Fear but not fright: Re-evaluating traumatic experience attenuates anxiety-like behaviors after fear conditioning

Frontiers in Behavioral Neuroscience

Volumn 8, Issue AUG, 2014, Pages

  Costanzi, Marco ^a,b   Saraulli, Daniele ^a,c   Cannas, Sara ^a   D'Alessandro, Francesca ^a,b   Florenzano, Fulvio ^d   Rossi Arnaud, Clelia ^c   Cestari, Vincenzo ^a,e  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b LUMSA UNIVERSITY   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^e SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Amygdala; Contextual fear conditioning; Fear reinstatement; Fear sensitization; Lateral orbitofrontal cortex; Spontaneous recovery

Indexed keywords

PROTEIN C FOS;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; AVERSIVE BEHAVIOR; BEHAVIOR CHANGE; CONDITIONING; CONTROLLED STUDY; ELECTRIC SHOCK; FEAR; FOOTSHOCK; LEARNING DISORDER; LIFE STRESS; MALE; MAZE TEST; MOUSE; NONHUMAN; ORBITAL CORTEX; PAIN THRESHOLD; PROTEIN EXPRESSION; SOCIAL AVOIDANCE BEHAVIOR;

EID: 84930341879     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00279     Document Type: Article

References (58)

1. Amstadter, A. (2008). Emotion regulation and anxiety disorders. J. Anxiety Dis. 22, 211-221. doi: 10.1016/j.janxdis.2007.02.004
2. Beck, C. H. M., and Fibiger, H. C. (1995). Conditioned fear-induced changes in behavior and in the expression of the immediate early gene c-fos: with and without diazepam pretreatment. J. Neurosci. 15, 709-720.
3. Bouton, M. E. (2004). Context and behavioral processes in extinction. Learn. Mem. 11, 485-494. doi: 10.1101/lm.78804
4. Ciocchi, S., Herry, C., Grenier, F., Wolff, S. B., Letzkus, J. J., Vlachos, I., et al. (2010). Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 468, 277-282. doi: 10.1038/nature09559
5. 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. doi: 10.1016/s0006-3223(02)01909-1
6. Costanzi, M., Cannas, S., Saraulli, D., Rossi-Arnaud, C., and Cestari, V. (2011). Extinction after retrieval: effects on the associative and nonassociative components of remote contextual fear memory. Learn. Mem. 18, 508-518. doi: 10.1101/lm.2175811
7. Davey, G. C. L. (1983). "An associative view of human classical conditioning, " in Animal Models of Human Behaviour, ed G. C. L. Davey (Chichester: Wiley), 95-114.
8. Davey, G. C. L. (1987). "The integration of human and animal models of Pavlovian conditioning: associations, cognitions and attributions, " in Cognitive Processes and Pavlovian Conditioning in Humans, ed G. C. L. Davey (Chichester: Wiley), 83-114.
9. Davey, G. C. L. (1989). UCS revaluation and conditioning models of acquired fears. Behav. Res. Ther. 27, 521-528. doi: 10.1016/0005-7967(89)90086-7
10. Davey, G. C. L., De Jong, P. J., and Tallis, F. (1993). UCS inflation in the aetiology of a variety of anxiety disorders: some case histories. Behav. Res. Ther. 31, 495-498. doi: 10.1016/0005-7967(93)90130-m
11. Delamater, A. R. (2007). The role of the orbitofrontal cortex in sensory-specific encoding of associations in pavlovian and instrumental conditioning. Ann. N Y Acad. Sci. 1121, 152-173. doi: 10.1196/annals.1401.030
12. Ehrlich, I., Humeau, Y., Grenier, F., Ciocchi, S., Herry, C., and Lüthi, A. (2009). Amygdala inhibitory circuits and the control of fear memory. Neuron 62, 757-771. doi: 10.1016/j.neuron.2009.05.026
13. Franklin, K. B. J., and Paxinos, G. (1997). The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press.
14. Gallagher, M., McMahan, R. W., and Schoenbaum, G. (1999). Orbitofrontal cortex and representation of incentive value in associative learning. J. Neurosci. 19, 6610-6614.
15. 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
16. Greenberg, N., and Wessely, S. (2009). The dangers of inflation: memories of trauma and post-traumatic stress disorder. Br. J. Psychiatry 194, 479-480. doi: 10.1192/bjp.bp.109.063586
17. Grillon, C. (2002). Startle reactivity and anxiety disorders: aversive conditioning, context and neurobiology. Biol. Psychiatry 52, 958-975. doi: 10.1016/s0006-3223(02)01665-7
18. Harris, J. D. (1943). Studies on nonassociative factors inherent in conditioning. Comm. Psychol. Monogr. 18, 1-74.
19. Hartley, C. A., and Phelps, E. A. (2010). Changing fear: the neurocircuitry of emotion regulation. Neuropsychopharmacology 35, 136-146. doi: 10.1038/npp.2009.121
20. Haubensak, W., Kunwar, P. S., Cai, H., Ciocchi, S., Wall, N. R., Ponnusamy, R., et al. (2010). Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 468, 270-276. doi: 10.1038/nature09553
21. Heir, T., Piatigorsky, A., and Weisaeth, L. (2009). Longitudinal changes in recalled perceived life threat after a natural disaster. Br. J. Psychiatry 194, 510-514. doi: 10.1192/bjp.bp.108.056580
22. Hosoba, T., Iwanaga, M., and Seiwa, H. (2001). The effect of UCS inflation and deflation procedures on 'fear' conditioning. Behav. Res. Ther. 39, 465-475. doi: 10.1016/s0005-7967(00)00025-5
23. Huh, K. H., Guzman, Y. F., Tronson, N. C., Guedea, A. L., Gao, C., and Radulovic, J. (2009). Hippocampal Erk mechanisms linking prediction error to fear extinction: roles of shock expectancy and contextual aversive valence. Learn. Mem. 16, 273-278. doi: 10.1101/lm.1240109
24. Jeffries, F. W., and Davis, P. (2013). What is the role of eye movements in eye movement desensitization and reprocessing (EMDR) for post-traumatic stress disorder (PTSD)? a review. Behav. Cogn. Psychother. 41, 290-300. doi: 10.1017/s1352465812000793
25. Kamprath, K., and Wotjak, C. T. (2004). Nonassociative learning processes determine expression and extinction of conditioned fear in mice. Learn. Mem. 11, 770-786. doi: 10.1101/lm.86104
26. Kehoe, E. J., and White, N. E. (2002). Extinction revisited: similarities between extinction and reductions in US intensity in classical conditioning of the rabbit's nictitating membrane response. Anim. Learn. Behav. 30, 96-111. doi: 10.3758/bf03192912
27. Kindt, M., Soeter, M., and Vervliet, B. (2009). Beyond extinction: erasing human fear responses and preventing the return of fear. Nat. Neurosci. 12, 256-258. doi: 10.1038/nn.2271
28. Knapska, E., and Maren, S. (2009). Reciprocal patterns of c-Fos expression in the medial prefrontal cortex and amygdala after extinction and renewal of conditioned fear. Learn. Mem. 16, 486-493. doi: 10.1101/lm.1463909
29. Kohda, K., Harada, K., Kato, K., Hoshino, A., Motohashi, J., Yamaji, T., et al. (2007). Glucocorticoid receptor activation is involved in producing abnormal phenotypes of single-prolonged stress rats: a putative post-traumatic stress disorder model. Neuroscience 148, 22-33. doi: 10.1016/j.neuroscience.2007.05.041
30. Lissek, S. (2012). Toward an account of clinical anxiety predicated on basic, neurally mapped mechanisms of Pavlovian fear-learning: the case for conditioned overgeneralization. Depress. Anxiety 29, 257-263. doi: 10.1002/da.21922
31. Louvart, H., Maccari, S., Ducrocq, F., Thomas, P., and Darnaudèry, M. (2005). Long-term behavioural alterations in female rats after a single intense footshock followed by situational reminders. Psychoneuroendocrinology 30, 316-324. doi: 10.1016/j.psyneuen.2004.09.003
32. Mahan, A. L., and Ressler, K. J. (2012). Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder. Trends Neurosci. 35, 24-35. doi: 10.1016/j.tins.2011.06.007
33. Marcia, J. E., Rubin, B. M., and Efran, J. S. (1969). Systematic desensitization: expectancy change or counterconditioning? J. Abnorm. Psychol. 74, 382-387. doi: 10.1037/h0027596
34. Maren, S. (2011). Seeking a spotless mind: extinction, deconsolidation and erasure of fear memory. Neuron 70, 830-845. doi: 10.1016/j.neuron.2011.04.023
35. Milekic, M. H., and Alberini, C. M. (2002). Temporally graded requirement for protein synthesis following memory reactivation. Neuron 36, 521-525. doi: 10.1016/s0896-6273(02)00976-5
36. Monfils, M.-H., Cowansage, K. K., Klann, E., and LeDoux, J. E. (2009). Extinction-reconsolidation boundaries: key to persistent attenuation of fear memories. Science 324, 951-955. doi: 10.1126/science.1167975
37. Otte, C. (2011). Cognitive behavioral therapy in anxiety disorders: current state of the evidence. Dialogues Clin. Neurosci. 13, 413-421.
38. Pare, D., and Duvarci, S. (2012). Amygdala microcircuits mediating fear expression and extinction. Curr. Opin. Neurobiol. 22, 717-723. doi: 10.1016/j.conb.2012.02.014
39. Pickens, C. L., Saddoris, M. P., Gallagher, M., and Holland, P. C. (2005). Orbitofrontal lesions impair use of cue-outcome associations in a devaluation task. Behav. Neurosci. 119, 317-322. doi: 10.1037/0735-7044.119.1.317
40. Pickens, C. L., Saddoris, M. P., Setlow, B., Gallagher, M., Holland, P. C., and Schoenbaum, G. (2003). Different roles for orbitofrontal cortex and basolateral amygdala in a reinforcer devaluation task. J. Neurosci. 23, 11078-11084.
41. Pitkänen, A., Savander, V., and LeDoux, J. E. (1997). Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala. Trends Neurosci. 20, 517-523. doi: 10.1016/s0166-2236(97)01125-9
42. Poulos, A. M., Li, V., Sterlace, S. S., Tokushige, F., Ponnusamy, R., and Fanselow, M. S. (2009). Persistence of fear memory across time requires the basolateral amygdala complex. Proc. Natl. Acad. Sci. U S A 106, 11737-11741. doi: 10.1073/pnas.0905257106
43. Prut, L., and Belzung, C. (2003). The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol. 463, 3-33. doi: 10.1016/s0014-2999(03)01272-x
44. Quirk, G. J., and Milad, R. M. (2010). Editing out fear. Nature 463, 36-37. doi: 10.1038/463036a
45. Rescorla, R. A. (1973). Effect of us habituation following conditioning. J. Comp. Physiol. Psychol. 82, 137-143. doi: 10.1037/h0033815
46. Rescorla, R. A., and Heth, C. D. (1975). Reinstatement of fear to an extinguished conditioned stimulus. J. Exp. Psychol. Anim. Behav. Process. 1, 88-96. doi: 10.1037//0097-7403.1.1.88
47. Schiller, D., Monfils, M.-H., Raio, C. M., Johnson, D. C., LeDoux, J. E., and Phelps, E. A. (2010). Preventing the return of fear in humans using reconsolidation update mechanisms. Nature 463, 49-53. doi: 10.1038/nature08637
48. Shalev, A. Y., Peri, T., Brandes, D., Orr, S. P., and Pitman, R. K. (2000). Auditory startle response in trauma survivors with posttraumatic stress disorder: a prospective study. Am. J. Psychiatry 157, 255-261. doi: 10.1176/appi.ajp.157.2.255
49. Siegmund, A., and Wotjak, C. T. (2006). Toward an animal model of posttraumatic stress disorder. Ann. N Y Acad. Sci. 1071, 324-334. doi: 10.1196/annals.1364.025
50. Siegmund, A., and Wotjak, C. T. (2007a). A mouse model of posttraumatic stress disorder that distinguishes between conditioned and sensitised fear. J. Psychiatr. Res. 41, 848-860. doi: 10.1016/j.jpsychires.2006.07.017
51. Siegmund, A., and Wotjak, C. T. (2007b). 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
52. Tye, K. M., Prakash, R., Kim, S. Y., Fenno, L. E., Grosenick, L., Zarabi, H., et al. (2011). Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471, 358-362. doi: 10.1038/nature09820
53. van den Hout, M. A., Bartelski, N., and Engelhard, I. M. (2013). On EMDR: eye movements during retrieval reduce subjective vividness and objective memory accessibility during future recall. Cogn. Emot. 27, 177-183. doi: 10.1080/02699931.2012.691087
54. West, E. A., DesJardin, J. T., Gale, K., and Malkova, L. (2011). Transient inactivation oforbitofrontal cortex blocks reinforcer devaluation in macaques. J. Neurosci. 31, 15128-15135. doi: 10.1523/jneurosci.3295-11.2011
55. West, E. A., Forcelli, P. A., McCue, D. L., and Malkova, L. (2013). Differential effects of serotonin-specific and excitotoxic lesions of OFC on conditioned reinforcer devaluation and extinction in rats. Behav. Brain Res. 246, 10-14. doi: 10.1016/j.bbr.2013.02.027
56. White, K., and Davey, G. C. L. (1989). Sensory preconditioning and UCS inflation in human fear conditioning. Behav. Res. Ther. 27, 161-166. doi: 10.1016/0005-7967(89)90074-0
57. Wilson, R. C., Takahashi, Y. K., Schoenbaum, G., and Niv, Y. (2014). Orbitofrontal cortex as a cognitive map of task space. Neuron 81, 267-279. doi: 10.1016/j.neuron.2013.11.005
58. Zantvoord, J. B., Diehle, J., and Lindauer, R. J. (2013). Using neurobiological measures to predict and assess treatment outcome of psychotherapy in posttraumatic stress disorder: systematic review. Psychother. Psychosom.82, 142-151. doi: 10.1159/000343258