Memory Reconsolidation Engages Only a Subset of Immediate-early Genes Induced During Consolidation

Overview

Journal J Neurosci

Specialty Neurology

Date 2005 Feb 25

PMID 15728833

Citations 78

Authors

Laura S J von Hertzen

K Peter Giese

Affiliations

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Abstract

The relationship between memory consolidation and reconsolidation at the molecular level is poorly understood. Here, we identify three immediate-early genes that are differentially regulated in the mouse hippocampus after contextual fear conditioning and reactivation of the context-shock memory: serum- and glucocorticoid-induced kinase 1 (SGK1), SGK3, and nerve growth factor-inducible gene B (NGFI-B). The upregulation of SGK1 expression was not specific for the context-shock association and therefore not suitable for a comparison of contextual memory consolidation and reconsolidation. SGK3 expression was upregulated during both consolidation and reconsolidation. Analysis of SGK3 expression showed that expression changes elicited by a context-shock association during consolidation can subsequently be recapitulated during reconsolidation and that the transcriptional changes induced by retrieval depend on the remoteness of the memory. On the other hand, we found that NGFI-B is regulated during consolidation but not reconsolidation. This consolidation-specific regulation occurs in hippocampal area CA1. Our discovery of a consolidation-specific transcription indicates that reconsolidation is only a partial recapitulation of consolidation at the transcriptional level. Such partial rather than total recapitulation may have evolved as a more economic and reliable mechanism for organisms to modify memory.

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References

Phillips R, LeDoux J . Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. Learn Mem. 1994; 1(1):34-44. View

Kobayashi T, Deak M, Morrice N, Cohen P . Characterization of the structure and regulation of two novel isoforms of serum- and glucocorticoid-induced protein kinase. Biochem J. 1999; 344 Pt 1:189-97. PMC: 1220630. View

Sara S . Retrieval and reconsolidation: toward a neurobiology of remembering. Learn Mem. 2001; 7(2):73-84. DOI: 10.1101/lm.7.2.73. View

Hall J, Thomas K, Everitt B . Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat Neurosci. 2000; 3(6):533-5. DOI: 10.1038/75698. View

Nader K, Schafe G, Le Doux J . Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature. 2000; 406(6797):722-6. DOI: 10.1038/35021052. View

Malkani S, Rosen J . Induction of NGFI-B mRNA following contextual fear conditioning and its blockade by diazepam. Brain Res Mol Brain Res. 2000; 80(2):153-65. DOI: 10.1016/s0169-328x(00)00130-3. View

Duffy S, Craddock K, Abel T, Nguyen P . Environmental enrichment modifies the PKA-dependence of hippocampal LTP and improves hippocampus-dependent memory. Learn Mem. 2001; 8(1):26-34. PMC: 311356. DOI: 10.1101/lm.36301. View

Jones M, Errington M, French P, Fine A, Bliss T, GAREL S . A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci. 2001; 4(3):289-96. DOI: 10.1038/85138. View

Hall J, Thomas K, Everitt B . Cellular imaging of zif268 expression in the hippocampus and amygdala during contextual and cued fear memory retrieval: selective activation of hippocampal CA1 neurons during the recall of contextual memories. J Neurosci. 2001; 21(6):2186-93. PMC: 6762622. View

10.

Taubenfeld S, Milekic M, Monti B, Alberini C . The consolidation of new but not reactivated memory requires hippocampal C/EBPbeta. Nat Neurosci. 2001; 4(8):813-8. DOI: 10.1038/90520. View

11.

Giese K, Peters M, Vernon J . Modulation of excitability as a learning and memory mechanism: a molecular genetic perspective. Physiol Behav. 2001; 73(5):803-10. DOI: 10.1016/s0031-9384(01)00517-0. View

12.

Stanciu M, Radulovic J, Spiess J . Phosphorylated cAMP response element binding protein in the mouse brain after fear conditioning: relationship to Fos production. Brain Res Mol Brain Res. 2001; 94(1-2):15-24. DOI: 10.1016/s0169-328x(01)00174-7. View

13.

French P, OConnor V, Voss K, Stean T, Hunt S, Bliss T . Seizure-induced gene expression in area CA1 of the mouse hippocampus. Eur J Neurosci. 2002; 14(12):2037-41. DOI: 10.1046/j.0953-816x.2001.01818.x. View

14.

Kida S, Josselyn S, Pena de Ortiz S, Kogan J, Chevere I, Masushige S . CREB required for the stability of new and reactivated fear memories. Nat Neurosci. 2002; 5(4):348-55. DOI: 10.1038/nn819. View

15.

Tsai K, Chen S, Ma Y, Hsu W, Lee E . sgk, a primary glucocorticoid-induced gene, facilitates memory consolidation of spatial learning in rats. Proc Natl Acad Sci U S A. 2002; 99(6):3990-5. PMC: 122636. DOI: 10.1073/pnas.062405399. View

16.

Warntges S, Friedrich B, Henke G, Duranton C, Lang P, Waldegger S . Cerebral localization and regulation of the cell volume-sensitive serum- and glucocorticoid-dependent kinase SGK1. Pflugers Arch. 2002; 443(4):617-24. DOI: 10.1007/s00424-001-0737-1. View

17.

Gamper N, Fillon S, Huber S, Feng Y, Kobayashi T, Cohen P . IGF-1 up-regulates K+ channels via PI3-kinase, PDK1 and SGK1. Pflugers Arch. 2002; 443(4):625-34. DOI: 10.1007/s00424-001-0741-5. View

18.

Tronel S, Sara S . Mapping of olfactory memory circuits: region-specific c-fos activation after odor-reward associative learning or after its retrieval. Learn Mem. 2002; 9(3):105-11. PMC: 182591. DOI: 10.1101/lm.47802. View

19.

Anokhin K, Tiunova A, Rose S . Reminder effects - reconsolidation or retrieval deficit? Pharmacological dissection with protein synthesis inhibitors following reminder for a passive-avoidance task in young chicks. Eur J Neurosci. 2002; 15(11):1759-65. DOI: 10.1046/j.1460-9568.2002.02023.x. View

20.

Rudy J, Barrientos R, OReilly R . Hippocampal formation supports conditioning to memory of a context. Behav Neurosci. 2002; 116(4):530-8. DOI: 10.1037//0735-7044.116.4.530. View