Neuronal ensembles in amygdala, hippocampus, and prefrontal cortex track differential components of contextual fear

Journal of Neuroscience

Volumn 34, Issue 25, 2014, Pages 8462-8466

  Zelikowsky, Moriel ^a,c   Hersman, Sarah ^a   Chawla, Monica K ^b   Barnes, Carol A ^b   Fanselow, Michael S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Amygdala; Arc; catFISH; Contextual fear; Hippocampus; Prefrontal cortex

Indexed keywords

MESSENGER RNA;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARC GENE; ARTICLE; BASOLATERAL AMYGDALA; CONDITIONING; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DORSAL HIPPOCAMPUS; ELECTRIC SHOCK; FEAR; FLUORESCENCE IN SITU HYBRIDIZATION; GENE; GENE EXPRESSION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; MALE; MEDIAL PREFRONTAL CORTEX; NERVE CELL; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; RECALL; TRAINING;

AMYGDALA; ARC; CATFISH; CONTEXTUAL FEAR; HIPPOCAMPUS; PREFRONTAL CORTEX;

AMYGDALA; ANIMALS; ELECTRIC STIMULATION; FEAR; HIPPOCAMPUS; MALE; NERVE NET; NEURONS; PREFRONTAL CORTEX; RATS; RATS, LONG-EVANS;

EID: 84902440135     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3624-13.2014     Document Type: Article

References (34)

1. Barot SK, Chung A, Kim JJ, Bernstein IL (2009) Functional imaging of stimulus convergence in amygdalar neurons during Pavlovian fear conditioning. PLoS One 4:e6156. CrossRef Medline
2. Cahill L, Weinberger NM, Roozendaal B, McGaugh JL (1999) Is the amygdala a locus of "conditioned fear"? Some questions and caveats. Neuron 23:227-228. CrossRef Medline
3. Chawla MK, Guzowski JF, Ramirez-Amaya V, Lipa P, Hoffman KL, Marriott LK, Worley PF, McNaughton BL, Barnes CA (2005) Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus 15:579-586. CrossRef Medline
4. Fanselow MS (1986) Conditioned fear-induced opiate analgesia: a competing motivational state theory of stress analgesia. Ann N Y Acad Sci 467: 40-54. CrossRef Medline
5. Fanselow MS (1990) Factors governing one-trial contextual conditioning. Anim Learn Behav 18:264-270. CrossRef
6. Fanselow MS (2000) Contextual fear, gestalt memories, and the hippocampus. Behav Brain Res 110:73-81. CrossRef Medline
7. Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7-19. CrossRef Medline
8. Fanselow MS, LeDoux JE (1999) Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neuron 23: 229-232. CrossRef Medline
9. Fanselow MS, DeCola JP, Young SL (1993) Mechanisms responsible for reduced contextual conditioning with massed unsignaled unconditional stimuli. J Exp Psychol Anim Behav Process 19:121-137. CrossRef Medline
10. Frankland PW, Bontempi B (2006) Fast track to the medial prefrontal cortex. Proc Natl Acad Sci U S A 103:509-510. CrossRef Medline
11. Frankland PW, Bontempi B, Talton LE, Kaczmarek L, Silva AJ (2004) The involvement of the anterior cingulate cortex in remote contextual fear memory. Science 304:881-883. CrossRef Medline
12. Guzowski JF, McNaughton BL, Barnes CA, Worley PF (1999) Environmentspecific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 2:1120-1124. CrossRef Medline
13. Han JH, Kushner SA, Yiu AP, Cole CJ, Matynia A, Brown RA, Neve RL, Guzowski JF, Silva AJ, Josselyn SA (2007) Neuronal competition and selection during memory formation. Science 316:457-460. CrossRef Medline
14. Han JH, Kushner SA, Yiu AP, Hsiang HL, Buch T, Waisman A, Bontempi B, Neve RL, Frankland PW, Josselyn SA (2009) Selective erasure of a fear memory. Science 323:1492-1496. CrossRef Medline
15. Josselyn SA, Kida S, Silva AJ (2004) Inducible repression of CREB function disrupts amygdala-dependent memory. Neurobiol Learn Mem 82:159-163. CrossRef Medline
16. Kida S, Josselyn SA, Peña de Ortiz S, Kogan JH, Chevere I, Masushige S, Silva AJ (2002) CREB required for the stability of new and reactivated fear memories. Nat Neurosci 5:348-355. CrossRef Medline
17. Kim JJ, Fanselow MS (1992) Modality-specific retrograde amnesia of fear. Science 256:675-677. CrossRef Medline
18. Lepicard EM, Mizuno K, Antunes-Martins A, von Hertzen LS, Giese KP (2006) An endogenous inhibitor of calcium/calmodulin-dependent kinase II is up-regulated during consolidation of fear memory. Eur J Neurosci 23:3063-3070. CrossRef Medline
19. Lyford GL, Yamagata K, Kaufmann WE, Barnes CA, Sanders LK, Copeland NG, Gilbert DJ, Jenkins NA, Lanahan AA, Worley PF (1995) Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeletonassociated protein that is enriched in neuronal dendrites. Neuron 14:433-445. CrossRef Medline
20. Maren S, Fanselow MS (1996) The amygdala and fear conditioning: has the nut been cracked? Neuron 16:237-240. CrossRef Medline
21. Matus-Amat P, Higgins EA, Barrientos RM, Rudy JW (2004) The role of the dorsal hippocampus in the acquisition and retrieval of context memory representations. J Neurosci 24:2431-2439. CrossRef Medline
22. Moita MA, Rosis S, Zhou Y, LeDoux JE, Blair HT (2003) Hippocampal place cells acquire location-specific responses to the conditioned stimulus during auditory fear conditioning. Neuron 37:485-497. CrossRef Medline
23. Morgan MA, LeDoux JE (1999) Contribution of ventrolateral prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Neurobiol Learn Mem 72:244-251. CrossRef Medline
24. Nalloor R, Bunting KM, Vazdarjanova A (2012) Encoding of emotionpaired spatial stimuli in the rodent hippocampus. Front Behav Neurosci 6:27. CrossRef Medline
25. Quinn JJ, Ma QD, Tinsley MR, Koch C, Fanselow MS (2008) Inverse temporal contributions of the dorsal hippocampus and medial prefrontal cortex to the expression of long-term fear memories. LearnMem15:368-372. CrossRef Medline
26. Quirk GJ, Milad MR (2010) Neuroscience: editing out fear. [Comment News]. Nature 463:36-37. CrossRef Medline
27. Reijmers LG, Perkins BL, Matsuo N, Mayford M (2007) Localization of a stable neural correlate of associative memory. Science 317:1230-1233. CrossRef Medline
28. Schafe GE, Nadel NV, Sullivan GM, Harris A, LeDoux JE (1999) Memory consolidation for contextual and auditory fear conditioning is dependent on protein synthesis, PKA, and MAP kinase. Learn Mem 6:97-110. Medline
29. Schafe GE, Nader K, Blair HT, LeDoux JE (2001) Memory consolidation of Pavlovian fear conditioning: a cellular and molecular perspective. Trends Neurosci 24:540-546. CrossRef Medline
30. Shimizu E, Tang YP, Rampon C, Tsien JZ (2000) NMDA receptordependent synaptic reinforcement as a crucial process for memory consolidation. Science 290:1170-1174. CrossRef Medline
31. Strekalova T, Zörner B, Zacher C, Sadovska G, Herdegen T, Gass P (2003) Memory retrieval after contextual fear conditioning induces c-Fos and JunB expression in CA1 hippocampus. Genes Brain Behav 2:3-10. CrossRef Medline
32. Vazdarjanova A, Guzowski JF (2004) Differences in hippocampal neuronal population responses to modifications of an environmental context: evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles. J Neurosci 24:6489-6496. CrossRef Medline
33. Zelikowsky M, Bissiere S, Hast TA, Bennett RZ, Abdipranoto A, Vissel B, Fanselow MS (2013) Prefrontal microcircuit underlies contextual learning after hippocampal loss. Proc Natl Acad Sci U S A 110:9938-9943. CrossRef Medline
34. Zhou Y, Won J, Karlsson MG, Zhou M, Rogerson T, Balaji J, Neve R, Poirazi P, Silva AJ (2009) CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala. Nat Neurosci 12:1438-1443. CrossRef Medline