of hierarchies, territories, defeat for depression in humans: hypotheses and clinical predictions. J Affect Disord 65:221-230.
69. Roozendaal B, Williams CL, McGaugh JL (1999) Glucocorticoid receptor activation in the rat nucleus of the solitary tract facilitates memory consolidation: involvement of the basolateral amygdala. Eur J Neurosci 11:1317-1323.
70. Roozendaal B, McReynolds JR, Van der Zee EA, Lee S, McGaugh JL, McIntyre CK (2009) Glucocorticoid effects on memory consolidation depend on functional interactions between the medial prefrontal cortex and basolateral amygdala. J Neurosci 29:14299-14308.
71. Ruis MA, te Brake JH, Buwalda B, De Boer SF, Meerlo P, Korte SM, Blokhuis HJ, Koolhaas JM (1999) Housing familiar male wildtype rats together reduces the long-term adverse behavioural and physiological effects of social defeat. Psychoneuroendocrinology 24:285-300.
72. Salim S, Sarraj N, Taneja M, Saha K, Tejada-Simon MV, Chugh G (2010) Moderate treadmill exercise prevents oxidative stress-induced anxiety-like behavior in rats. Behav Brain Res 208:545-552.
73. Sandi C, Pinelo-Nava MT (2007) Stress and memory: behavioral effects and neurobiological mechanisms. Neural Plast 2007:78970.
74. Sawchenko PE, Brown ER, Chan RK, Ericsson A, Li HY, Roland BL, Kovacs KJ (1996) The paraventricular nucleus of the hypothalamus and the functional neuroanatomy of visceromotor responses to stress. Prog Brain Res 107:201-222.
75. Schrijver NC, Pallier PN, Brown VJ, Wurbel H (2004) Double dissociation of social and environmental stimulation on spatial learning and reversal learning in rats. Behav Brain Res 152:307-314.
76. Selye H (1936) Thymus and Adrenals in the response of the Organism to injuries and Intoxication. Br J Exp Pathol 17:234-248.
77. Stein MB (2002) Taking aim at posttraumatic stress disorder: understanding its nature and shooting down myths. Can J Psychiatry 47:921-922.
78. Stein MB, Walker JR, Forde DR (2000) Gender differences in susceptibility to posttraumatic stress disorder. Behav Res Ther 38:619-628.
79. Tamashiro KL, Nguyen MM, Fujikawa T, Xu T, Yun Ma L, Woods SC, Sakai RR (2004) Metabolic and endocrine consequences of social stress in a visible burrow system. Physiol Behav 80:683-693.
80. Valsecchi P, Bosellini I, Sabatini F, Mainardi M, Fiorito G (2002) Behavioral analysis of social effects on the problem-solving ability in the house mouse Ethology 108:1115-1134.
81. Vollert C, Zagaar M, Hovatta I, Taneja M, Vu A, Dao A, Levine A, Alkadhi K, Salim S (2011) Exercise prevents sleep deprivation-associated anxiety-like behavior in rats: potential role of oxidative stress mechanisms. Behav Brain Res 224:233-240.
82. Warren BL, Vialou VF, Iniguez SD, Alcantara LF, Wright KN, Feng J, Kennedy PJ, Laplant Q, Shen L, Nestler EJ, Bolanos-Guzman CA (2013) Neurobiological sequelae of witnessing stressful events in adult mice. Biol Psychiatry 73:7-14.
83. Willner P, Muscat R, Papp M (1992) Chronic mild stress-induced anhedonia: a realistic animal model of depression. Neurosci Biobehav Rev 16:525-534.
84. Wood SK, Walker HE, Valentino RJ, Bhatnagar S (2010) Individual differences in reactivity to social stress predict susceptibility and resilience to a depressive phenotype: role of corticotropin-releasing factor. Endocrinology 151:1795-1805.
85. Wood SK, McFadden KV, Grigoriadis D, Bhatnagar S, Valentino RJ (2012) Depressive and cardiovascular disease comorbidity in a rat model of social stress: a putative role for corticotropin-releasing factor. Psychopharmacology (Berl) 222:325-336.
86. Yehuda R (2002) Post-traumatic stress disorder. N Engl J Med 346:108-114.
87. Yu T, Guo M, Garza J, Rendon S, Sun XL, Zhang W, Lu XY (2011) Cognitive and neural correlates of depression-like behaviour in socially defeated mice: an animal model of depression with cognitive dysfunction. Int J Neuropsychopharmacol 14:303-317.
88. Zalaquett C, Thiessen D (1991) The effects of odors from stressed mice on conspecific behavior. Physiol Behav 50:221-227.
89. Zentall TR, Levine JM (1972) Observational learning and social facilitation in the rat. Science 178:1220-1221.