Amygdala Regulation of Immediate-early Gene Expression in the Hippocampus Induced by Contextual Fear Conditioning

Overview

Journal J Neurosci

Specialty Neurology

Date 2006 Feb 3

PMID 16452685

Citations 75

Authors

Nicole C Huff

Matthew Frank

Karli Wright-Hardesty

David Sprunger

Patricia Matus-Amat

Emily Higgins

Jerry W Rudy

Affiliations

Soon will be listed here.

Abstract

The basolateral nuclei of the amygdala (BLA) are thought to modulate memory storage in other brain regions (McGaugh, 2004). We reported that BLA modulates the memory for both an explored context and for contextual fear conditioning. Both of these memories depend on the hippocampus. Here, we examined the hypothesis that the BLA exerts its modulatory effect by regulating the expression of immediate-early genes (IEGs) in the hippocampus. The main findings of these experiments were: (1) Arc activity-regulated cytoskeletal protein (Arc), an immediate-early gene (also termed Arg 3.1) and c-fos mRNA are induced in the hippocampus after a context exposure, or context plus shock experience, but not after an immediate shock; and (2) BLA inactivation with muscimol attenuated the increase in Arc and c-fos mRNA in the hippocampus associated with contextual fear conditioning but did not influence Arc mRNA associated with context exploration. These results support the hypothesis that the amygdala modulates contextual fear memory by regulating expression of IEGs in the hippocampus.

Citing Articles

Impact of amygdala functional connectivity on cognitive impairment in Alzheimer's disease.

Kicik A, Kurt E, Hari E, Ulasoglu-Yildiz C, Gurvit H, Demiralp T Neurol Sci. 2025; .

PMID: 40055296 DOI: 10.1007/s10072-025-08091-0.

Learned phenotypes emerge during social stress modifying hippocampal orexin receptor gene expression.

Yaeger J, Achua J, Booth C, Khalid D, John M, Ledesma L Sci Rep. 2024; 14(1):31691.

PMID: 39738291 PMC: 11685668. DOI: 10.1038/s41598-024-81590-w.

Fear Reduced Through Unconditional Stimulus Deflation Is Behaviorally Distinct From Extinction and Differentially Engages the Amygdala.

Bonanno G, Met Hoxha E, Robinson P, Ferrara N, Trask S Biol Psychiatry Glob Open Sci. 2023; 3(4):756-765.

PMID: 37881558 PMC: 10593882. DOI: 10.1016/j.bpsgos.2023.01.001.

The amygdala mediates the facilitating influence of emotions on memory through multiple interacting mechanisms.

Pare D, Headley D Neurobiol Stress. 2023; 24:100529.

PMID: 36970449 PMC: 10034520. DOI: 10.1016/j.ynstr.2023.100529.

Structural brain abnormalities in endothelial nitric oxide synthase-deficient mice revealed by high-resolution magnetic resonance imaging.

George H, Mercer G, Stapleton D, Dawson L, MacCallum P, Spring S Brain Behav. 2022; 12(11):e2801.

PMID: 36259950 PMC: 9660425. DOI: 10.1002/brb3.2801.

References

Huff N, Wright-Hardesty K, Higgins E, Matus-Amat P, Rudy J . Context pre-exposure obscures amygdala modulation of contextual-fear conditioning. Learn Mem. 2005; 12(5):456-60. DOI: 10.1101/lm.6705. View

Matus-Amat P, Higgins E, Barrientos R, Rudy J . The role of the dorsal hippocampus in the acquisition and retrieval of context memory representations. J Neurosci. 2004; 24(10):2431-9. PMC: 6729490. DOI: 10.1523/JNEUROSCI.1598-03.2004. 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

Link W, Konietzko U, Kauselmann G, Krug M, Schwanke B, Frey U . Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc Natl Acad Sci U S A. 1995; 92(12):5734-8. PMC: 41771. DOI: 10.1073/pnas.92.12.5734. View

Rudy J, OReilly R . Contextual fear conditioning, conjunctive representations, pattern completion, and the hippocampus. Behav Neurosci. 1999; 113(5):867-80. DOI: 10.1037//0735-7044.113.5.867. View

Guzowski J . Insights into immediate-early gene function in hippocampal memory consolidation using antisense oligonucleotide and fluorescent imaging approaches. Hippocampus. 2002; 12(1):86-104. DOI: 10.1002/hipo.10010. View

Hess U, Gall C, Granger R, Lynch G . Differential patterns of c-fos mRNA expression in amygdala during successive stages of odor discrimination learning. Learn Mem. 1999; 4(3):262-83. DOI: 10.1101/lm.4.3.262. View

Tischmeyer W, Grimm R . Activation of immediate early genes and memory formation. Cell Mol Life Sci. 1999; 55(4):564-74. PMC: 11146814. DOI: 10.1007/s000180050315. View

Chomczynski P, Sacchi N . Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987; 162(1):156-9. DOI: 10.1006/abio.1987.9999. View

10.

McGaugh J . The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci. 2004; 27:1-28. DOI: 10.1146/annurev.neuro.27.070203.144157. View

11.

Huff N, Rudy J . The amygdala modulates hippocampus-dependent context memory formation and stores cue-shock associations. Behav Neurosci. 2004; 118(1):53-62. DOI: 10.1037/0735-7044.118.1.53. View

12.

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

13.

Fanselow M . Contextual fear, gestalt memories, and the hippocampus. Behav Brain Res. 2000; 110(1-2):73-81. DOI: 10.1016/s0166-4328(99)00186-2. View

14.

Guzowski J, Setlow B, Wagner E, McGaugh J . Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J Neurosci. 2001; 21(14):5089-98. PMC: 6762831. View

15.

McIntyre C, Power A, Roozendaal B, McGaugh J . Role of the basolateral amygdala in memory consolidation. Ann N Y Acad Sci. 2003; 985:273-93. DOI: 10.1111/j.1749-6632.2003.tb07088.x. View

16.

Roozendaal B . Systems mediating acute glucocorticoid effects on memory consolidation and retrieval. Prog Neuropsychopharmacol Biol Psychiatry. 2003; 27(8):1213-23. DOI: 10.1016/j.pnpbp.2003.09.015. View

17.

Martin J . Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat. Neurosci Lett. 1991; 127(2):160-4. DOI: 10.1016/0304-3940(91)90784-q. View

18.

Guzowski J, McNaughton B, Barnes C, Worley P . Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci. 1999; 2(12):1120-4. DOI: 10.1038/16046. View

19.

Barrientos R, OReilly R, Rudy J . Memory for context is impaired by injecting anisomycin into dorsal hippocampus following context exploration. Behav Brain Res. 2002; 134(1-2):299-306. DOI: 10.1016/s0166-4328(02)00045-1. View

20.

Lyford G, Yamagata K, Kaufmann W, Barnes C, Sanders L, Copeland N . Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron. 1995; 14(2):433-45. DOI: 10.1016/0896-6273(95)90299-6. View