Dorsal subcoeruleus nucleus (SubCD) involvement in context-associated fear memory consolidation
- 367 Downloads
The neurobiological mechanisms of emotional memory processing can be investigated using classical fear conditioning as a model system, and evidence from multiple lines of research suggests that sleep influences consolidation of emotional memory. In rodents, some of this evidence comes from a common finding that sleep deprivation from 0 to 6 h after fear conditioning training impairs processing of conditioned fear memory. Here, we show that during a 6-h session of sleep–wake (S–W) recording, immediately after a session of context-associated fear conditioning training, rats spent more time in wakefulness (W) and less time in slow-wave sleep (SWS) and rapid eye movement (REM) sleep. This context-associated fear conditioning training-induced reduction in SWS lasts for 2 h, and the REM sleep reduction lasts throughout the entire 6-h post-training S–W recording period. Interestingly, these reductions in SWS and REM sleep during this 6-h period did not impair memory consolidation for context-associated fear conditioning. The results of this study show, for the first time, that lesions within the dorsal part of the subcoeruleus nucleus (SubCD), which were unintentionally caused by the implantation of bipolar recording electrodes, impair consolidation of context-associated fear conditioning memory. Together, the results of these experiments suggest that emotional memory processing associated with fear conditioning can be completed successfully within less than a normal amount of sleep, but it requires a structurally and functionally intact SubCD, an area in the brain stem where phasic pontine wave (P-wave) generating cells are located.
KeywordsFear conditioning Memory consolidation Wakefulness Slow-wave sleep REM sleep Subcoeruleus nucleus
This study was supported by Boston University School of Medicine and National Institute of Health Research Grant (MH59839). We thank Dr. D. A. Ciraulo and Dr. E. H. Patterson for critical reading and constructive suggestions to improve the quality of this manuscript. We also thank Matthew W. O’Malley for his technical support.
- Datta S (2000) Avoidance task training potentiates phasic pontine-wave density in the rat: a mechanism for sleep-dependent plasticity. J Neurosci 20:8607–8613 Google Scholar
- Datta S (2010) Sleep: learning and memory. Encyclopedia of behavioral neuroscience, vol 3, Elsevier Inc., Oxford Academic Press: New York, pp 218–226Google Scholar
- Kumar T, Jha SK (2012) Sleep deprivation impairs consolidation of cued fear memory in rats. PLoS ONE 7(e47042):1–8Google Scholar
- Lavie P (2001b) Eye movements during REM sleep. Exp Brain Res 192:657–667Google Scholar
- LeDoux JE (2002) Emotion, memory and the brain. In: Scientific American, Special Edition, pp 62–71Google Scholar
- Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates. Academic Press, San DiegoGoogle Scholar
- Rebeiro S, Mello CV, Velho T, Gardner TJ, Jarvis ED, Pavlides C (2002) Induction of hippocampal long-term potentiation during waking leads to increased extrahippocampal zif-268 expression during ensuing rapid-eye-movement sleep. J Neurosci 22:10914–10923Google Scholar
- Rosales-Lagarde A, Armony JL, Del Rio-Portilla Y, Trejo-Martinez D, Conde R, Corsi-Cabrera M (2012) Enhanced emotional reactivity after selective REM sleep deprivation in humans: an fMRI study. Front Behav Neurosci 6(25):p1–p13Google Scholar
- Soliman F, Glatt CE, Bath KG, Levita L, Jones RM, Pattwell SS, Jing D, Tottenham N, Amso D, Somerville LH, Voss HU, Glover G, Ballon DJ, Liston C, Teslovich T, Van Kempen T, Lee FS, Casey BJ (2010) A genetic variant BDNF polymorphism alters extinction learning in both mouse and human. Science 327:863–866PubMedCentralPubMedCrossRefGoogle Scholar