Circadian Rhythms in Fear Conditioning: An Overview of Behavioral, Brain System, and Molecular Interactions

Overview

Journal Neural Plast

Specialty Neurology

Date 2017 Jul 13

PMID 28698810

Citations 14

Authors

Anne Albrecht

Oliver Stork

Affiliations

Soon will be listed here.

Abstract

The formation of fear memories is a powerful and highly evolutionary conserved mechanism that serves the behavioral adaptation to environmental threats. Accordingly, classical fear conditioning paradigms have been employed to investigate fundamental molecular processes of memory formation. Evidence suggests that a circadian regulation mechanism allows for a timestamping of such fear memories and controlling memory salience during both their acquisition and their modification after retrieval. These mechanisms include an expression of molecular clocks in neurons of the amygdala, hippocampus, and medial prefrontal cortex and their tight interaction with the intracellular signaling pathways that mediate neural plasticity and information storage. The cellular activities are coordinated across different brain regions and neural circuits through the release of glucocorticoids and neuromodulators such as acetylcholine, which integrate circadian and memory-related activation. Disturbance of this interplay by circadian phase shifts or traumatic experience appears to be an important factor in the development of stress-related psychopathology, considering these circadian components are of critical importance for optimizing therapeutic approaches to these disorders.

Citing Articles

Differential Expression of Circadian Clock Genes in the Bovine Neuroendocrine Adrenal System.

Earnhardt-San A, Baker E, Riley D, Ghaffari N, Long C, Cardoso R Genes (Basel). 2023; 14(11).

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Emotionally clocked out: cell-type specific regulation of mood and anxiety by the circadian clock system in the brain.

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Time of Day-Dependent Alteration of Hippocampal Rac1 Activation Regulates Contextual Fear Memory in Rats.

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References

Kaouane N, Porte Y, Vallee M, Brayda-Bruno L, Mons N, Calandreau L . Glucocorticoids can induce PTSD-like memory impairments in mice. Science. 2012; 335(6075):1510-3. DOI: 10.1126/science.1207615. View

Cestari V, Rossi-Arnaud C, Saraulli D, Costanzi M . The MAP(K) of fear: from memory consolidation to memory extinction. Brain Res Bull. 2013; 105:8-16. DOI: 10.1016/j.brainresbull.2013.09.007. View

Phillips R, LeDoux J . Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci. 1992; 106(2):274-85. DOI: 10.1037//0735-7044.106.2.274. View

Woodruff E, Greenwood B, Chun L, Fardi S, Hinds L, Spencer R . Adrenal-dependent diurnal modulation of conditioned fear extinction learning. Behav Brain Res. 2015; 286:249-55. PMC: 4465528. DOI: 10.1016/j.bbr.2015.03.006. View

Fanselow M, Dong H . Are the dorsal and ventral hippocampus functionally distinct structures?. Neuron. 2010; 65(1):7-19. PMC: 2822727. DOI: 10.1016/j.neuron.2009.11.031. View

Yeckel M, Berger T . Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. Proc Natl Acad Sci U S A. 1990; 87(15):5832-6. PMC: 54422. DOI: 10.1073/pnas.87.15.5832. View

Moustafa A, Gilbertson M, Orr S, Herzallah M, Servatius R, Myers C . A model of amygdala-hippocampal-prefrontal interaction in fear conditioning and extinction in animals. Brain Cogn. 2012; 81(1):29-43. PMC: 3808183. DOI: 10.1016/j.bandc.2012.10.005. View

Lamont E, Robinson B, Stewart J, Amir S . The central and basolateral nuclei of the amygdala exhibit opposite diurnal rhythms of expression of the clock protein Period2. Proc Natl Acad Sci U S A. 2005; 102(11):4180-4. PMC: 554834. DOI: 10.1073/pnas.0500901102. View

Mahan A, Ressler K . Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder. Trends Neurosci. 2011; 35(1):24-35. PMC: 3206195. DOI: 10.1016/j.tins.2011.06.007. View

10.

Keiser A, Turnbull L, Darian M, Feldman D, Song I, Tronson N . Sex Differences in Context Fear Generalization and Recruitment of Hippocampus and Amygdala during Retrieval. Neuropsychopharmacology. 2016; 42(2):397-407. PMC: 5399239. DOI: 10.1038/npp.2016.174. View

11.

Harrison E, Carmack S, Block C, Sun J, Anagnostaras S, Gorman M . Circadian waveform bifurcation, but not phase-shifting, leaves cued fear memory intact. Physiol Behav. 2016; 169:106-113. DOI: 10.1016/j.physbeh.2016.11.033. View

12.

Dalm S, Enthoven L, Meijer O, van der Mark M, Karssen A, de Kloet E . Age-related changes in hypothalamic-pituitary-adrenal axis activity of male C57BL/6J mice. Neuroendocrinology. 2005; 81(6):372-80. DOI: 10.1159/000089555. View

13.

Pantazopoulos H, Dolatshad H, Davis F . A fear-inducing odor alters PER2 and c-Fos expression in brain regions involved in fear memory. PLoS One. 2011; 6(5):e20658. PMC: 3105109. DOI: 10.1371/journal.pone.0020658. View

14.

Schafe G, Nader K, Blair H, LeDoux J . Memory consolidation of Pavlovian fear conditioning: a cellular and molecular perspective. Trends Neurosci. 2001; 24(9):540-6. DOI: 10.1016/s0166-2236(00)01969-x. View

15.

Maren S . Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci. 2001; 24:897-931. DOI: 10.1146/annurev.neuro.24.1.897. View

16.

Schwabe L, Joels M, Roozendaal B, Wolf O, Oitzl M . Stress effects on memory: an update and integration. Neurosci Biobehav Rev. 2011; 36(7):1740-9. DOI: 10.1016/j.neubiorev.2011.07.002. View

17.

Genzel L, Spoormaker V, Konrad B, Dresler M . The role of rapid eye movement sleep for amygdala-related memory processing. Neurobiol Learn Mem. 2015; 122:110-21. DOI: 10.1016/j.nlm.2015.01.008. View

18.

Ressler K, Paschall G, Davis M . Regulation of synaptic plasticity genes during consolidation of fear conditioning. J Neurosci. 2002; 22(18):7892-902. PMC: 6758105. View

19.

Jin X, Lu Y, Yang X, Ma L, Li B . Glucocorticoid receptors in the basolateral nucleus of amygdala are required for postreactivation reconsolidation of auditory fear memory. Eur J Neurosci. 2007; 25(12):3702-12. DOI: 10.1111/j.1460-9568.2007.05621.x. View

20.

Akirav I, Richter-Levin G . Mechanisms of amygdala modulation of hippocampal plasticity. J Neurosci. 2002; 22(22):9912-21. PMC: 6757810. View