Vulnerability factors in anxiety determined through differences in active-avoidance behavior

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 34, Issue 6, 2010, Pages 852-860

  Beck, Kevin D ^a,b   Jiao, Xilu ^b   Pang, Kevin C H ^a,b   Servatius, Richard J ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Avoidance; Instrumental learning; PTSD; Sex differences; Wistar Kyoto (WKY)

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; FEMALE; INSTRUMENTAL CONDITIONING; LATENT PERIOD; MALE; NONHUMAN; RAT; RISK ASSESSMENT; SEX DIFFERENCE; TEMPERAMENT; WISTAR KYOTO RAT; ANALYSIS OF VARIANCE; ANIMAL; ANXIETY; ESCAPE BEHAVIOR; PHYSIOLOGY; PSYCHOLOGY; SPECIES DIFFERENCE; SPRAGUE DAWLEY RAT;

ANALYSIS OF VARIANCE; ANIMALS; ANXIETY; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; CONDITIONING, OPERANT; ESCAPE REACTION; FEMALE; MALE; RATS; RATS, INBRED WKY; RATS, SPRAGUE-DAWLEY; SEX FACTORS; SPECIES SPECIFICITY;

EID: 77955054636     PISSN: 02785846     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2010.03.036     Document Type: Article

References (64)

1. Bangasser D.A., Santollo J., Shors T.J. The bed nucleus of the stria terminalis is critically involved in enhancing associative learning after stressful experience. Behav Neurosci 2005, 119:1459-1466.
2. Baum A.E., Solberg L.C., Churchill G.A., Ahmadiyeh N., Takahashi J.S., Redei E.E. Test- and behavior-specific genetic factors affect WKY hypoactivity in tests of emotionality. Behav Brain Res 2006, 169:220-230.
3. Beatty W.W., Beatty P.A. Hormonal determinants of sex differences in avoidance behavior and reactivity to electric shock in the rat. J Comp Physiol Psychol 1970, 73:446-455.
4. Beatty W.W., Bengelloun W.A., Vilberg T.R., Klepac R.K., Steiner J.M. Differential effects of US intensity and flooding on the acquisition and extinction of one-way active avoidance responding in female rats with septal lesions. Behav Biol 1975, 13:311-321.
5. Beck K.D., Zhu G., Beldowicz D., Brennan F.X., Ottenweller J.E., Moldow R.L., et al. Central nervous system effects from a peripherally acting cholinesterase inhibiting agent: interaction with stress or genetics. Ann N Y Acad Sci 2001, 933:310-314.
6. Bleich A., Gelkopf M., Melamed Y., Solomon Z. Mental health and resiliency following 44months of terrorism: a survey of an Israeli national representative sample. BMC Med 2006, 4:21.
7. Bolles R.C. Species-specific defense reactions and avoidance learning. Psychol Rev 1970, 77:32-48.
8. Braw Y., Malkesman O., Dagan M., Bercovich A., Lavi-Avnon Y., Schroeder M., et al. Anxiety-like behaviors in pre-pubertal rats of the Flinders Sensitive Line (FSL) and Wistar-Kyoto (WKY) animal models of depression. Behav Brain Res 2006, 167:261-269.
9. Brennan F.X., Beck K.D., Servatius R.J. Leverpress escape/avoidance conditioning in rats: safety signal length and avoidance performance. Integr Physiol Behav Sci 2003, 38:36-44.
10. Carr V.J., Lewin T.J., Kenardy J.A., Webster R.A., Hazell P.L., Carter G.L., et al. Psychosocial sequelae of the 1989 Newcastle earthquake: III. Role of vulnerability factors in post-disaster morbidity. Psychol Med 1997, 27:179-190.
11. Clements K.M., Wainwright P.E. Spontaneously hypertensive, Wistar-Kyoto and Sprague-Dawley rats differ in performance on a win-shift task in the water radial arm maze. Behav Brain Res 2006, 167:295-304.
12. Clements K.M., Saunders A.J., Robertson B.A., Wainwright P.E. Spontaneously hypertensive, Wistar Kyoto and Sprague-Dawley rats differ in their use of place and response strategies in the water radial arm maze. Neurobiol Learn Mem 2007, 87:285-294.
13. Denti A., Epstein A. Sex differences in the acquisition of two kinds of avoidance behavior in rats. Physiol Behav 1972, 8:611-615.
14. Diaz-Veliz G., Soto V., Dussaubat N., Mora S. Influence of the estrous cycle, ovariectomy and estradiol replacement upon the acquisition of conditioned avoidance responses in rats. Physiol Behav 1989, 46:397-401.
15. Diaz-Veliz G., Urresta F., Dussaubat N., Mora S. Effects of estradiol replacement in ovariectomized rats on conditioned avoidance responses and other behaviors. Physiol Behav 1991, 50:61-65.
16. Diaz-Veliz G., Urresta F., Dussaubat N., Mora S. Progesterone effects on the acquisition of conditioned avoidance responses and other motoric behaviors in intact and ovariectomized rats. Psychoneuroendocrinology 1994, 19:387-394.
17. Diaz-Veliz G., Benavides M.S., Butron S., Dussaubat N., Mora S. Behavioral effects of dopamine agonists and antagonists: influence of estrous cycle, ovariectomy, and estrogen replacement in rats. Pharmacol Biochem Behav 1999, 62:21-29.
18. Diaz-Veliz G., Butron S., Benavides M.S., Dussaubat N., Mora S. Gender, estrous cycle, ovariectomy, and ovarian hormones influence the effects of diazepam on avoidance conditioning in rats. Pharmacol Biochem Behav 2000, 66:887-892.
19. Dillow P.V., Myerson J., Slaughter L., Hurwitz H.M. Safety signals and the acquisition and extinction of lever-press discriminated avoidance in rats. Br J Psychol 1972, 63:583-591.
20. Ferguson S.A., Cada A.M. Spatial learning/memory and social and nonsocial behaviors in the spontaneously hypertensive, Wistar-Kyoto and Sprague-Dawley rat strains. Pharmacol Biochem Behav 2004, 77:583-594.
21. Foa E.B., Stein D.J., McFarlane A.C. Symptomatology and psychopathology of mental health problems after disaster. J Clin Psychiatry 2006, 67(Suppl 2):15-25.
22. Fox N.A., Henderson H.A., Marshall P.J., Nichols K.E., Ghera M.M. Behavioral inhibition: linking biology and behavior within a developmental framework. Annu Rev Psychol 2005, 56:235-262.
23. Gilad G.M., Shiller I. Differences in open-field behavior and in learning tasks between two rat strains differing in their reactivity to stressors. Behav Brain Res 1989, 32:89-93.
24. Gray J.A., Lalljee B. Sex differences in emotional behaviour in the rat: correlation between open-field defecation and active avoidance. Anim Behav 1974, 22:856-861.
25. Hapke U., Schumann A., Rumpf H.J., John U., Meyer C. Post-traumatic stress disorder: the role of trauma, pre-existing psychiatric disorders, and gender. Eur Arch Psychiatry Clin Neurosci 2006, 256:299-306.
26. Heinsbroek R.P., Van Oyen H.G., van de Poll N.E., Boer G.J. Failure of dexamethasone to influence sex differences in acquisition of discriminated lever press avoidance. Pharmacol Biochem Behav 1983, 19:599-604.
27. Hineline P.N. Warmup in avoidance as a function of time since prior training. J Exp Anal Behav 1978, 29:87-103.
28. Hoffman H.S., Fleshler M. The course of emotionality in the development of avoidance. J Exp Psychol 1962, 64:288-294.
29. Hoffman H.S., Fleshler M., Chorny H. Discriminated bar-press avoidance. J Exp Anal Behav 1961, 4:309-316.
30. Jiao X., Pare W.P., Tejani-Butt S. Strain differences in the distribution of dopamine transporter sites in rat brain. Prog Neuropsychopharmacol Biol Psychiatry 2003, 27:913-919.
31. Jiao X, Pang KC, Beck KD, Minor TR, Servatius RJ. Avoidance perseveration during extinction in Wistar-Kyoto rats: an interaction of innate vulnerability and stressor intensity. Submitted manuscript 2010.
32. Karamustafalioglu O.K., Zohar J., Guveli M., Gal G., Bakim B., Fostick L., et al. Natural course of posttraumatic stress disorder: a 20-month prospective study of Turkish earthquake survivors. J Clin Psychiatry 2006, 67:882-889.
33. Kashdan T.B., Elhai J.D., Frueh B.C. Anhedonia and emotional numbing in combat veterans with PTSD. Behav Res Ther 2006, 44:457-467.
34. Lapiz-Bluhm M.D., Bondi C.O., Doyen J., Rodriguez G.A., Bedard-Arana T., Morilak D.A. Behavioural assays to model cognitive and affective dimensions of depression and anxiety in rats. J Neuroendocrinol 2008, 20:1115-1137.
35. LeDoux J.E., Sakaguchi A., Reis D.J. Strain differences in fear between spontaneously hypertensive and normotensive rats. Brain Res 1983, 277:137-143.
36. Malkesman O., Braw Y., Zagoory-Sharon O., Golan O., Lavi-Avnon Y., Schroeder M., et al. Reward and anxiety in genetic animal models of childhood depression. Behav Brain Res 2005, 164:1-10.
37. McAuley J.D., Stewart A.L., Webber E.S., Cromwell H.C., Servatius R.J., Pang K.C. Wistar-Kyoto rats as an animal model of anxiety vulnerability: support for a hypervigilance hypothesis. Behav Brain Res 2009, 204:162-168.
38. Mora S., Urresta F., Dussaubat N., Benavente F., Baeza R., az-Veliz G. Behavioral effects of a LHRH antagonist in intact and ovariectomized rats. Pharmacol Biochem Behav 1993, 46:673-677.
39. Mora S., Dussaubat N., az-Veliz G. Effects of LHRH on avoidance conditioning in normally cycling and ovariectomized female rats. Pharmacol Biochem Behav 1998, 61:221-228.
40. Nakamura C.Y., Anderson N.H. Avoidance behavior differences within and between strains of rats. J Comp Physiol Psychol 1962, 55:740-747.
41. North C.S., Nixon S.J., Shariat S., Mallonee S., McMillen J.C., Spitznagel E.L., et al. Psychiatric disorders among survivors of the Oklahoma City bombing. JAMA 1999, 282:755-762.
42. North C.S., Pfefferbaum B., Tivis L., Kawasaki A., Reddy C., Spitznagel E.L. The course of posttraumatic stress disorder in a follow-up study of survivors of the Oklahoma City bombing. Ann Clin Psychiatry 2004, 16:209-215.
43. O'Donnell M.L., Elliott P., Lau W., Creamer M. PTSD symptom trajectories: from early to chronic response. Behav Res Ther 2007, 45:601-606.
44. Olff M., Sijbrandij M., Opmeer B.C., Carlier I.V., Gersons B.P. The structure of acute posttraumatic stress symptoms: 'reexperiencing,' 'active avoidance,' 'dysphoria,' and 'hyperarousal'. J Anxiety Disord 2009, 23:656-659.
45. 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. Neuroscience 2002, 115:229-242.
46. Pare W.P. Stress ulcer and open-field behavior of spontaneously hypertensive, normotensive, and Wistar rats. Pavlov J Biol Sci 1989, 24:54-57.
47. Pare W.P. Open field, learned helplessness, conditioned defensive burying, and forced-swim tests in WKY rats. Physiol Behav 1994, 55:433-439.
48. Pietrefesa A.S., Coles M.E. Moving beyond an exclusive focus on harm avoidance in obsessive compulsive disorder: considering the role of incompleteness. Behav Ther 2008, 39:224-231.
49. Pietrefesa A.S., Coles M.E. Moving beyond an exclusive focus on harm avoidance in obsessive-compulsive disorder: behavioral validation for the separability of harm avoidance and incompleteness. Behav Ther 2009, 40:251-259.
50. Powell R.W. Analysis of warm-up effects during avoidance in wild and domesticated rodents. J Comp Physiol Psychol 1972, 78:311-316.
51. Rosenbaum J.F., Biederman J., Bolduc-Murphy E.A., Faraone S.V., Chaloff J., Hirshfeld D.R., et al. Behavioral inhibition in childhood: a risk factor for anxiety disorders. Harv Rev Psychiatry 1993, 1:2-16.
52. Schafe G.E., Doyere V., LeDoux J.E. Tracking the fear engram: the lateral amygdala is an essential locus of fear memory storage. J Neurosci 2005, 25:10,010-10,014.
53. Schneier F.R., Blanco C., Antia S.X., Liebowitz M.R. The social anxiety spectrum. Psychiatr Clin North Am 2002, 25:757-774.
54. Schwartz C.E., Wright C.I., Shin L.M., Kagan J., Rauch S.L. Inhibited and uninhibited infants "grown up": adult amygdalar response to novelty. Science 2003, 300:1952-1953.
55. Scouten C.W., Groteleuschen L.K., Beatty W.W. Androgens and the organization of sex differences in active avoidance behavior in the rat. J Comp Physiol Psychol 1975, 88:264-270.
56. Servatius R.J., Ottenweller J.E., Beldowicz D., Guo W., Zhu G., Natelson B.H. Persistently exaggerated startle responses in rats treated with pyridostigmine bromide. J Pharmacol Exp Ther 1998, 287:1020-1028.
57. Servatius R.J., Beck K.D., Moldow R.L., Salameh G., Tumminello T.P., Short K.R. A stress-induced anxious state in male rats: corticotropin-releasing hormone induces persistent changes in associative learning and startle reactivity. Biol Psychiatry 2005, 57:865-872.
58. Servatius R.J., Jiao X., Beck K.D., Pang K.C., Minor T.R. Rapid avoidance acquisition in Wistar-Kyoto rats. Behav Brain Res 2008, 192:191-197.
59. Smith R.P., Larkin G.L., Southwick S.M. Trends in U.S. emergency department visits for anxiety-related mental health conditions, 1992-2001. J Clin Psychiatry 2008, 69:286-294.
60. Steenbergen H.L., Heinsbroek R.P., Van H.A., van de Poll N.E. Sex-dependent effects of inescapable shock administration on shuttlebox-escape performance and elevated plus-maze behavior. Physiol Behav 1990, 48:571-576.
61. Van Oyen H.G., Walg H., van de Poll N.E. Discriminated lever press avoidance conditioning in male and female rats. Physiol Behav 1981, 26:313-317.
62. Vincler M., Maixner W., Vierck C.J., Light A.R. Estrous cycle modulation of nociceptive behaviors elicited by electrical stimulation and formalin. Pharmacol Biochem Behav 2001, 69:315-324.
63. Vogt D.S., Pless A.P., King L.A., King D.W. Deployment stressors, gender, and mental health outcomes among Gulf War I veterans. J Trauma Stress 2005, 18:272-284.
64. Wittchen H.U., Hoyer J. Generalized anxiety disorder: nature and course. J Clin Psychiatry 2001, 62:15-19.