Extinction and Retrieval + Extinction of Conditioned Fear Differentially Activate Medial Prefrontal Cortex and Amygdala in Rats

Frontiers in Behavioral Neuroscience

Volumn 9, Issue , 2016, Pages

  Lee, Hongjoo J ^a   Haberman, Rebecca P ^b   Roquet, Rheall F ^a   Monfils, Marie H ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Arc catFISH; extinction; fear conditioning; reconsolidation; retrieval + extinction

Indexed keywords

AMYGDALA; ANIMAL EXPERIMENT; ARTICLE; CATFISH; FEAR; FLUORESCENCE IN SITU HYBRIDIZATION; INTRACELLULAR SPACE; MALE; MEDIAL PREFRONTAL CORTEX; NONHUMAN; RAT; RODENT;

EID: 84991783261     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2015.00369     Document Type: Article

References (35)

1. Auber A. Tedesco V. Jones C. E. Monfils M. H. Chiamulera C. (2013). Post-retrieval extinction as reconsolidation interference: methodological issues or boundary conditions? Psychopharmacology (Berl) 226, 631–647. 10.1007/s00213-013-3004-126687805
2. Bouton M. E. Bolles R. C. (1979a). Contextual control of the extinction of conditioned fear. Learn. Motivat. 10, 445–466. 10.1016/0023-9690(79)90057-2
3. Bouton M. E. Bolles R. C. (1979b). Role of conditioned contextual stimuli in reinstatement of extinguished fear. J. Exp. Psychol. Anim. Behav. Processes 5, 368–378. 10.1037/0097-7403.5.4.368528893
4. Chan W. Y. Leung H. T. Westbrook R. F. McNally G. P. (2010). Effects of recent exposure to a conditioned stimulus on extinction of Pavlovian fear conditioning. Learn. Mem. 17, 512–521. 10.1101/lm.191251020884753
5. Clem R. L. Huganir R. L. (2010). Calcium-permeable AMPA receptor dynamics mediate fear memory erasure. Science 330, 1108–1112. 10.1126/science.119529821030604
6. Do-Monte F. H. Manzano-Nieves G. Quiñones-Laracuente K. Ramos-Medina L. Quirk G. J. (2015). Revisiting the role of infralimbic cortex in fear extinction with optogenetics. J. Neurosci. 35, 3607–3615. 10.1523/JNEUROSCI.3137-14.201525716859
7. Guzowski J. F. Lyford G. L. Stevenson G. D. Houston F. P. McGaugh J. L. Worley P. F. et al. (2000). Inhibition of activity-dependent Arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation. J. Neurosci. 20, 3993–4001. 10818134
8. Guzowski J. F. McNaughton B. L. Barnes C. A. Worley P. F. (1999). Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat. Neurosci. 2, 1120–1124. 10.1038/1604610570490
9. Kindt M. Soeter M. Vervliet B. (2009). Beyond extinction: erasing human fear responses and preventing the return of fear. Nat. Neurosci. 12, 256–258. 10.1038/nn.227119219038
10. Knapska E. 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. 10.1101/lm.146390919633138
11. McGaugh J. L. (2000). Memory-a century of consolidation. Science 287, 248–251. 10.1126/science.287.5451.24810634773
12. Messaoudi E. Kanhema T. Soulé J. Tiron A. Dagyte G. da Silva B. et al. (2007). Sustained Arc/Arg 3.1 synthesis controls long-term potentiation consolidation through regulation of local action polymerization in the dentate gyrus in vivo. J. Neurosci. 27, 10445–10455. 10.1523/jneurosci.2883-07.200717898216
13. Milad M. R. Quirk G. J. (2002). Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420, 70–74. 10.1038/nature0113812422216
14. Monfils M.-H. Cowansage K. K. Klann E. LeDoux J. E. (2009). Extinction-reconsolidation boundaries: key to persistent attenuation of fear memories. Science 324, 951–955. 10.1126/science.116797519342552
15. Nader K. Schafe G. E. LeDoux J. E. (2000). Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406, 722–726. 10.1038/3502105210963596
16. Olshavsky M. E. Jones C. E. Lee H. J. Monfils M. H. (2013a). Appetitive behavioral traits and stimulus intensity influence maintenance of conditioned fear. Front. Behav. Neurosci. 7:179. 10.3389/fnbeh.2013.0017924348354
17. Olshavsky M. E. Song B. Powell D. J. Jones C. E. Monfils M. H. Lee H. J. (2013b). Updating appetitive memory during reconsolidation window: critical role of enhanced cue-directed behavior and amygdala central nucleus. Front. Behav. Neurosci. 7:186. 10.3389/fnbeh.2013.0018624367304
18. Pavlov I. P. (1927). Conditioned Reflexes. trans G.V. Anrep (London: Oxford University Press).
19. Petrovich G. D. Holland P. C. Gallagher M. (2005). Amygdala and prefrontal pathways to the lateral hypothalamus are activated by a learned cue that stimulates eating. J. Neurosci. 25, 8295–8302. 10.1523/jneurosci.2480-05.200516148237
20. Phillips R. G. LeDoux J. E. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 106, 274–285. 10.1037/0735-7044.106.2.2741590953
21. Plath N. Ohana O. Dammermann B. Errington M. L. Schmitz D. Gross C. et al. (2006). Arc/Arg 3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52, 437–444. 10.1016/j.neuron.2006.08.02417088210
22. Quirk G. J. Armony J. L. LeDoux J. E. (1997). Fear conditioning enhances different temporal components of tone-evoked spike train in auditory cortex and lateral amygdala. Neuron 19, 613–624. 10.1016/s0896-6273(00)80375-x9331352
23. Rao-Ruiz P. Rotaru D. C. van der Loo R. J. Mansvelder H. D. Stiedl O. Smit A. B. et al. (2011). Retrieval-specific endocytosis of GluA2-AMPARs underlies adaptive reconsolidation of contextual fear. Nat. Neurosci. 14, 1302–1308. 10.1038/nn.290721909089
24. Rescorla R. A. Heth C. D. (1975). Reinstatement of fear to an extinguished conditioned stimulus. J. Exp. Psychol. Anim. Behav. Processes 1, 88–96. 10.1037/0097-7403.1.1.881151290
25. Robbins S. J. (1990). Mechanisms underlying spontaneous recovery in autoshaping. J. Exp. Psychol. Anim. Behav. Processes 16, 235–249. 10.1037/0097-7403.16.3.235
26. Schiller D. Kanen J. W. LeDoux J. E. Monfils M. H. Phelps E. A. (2013). Extinction during reconsolidation of threat memory diminishes prefrontal cortex involvement. Proc. Natl. Acad. Sci. U S A 110, 20040–20045. 10.1073/pnas.132032211024277809
27. Schiller D. Monfils M.-H. Raio C. M. Johnson D. C. Ledoux J. E. Phelps E. A. (2010). Preventing the return of fear in humans using reconsolidation update mechanisms. Nature 463, 49–53. 10.1038/nature0863720010606
28. Sevenster D. Beckers T. Kindt M. (2012). Prediction error demarcates the transition from retrieval, to reconsolidation, to new learning. Learn. Mem. 21, 580–584. 10.1101/lm.035493.11425320349
29. Sevenster D. Beckers T. Kindt M. (2014). Retrieval per se is not sufficient to trigger reconsolidation of human fear memory. Neurobiol. Learn. Mem. 97, 338–345. 10.1016/j.nlm.2012.01.00922406658
30. Sierra-Mercado D. Padilla-Coreano N. Quirk G. J. (2011). Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharm 36, 529–538. 10.1038/npp.2010.18420962768
31. Swanson L. W. (2004). Brain Maps: Structure of the Rat Brain. 3rd Edn. San Diego, CA: Academic Press.
32. Tedesco V. Roquet R. F. DeMis J. Chiamulera C. Monfils M. H. (2014). Extinction, applied after retrieval of auditory fear memory, selectively increases zinc-finger protein 268 and phosphorylated ribosomal protein S6 expression in prefrontal cortex and lateral amygdala. Neurobiol. Learn. Mem. 115, 78–85. 10.1016/j.nlm.2014.08.01525196703
33. Vazdarjanova A. McNaughton B. L. Barnes C. A. Worley P. F. Guzowski J. F. (2002). Experience-dependent coincident expression of the effector immediate-early genes Arc and Homer 1a in hippocampal and neocortical neuronal networks. J. Neurosci. 22, 10067–10071. 12451105
34. Wolpe J. (1969). The Practice of Behavior Therapy. New York: Pergamon Press.
35. Xue Y. X. Luo Y. X. Wu P. Shi H. S. Xue L. F. Chen C. et al. (2012). A memory retrieval-extinction procedure to prevent drug craving and relapse. Science 336, 241–245. 10.1126/science.121507022499948