Segregated populations of hippocampal principal CA1 neurons mediating conditioning and extinction of contextual fear

Journal of Neuroscience

Volumn 29, Issue 11, 2009, Pages 3387-3394

  Tronson, Natalie C ^a   Schrick, Christina ^a   Guzman, Yomayra F ^a   Huh, Kyu Hwan ^a   Srivastava, Deepak P ^a   Penzes, Peter ^a   Guedea, Anita L ^a   Gao, Can ^a   Radulovic, Jelena ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOTOXIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN FOS; PROTEIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL POPULATION; CHOLINERGIC ACTIVITY; CHOLINERGIC NERVE CELL; CONDITIONING; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME REGULATION; FEAR; HIPPOCAMPUS; MEMORY CONSOLIDATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REINFORCEMENT; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; CONDITIONING (PSYCHOLOGY); EXTINCTION, PSYCHOLOGICAL; FEAR; HIPPOCAMPUS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS;

EID: 63849102017     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5619-08.2009     Document Type: Article

References (46)

1. Atkins CM, Selcher JC, Petraitis JJ, Trzaskos JM, Sweatt JD (1998) The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1:602-609.
2. Berlau DJ, McGaugh JL (2006) Enhancement of extinction memory consolidation: the role of the noradrenergic and GABAergic systems within the basolateral amygdala. Neurobiol Learn Mem 86:123-132.
3. Bouton ME (2004) Context and behavioral processes in extinction. Learn Mem 11:485-494.
4. Brown HE, Garcia MM, Harlan RE (1998) A two focal plane method for digital quantification of nuclear immunoreactivity in large brain areas using NIH-image software. Brain Res Brain Res Protoc 2:264-272.
5. Buhusi CV, Schmajuk NA (1996) Attention, configuration, and hippocampal function. Hippocampus 6:621-642.
6. Chen X, Garelick MG, Wang H, Lil V, Athos J, Storm DR (2005) PI3 kinase signaling is required for retrieval and extinction of contextual memory. Nat Neurosci 8:925-931.
7. Chhatwal JP, Myers KM, Ressler KJ, Davis M (2005) Regulation of gephyrin and GABAA receptor binding within the amygdala after fear acquisition and extinction. J Neurosci 25:502-506.
8. Falls WA, Miserendino MJ, Davis M (1992) Extinction of fear-potentiated startle: blockade by infusion of an NMDA antagonist into the amygdala. J Neurosci 12:854-863.
9. Feld M, Dimant B, Delorenzi A, Coso O, Romano A (2005) Phosphorylation of extra-nuclear ERK/MAPK is required for long-term memory consolidation in the crab Chasmagnathus. Behav Brain Res 158:251-261.
10. Fischer A, Sananbenesi F, Schrick C, Spiess J, Radulovic J (2004) Distinct roles of hippocampal de novo protein synthesis and actin rearrangement in extinction of contextual fear. J Neurosci 24:1962-1966.
11. Fischer A, Radulovic M, Schrick C, Sananbenesi F, Godovac-Zimmermann J, Radulovic J (2007) Hippocampal Mek/Erk signaling mediates extinction of contextual freezing behavior. Neurobiol Learn Mem 87:149-158.
12. Fleischmann A, Hvalby O, Jensen V, Strekalova T, Zacher C, Layer LE, Kvello A, Reschke M, Spanagel R, Sprengel R, Wagner EF, Gass P (2003) Impaired long-term memory and NR2A-type NMDA receptor-dependent synaptic plasticity in mice lacking c-Fos in the CNS. J Neurosci 23:9116-9122.
13. Fletcher BR, Baxter MG, Guzowski JF, Shapiro ML, Rapp PR (2007) Selective cholinergic depletion of the hippocampus spares both behaviorally induced Arc transcription and spatial learning and memory. Hippocampus 17:227-234.
14. Gray J, McNaughton N (2000) The neuropsychology of anxiety, Ed 2. Oxford: Oxford UP.
15. Grillon C (2002) Startle reactivity and anxiety disorders: aversive conditioning, context, and neurobiology. Biol Psychiatry 52:958-975.
16. Herry C, Ciocchi S, Senn V, Demmou L, Müller C, Lüthi A (2008) Switching on and off fear by distinct neuronal circuits. Nature 454:600-606.
17. Isiegas C, Park A, Kandel ER, Abel T, Lattal KM (2006) Transgenic inhibition of neuronal protein kinase A activity facilitates fear extinction. J Neurosci 26:12700-12707.
18. Kim J, Lee S, Park K, Hong I, Song B, Son G, Park H, Kim WR, Park E, Choe HK, Kim H, Lee C, Sun W, Kim K, Shin KS, Choi S (2007) Amygdala depotentiation and fear extinction. Proc Natl Acad Sci USA 104:20955-20960.
19. Kovalovsky D, Refojo D, Liberman AC, Hochbaum D, Pereda MP, Coso OA, Stalla GK, Holsboer F, Arzt E (2002) Activation and induction of NUR77/NURR1 in corticotrophs by CRH/cAMP: involvement of calcium, protein kinase A, and MAPK pathways. Mol Endocrinol 16:1638-1651.
20. Lee SH, Choi JH, Lee N, Lee HR, Kim JI, Yu NK, Choi SL, Lee SH, Kim H, Kaang BK (2008) Synaptic protein degradation underlies destabilization of retrieved fear memory. Science 319:1253-1256.
21. Maren S, Quirk GJ (2004) Neuronal signalling of fear memory. Nat Rev Neurosci 5:844-852.
22. Matsuo N, Reijmers L, Mayford M (2008) Spine-type-specific recruitment of newly synthesized AMPA receptors with learning. Science 319:1104-1107.
23. Milad MR, Quirk GJ (2002) Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420:70-74.
24. Navarro M, Spray KJ, Cubero I, Thiele TE, Bernstein IL (2000) cFos induction during conditioned taste aversion expression varies with aversion strength. Brain Res 887:450-453.
25. Nirenberg S, Cepko C (1993) Targeted ablation of diverse cell classes in the nervous system in vivo. J Neurosci 13:3238-3251.
26. Ouyang M, Thomas SA (2005) A requirement for memory retrieval during and after long-term extinction learning. Proc Natl Acad Sci USA 102:9347-9352.
27. Patterson SL, Pittenger C, Morozov A, Martin KC, Scanlin H, Drake C, Kandel ER (2001) Some forms of cAMP-mediated long-lasting potentiation are associated with release of BDNF and nuclear translocation of phospho-MAP kinase. Neuron 32:123-140.
28. Radulovic J, Kammermeier J, Spiess J ( 1998) Relationship between fos production and classical fear conditioning: effects of novelty, latent inhibition, and unconditioned stimulus preexposure. J Neurosci 18:7452-7461.
29. Radulovic J, Rühmann A, Liepold T, Spiess J (1999) Modulation of learning and anxiety by corticotropin-releasing factor (CRF) and stress: differential roles of CRF receptors 1 and 2. J Neurosci 19:5016-5025.
30. Reijmers LG, Perkins BL, Matsuo N, Mayford M (2007) Localization of a stable neural correlate of associative memory. Science 317:1230-1233.
31. Rovira C, Cherubini E, Ben-Ari Y (1982) Opposite actions of muscarinic and nicotinic agents on hippocampal dendritic negative fields recorded in rats. Neuropharmacology 21:933-936.
32. Ryu J, Futai K, Feliu M, Weinberg R, Sheng M (2008) Constitutively active Rap2 transgenic mice display fewer dendritic spines, reduced extracellular signal-regulated kinase signaling, enhanced long-term depression, and impaired spatial learning and fear extinction. J Neurosci 28:8178-8188.
33. Sananbenesi F, Fischer A, Schrick C, Spiess J, Radulovic J (2002) Phosphorylation of hippocampal Erk-1/2, Elk-1, and p90-Rsk-1 during contextual fear conditioning: interactions between Erk-1/2 and Elk-1. MoI Cell Neurosci 21:463-476.
34. Sananbenesi F, Fischer A, Wang X, Schrick C, Neve R, Radulovic J, Tsai LH (2007) A hippocampal Cdk5 pathway regulates extinction of contextual fear. Nat Neurosci 10:1012-1019.
35. Schilling K, Luk D, Morgan JI, Curran T (1991) Regulation of a fos-lacZ fusion gene: a paradigm for quantitative analysis of stimulustranscription coupling. Proc Natl Acad Sci U S A 88:5665-5669.
36. Schrick C, Fischer A, Srivastava DP, Tronson NC, Penzes P, Radulovic J (2007) N-cadherin regulates cytoskeletally associated IQGAP1/ERK signaling and memory formation. Neuron 55:786-798.
37. Sindreu CB, Scheiner ZS, Storm DR (2007) Ca2 +-stimulated adenylyl cyclases regulate ERK-dependent activation of MSK1 during fear conditioning. Neuron 53:79-89.
38. Smeyne RJ, Schilling K, Robertson L, Luk D, Oberdick J, Curran T, Morgan JI (1992) fos-lacZ transgenic mice: mapping sites of gene induction in the central nervous system. Neuron 8:13-23.
39. Sotres-Bayon F, Bush DE, LeDoux JE (2004) Emotional perseveration: an update on prefrontal-amygdala interactions in fear extinction. Learn Mem 11:525-535.
40. Sweatt JD (2004) Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 14:311-317.
41. Szapiro G, Vianna MR, McGaugh JL, Medina JH, Izquierdo I (2003) The role of NMDA glutamate receptors, PKA, MAPK, and CAMKII in the hippocampus in extinction of conditioned fear. Hippocampus 13:53-58.
42. Trifilieff P, Herry C, Vanhoutte P, Caboche J, Desmedt A, Riedel G, Mons N, Micheau J (2006) Foreground contextual fear memory consolidation requires two independent phases of hippocampal ERK/CREB activation. Learn Mem 13:349-358.
43. Tronson NC, Schrick C, Fischer A, Sananbenesi F, Pagès G, Pouysségur J, Radulovic J (2008) Regulatory mechanisms of fear extinction and depression-like behavior. Neuropsychopharmacology 33:1570-1583.
44. Vinogradova OS (2001 ) Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11:578-598.
45. Wheal HV, Miller JJ (1980) Pharmacological identification of acetylcholine and glutamate excitatory systems in the dentate gyrus of the rat. Brain Res 182:145-155.
46. Winder DG, Martin KC, Muzzio IA, Rohrer D, Chruscinski A, Kobilka B, Kandel ER (1999) ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors. Neuron 24:715-726.