Not all stressors are equal: Behavioural and endocrine evidence for development of contextual fear conditioning after a single session of footshocks but not of immobilization

Frontiers in Behavioral Neuroscience

Volumn , Issue OCTOBER 2012, 2012, Pages 1-19

  Daviu, Núria ^a   Delgado Morales, Raúl ^a,b   Nadal, Roser ^a   Armario, Antonio ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

Contextual fear conditioning; Foot shock; Freezing; Hypothalamic pituitary adrenal axis; Immobilization; Stress

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN;

ANIMAL EXPERIMENT; ARTICLE; AVERSION; BEHAVIOR CHANGE; CONDITIONING; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOTROPIN BLOOD LEVEL; ENVIRONMENTAL EXPOSURE; FEAR; FOOTSHOCK; FREEZING; HABITUATION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION; LONG TERM CARE; MALE; MOTOR ACTIVITY; NONHUMAN; OPEN FIELD TEST; OUTCOME ASSESSMENT; RAT; SHORT COURSE THERAPY; STIMULUS RESPONSE;

EID: 84867621448     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2012.00069     Document Type: Article

References (58)

1. Adamec, R. E., and Shallow, T. (1993). Lasting effects on rodent anxiety of a single exposure to a cat. Physiol Behav 54, 101-109.
2. Andero, R., Heldt, S. A., Ye, K., Liu, X., Armario, A., and Ressler, K. J. (2011). Effect of 7,8-dihydroxyflavone, a small-molecule TrkB agonist, on emotional learning. Am J Psychiatry 168, 163-172.
3. Andero, R., Daviu, N., Escorihuela, R. M., Nadal, R., and Armario, A. (2012). 7,8-dihydroxyflavone, a TrkB receptor agonist, blocks long-term spatial memory impairment caused by immobilization stress in rats. Hippocampus 22, 399-408.
4. Antoniadis, E. A., and McDonald, R. J. (1999). Discriminative fear conditioning to context expressed by multiple measures of fear in the rat. Behav Brain Res 101, 1-13.
5. Armario, A. (2006). The hypothalamic-pituitary-adrenal axis: what can it tell us about stressors? CNS Neurol Disord Drug Targets 5, 485-501.
6. Armario, A., Escorihuela, R. M., and Nadal, R. (2008). Long-term neuroendocrine and behavioural effects of a single exposure to stress in adult animals. Neurosci Biobehav Rev 32, 1121-1135.
7. Armario, A., Daviu, N., Muñoz-Abellán, C., Rabasa, C., Fuentes, S., Belda, X., Gagliano, H., and Nadal, R. (2012). What can We Know from Pituitary-Adrenal Hormones About the Nature and Consequences of Exposure to Emotional Stressors? Cell Mol Neurobiol.
8. Belda, X., Márquez, C., and Armario, A. (2004). Long-term effects of a single exposure to stress in adult rats on behavior and hypothalamic-pituitary-adrenal responsiveness: comparison of two outbred rat strains. Behav Brain Res 154, 399-408.
9. Belda, X., Fuentes, S., Nadal, R., and Armario, A. (2008). A single exposure to immobilization causes long-lasting pituitary-adrenal and behavioral sensitization to mild stressors. Horm Behav 54, 654-661.
10. Blanchard, R. J., Yang, M., Li, C. I., Gervacio, A., and Blanchard, D. C. (2001). Cue and context conditioning of defensive behaviors to cat odor stimuli. Neurosci Biobehav Rev 25, 587-595.
11. Blanchard, D. C., Markham, C., Yang, M., Hubbard, D., Madarang, E., and Blanchard, R. J. (2003). Failure to produce conditioning with low-dose trimethylthiazoline or cat feces as unconditioned stimuli. Behav Neurosci 117, 360-368.
12. Campeau, S., Falls, W. A., Cullinan, W. E., Helmreich, D. L., Davis, M., and Watson, S. J. (1997). Elicitation and reduction of fear: behavioural and neuroendocrine indices and brain induction of the immediate-early gene c-fos. Neuroscience 78, 1087-1104.
13. Cohen, H., Zohar, J., and Matar, M. (2003). The relevance of differential response to trauma in an animal model of posttraumatic stress disorder. Biol Psychiatry 53, 463-473.
14. Davis, M. (1990). Animal models of anxiety based on classical conditioning: the conditioned emotional response (CER) and the fear-potentiated startle effect. Pharmacol Ther 47, 147-165.
15. Daviu, N., Fuentes, S., Nadal, R., and Armario, A. (2010). A single footshock causes long-lasting hypoactivity in unknown environments that is dependent on the development of contextual fear conditioning. Neurobiol Learn Mem 94, 183-190.
16. de Quervain, D. J., Aerni, A., Schelling, G., and Roozendaal, B. (2009). Glucocorticoids and the regulation of memory in health and disease. Front Neuroendocrinol 30, 358-370.
17. Dielenberg, R. A., Arnold, J. C., and McGregor, I. S. (1999). Low-dose midazolam attenuates predatory odor avoidance in rats. Pharmacol Biochem Behav 62, 197-201.
18. Dielenberg, R. A., Carrive, P., and McGregor, I. S. (2001). The cardiovascular and behavioral response to cat odor in rats: unconditioned and conditioned effects. Brain Res 897, 228-237.
19. Engeland, W. C., Miller, P., and Gann, D. S. (1989). Dissociation between changes in plasma bioactive and immunoreactive adrenocorticotropin after hemorrhage in awake dogs. Endocrinology 124, 2978-2985.
20. Fanselow, M. S. (1980). Conditioned and unconditional components of post-shock freezing. Pavlov J Biol Sci 15, 177-182.
21. Fleshner, M., Deak, T., Spencer, R. L., Laudenslager, M. L., Watkins, L. R., and Maier, S. F. (1995). A long-term increase in basal levels of corticosterone and a decrease in corticosteroid-binding globulin after acute stressor exposure. Endocrinology 136, 5336-5342.
22. Gao, Y., Han, H., Xu, R., Cao, J., Luo, J., and Xu, L. (2008). Effects of prolonged exposure to context following contextual fear conditioning on synaptic properties in rat hippocampal slices. Neurosci Res 61, 385-389.
23. García, J., and Koelling, R. A. (1966). Relation of the cue to consequence in avoidance learning. Psychonom Sci 4, 123-124.
24. García, A., Martí, O., Vallès, A., Dal-Zotto, S., and Armario, A. (2000). Recovery of the hypothalamic-pituitary-adrenal response to stress. Effect of stress intensity, stress duration and previous stress exposure. Neuroendocrinology 72, 114-125.
25. Grahn, R. E., Kalman, B. A., Brennan, F. X., Watkins, L. R., and Maier, S. F. (1995). The elevated plus-maze is not sensitive to the effect of stressor controllability in rats. Pharmacol Biochem Behav 52, 565-570.
26. Hardin, J. W., and Hilbe, J. M. (2003). Generalized estimating equations. Boca Raton: Chapman & Hall/CRC.
27. Kamprath, K., and Wotjak, C. T. (2004). Nonassociative learning processes determine expression and extinction of conditioned fear in mice. Learn Mem 11, 770-786.
28. Katz, R. J., Roth, K. A., and Carroll, B. J. (1981). Acute and chronic stress effects on open field activity in the rat: implications for a model of depression. Neurosci Biobehav Rev 5, 247-251.
29. Laxmi, T. R., Stork, O., and Pape, H. C. (2003). Generalisation of conditioned fear and its behavioural expression in mice. Behav Brain Res 145, 89-98.
30. Maier, S. F. (1984). Learned helplessness and animal models of depression. Prog Neuropsychopharmacol Biol Psychiatry 8, 435-446.
31. Maier, S. F., Ryan, S. M., Barksdale, C. M., and Kalin, N. H. (1986). Stressor controllability and the pituitary-adrenal system. Behav Neurosci 100, 669-674.
32. Manion, S. T., Gamble, E. H., and Li, H. (2007). Prazosin administered prior to inescapable stressor blocks subsequent exaggeration of acoustic startle response in rats. Pharmacol Biochem Behav 86, 559-565.
33. Maren, S., DeCola, J. P., and Fanselow, M. S. (1994). Water deprivation enhances fear conditioning to contextual, but not discrete, conditional stimuli in rats. Behav Neurosci 108, 645-649.
34. Márquez, C., Belda, X., and Armario, A. (2002). Post-stress recovery of pituitary-adrenal hormones and glucose, but not the response during exposure to the stressor, is a marker of stress intensity in highly stressful situations. Brain Res 926, 181-185.
35. Márquez, C., Nadal, R., and Armario, A. (2005). Responsiveness of the hypothalamic-pituitary-adrenal axis to different novel environments is a consistent individual trait in adult male outbred rats. Psychoneuroendocrinology 30, 179-187.
36. Martí, O., Garcia, A., Valles, A., Harbuz, M. S., and Armario, A. (2001). Evidence that a single exposure to aversive stimuli triggers long-lasting effects in the hypothalamus-pituitary-adrenal axis that consolidate with time. Eur J Neurosci 13, 129-136.
37. McCulloch, C., and Searle, S. (2001). Generalized, linear and mixed models. New York: Wiley and Sons.
38. McGregor, I. S., and Dielenberg, R. A. (1999). Differential anxiolytic efficacy of a benzodiazepine on first versus second exposure to a predatory odor in rats. Psychopharmacology (Berl) 147, 174-181.
39. McNally, R. J. (1998). Experimental approaches to cognitive abnormality in posttraumatic stress disorder. Clin Psychol Rev 18, 971-982.
40. Merino, J. J., Cordero, M. I., and Sandi, C. (2000). Regulation of hippocampal cell adhesion molecules NCAM and L1 by contextual fear conditioning is dependent upon time and stressor intensity. Eur J Neurosci 12, 3283-3290.
41. Moore, S. A. (2009). Cognitive abnormalities in posttraumatic stress disorder. Curr Opin Psychiatry 22, 19-24.
42. Morrow, B. A., Redmond, A. J., Roth, R. H., and Elsworth, J. D. (2000). The predator odor, TMT, displays a unique, stress-like pattern of dopaminergic and endocrinological activation in the rat. Brain Res 864, 146-151.
43. Muñoz-Abellán, C., Andero, R., Nadal, R., and Armario, A. (2008). Marked dissociation between hypothalamic-pituitary-adrenal activation and long-term behavioral effects in rats exposed to immobilization or cat odor. Psychoneuroendocrinology 33, 1139-1150.
44. Muñoz-Abellán, C., Daviu, N., Rabasa, C., Nadal, R., and Armario, A. (2009). Cat odor causes long-lasting contextual fear conditioning and increased pituitary-adrenal activation, without modifying anxiety. Horm Behav 56, 465-471.
45. Muñoz-Abellán, C., Rabasa, C., Daviu, N., Nadal, R., and Armario, A. (2011). Behavioral and endocrine consequences of simultaneous exposure to two different stressors in rats: interaction or independence? PLoS One 6, e21426.
46. Pol, O., Campmany, L., Gil, M., and Armario, A. (1992). Behavioral and neurochemical changes in response to acute stressors: influence of previous chronic exposure to immobilization. Pharmacol Biochem Behav 42, 407-412.
47. Radulovic, J., Kammermeier, J., and Spiess, J. (1998). Generalization of fear responses in C57BL/6N mice subjected to one-trial foreground contextual fear conditioning. Behav Brain Res 95, 179-189.
48. Rau, V., DeCola, J. P., and Fanselow, M. S. (2005). Stress-induced enhancement of fear learning: an animal model of posttraumatic stress disorder. Neurosci Biobehav Rev 29, 1207-1223.
49. Reinstein, D. K., Lehnert, H., Scott, N. A., and Wurtman, R. J. (1984). Tyrosine prevents behavioral and neurochemical correlates of an acute stress in rats. Life Sci 34, 2225-2231.
50. Rudy, J. W. (1993). Contextual conditioning and auditory cue conditioning dissociate during development. Behav Neurosci 107, 887-891.
51. Sandi, C., and Pinelo-Nava, M. T. (2007). Stress and memory: behavioral effects and neurobiological mechanisms. Neural Plast 2007, 78970.
52. Seligman, M. E. P. (1971). Phobias and preparedness. Behav Ther 2, 307-320.
53. Servatius, R. J., Ottenweller, J. E., and Natelson, B. H. (1995). Delayed startle sensitization distinguishes rats exposed to one or three stress sessions: further evidence toward an animal model of PTSD. Biol Psychiatry 38, 539-546.
54. Takahashi, L. K., Chan, M. M., and Pilar, M. L. (2008). Predator odor fear conditioning: current perspectives and new directions. Neurosci Biobehav Rev 32, 1218-1227.
55. Vahl, T. P., Ulrich-Lai, Y. M., Ostrander, M. M., Dolgas, C. M., Elfers, E. E., Seeley, R. J., D'Alessio, D. A., and Herman, J. P. (2005). Comparative analysis of ACTH and corticosterone sampling methods in rats. Am J Physiol Endocrinol Metab 289, E823-828.
56. Vallés, A., Martí, O., García, A., and Armario, A. (2000). Single exposure to stressors causes long-lasting, stress-dependent reduction of food intake in rats. Am J Physiol Regul Integr Comp Physiol 279, R1138-1144.
57. Van de Kar, L. D., Piechowski, R. A., Rittenhouse, P. A., and Gray, T. S. (1991). Amygdaloid lesions: differential effect on conditioned stress and immobilization-induced increases in corticosterone and renin secretion. Neuroendocrinology 54, 89-95.
58. Van den Berg, C. L., Lamberts, R. R., Wolterink, G., Wiegant, V. M., and Van Ree, J. M. (1998). Emotional and footshock stimuli induce differential long-lasting behavioural effects in rats; involvement of opioids. Brain Res 799, 6-15.