Fear conditioning fragments REM sleep in stress-sensitive Wistar-Kyoto, but not Wistar, rats

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 35, Issue 1, 2011, Pages 67-73

  DaSilva, Jamie K ^a   Lei, Yanlin ^a   Madan, Vibha ^b   Mann, Graziella L ^b   Ross, Richard J ^b,c,d   Tejani Butt, Shanaz ^a   Morrison, Adrian R ^b  

^a UNIVERSITY OF THE SCIENCES   (United States)

^b UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Fear conditioning; Posttraumatic stress disorder; REMS microarchitecture; Sleep; Wistar Kyoto rat

Indexed keywords

ANIMAL EXPERIMENT; ANXIETY; ARTICLE; ASSOCIATION; CONDITIONING; CONTROLLED STUDY; FEAR; FOOTSHOCK; MALE; MENTAL STRESS; NONHUMAN; RAT; REM SLEEP; STRAIN DIFFERENCE; WISTAR KYOTO RAT; WISTAR RAT;

ANALYSIS OF VARIANCE; ANIMALS; CONDITIONING, CLASSICAL; CUES; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; ELECTROSHOCK; FEAR; MALE; RATS; RATS, INBRED WKY; RATS, WISTAR; SLEEP, REM; STRESS, PSYCHOLOGICAL; TIME FACTORS;

EID: 78650939357     PISSN: 02785846     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2010.08.023     Document Type: Article

References (65)

1. Diagnostic and statistical manual of mental disorders 2000, American Psychiatric Association, Author, Washington, DC. 4th ed., text revision.
2. Amici R., Zamboni G., Perez E., Jones C.A., Toni I., Culin F. Pattern of desynchronized sleep during deprivation and recovery induced in the rat by changes in ambient temperature. J Sleep Res 1994, 3:250-256.
3. Amici R., Zamboni G., Perez E., Jones C.A., Parmeggiani P.L. The influence of a heavy thermal load on REM sleep in the rat. Brain Res 1998, 781:252-258.
4. Andersen M.L., Hoshino K., Tufik S. Increased susceptibility to development of anhedonia in rats with chronic peripheral nerve injury: involvement of sleep deprivation?. Prog Neuropsychopharmacol Biol Psychiatry 2009, 33:960-966.
5. Armario A., Gavaladà A., Martí J. Comparison of the behavioural and endocrine response to forced swimming stress in five inbred strains of rats. Psychoneuroendocrinology 1995, 20(8):879-890.
6. Aston-Jones G., Bloom F.E. Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. J Neurosci 1981, 1:876-886.
7. Beck K., Jiao X., Pang K.C.H., Servatius R.J. Vulnerability factors in anxiety determined through differences in active-avoidance behavior. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34(6):852-860.
8. Berger D.F., Starzec J.J. Contrasting lever-press avoidance behaviors of spontaneously hypertensive and normotensive rats (Rattus norvegicus). J Comp Psychol 1988, 102(3):279-286.
9. Breslau N., Roth T., Burduvali E., Kapke A., Schultz L., Roehrs T. Sleep in lifetime posttraumatic stress disorder: a community based polysomnographic study. Arch Gen Psychiatry 2004, 61:508-516.
10. Datta S. Avoidance task training potentiates phasic pontine-wave density in the rat: a mechanism for sleep-dependent plasticity. J Neurosci 2000, 20:8607-8613.
11. Davidson J., Smith R., Kudler H. Familial psychiatric illness in chronic posttraumatic stress disorder. Compr Psychiatry 1989, 30:339-345.
12. De La Garza R., Mahoney J.J. A distinct neurochemical profile in WKY rats at baseline and in response to acute stress: implications for animal models of anxiety and depression. Brain Res 2004, 1021:209-218.
13. Dugovic C., Solberg L., Redei E., Reeth O.V., Turek F.W. Sleep in the Wistar-Kyoto rat, a putative genetic animal model for depression. NeuroReport 2000, 11(3):627-631.
14. Gervasoni D., Darracq L., Fort P., Souliere F., Chouvet G., Luppi P.H. Electrophysiological evidence that noradrenergic neurons of the rat locus coeruleus are tonically inhibited by GABA during sleep. Eur J Neurosci 1998, 10:964-970.
15. Gómez F., De Kloet R.E., Armario A. Glucocorticoid negative feedback on the HPA axis in five inbred rat strains. Am J Physiol Regul Integr Comp Physiol 1998, 274:420-427.
16. Habukawa M., Uchimura N., Maeda M., Kotorii N., Maeda H. Sleep findings in young adult patients with posttraumatic stress disorder. Biol Psychiatry 2007, 62:1179-1182.
17. Jha S.K., Brennan F.X., Pawlyk A.C., Ross R.J., Morrison A.R. REM sleep: a sensitive index of fear conditioning in rats. Eur J Neurosci 2005, 21:1077-1080.
18. Lyons M.J., Goldberg J., Eisen S.A., True W., Tsuang M.T., Meyer J.M., et al. Do genes influence exposure to trauma? A twin study of combat. Am J Med Genet 1993, 48:22-27.
19. Madan V., Brennan F.X., Mann G.L., Horbal A.A., Dunn G.A., Ross R.J., et al. Long-term effect of cued fear conditioning on REM sleep microarchitecture in rats. Sleep 2008, 31:497-503.
20. Malkesman O., Maayan R., Weizman A., Weller A. Aggressive behavior and HPA axis hormones after social isolation in adult rats of two different genetic animal models for depression. Behav Brain Res 2006, 175:408-414.
21. Mavanji V., Datta S. Activation of the phasic pontine-wave generator enhances improvement of learning performance: a mechanism for sleep-dependent plasticity. Eur J Neurosci 2003, 17(2):359-370.
22. McGinty D.J., Harper R.M. Dorsal raphe neurons: depression of firing during sleep in cats. Brain Res 1976, 101:569-575.
23. Mellman T.A., Nolan B., Hebding J., Kulick-Bell R., Dominguez R. A polysomnographic comparison of veterans with combat-related PTSD, depressed men, and non-ill controls. Sleep 1997, 20:46-51.
24. Mellman T.A., Bustamante V., Fins A.I., Pigeon W.R., Nolan B. REM sleep and the early development of posttraumatic stress disorder. Am J Psychiatry 2002, 159:1696-1701.
25. Morilak D.A., Barrera G., Echevarria D.J., Garcia A.S., Hernandez A., Ma S., et al. Role of brain norepinephrine in the behavioral response to stress. Prog Neuropsychopharmacol Biol Psychiatry 2005, 29:1214-1224.
26. Papale L.A., Andersen M.L., Antunes I.B., Alvarenga T.A.F., Tufik S. Sleep pattern in rats under different stress modalities. Brain Res 2005, 1060:47-54.
27. Pardon M.C., Gould G.G., Garcia A., Phillips L., Cook M.C., Miller S.A., et al. Stress reactivity of the brain noradrenergic system in three rat strains differing in their neuroendocrine and behavioral responses to stress: implications for susceptibility to stress-related neuropsychiatric disorders. J Neurosci 2002, 115:229-242.
28. Pardon M.C., Ma S., Morilak D.A. Chronic cold stress sensitizes brain noradrenergic reactivity and noradrenergic facilitation of the HPA stress response in Wistar Kyoto rats. Brain Res 2003, 971:55-65.
29. Paré W.P. Technique and strain comparisons in stress ulcer. Ann NY Acad Sci 1990, 597:223-230.
30. Paré W.P. The performance of WKY rats on three tests of emotional behavior. Physiol Behav 1992, 51:1051-1056.
31. Paré W.P. Passive-avoidance behavior in Wistar-Kyoto (WKY), Wistar, and Fischer-344 rats. Physiol Behav 1993, 54:845-852.
32. Paré W.P. Open field, learned helplessness, conditioned defensive burying, and forced-swim tests in WKY rats. Physiol Behav 1994, 55(3):433-439.
33. Paré W.P. Hyponeophagia in Wistar Kyoto (WKY) rats. Physiol Behav 1994, 55(5):975-978.
34. Paré W.P. Enhanced retrieval of unpleasant memories influenced by shock controllability, shock sequence, and rat strain. Biol Psychiatry 1996, 39:808-813.
35. Paré W.P., Redei E. Depressive behavior and stress ulcer in Wistar-Kyoto rats. J Physiol Paris 1993, 87(4):229-238.
36. Paré A.M.T., Paré W.P., Kluczynski J. Negative affect and voluntary alcohol consumption in Wistar-Kyoto (WKY) and Sprague-Dawley rats. Physiol Behav 1999, 62(2):219-225.
37. Pawlyk A.C., Jha S.K., Brennan F.X., Morrison A.R., Ross R.J. A rodent model of sleep disturbances in posttraumatic stress disorder: the role of context after fear conditioning. Biol Psychiatry 2005, 57:268-277.
38. Pawlyk A.C., Morrison A.R., Ross R.J., Brennan F.X. Stress-induced changes in sleep in rodents: models and mechanisms. Neurosci Biobehav Rev 2008, 32:99-117.
39. Pickens C.L., Golden S.A., Adams-Deutsch T., Nair S.G., Shaham Y. Long-lasting incubation of conditioned fear in rats. Biol Psychiatry 2009, 65(10):881-886.
40. Raskind M.A., Peskind E.R., Kanter E.D., Petrie E.C., Radant A., Thompson C.E., et al. Reduction of nightmares and other PTSD symptoms in combat veterans by prazosin: a placebo-controlled study. Am J Psychiatry 2003, 160:371-373.
41. Raskind M.A., Peskind E.R., Hoff D.J., Hart K.L., Holmes H.A., Warren D., et al. A parallel group placebo controlled study of prazosin for trauma nightmares and sleep disturbance in combat veterans with post-traumatic stress disorder. Biol Psychiatry 2007, 61(8):928-934.
42. Redei E., Paré W.P., Arid F., Kluczynski J. Strain differences in hypothalamic-pituitary-adrenal activity and stress ulcer. Am J Physiol 1994, 266:R353-R360.
43. Reiner P.B. Correlational analysis of central noradrenergic neuronal activity and sympathetic tone in behaving cats. Brain Res 1986, 378:86-96.
44. Rosen J.B., West E.A., Donley M.P. Not all rat strains are equal: differential unconditioned fear responses to the synthetic fox odor 2, 4, 5-trimethylthiazoline in three outbred rat strains. Behav Neurosci 2006, 120(2):290-297.
45. Ross R.J., Ball W.A., Sullivan K., Caroff S.N. Sleep disturbance as the hallmark of posttraumatic stress disorder. Am J Psychiatry 1989, 146:697-707.
46. Ross R.J., Ball W.A., Dinges D.F., Kribbs N.B., Morrison A.R., Silver S.M., et al. Motor dysfunction during sleep in posttraumatic stress disorder. Sleep 1994, 17:723-732.
47. Ross R.J., Ball W.A., Dinges D.F., Kribbs N.B., Morrison A.R., Silver S.M., et al. Rapid eye movement sleep disturbance in post-traumatic stress disorder. Biol Psychiatry 1994, 35:195-200.
48. Sanford L.D., Tang X., Ross R.J., Morrison A.R. Influence of shock training and explicit fear-conditioned cues on sleep architecture in mice: a strain comparison. Behav Genet 2003, 33:43-58.
49. Scholl J.L., Renner K.J., Forster G.L., Tejani-Butt S. Central monoamine levels differ between rat strains used in studies of depressive behavior. Brain Res 2010, 1355:41-51.
50. Servatius R.J., Jiao X., Beck K.D., Pang K.C.H., Minor T.R. Rapid avoidance acquisition in Wistar-Kyoto rats. Behav Brain Res 2008, 192(2):191-197.
51. Shepard J.D., Myers D.A. Strain differences in anxiety-like behavior: association with corticotropin-releasing factor. Behav Brain Res 2008, 186:239-245.
52. Skre I., Onstad S., Torgesen S., Lygren S., Kringlen E. A twin study of DSM-III-R anxiety disorders. Acta Psychiatr Scand 1993, 88:85-92.
53. Solberg L.C., Olsen S.L., Turek F.W., Redei E. Altered hormone levels and circadian rhythm of activity in the WKY rat, a putative animal model of depression. Am J Physiol Regulatory Integrative Comp Physiol 2001, 281:786-794.
54. Stam R. PTSD and stress sensitization: a tale of brain and body: part 2: animal models. Neurosci Biobehav Rev 2007, 31:558-584.
55. Tang X., Yang L., Sanford L.D. Rat strain differences in freezing and sleep alterations associated with contextual fear. Sleep 2005, 28:1235-1244.
56. Taylor F., Raskind M.A. The [alpha]1-adrenergic antagonist prazosin improves sleep and nightmares in civilian trauma posttraumatic stress disorder. J Clin Psychopharmacol 2002, 22:82-85.
57. Taylor F.B., Lowe K., Thompson C., McFall M.M., Peskind E.R., Kanter E.D., et al. Daytime prazosin reduces psychological distress to trauma specific cues in civillian trauma posttraumatic stress disorder. Biol Psychiatry 2006, 7:577-581.
58. Taylor F.B., Martin P., Thompson C., Williams J., Mellman T.A., Gross C., et al. Prazosin effects on objective sleep measures and clinical symptoms in civilian posttraumatic stress disorder: a placebo-controlled study. Biol Psychiatry 2008, 63:629-632.
59. Tejani-Butt S.M., Paré W.P., Yang J. Effect of repeated novel stressors on depressive behavior and brain norepinephrine receptor system in Sprague-Dawley and Wistar Kyoto (WKY) rats. Brain Res 1994, 649:27-35.
60. Tejani-Butt S.M., Kluczynski J., Paré W.P. Strain-dependent modification of behavior following antidepressant treatment. Prog Neuropsychopharmacol Biol Psychiatry 2003, 27:7-14.
61. True W.R., Rice J., Eisen S.A., Heath A.C., Goldberg J., Lyons M.J., et al. A twin study of genetic and environmental contributions to liability of posttraumatic stress symptoms. Arch Gen Psychiatry 1993, 50:257-264.
62. Ursin R. Serotonin and sleep. Sleep Med Rev 2002, 6:55-69.
63. Walker M.P., van der Helm E. Overnight therapy? The role of sleep in emotional brain processing. Psychol Bull 2009, 135:731-748.
64. Yehuda R. Biological factors associated with susceptibility to posttraumatic stress disorder. Can J Psychiatry 1999, 44:34-39.
65. Zamboni G., Amici R., Perez E., Jones C.A., Parmeggiani P.L. Pattern of REM sleep occurrence in continuous darkness following the exposure to low ambient temperature in the rat. Behav Brain Res 2001, 122:25-32.