Infant stress exposure produces persistent enhancement of fear learning across development

Developmental Psychobiology

Volumn 56, Issue 5, 2014, Pages 1008-1016

  Quinn, Jennifer J ^a   Skipper, Rachel A ^a   Claflin, Dragana I ^b  

^a MIAMI UNIVERSITY   (United States)

^b WRIGHT STATE UNIVERSITY   (United States)

Author keywords

Early life stress; Fear conditioning; Forgetting; Infantile amnesia; Rat; SEFL

Indexed keywords

ANIMAL; CATALEPSY; CONDITIONING; ELECTRIC SHOCK; FEAR; FEMALE; LEARNING; LONG EVANS RAT; MALE; MENTAL STRESS; PATHOPHYSIOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RAT;

ANIMALS; ASSOCIATION LEARNING; CONDITIONING (PSYCHOLOGY); ELECTROSHOCK; FEAR; FEMALE; FREEZING REACTION, CATALEPTIC; MALE; RATS; RATS, LONG-EVANS; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL;

EID: 84901695254     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.21181     Document Type: Article

References (58)

1. Alexander, N., Rosenlöcher, F., Stalder, T., Linke, J., Distler, W., Morgner, J., & Kirschbaum, C. (2012). Impact of antenatal synthetic glucocorticoid exposure on endocrine stress reactivity in term-born children. Journal of Clinical Endocrinology and Metabolism, 97, 3538-3544. doi: 10.1210/jc.2012-1970
2. Anagnostaras, S. G., Wood, S. C., Shuman, T., Cai, D. J., Leduc, A. D., Zurn, K. R., ... Herrera, G. M. (2010). Automated assessment of pavlovian conditioned freezing and shock reactivity in mice using the video freeze system. Frontiers in Behavioral Neuroscience, pii, 158. doi: 10.3389/fnbeh.2010.00158
3. Bilbo, S. D., & Schwarz, J. M. (2012). The immune system and developmental programming of brain and behavior. Frontiers in Neuroendocrinology, 33, 267-286. doi: 10.1016/j.yfrne.2012.08.006
4. Callaghan, B. L., & Richardson, R. (2012). The effect of adverse rearing environments on persistent memories in young rats: Removing the brakes on infant fear memories. Translational Psychiatry, 2, e138. doi: 10.1038/tp.2012.65
5. Campbell, B. A., & Jaynes, J. (1966). Reinstatement. Psychological Review, 73, 478-480.
6. Campbell, B. A., & Spear, N. E. (1972). Ontogeny of memory. Psychological Review, 79, 215-236.
7. Davis, J. M., & Rovee-Collier, C. K. (1983). Alleviated forgetting of a learned contingency in 8-week-old infants. Developmental Psychology, 19(3), 353-365. doi: 10.1037/0012-1649.19.3.353
8. Dias, B. G., Banerjee, S. B., Goodman, J. V., & Ressler, K. J. (2013). Towards new approaches to disorders of fear and anxiety. Current Opinions in Neurobiology, 23, 346-352. doi: piiS0959-4388(13)00029-9.10.1016/j.conb.2013.01.013
9. Fanselow, M. S. (1980) Conditioned and unconditional components of post-shock freezing. Pavlovian Journal of Biological Science, 15, 177-182.
10. Farrell, M. R., Sengelaub, D. R., & Wellman, C. L. (2013). Sex differences and chronic stress effects on the neural circuitry underlying fear conditioning and extinction. Physiology and Behavior, Epub ahead of print. doi: piiS0031-9384(13)00116-9.10.1016/j.physbeh.2013.04.002
11. Forcato, C., Fernandez, R. S., & Pedreira, M. E. (2013). The role and dynamic of strengthening in the reconsolidation process in a human declarative memory: What decides the fate of recent and older memories? PLoS ONE, 8(4), 1-12.
12. Gale, G. D., Anagnostaras, S. G., Godsil, B. P., Mitchell, S., Nozawa, T., Sage, J. R., ... Fanselow, M. S. (2004). Role of the basolateral amygdala in the storage of fear memories across the adult lifetime of rats. Journal of Neuroscience, 24, 3810-3815.
13. Haroutunian, V., & Campbell, R. C. (1977). Effect of arousal conditions during reinstatement treatment upon learned fear in young rats. Developmental Psychobiology, 10, 25-32.
14. Hill, M. N., Hellemans, K. G., Verma, P., Gorzalka, B. B., & Weinberg, J. (2012). Neurobiology of chronic mild stress: Parallels to major depression. Neuroscience Biobehavioral Review, 36, 2085-2117. doi: 10.1016/j.neubiorev.2012.07.001
15. Hunt, P. S., & Campbell, B. A. (1997). Developmental dissociation of the components of conditioned fear. In: M. E. Bouton & M. S. Fanselow (Eds.), Learning, motivation, and cognition: The functional behaviorism of Robert C. Bolles (pp. 53-74). Washington, DC: American Psychological Association.
16. Hunt, P. S., Fanselow, M. S., Richardson, R., Mauk, M. D., Freeman, J. H., Jr., & Stanton, M. E. (2007). Synapses, circuits, and the ontogeny of learning. Developmental Psychobiology, 49, 649-663.
17. Hunt, P. S., Hess, M. F., & Campbell, B. A. (1998). Inhibition of the expression of conditioned cardiac responses in the developing rat. Developmental Psychobiology, 32, 221-233.
18. Hunter, A. L., Minnis, H., & Wilson, P. (2011). Altered stress responses in children exposed to early adversity: A systematic review of salivary cortisol studies. Stress, 14, 614-626. doi: 10.3109/10253890.2011.577848
19. Jankord, R., Solomon, M. B., Albertz, J., Flak, J. N., Zhang, R., & Herman, J. P. (2011). Stress vulnerability during adolescent development in rats. Endocrinology, 152, 629-638. doi: 10.1210/en.2010-0658
20. Kim, J. H., Li, S., Hamlin, A. S., McNally, G. P., & Richardson, R. (2012). Phosphorylation of mitogen-activated protein kinase in the medial prefrontal cortex and the amygdala following memory retrieval or forgetting in developing rats. Neurobiology of Learning and Memory, 97, 59-68. doi: 10.1016/j.nlm.2011.09.005
21. Kim, J. H., McNally, G. P., & Richardson, R. (2006). Recovery of fear memories in rats: Role of gamma-amino butyric acid (GABA) in infantile amnesia. Behavioral Neuroscience, 120, 40-48.
22. Kosten, T. A., Kim, J. J., & Lee, H. J. (2012). Early life manipulations alter learning and memory in rats. Early life manipulations alter learning and memory in rats. Neuroscience and Biobehavioral Reviews, 36, 1985-2006. doi: 10.1016/j.neubiorev.2012.07.003
23. Li, S., & Richardson, R. (2013). Traces of memory: Reacquisition of fear following forgetting is NMDAr-independent. Learning and Memory, 20, 174-182. doi: 10.1101/lm.029504.112
24. Long, V. A., & Fanselow, M. S. (2012). Stress enhanced fear learning in rats is resistant to the effects of immediate massed extinction. Stress, 15, 627-636. doi: 10.3109/10253890.2011.650251
25. Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behavior, and cognition. Nature Reviews Neuroscience, 10, 434-445.
26. Macrì, S., Zoratto, F., & Laviola, G. (2011). Early-stress regulates resilience, vulnerability and experimental validity in laboratory rodents through mother-offspring hormonal transfer. Neuroscience and Biobehavioral Reviews, 35, 1534-1543. doi: 10.1016/j.neubiorev.2010.12.014
27. Matsumoto, M., Yoshioka, M., & Togashi, H. (2009). Early postnatal stress and neural circuit underlying emotional regulation. International Review of Neurobiology, 85, 95-107. doi: 10.1016/S0074-7742(09)85007-1
28. McKinzie, D. L., Chen, W. J., & Spear, N. E. (1998). Ontogenetic differences in the expression of conditioned stimulus conditioning: Effects of retention interval. Behavioral Neuroscience, 112, 920-928.
29. Moriceau, S., Raineki, C., Holman, J. D., Holman, J. G., & Sullivan, R. M. (2009). Enduring neurobehavioral effects of early life trauma mediated through learning and corticosterone suppression. Frontiers in Behavioral Neuroscience, 3, 22. doi: 10.3389/neuro.08.022.2009
30. Moriceau, S., Shionoya, K., Jakubs, K., & Sullivan, R. M. (2009). Early-life stress disrupts attachment learning: The role of amygdala corticosterone, locus ceruleus corticotropin releasing hormone, and olfactory bulb norepinephrine. Journal of Neuroscience, 29, 15745-15755. doi: 10.1523/JNEUROSCI;1;4106-09.2009
31. Moriceau, S., & Sullivan, R. M. (2004). Corticosterone influences on Mammalian neonatal sensitive-period learning. Behavioral Neuroscience, 118, 274-281.
32. Morley-Fletcher, S., Rea, M., Maccari, S., & Laviola, G. (2003). Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. European Journal of Neuroscience, 18, 3367-3374.
33. Nishi, M., Horii-Hayashi, N., Sasagawa, T., & Matsunaga, W. (2013). Effects of early life stress on brain activity: Implications from maternal separation model in rodents. General Comparative Endocrinology, 181, 306-309. doi: 10.1016/j.ygcen.2012.09.024
34. Pisano, M. V., Ferreras, S., Krapacher, F. A., Paglini, G., & Arias, C. (2012). Re-examining the ontogeny of the context preexposure facilitation effect in the rat through multiple dependent variables. Behavioural Brain Research, 233, 176-190.
35. Ponomarev, I., Rau, V., Eger, E. I., Harris, R. A., & Fanselow, M. S. (2010). Amygdala transcriptome and cellular mechanisms underlying stress-enhanced fear learning in a rat model of posttraumatic stress disorder. Neuropsychopharmacology, 35, 1402-1411.
36. Quinn, J. J., Ma, Q. D., Tinsley, M. R., Koch, C., & Fanselow, M. S. (2008). Inverse temporal contributions of the dorsal hippocampus and medial prefrontal cortex to the expression of long-term fear memories. Learning and Memory, 15, 368-372. doi: 10.1101/lm.813608
37. Rau, V., DeCola, J. P., & Fanselow, M. S. (2005). Stress-induced enhancement of fear learning: An animal model of posttraumatic stress disorder. Neuroscience and Biobehavioral Review, 29, 1207-1223.
38. Rau, V., & Fanselow, M. S. (2009). Exposure to a stressor produces a long lasting enhancement of fear learning in rats. Stress, 12, 125-133. doi: 10.1080/10253890802137320
39. Richardson, R., & Fan, M. (2002). Behavioral expression of learned fear in rats is appropriate to their age at training, not their age at testing. Animal Learning and Behavior, 30, 394-404.
40. Richardson, R., Paxinos, G., & Lee, J. (2000). The ontogeny of conditioned odor potentiation of startle. Behavioral Neuroscience, 114, 1167-1173.
41. Richardson, R., Wang, P., & Campbell, B. A. (1995). Delayed development of conditioned heart rate responses to auditory stimuli in the rat. Developmental Psychobiology, 28, 221-238.
42. Rudy, J. W. (1991) Elemental and configural associations, the hippocampus, and development. Developmental Psychobiology, 24, 221-236.
43. Rudy, J. W. (1993) Contextual conditioning and auditory cue conditioning dissociate during development. Behavioral Neuroscience, 107, 887-891.
44. Rudy, J. W., & Morledge, P. (1994). Ontogeny of contextual fear conditioning in rats: Implications for consolidation, infantile amnesia, and hippocampal system function. Behavioral Neuroscience, 108, 227-234.
45. Rudy, J. W., Vogt, M. B., & Hyson, R. L. (1984). A developmental analysis of the rat's learned reactions to gustatory and auditory stimulation. In: R. Kail & N. E. Spear (Eds.), Comparative perspectives on the development of memory (pp. 181-208). Hillsdale, NJ: Erlbaum.
46. Sanders, M. J., & Fanselow, M. S. (2003). Pre-training prevents context fear conditioning deficits produced by hippocampal NMDA receptor blockade. Neurobiology of Learning and Memory, 80, 123-129.
47. Sapolsky, R. M., & Meaney, M. J. (1986). Maturation of the adrenocortical stress response: Neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Research, 396, 64-76.
48. Schapiro, S. (1962) Pituitary ACTH and compensatory adrenal hypertrophy in stress-non-responsive infant rats. Endocrinology, 71, 986-989.
49. Schiffino, F. L., Murawski, N. J., Rosen, J. B., & Stanton, M. E. (2011). Ontogeny and neural substrates of the context preexposure facilitation effect. Neurobiology of Learning and Memory, 95, 190-198. doi: 10.1016/j.nlm.2010.11.011
50. Sevelinges, Y., Moriceau, S., Holman, P., Miner, C., Muzny, K., Gervais, R., ... Sullivan, R. M. (2007). Enduring effects of infant memories: Infant odor-shock conditioning attenuates amygdala activity and adult fear conditioning. Biological Psychiatry, 62, 1070-1079.
51. Shors, T. J., & Servatius, R. J. (1997). The contribution of stressor intensity, duration, and context to the stress-induced facilitation of associative learning. Neurobiology of Learning and Memory, 68, 92-96.
52. Shors, T. J., Weiss, C., & Thompson, R. F. (1992). Stress-induced facilitation of classical conditioning. Science, 257, 537-539.
53. Spear, N. E., & Parsons, P. (1976). Analysis of a reactivation treatment: Ontogenetic determinants of alleviated forgetting. In: D. Medin, W. Roberts, & R. Davis (Eds.), Processes in animal memory (pp. 135-166). Hillsdale, NJ: Erlbaum.
54. Tang, H. H., McNally, G. P., & Richardson, R. (2007). The effects of FG7142 on two types of forgetting in 18-day-old rats. Behavioral Neuroscience, 121, 1421-1425.
55. Tayler, K. K., Lowry, E., Tanaka, K., Levy, B., Reijmers, L., Mayford, M., & Wiltgen, B. J. (2011). Characterization of NMDAR-independent learning in the hippocampus. Frontiers in Behavioral Neuroscience, 5, 28. doi: 10.3389/fnbeh.2011.00028
56. Toledo-Rodriguez, M., & Sandi, C. (2007). Stress before puberty exerts a sex- and age-related impact on auditory and contextual fear conditioning in the rat. Neural Plasticity, Article ID 71203. doi: 10.1155/2007/71203
57. Weber, M., McNally, G. P., & Richardson, R. (2006). Opioid receptors regulate retrieval of infant fear memories: Effects of naloxone on infantile amnesia. Behavioral Neuroscience, 120, 702-709.
58. Yap, C. S., Stapinski, L., & Richardson, R. (2005). Behavioral expression of learned fear: Updating of early memories. Behavioral Neuroscience, 119, 1467-1476.