Contextual exploration previous to an aversive event predicts long-term emotional consequences of severe stress

Frontiers in Behavioral Neuroscience

Volumn , Issue OCT, 2013, Pages

  Carlos, E N Girardi ^a   Tiba, Paula A ^a,b   Llobet, Gisela B ^a   Levin, Raquel ^a   Abilio, Vanessa C ^a   Suchecki, Deborah ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSIDADE FEDERAL DO ABC   (Brazil)

Author keywords

Animal model; Context fear conditioning; Contextual configuration; Emotional behavior; Psychiatric disorder; PTSD

Indexed keywords

ACOUSTIC STRESS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AVERSIVE BEHAVIOR; CONDITIONED REFLEX; CONTROLLED STUDY; EMOTION; EXPLORATORY BEHAVIOR; FEAR; FOOTSHOCK; FREEZING; IMMOBILITY; MALE; MAZE TEST; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PREDICTION; RAT; STARTLE REFLEX; STIMULUS RESPONSE;

EID: 84886258220     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2013.00134     Document Type: Article

References (51)

1. Belzung, C., and Griebel, G. (2001). Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav. Brain Res. 125, 141-149. doi: 10.1016/s0166-4328(01)00291-1
2. Blanchard, R. J., Flannelly, K. J., and Blanchard, D. C. (1986). Defensive behaviors of laboratory and wild Rattus-Norvegicus. J. Comp. Psychol. 100, 101-107. doi: 10. 1037/0735-7036.100.2.101
3. Blanchard, R. J., Fukunaga, K. K., and Blanchard, D. C. (1976). Environmental-control of defensive reactions to footshock. Bull. Psychon. Soc. 8, 129-130.
4. Bremner, J. D., Narayan, M., Staib, L. H., Southwick, S. M., Mcglashan, T., and Charney, D. S. (1999). Neural correlates of memories of childhood sexual abuse in women with and without posttraumatic stress disorder. Am. J. Psychiatry 156, 1787-1795.
5. Breslau, N., Davis, G. C., Andreski, P., and Peterson, E. (1991). Traumatic events and posttraumatic stress disorder in an urban population of young adults. Arch. Gen. Psychiatry 48, 216-222. doi: 10.1001/archpsyc. 1991.01810270028003
6. Breslau, N., Kessler, R. C., Chilcoat, H. D., Schultz, L. R., Davis, G. C., and Andreski, P. (1998). Trauma and posttraumatic stress disorder in the community: the 1996 Detroit area survey of Trauma. Arch. Gen. Psychiatry 55, 626-632. doi: 10. 1001/archpsyc.55.7.626
7. Breslau, N., Reboussin, B. A., Anthony, J. C., and Storr, C. L. (2005). The structure of posttraumatic stress disorder: latent class analysis in 2 community samples. Arch. Gen. Psychiatry 62, 1343-1351. doi: 10. 1001/archpsyc.62.12.1343
8. Cannistraro, P. A., and Rauch, S. L. (2003). Neural circuitry of anxiety: evidence from structural and functional neuroimaging studies. Psy-chopharmacol. Bull. 37, 8-25.
9. Carobrez, A. P., and Bertoglio, L. J. (2005). Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci. Biobehav. Rev. 29, 1193-1205. doi: 10.1016/j. neubiorev.2005.04.017
10. Charney, D. S., Deutch, A. Y., Krystal, J. H., Southwick, S. M., and Davis, M. (1993). Psychobiologic mechanisms of posttraumatic stress disorder. Arch. Gen. Psychiatry 50, 295-305. doi: 10.1001/archpsyc. 1993.01820160064008
11. Clay, R., Hebert, M., Gill, G., Stapleton, L. A., Pridham, A., Coady, M., et al. (2011). Glucocorticoids are required for extinction of predator stress-induce hyperarousal. Neurobiol. Learn. Mem. 96, 367-377. doi: 10.1016/j.nlm.2011. 06.012
12. Diehl, L. A., Alvares, L. O., Noschang, C., Engelke, D., Andreazza, A. C., Goncalves, C. A., et al. (2012). Long-lasting effects of maternal separation on an animal model of post-traumatic stress disorder: effects on memory and hippocampal oxidative stress. Neurochem. Res. 37, 700-707. doi: 10.1007/s11064-011-0660-6
13. DSM-IV (2000). Diagnostic and Statistical Manual of Mental Disorders: DSM-IV-TR. Washington, D C: American Psychiatric Association.
14. Elzinga, B. M., and Bremner, J. D. (2002). Are the neural substrates of memory the final common pathway in posttraumatic stress disorder (PTSD)? J. Affect. Disord. 70, 1-17. doi: 10.1016/s0165-0327(01) 00351-2
15. Fanselow, M. S. (1984). What is conditioned fear. Tre n d s Ne urosc i. 7, 460-462. doi: 10.1016/s0166-2236(84)80253-2
16. Fanselow, M. S. (1986). Associative vs topographical accounts of the immediate shock freezing deficit in rats - implications for the response selection-rules governing species-specific defensive reactions. Learn. Motiv. 17, 16-39. doi: 10.1016/0023-9690(86)90018-4
17. Fanselow, M. S. (1990). Factors governing one-trial contextual conditioning. Anim. Behav. 18, 264-270. doi: 10.3758/bf03205285
18. Frankland, P. W., Josselyn, A., Anagnostaras, S. G., Kogan, J. H., Takahashi, E., and Silva, A. J. (2004). Consolidation of CS and US representations in associative fear conditioning. Hippocampus 14, 557-569. doi: 10.1002/hipo.10208
19. Gewirtz, J. C., Mcnish, K. A., and Davis, M. (1998). Lesions of the bed nucleus of the stria terminalis block sensitization of the acoustic startle reflex produced by repeated stress, but not fear-potentiated startle. Prog. Neuropsychopharmacol. Biol. Psychiatry 22, 625-648. doi: 10. 1016/s0278-5846(98)00028-1
20. Golub, Y., Kaltwasser, S. F., Mauch, C. P., Herrmann, L., Schmidt, U., Holsboer, F., et al. (2011). Reduced hippocampus volume in the mouse model of Posttraumatic Stress Disorder. J. Psychiatr. Res. 45, 650-659. doi: 10.1016/j.jpsychires.2010. 10.014
21. Golub, Y., Mauch, C. P., Dahlhoff, M., and Wotjak, C. T. (2009). Consequences of extinction training on associative and non-associative fear in a mouse model of Posttraumatic Stress Disorder (PTSD). Behav. Brain Res. 205, 544-549. doi: 10.1016/j.bbr.2009.08. 019
22. Jha, S. K., Brennan, F. X., Pawlyk, A. C., Ross, R. J., and Morrison, A. R. (2005). REM sleep: a sensitive index of fear conditioning in rats. Eur. J. Neurosci. 21, 1077-1080. doi: 10.1111/j.1460-9568.2005.03920.x
23. Joels, M., Fernandez, G., and Roozendaal, B. (2011). Stress and emotional memory: a matter of timing. Trends Cogn. Sci. 15, 280-288. doi: 10.1016/j.tics.2011.04. 004
24. Landeira-Fernandez, J., Kim, J. J., Decola, J. P., and Fanselow, M. S. (2006). Immediate shock deficit in fear conditioning: effects of shock manipulations. Behav. Neurosci. 120, 873-879. doi: 10.1037/0735-7044.120.4.873
25. Lanius, R. A., Williamson, P. C., Densmore, M., Boksman, K., Gupta, M. A., Neufeld, R. W., et al. (2001). Neural correlates of traumatic memories in posttraumatic stress disorder: a functional MRI investigation. Am. J. Psychiatry 158, 1920-1922. doi: 10.1176/appi.ajp. 158.11.1920
26. Lanius, R. A., Williamson, P. C., Hopper, J., Densmore, M., Boks-man, K., Gupta, M. A., et al. (2003). Recall of emotional states in posttraumatic stress disorder: an fMRI investigation. Biol. Psychiatry 53, 204-210. doi: 10.1016/s0006-3223(02)01466-x
27. Ledoux, J. E. (2000). Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155-184.
28. Mackintosh, N. J. (1965). Selective attention in animal discrimination learning. Psychol. Bull. 64, 124-150. doi: 10.1037/h0022347
29. Maren, S., Phan, K. L., and Liber-zon, I. (2013). The contextual brain: implications for fear conditioning, extinction and psychopathol-ogy. Nat. Rev. Neurosci. 14, 417-428. doi: 10.1038/nrn3492
30. North, C. S., Suris, A. M., Davis, M., and Smith, R. P. (2009). Toward validation of the diagnosis of posttrau-matic stress disorder. Am. J. Psychiatry 166, 34-41. doi: 10.1176/appi. ajp.2008.08050644
31. Pamplona, F. A., Henes, K., Micale, V., Mauch, C. P., Takahashi, R. N., and Wotjak, C. T. (2011). Prolonged fear incubation leads to generalized avoidance behavior in mice. J. Psychiatr. Res. 45, 354- 360. doi: 10.1016/j.jpsychires.2010. 06.015
32. Pawlyk, A. C., Jha, S. K., Brennan, F. X., Morrison, A. R., and Ross, R. J. (2005). A rodent model of sleep disturbances in posttraumatic stress disorder: the role of context after fear conditioning. Biol. Psychiatry 57, 268-277. doi: 10.1016/j. biopsych.2004.11.008
33. Pellow, S., Chopin, P., File, S. E., and Briley, M. (1985). Validation of open - closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods 14, 149-167. doi: 10.1016/0165-0270(85)90031-7
34. Pynoos, R. S., Ritzmann, R. F., Steinberg, A. M., Goenjian, A., and Prisecaru, I. (1996). A behavioral animal model of posttraumatic stress disorder featuring repeated exposure to situational reminders. Biol. Psychiatry 39, 129-134. doi: 10. 1016/0006-3223(95)00088-7
35. Quirarte, G. L., Roozendaal, B., and Mcgaugh, J. L. (1997). Glucocorti-coid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proc. Natl. Acad. Sci. U S A 94, 14048-14053. doi: 10.1073/pnas.94. 25.14048
36. Rescorla, R. A. (1968). Probability of shock in tresence and absence of Cs in fear conditioning. J. Comp. Physiol. Psychol. 66, 1-5. doi: 10. 1037/h0025984
37. Roozendaal, B., Nguyen, B. T., Power, A. E., and Mcgaugh, J. L. (1999). Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proc. Natl. Acad. Sci. U S A 96, 11642-11647. doi: 10.1073/pnas.96.20. 11642
38. Roozendaal, B., Quirarte, G. L., and Mcgaugh, J. L. (2002). Glucocor-ticoids interact with the basolat-eral amygdala beta-adrenoceptor- cAMP/cAMP/PKA system in influencing memory consolidation. Eur. J. Neurosci. 15, 553-560. doi: 10. 1046/j.0953-816x.2001.01876.x
39. Rougemont-Bucking, A., Linnman, C., Zeffiro, T. A., Zeidan, M. A., Lebron-Milad, K., Rodriguez-Romaguera, J., et al. (2011). Altered processing of contextual information during fear extinction in PTSD: an fMRI study. CNS Neurosci. Ther. 17, 227-236. doi: 10. 1111/j.1755-5949.2010.00152.x
40. Rudy, J. W., Huff, N. C., and Matus-Amat, P. (2004). Understanding contextual fear conditioning: insights from a two-process model. Neurosci. Biobehav. Rev. 28, 675-685. doi: 10.1016/j.neubiorev.2004. 09.004
41. Sanders, M. J., Wiltgen, B. J., and Fanselow, M. S. (2003). The place of the hippocampus in fear conditioning. Eur. J. Pharmacol. 463, 217-223. doi: 10.1016/S0014-2999(03) 01283-4
42. Sanford, L. D., Tang, X., Ross, R. J., and Morrison, A. R. (2003). Influence of shock training and explicit fear-conditioned cues on sleep architecture in mice: strain comparison. Behav. Genet. 33, 43-58. doi: 10. 1016/s0166-4328(03)00180-3
43. Shin, L. M., Rauch, S. L., and Pitman, R. K. (2006). Amygdala, medial prefrontal cortex, and hippocam-pal function in PTSD. Ann. N Y Acad. Sci. 1071, 67-79. doi: 10. 1196/annals.1364.007
44. Siegmund, A., and Wotjak, C. T. (2006). Toward an animal model of post-traumatic stress disorder. Ann. N Y Acad. Sci. 1071, 324-334. doi: 10. 1196/annals.1364.025
45. Siegmund, A., and Wotjak, C. T. (2007a). Hyperarousal does not depend on trauma-related contextual memory in an animal model of Posttraumatic Stress Disorder. Physiol. Behav. 90, 103-107. doi: 10.1016/j.physbeh.2006. 08.032
46. Siegmund, A., and Wotjak, C. T. (2007b). A mouse model of post-traumatic stress disorder that distinguishes between conditioned and sensitised fear. J. Psychiatr. Res. 41, 848-860. doi: 10.1016/j.jpsychires. 2006.07.017
47. Siegmund, A., Kaltwasser, S. F., Holsboer, F., Czisch, M., and Wotjak, C. T. (2009). Hippocampal N-acetylaspartate levels before trauma predict the development of long-lasting posttraumatic stress disorder-like symptoms in mice. Biol. Psychiatry 65, 258-262. doi: 10. 1016/j.biopsych.2008.08.023
48. Wall, P. M., and Messier, C. (2001). Methodological and conceptual issues in the use of the elevated plus-maze as a psychological measurement instrument of animal anxiety-like behavior. Neurosci.Biobehav. Rev. 25, 275-286. doi: 10. 1016/s0149-7634(01)00013-6
49. Williams, L. M., Kemp, A. H., Felmingham, K., Barton, M., Olivieri, G., Peduto, A., et al. (2006). Trauma modulates amygdala and medial prefrontal responses to consciously attended fear. Neuroimage 29, 347-357. doi: 10.1016/j.neuroimage.2005.03.047
50. Witvliet, C. V. (1997). Traumatic intrusive imagery as an emotional memory phenomenon: a review of research and explanatory information processing theories. Clin. Psychol. Rev. 17, 509-536. doi: 10.1016/s0272-7358(97)00025-1
51. Yehuda, R., and Antelman, S. M. (1993). Criteria for rationally evaluating animal models of posttrau-matic stress disorder. Biol. Psychiatry 33, 479-486. doi: 10.1016/0006-3223(93)90001-t