Effects of sleep deprivation on different phases of memory in the rat: dissociation between contextual and tone fear conditioning tasks

Abstract

Numerous studies show that sleep deprivation (SD) impacts negatively on cognitive processes, including learning and memory. Memory formation encompasses distinct phases of which acquisition, consolidation and retrieval are better known. Previous studies with pre-training SD induced by the platform method have shown impairment in fear conditioning tasks. Nonetheless, pre-training manipulations do not allow the distinction between effects on acquisition and/or consolidation, interfering, ultimately, on recall of/performance in the task. In the present study, animals were first trained in contextual and tone fear conditioning (TFC) tasks and then submitted to SD with the purpose to evaluate the effect of this manipulation on different stages of the learning process, e.g., in the uptake of (new) information during learning, its encoding and stabilization, and the recall of stored memories. Besides, we also investigated the effect of SD in the extinction of fear memory and a possible state-dependent learning induced by this manipulation. For each task (contextual or TFC), animals were trained and then distributed into control, not sleep-deprived (CTL) and SD groups, the latter being submitted to the modified multiple platform paradigm for 96 h. Subsets of eight rats in each group/experiment were submitted to the test of the tasks, either immediately or at different time intervals after SD. The results indicated that (a) pre- but not post-training SD impaired recall in the contextual and TFC; (b) this impairment was not state-dependent; and (c) in the contextual fear conditioning (CFC), pre-test SD prevented extinction of the learned task. Overall, these results suggest that SD interferes with acquisition, recall and extinction, but not necessarily with consolidation of emotional memory.

Behavioral and Neurobiological Assessments of Predator-Based Fear Conditioning and Extinction

“…Finally, Experiment 3 provided support for the hypothesis that sleep deprivation would impair hippocampus-dependent contextual, but not amygdala-mediated cue, fear memory. This finding is consistent with other work that demonstrates that sleep deprivation targets contextual, but not cued, fear memory with shock as reinforcement [101] [104] [106] [142].…”

Explicit memory, anxiety and depressive like behavior in mice exposed to chronic intermittent hypoxia, sleep fragmentation, or both during the daylight period

“…Our findings are congruent with the previous findings involving sleep manipulations or IH models of OSA in rodents. Indeed, cognitive impairments have emerged with sleep deprivation by exploring different learning and memory test paradigms, such as the Morris water maze ( Nair et al, 2011a , 2011b ; Tartar et al, 2006 ; Xie et al, 2020 ), contextual fear conditioning ( Rossi et al, 2014 ; Sharma et al, 2021 ), inhibitory avoidance discrimination task ( Bueno et al, 1994 ; Perry et al, 2008 ) and the NOR test ( Djonlagic et al, 2012 ; Gozal et al, 2017 ; Kim et al, 2015 ; Palchykova et al, 2006 ). The latter NOR task has gained popularity in the investigation of memory alterations, since this test is based on the innate exploratory behavior of the rodent in the absence of externally applied rules or reinforcement ( Antunes and Biala, 2012 ).…”

The basolateral amygdala can mediate the effects of fear memory on sleep independently of fear behavior and the peripheral stress response

“…Recent work (Wellman et al, 2016) and the current study also demonstrate that individual outbred rats can show either decreases or increases in REM in response to IS, also without differences in freezing or SIH. Thus, while several studies have demonstrated that sleep may play a role in the consolidation of contextual fear memory associated with brief or mild fearful experiences (e.g., Graves, Heller, Pack, and Abel, 2003; Greenwood, Thompson, Opp, and Fleshner, 2014; Hagewoud, Bultsma, Barf, Koolhaas, and Meerlo, 2011; Hellman and Abel, 2007; Kumar and Jha, 2012; Menz, Rihm, and Büchel, 2016; Menz, Rihm, Salari, Born, Kalisch, Pape, Marshall, and Buchel, 2013; Rossi, Tiba, Moreira, Ferreira, Oliveira, and Suchecki, 2014; Silvestri, 2005; for recent review see Havekes, Meerlo, and Abel, 2015), there is no evidence that REM sleep is necessary for the formation of contextual fear memory associated with relatively intense stressful experiences. Interestingly, we found no correlation between freezing and either REM or NREM sleep.…”