Acquisition and extinction of human avoidance behavior: Attenuating effect of safety signals and associations with anxiety vulnerabilities

Frontiers in Behavioral Neuroscience

Volumn 8, Issue SEP, 2014, Pages

  Sheynin, Jony ^a,b,c   Beck, Kevin D ^a,b,c   Servatius, Richard J ^a,b,c   Myers, Catherine E ^a,b,c  

^a DEPARTMENT OF VETERANS AFFAIRS   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Anxiety disorders; Anxiety vulnerability; Avoidance; Computer based task; Individual differences; Inhibited temperament; Safety signal; Sex differences

Indexed keywords

ADULT; ANXIETY DISORDER; ARTICLE; ASSOCIATION; AVOIDANCE BEHAVIOR; FEMALE; HUMAN; HUMAN EXPERIMENT; LEARNING; LOCOMOTION; MALE; NORMAL HUMAN; PREDICTION; QUESTIONNAIRE; REINFORCEMENT; SCORING SYSTEM; SEX DIFFERENCE; TASK PERFORMANCE;

EID: 84908157492     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00323     Document Type: Article

References (64)

1. Aguilar, M. A., Minarro, J., and Simon, V. M. (1998). Dose-dependent impairing effects of morphine on avoidance acquisition and performance in male mice. Neurobiol. Learn. Mem. 69, 92-105. doi:10.1006/nlme.1997.3804
2. American Psychiatric Association. (2000). Diagnostic and Statistical Manual of Mental Disorders: DSM-IV-TR, 4th Edn. Washington, DC: APA.
3. Arcediano, F., Ortega, N., and Matute, H. (1996). A behavioural preparation for the study of human Pavlovian conditioning. Q. J. Exp. Psychol. B 49, 270-283. doi:10.1080/713932633
4. Baeken, C., De Raedt, R., Ramsey, N., Van Schuerbeek, P., Hermes, D., Bossuyt, A., et al. (2009). Amygdala responses to positively and negatively valenced baby faces in healthy female volunteers: influences of individual differences in harm avoidance. Brain Res. 1296, 94-103. doi:10.1016/j.brainres.2009.08.010
5. Bailer, U. F., Frank, G. K., Price, J. C., Meltzer, C. C., Becker, C., Mathis, C. A., et al. (2013). Interaction between serotonin transporter and dopamine D2/D3 receptor radioligand measures is associated with harm avoidant symptoms in anorexia and bulimia nervosa. Psychiatry Res. 211, 160-168. doi:10.1016/j.pscychresns.2012.06.010
6. Balooch, S. B., Neumann, D. L., and Boschen, M. J. (2012). Extinction treatment in multiple contexts attenuates ABC renewal in humans. Behav. Res. Ther. 50, 604-609. doi:10.1016/j.brat.2012.06.003
7. Beatty, W. W., and Beatty, P. A. (1970). Hormonal determinants of sex differences in avoidance behavior and reactivity to electric shock in the rat. J. Comp. Physiol. Psychol. 73, 446-455. doi:10.1037/h0030216
8. Beck, K. D., Jiao, X., Pang, K. C., and Servatius, R. J. (2010). Vulnerability factors in anxiety determined through differences in active-avoidance behavior. Prog. Neuropsychopharmacol. Biol. Psychiatry 34, 852-860. doi:10.1016/j.pnpbp.2010.03.036
9. Beck, K. D., Jiao, X., Ricart, T. M., Myers, C. E., Minor, T. R., Pang, K. C., et al. (2011). Vulnerability factors in anxiety: strain and sex differences in the use of signals associated with non-threat during the acquisition and extinction of active- avoidance behavior. Prog. Neuropsychopharmacol. Biol. Psychiatry 35, 1659-1670. doi:10.1016/j.pnpbp.2011.05.002
10. Berger, D. F., and Brush, F. R. (1975). Rapid acquisition of discrete-trial lever-press avoidance: effects of signal-shock interval. J. Exp. Anal. Behav. 24, 227-239. doi:10.1901/jeab.1975.24-227
11. Berger, D. F., and Starzec, J. J. (1988). Contrasting lever-press avoidance behaviors of spontaneously hypertensive and normotensive rats (Rattus norvegicus). J. Comp. Psychol. 102, 279-286. doi:10.1037/0735-7036.102.3.279
12. Bolles, R. C., and Grossen, N. E. (1969). Effects of an informational stimulus on the acquisition of avoidance behavior in rats. J. Comp. Physiol. Psychol. 68, 90-99. doi:10.1037/h0027677
13. Bond, N. W. (1981). Effects of prenatal ethanol exposure on avoidance conditioning in high- and low-avoidance rat strains. Psychopharmacology (Berl.) 74, 177-181. doi:10.1007/BF00432689
14. Bower, G., Starr, R., and Lazarovitz, L. (1965). Amount of response-produced change in the CS and avoidance learning. J. Comp. Physiol. Psychol. 59, 13-17. doi:10.1037/h0021623
15. Brennan, F. X., Beck, K. D., and Servatius, R. J. (2003). Leverpress escape/avoidance conditioning in rats: safety signal length and avoidance performance. Integr. Physiol. Behav. Sci. 38, 36-44. doi:10.1007/BF02734259
16. Byron Nelson, J., and del Carmen Sanjuan, M. (2006). A context-specific latent inhibition effect in a human conditioned suppression task. Q. J. Exp. Psychol. (Hove) 59, 1003-1020. doi:10.1080/17470210500417738
17. Candido, A., Maldonado, A., and Vila, J. (1991). Effects of duration of feedback on signaled avoidance. Anim. Learn. Behav. 19, 81-87. doi:10.3758/BF03197863
18. Cloninger, C. R. (1986). A unified biosocial theory of personality and its role in the development of anxiety states. Psychiatr. Dev. 4, 167-226.
19. Cloninger, C. R. (1987). A systematic method for clinical description and classification of personality variants. A proposal. Arch. Gen. Psychiatry 44, 573-588. doi:10.1001/archpsyc.1987.01800180093014
20. Cloninger, C. R., Przybeck, T. R., and Svrakic, D. M. (1991). The tridimensional personality questionnaire: U.S. normative data. Psychol. Rep. 69, 1047-1057. doi:10.2466/PR0.69.7.1047-1057
21. D’Amato, M. R., and Fazzaro, J. (1966). Discriminated lever-press avoidance learning as a function of type and intensity of shock. J. Comp. Physiol. Psychol. 61, 313-315. doi:10.1037/h0023146
22. De Man, A., Dolan, D., Pelletier, R., and Reid, C. (1994). Adolescent running away behavior: active or passive avoidance? J. Gen. Psychol. 155, 59-64. doi:10.1080/00221325.1994.9914758
23. Denny, M. R., and Weisman, R. G. (1964). Avoidance behavior as a function of length of nonshock confinement. J. Comp. Physiol. Psychol. 58, 252-257. doi:10.1037/h0048966
24. Dillow, P. V., Myerson, J., Slaughter, L., and Hurwitz, H. M. B. (1972). Safety signals and the acquisition and extinction of lever-press discriminated avoidance in rats. Br. J. Psychol. 63, 583-591. doi:10.1111/j.2044-8295.1972.tb01311.x
25. Dubrovina, N. I., and Tomilenko, R. A. (2007). Characteristics of extinction of a conditioned passive avoidance reflex in mice with different levels of anxiety. Neurosci. Behav. Physiol. 37, 27-32. doi:10.1007/s11055-007-0145-x
26. Falls, W. A., and Davis, M. (1997). Inhibition of fear-potentiated startle can be detected after the offset of a feature trained in a serial feature-negative discrimination. J. Exp. Psychol. Anim. Behav. Process. 23, 3-14. doi:10.1037/0097-7403.23.1.3
27. Fernando, A. B., Urcelay, G. P., Mar, A. C., Dickinson, T. A., and Robbins, T. W. (2014). The role of the nucleus accumbens shell in the mediation of the reinforcing properties of a safety signal in free-operant avoidance: dopamine-dependent inhibitory effects of d-amphetamine. Neuropsychopharmacology 39, 1420-1430. doi:10.1038/npp.2013.337
28. Fernando, A. B., Urcelay, G. P., Mar, A. C., Dickinson, A., and Robbins, T. W. (2013). Comparison of the conditioned reinforcing properties of a safety signal and appetitive stimulus: effects of d-amphetamine and anxiolytics. Psychopharmacology (Berl.) 227, 195-208. doi:10.1007/s00213-012-2952-1
29. Galvani, P. F., and Twitty, M. T. (1978). Effects of intertrial interval and exteroceptive feedback duration on discriminative avoidance acquisition in the gerbil. Anim. Learn. Behav. 6, 166-173. doi:10.3758/BF03209596
30. Graham, B. M., and Milad, M. R. (2011). The study of fear extinction: implications for anxiety disorders. Am. J. Psychiatry 168, 1255-1265. doi:10.1176/appi.ajp.2011.11040557
31. Grossen, N. E., and Bolles, R. C. (1968). Effects of a classical conditioned "fear signal" and "safety signal" on nondiscriminated avoidance behavior. Psychon. Sci. 11, 321-322. doi:10.3758/BF03328212
32. Heinsbroek, R. P., van Oyen, H. G., van de Poll, N. E., and Boer, G. J. (1983). Failure of dexamethasone to influence sex differences in acquisition of discriminated lever press avoidance. Pharmacol. Biochem. Behav. 19, 599-604. doi:10.1016/0091-3057(83)90334-9
33. Hurwitz, H. M. B., Harzem, P., and Kulig, B. (1972). Comparisons of two measures of free-operant avoidance under two conditions of response feedback. Q. J. Exp. Psychol. 24, 92-97. doi:10.1080/14640747208400272
34. Jacobs, W. J., Moot, S. A., and Harris, C. (1983). Feedback stimuli and the extinction of avoidance responding in rats. Can. J. Psychol. 37, 557-564. doi:10.1037/h0080753
35. Jovanovic, T., Keyes, M., Fiallos, A., Myers, K. M., Davis, M., and Duncan, E. J. (2005). Fear potentiation and fear inhibition in a human fear-potentiated startle paradigm. Biol. Psychiatry 57, 1559-1564. doi:10.1016/j.biopsych.2005.02.025
36. Kagan, J., Reznick, J. S., and Gibbons, J. (1989). Inhibited and uninhibited types of children. Child Dev. 60, 838-845. doi:10.2307/1131025
37. Karamustafalioglu, O. K., Zohar, J., Guveli, M., Gal, G., Bakim, B., Fostick, L., et al. (2006). Natural course of posttraumatic stress disorder: a 20-month prospective study of Turkish earthquake survivors. J. Clin. Psychiatry 67, 882-889. doi:10.4088/JCP.v67n0604
38. Kuribara, H. (1982). Strain differences to the effects of central acting drugs on Sidman avoidance response in Wistar and Fischer 344 rats. Pharmacol. Biochem. Behav. 17, 425-429. doi:10.1016/0091-3057(82)90299-4
39. Li, C. R., Huang, C.-Y., Lin, W.-Y., and Sun, C.-W. V. (2007). Gender differences in punishment and reward sensitivity in a sample of Taiwanese college students. Pers. Individ. Dif. 43, 475-483. doi:10.1016/j.paid.2006.12.016
40. Mardaga, S., and Hansenne, M. (2007). Relationships between Cloninger’s biosocial model of personality and the behavioral inhibition/approach systems (BIS/BAS). Pers. Individ. Dif. 42, 715-722. doi:10.1016/j.paid.2006.08.013
41. McEvoy, P. M., and Mahoney, A. E. (2012). To be sure, to be sure: intolerance of uncertainty mediates symptoms of various anxiety disorders and depression. Behav. Ther. 43, 533-545. doi:10.1016/j.beth.2011.02.007
42. McLean, C. P., and Hope, D. A. (2010). Subjective anxiety and behavioral avoidance: gender, gender role, and perceived confirmability of self-report. J. Anxiety Disord. 24, 494-502. doi:10.1016/j.janxdis.2010.03.006
43. Molet, M., Leconte, C., and Rosas, J. M. (2006). Acquisition, extinction and temporal discrimination in human conditioned avoidance. Behav. Processes 73, 199-208. doi:10.1016/j.beproc.2006.05.009
44. Moscovitch, A., and LoLordo, V. M. (1968). Role of safety in the Pavlovian backward fear conditioning procedure. J. Comp. Physiol. Psychol. 66, 673-678. doi:10.1037/h0026548
45. Myers, K. M., and Davis, M. (2004). AX+, BX- discrimination learning in the fear- potentiated startle paradigm: possible relevance to inhibitory fear learning in extinction. Learn. Mem. 11, 464-475. doi:10.1101/lm.74704
46. Pfister, R. (2011). Gender effects in gaming research: a case for regression residuals? Cyberpsychol. Behav. Soc. Netw. 14, 603-606. doi:10.1089/cyber.2010.0547
47. Pigott, T. A. (1999). Gender differences in the epidemiology and treatment of anxiety disorders. J. Clin. Psychiatry 60(Suppl. 18), 4-15.
48. Pollak, D. D., Rogan, M. T., Egner, T., Perez, D. L., Yanagihara, T. K., and Hirsch, J. (2010). A translational bridge between mouse and human models of learned safety. Ann. Med. 42, 115-122. doi:10.3109/07853890903583666
49. Rachman, S. (1984). Agoraphobia - a safety-signal perspective. Behav. Res. Ther. 22, 59-70. doi:10.1016/0005-7967(84)90033-0
50. Roberts, A. E., Greenway, L., and Hurwitz, H. M. B. (1970). Extinction of free- operant avoidance with and without feedback. Psychon. Sci. 20, 283-285. doi:10.3758/BF03329068
51. Sartory, G., Master, D., and Rachman, S. (1989). Safety-signal therapy in agoraphobics: a preliminary test. Behav. Res. Ther. 27, 205-209. doi:10.1016/0005-7967(89)90081-8
52. Schiller, D., Levy, I., Niv, Y., LeDoux, J. E., and Phelps, E. A. (2008). From fear to safety and back: reversal of fear in the human brain. J. Neurosci. 28, 11517-11525. doi:10.1523/JNEUROSCI.2265-08.2008
53. Scouten, C. W., Groteleuschen, L. K., and Beatty, W. W. (1975). Androgens and the organization of sex differences in active avoidance behavior in the rat. J. Comp. Physiol. Psychol. 88, 264-270. doi:10.1037/h0076184
54. Seligman, M. E., and Johnston, J. C. (1973). "A cognitive theory of avoidance learning," in Contemporary Approaches to Conditioning and Learning, eds F. J. McGuigan and D. B. Lumsden (Washington, DC: Winston), 69-110.
55. Servatius, R. J., Jiao, X., Beck, K. D., Pang, K. C., and Minor, T. R. (2008). Rapid avoidance acquisition in Wistar-Kyoto rats. Behav. Brain Res. 192, 191-197. doi:10.1016/j.bbr.2008.04.006
56. Sheynin, J., Beck, K. D., Pang, K. C., Servatius, R. J., Shikari, S., Ostovich, J., et al. (2014a). Behaviourally inhibited temperament and female sex, two vulnerability factors for anxiety disorders, facilitate conditioned avoidance (also) in humans. Behav. Processes 103, 228-235.doi:10.1016/j.beproc.2014.01.003
57. Sheynin, J., Moustafa, A. A., Beck, K. D., Servatius, R. J., Casbolt, P. A., Haber, P., et al. (2014b). Exaggerated acquisition and resistance to extinction of avoidance behavior in treated heroin-dependent males (but not females). Soc. Neurosci. Annu. Meet. Session 262.21/RR12 [abstract].
58. Sheynin, J., Shikari, S., Gluck, M. A., Moustafa, A. A., Servatius, R. J., and Myers, C. E. (2013). Enhanced avoidance learning in behaviorally inhibited young men and women. Stress 16, 289-299. doi:10.3109/10253890.2012.744391
59. Sutterer, J. R., Perry, J., and DeVito, W. (1980). Two-way shuttle box and lever-press avoidance in the spontaneously hypertensive and normotensive rat. J. Comp. Physiol. Psychol. 94, 155-163. doi:10.1037/h0077649
60. van den Bos, R., Jolles, J., van der Knaap, L., Baars, A., and de Visser, L. (2012). Male and female Wistar rats differ in decision-making performance in a rodent version of the Iowa gambling task. Behav. Brain Res. 234, 375-379. doi:10.1016/j.bbr.2012.07.015
61. Van Oyen, H. G., Walg, H., and Van De Poll, N. E. (1981). Discriminated lever press avoidance conditioning in male and female rats. Physiol. Behav. 26, 313-317. doi:10.1016/0031-9384(81)90028-7
62. Weisman, R. G., and Litner, J. S. (1969). Positive conditioned reinforcement of Sidman avoidance behavior in rats. J. Comp. Physiol. Psychol. 68, 597-603. doi:10.1037/h0027682
63. Wilson, R. S., Boyle, P. A., Buchman, A. S., Yu, L., Arnold, S. E., and Bennett, D. A. (2011). Harm avoidance and risk of Alzheimer’s disease. Psychosom. Med. 73, 690-696. doi:10.1097/PSY.0b013e3182302ale
64. Zinbarg, R. E., Barlow, D. H., Brown, T. A., and Hertz, R. M. (1992). Cognitive- behavioral approaches to the nature and treatment of anxiety disorders. Annu. Rev. Psychol. 43, 235-267. doi:10.1146/annurev.ps.43.020192.001315