Heterogeneity in signaled active avoidance learning: Substantive and methodological relevance of diversity in instrumental defensive responses to threat cues

Frontiers in Systems Neuroscience

Volumn 8, Issue SEP, 2014, Pages

  Galatzer Levy, Isaac R ^a   Moscarello, Justin ^b   Blessing, Esther M ^a   Klein, JoAnna ^b   Cain, Christopher K ^a,b,c   LeDoux, Joseph E ^b,c  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c Nathan Klein Institute   (United States)

Author keywords

Fear conditioning; Heterogeneity; Latent growth mixture modeling; Posttraumatic Stress Disorder (PTSD); Resilience; Signaled active avoidance; Threat conditioning

Indexed keywords

ACCLIMATIZATION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; COPING BEHAVIOR; DEFENSIVE BEHAVIOR; EXPLORATORY BEHAVIOR; FEAR; HABITUATION; INSTRUMENTAL CONDITIONING; INSTRUMENTAL DEFENSIVE RESPONSE; LATENT GROWTH MIXTURE MODELING; MALE; NONHUMAN; PHENOTYPE; POST HOC ANALYSIS; POSTTRAUMATIC STRESS DISORDER; RAT; THREAT; TRAINING; TWO-WAY ACTIVE AVOIDANCE TEST;

EID: 84907581486     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2014.00179     Document Type: Article

References (62)

1. Andero, R., Brothers, S. P., Jovanovic, T., Chen, Y. T., Salah-Uddin, H., Cameron, M., et al. (2013). Amygdala-dependent fear is regulated by Oprl1 in mice and humans with PTSD. Sci. Transl. Med. 5, 188ra173. doi: 10.1126/sci-translmed.3005656
2. Blanchard, R. J., and Blanchard, D. C. (1969). Passive and active reactions to fear-eliciting stimuli. J. Comp. Physiol. Psychol. 68, 129. doi: 10.1037/h0027676
3. Bonanno, G. A. (2004). Loss, trauma, and human resilience: have we underestimated the human capacity to thrive after extremely aversive events? Am. Psychol. 59, 20-28. doi: 10.1037/0003-066X.59.1.20
4. Bonanno, G. A., and Burton, C. L. (2013). Regulatory flexibility an individual differences perspective on coping and emotion regulation. Perspect. Psychol. Sci. 8, 591-612. doi: 10.1177/1745691613504116
5. Bonanno, G. A., Kennedy, P., Galatzer-Levy, I. R., Lude, P., and Elfstom, M. L. (2012a). Trajectories of resilience, depression, and anxiety following spinal cord injury. Rehabil. Psychol. 57, 236-247. doi: 10.1037/a0029256
6. Bonanno, G. A., Mancini, A. D., Horton, J. L., Powell, T. M., Leardmann, C. A., Boyko, E. J., et al. (2012b). Trajectories of trauma symptoms and resilience in deployed US military service members: prospective cohort study. Br. J. Psychiatry 200, 317-323. doi: 10.1192/bjp.bp.111.096552
7. Boscardin, C. K. (2008). Early identification of reading difficulties using heterogeneous developmental trajectories. J. Educ. Psychol. 100, 192-208. doi: 10.1037/0022-0663.100.1.192
8. Boschen, S. L., Wietzikoski, E. C., Winn, P., and Cunha, C. D. (2011). The role of nucleus accumbens and dorsolateral striatal D2 receptors in active avoidance conditioning. Neurobiol. Learn. Mem. 96, 254-262. doi: 10.1016/j.nlm.2011.05.002
9. Bozdogan, H. (1987). Model selection and Akaike’s information criterion (AIC): the general theory and its analytical extensions. Psychometrika 52, 345-370. doi: 10.1007/BF02294361
10. Bush, D. E. A., Sotres-Bayon, F., and Ledoux, J. E. (2007). Individual differences in fear: isolating fear reactivity and fear recovery phenotypes. J. Trauma. Stress 20, 413-422. doi: 10.1002/jts.20261
11. Buzsaki, G., and Mizuseki, K. (2014). The log-dynamic brain: how skewed distributions affect network operations. Nat. Rev. Neurosci. 15, 264-278. doi: 10.1038/nrn3687
12. Cain, C. K., and LeDoux, J. E. (2007). Escape from fear: a detailed behavioral analysis of two atypical responses reinforced by CS termination. J. Exp. Psychol. 33, 451. doi: 10.1037/0097-7403.33.4.451
13. Cain, C. K., and LeDoux, J. E. (2008). 1 Brain mechanisms of Pavlovian and instrumental aversive conditioning. Handb. Behav. Neurosci. 17, 103-124. doi: 10.1016/S1569-7339(07)00007-0
14. Choi, J.-S., Cain, C. K., and Ledoux, J. E. (2010). The role of amygdala nuclei in the expression of auditory signaled two-way active avoidance in rats. Learn. Mem. 17, 139-147. doi: 10.1101/lm.1676610
15. Cohen, H., Matar, M. A., Richter-Levin, G. A. L., and Zohar, J. (2006). The contribution of an animal model toward uncovering biological risk factors for PTSD. Ann. N.Y.Acad. Sci. 1071, 335-350. doi: 10.1196/annals.1364.026
16. Cowansage, K. K., Bush, D. E. A., Josselyn, S. A., Klann, E., and Ledoux, J. E. (2013). Basal variability in CREB phosphorylation predicts trait-like differences in amygdala-dependent memory. Proc. Natl. Acad. Sci. U.S.A. 110, 16645-16650. doi: 10.1073/pnas.1304665110
17. Curran, P. J., and Hussong, A. M. (2003). The use of latent trajectory models in psychopathology research. J. Abnorm. Psychol. 112, 526-544. doi: 10.1037/0021-843X.112.4.526
18. Del Boca, F. K. (2004). Up close and personal: temporal variability in the drinking of individual college students during their first year. J. Consult. Clin. Psychol. 72, 155-164. doi: 10.1037/0022-006X.72.2.155
19. Deroon-Cassini, T. A. (2010). Psychopathology and resilience following traumatic injury: a latent growth mixture model analysis. Rehabil. Psychol. 55, 1-11. doi: 10.1037/a0018601
20. Duncan, T. E., Duncan, S. C., and Strycker, L. A. (2006). An Introduction to Latent Variable Growth Curve Modeling: Concepts, Issues, and Applications. Mahwah, NJ: Lawrence Erlbaum Associates.
21. Fanselow, M. S., and Poulos, A. M. (2005). The neuroscience of mammalian associative learning. Annu. Rev. Psychol. 56, 207-234. doi: 10.1146/annurev.psych. 56.091103.070213
22. Ferreira, R., and Nobre, M. J. (2014). Conditioned fear in low-and high-anxious rats is differentially regulated by cortical subcortical and midbrain 5-HT< sub> 1A receptors. Neuroscience. 268, 159-168. doi: 10.1016/j.neuroscience.2014.03.005
23. Flora, D. B. (2008). Specifying piecewise latent trajectory models for longitudinal data. Struct. Equ. Model. 15, 513-533. doi: 10.1080/10705510802154349
24. Fox, J. (2008). Applied Regression Analysis and Generalized Linear Models. Los Angeles, CA: Sage.
25. Galatzer-Levy, I. R., Ankri, Y., Freedman, S., Israeli-Shalev, Y., Roitman, P., Gilad, M., et al. (2013a). Early PTSD symptom trajectories: persistence, recovery, and response to treatment: results from the jerusalem trauma outreach and prevention study (J-TOPS). PLoS ONE 8:e70084. doi: 10.1371/journal.pone. 0070084
26. Galatzer-Levy, I. R., and Bonanno, G. A. (2012). Beyond normality in the study of bereavement: heterogeneity in depression outcomes following loss in older adults. Soc. Sci. Med. 74, 1987-1994. doi: 10.1016/j.socscimed.2012. 02.022
27. Galatzer-Levy, I. R., Bonanno, G. A., Bush, D. E., and Ledoux, J. E. (2013b). Heterogeneity in threat extinction learning: substantive and methodological considerations for identifying individual difference in response to stress. Front. Behav. Neurosci. 7:55. doi: 10.3389/fnbeh.2013.00055
28. Galatzer-Levy, I. R., Brown, A. D., Henn-Haase, C., Metzler, T. J., Neylan, T. C., and Marmar, C. R. (2013c). Positive and negative emotion prospectivelypredict trajectories of resilience and distress among high-exposure police officers. Emotion 545-553. doi: 10.1037/a0031314
29. Galatzer-Levy, I. R., and Bryant, R. A. (2013). 636,120 Ways to have post-traumatic stress disorder. Perspect. Psychol. Sci. 8, 651-662. doi: 10.1177/1745691613504115
30. Galatzer-Levy, I. R., Burton, C. L., and Bonanno, G. A. (2012). Coping flexibility, potentially traumatic life events, and resilience: a prospective study of college student adjustment. J. Soc. Clin. Psychol. 31, 542-567. doi: 10.1521/jscp.2012.31.6.542
31. Galatzer-Levy, I. R., Madan, A., Neylan, T. C., Henn-Haase, C., and Marmar, C. R. (2011). Peritraumatic and trait dissociation differentiate police officers with resilient versus symptomatic trajectories ofposttraumatic stress symptoms. J. Trauma. Stress 24, 557-565. doi: 10.1002/jts.20684
32. Galatzer-Levy, I. R., Steenkamp, M. M., Qian, M., Inslicht, S., Henn-Haase, C., Otte, C., et al. (2014). Cortisol response to an experimental stress paradigm prospectively predicts long-term distress and resilience trajectories in response to active police service. J. Psychiatr. Res. 56, 36-42. doi: 10.1016/j.jpsychires.2014.04.020
33. Gallistel, C. R., Fairhurst, S., and Balsam, P. (2004). The learning curve: implications of a quantitative analysis. Proc. Natl. Acad. Sci. U.S.A. 101, 13124-13131. doi: 10.1073/pnas.0404965101
34. Gozzi, A., Jain, A., Giovanelli, A., Bertollini, C., Crestan, V., Schwarz, A. J., et al. (2010). A neural switch for active and passive fear. Neuron 67, 656-666. doi: 10.1016/j.neuron.2010.07.008
35. Greenbaum, P., Del Boca, F., Darkes, J., Wang, C., and Goldman, M. S. (2005). Variation in the drinking trajectories of freshman college students. J. Consult. Clin. Psychol. 73,229-238. doi: 10.1037/0022-006X.73.2.229
36. Gross, J. J., and Thompson, R. A. (2007). “Emotion regulation: conceptual foundations," in Handbook of Emotion Regulation, ed J. J. Gross (New York, NY: Guilford Press), 3-24.
37. Hald, A. (2007). A History of Parametric Statistical Inference from Bernoulli to Fischer. New York, NY: Springer.
38. 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
39. Hefner, K., Whittle, N., Juhasz, J., Norcross, M., Karlsson, R.-M., Saksida, L. M., et al. (2008). Impaired fear extinction learning and cortico-amygdala circuit abnormalities in a common genetic mouse strain. J. Neurosci. 28, 8074-8085. doi: 10.1523/JNEUROSCI.4904-07.2008
40. Johansen, J. P., Cain, C. K., Ostroff, L. E., and Ledoux, J. E. (2011). Molecular mechanisms of fear learning and memory. Cell 147, 509-524. doi: 10.1016/j.cell.2011.10.009
41. Kessler, R. C., Berglund, P., Demler, O., Jin, R., Merikangas, K. R., and Walters, E. E. (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey replication. Arch. Gen. Psychiatry 62, 593-602. doi: 10.1001/archpsyc.62.6.593
42. Kline, R. B. (2011). Principles and Practice of Structural Equation Modeling.New York, NY: Guilford press.
43. Lazaro-Munoz, G., Ledoux, J. E., and Cain, C. K. (2010). Sidman instrumental avoidance initially depends on lateral and basal amygdala and is constrained by central amygdala-mediated Pavlovian processes. Biol. Psychiatry 67, 1120-1127. doi: 10.1016/j.biopsych.2009.12.002
44. Ledoux, J. (2012). Rethinking the emotional brain. Neuron 73, 653-676. doi: 10.1016/j.neuron.2012.02.004
45. Ledoux, J. E. (2014). Coming to terms with fear. Proc. Natl. Acad. Sci. U.S.A. 111, 2871-2878. doi: 10.1073/pnas.1400335111
46. Ledoux, J. E., and Gorman, J. M. (2001). A call to action: overcoming anxiety through active coping. Am. J. Psychiatry 158, 1953-1955. doi: 10.1176/appi.ajp.158.12.1953
47. 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
48. Martinez, R. C. R., Gupta, N., Lazaro-Munoz, G., Sears, R. M., Kim, S., Moscarello, J. M., et al. (2013). Active vs. reactive threat responding is associated with differential c-Fos expression in specific regions of amygdala and prefrontal cortex. Learn. Mem. 20, 446-452. doi: 10.1101/lm.0310 47.113
49. Moscarello, J. M., and Ledoux, J. E. (2013). Active avoidance learning requires pre-frontal suppression of amygdala-mediated defensive reactions. J. Neurosci. 33, 3815-3823. doi: 10.1523/JNEUROSCI.2596-12.2013
50. Mowrer, O. H., and Lamoreaux, R. R. (1946). Fear as an intervening variable in avoidance conditioning. J. Comp. Psychol. 39, 29. doi: 10.1037/h0060150
51. Muthen, B. (2003). Statistical and substantive checking in growth mixture modeling: comment on Bauer and Curran (2003). Psychol. Methods 8, 369-377. Discussion: 384-393. doi: 10.1037/1082-989X. 8.3.369
52. Muthen, L. K., and Muthen, B. (2006). Mplus User’s Guide, 4th Edn. Los Angeles, CA: Muthen and Muthen.
53. Nylund, K., Asparouhov, T., and Muthen, B. (2007). Deciding on the number of classes in latent class analysis and growth mixture modeling: a Monte Carlo simulation study. Struct. Equ. Model. 14, 535-569. doi: 10.1080/10705510701575396
54. Nylund (2007). Deciding on the number of classes in latent class analysis and growth mixture modeling: a Monte Carlo simulation study. Struct. Equ. Model. 535-569. doi: 10.1080/10705510701575396
55. Parsons, R. G., and Ressler, K. J. (2013). Implications of memory modulation for post-traumatic stress and fear disorders. Nat. Neurosci. 16, 146-153. doi: 10.1038/nn.3296
56. Schaeffer, C. M., Petras, H., Ialongo, N., Poduska, J., and Kellam, S. (2003). Modeling growth in boys’ aggressive behavior across elementary school: links to later criminal involvement, conduct disorder, and antisocial personality disorder. Dev. Psychol. 39, 1020-1035. doi: 10.1037/0012-1649.39. 6.1020
57. Schwartz, G. (1978). Estimating the dimension of a model. Ann. Stat. 6, 461-464.doi: 10.1214/aos/1176344136
58. Sclove, S. L. (1987). Application of model-selection criteria to some problems in multivariate analysis. Psychometrika 52, 333-343. doi: 10.1007/BF022 94360
59. Stigler, S. M. (1986). The History of Statistics: the Measurement of Uncertainty Before 1900. Cambridge, MA: Harvard University Press.
60. Vicens-Costa, E., Martmez-Membrives, E., Lopez-Aumatell, R., Guitart-Masip, M., Canete, T., Blazquez, G., et al. (2011). Two-way avoidance acquisition is negatively related to conditioned freezing and positively associated with startle reactions: a dissection of anxiety and fear in genetically heterogeneous rats. Physiol. Behav. 103, 148-156. doi: 10.1016/j.physbeh.2010. 12.009
61. Yehuda, R., and Antelman, S. M. (1993). Criteria for rationally evaluating animal models of posttraumatic stress disorder. Biol. Psychiatry 33, 479-486. doi: 10.1016/0006-3223(93)90001-T
62. Yehuda, R., and Ledoux, J. (2007). Response variation following trauma: a translational neuroscience approach to understanding PTSD. Neuron 56, 19-32. doi: 10.1016/j.neuron.2007.09.006