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Elucidating the role of protein synthesis in hippocampus-dependent memory consolidation across the day and night.

ABSTRACT: It is widely acknowledged that de novo protein synthesis is crucial for the formation and consolidation of long-term memories. While the basal activity of many signaling cascades that modulate protein synthesis fluctuates in a circadian fashion, it is unclear whether the temporal dynamics of protein synthesis-dependent memory consolidation vary depending on the time of day. More specifically, it is unclear whether protein synthesis inhibition affects hippocampus-dependent memory consolidation in rodents differentially across the day (i.e., the inactive phase with an abundance of sleep) and night (i.e., the active phase with little sleep). To address this question, male and female C57Bl6/J mice were trained in a contextual fear conditioning task at the beginning or the end of the light phase. Animals received a single systemic injection with the protein synthesis inhibitor anisomycin or vehicle directly, 4, 8 hr, or 11.5 hr following training, and memory was assessed after 24 hr. Here, we show that protein synthesis inhibition impaired the consolidation of context-fear memories selectively when the protein synthesis inhibitor was administered at the first three time points, irrespective of timing of training. Even though the basal activity of signaling pathways regulating de novo protein synthesis may fluctuate across the 24-hr cycle, these results suggest that the temporal dynamics of protein synthesis-dependent memory consolidation are similar for day-time and night-time learning.

SUBMITTER: Raven F

PROVIDER: S-EPMC8596627 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The sleep-to-forget, sleep-to-remember (SFSR) hypothesis states that the neurobiological environment provided by rapid-eye movement (REM)-rich sleep decouples the content of an emotional memory from its attendant emotional arousal. This decoupling allows divergent attenuation and enhancement effects (i.e., erosion of the memory's emotional tone and simultaneous strengthening of its content). However, support for this proposal is mixed. An alternative account suggests there might be convergent attenuation and enhancement (i.e., elevated emotional arousal is positively coupled with enhanced emotional memory). We tested predictions emerging from the SFSR hypothesis using (a) individuals diagnosed with post-traumatic stress disorder (PTSD; n = 21), (b) trauma-exposed non-PTSD individuals (n = 19), and (c) healthy controls (n = 20). We included PTSD-diagnosed individuals because they typically experience altered REM sleep, impaired emotional memory, and heightened emotional arousal in response to threatening stimuli. Participants were assessed before and after both an 8-h period of polysomnographically monitored sleep and an 8-h period of waking activity. The assessment included exposure to negatively valenced, positively valenced, and neutral pictures before the 8-h delay, and a recognition task afterward. We measured emotional arousal by recording psychophysiological responses to the pictures, both pre- and post-delay. Results indicated no significant between-group differences in emotional memory accuracy or arousal. However, after a sleep-filled delay, pictures of all categories were recognized with equal accuracy, whereas after a wake-filled delay, negative pictures were recognized preferentially. Furthermore, the findings demonstrated that a sleep-filled delay was associated with attenuated emotional arousal to pictures of all categories, whereas a wake-filled delay was associated with a rise in emotional arousal across the day. Intriguingly, poorer recognition accuracy for valenced (but not neutral) pictures was predicted by an interaction of increased REM fragmentation and increased emotional arousal. In summary, we found some support for the SFSR hypothesis in the way it describes the REM- and arousal-based mechanisms that process emotional material. We also, however, found disconfirming evidence regarding the outcome of that process (i.e., sleep did not favor consolidation of emotional over neutral memory), and we demonstrated a convergence between attenuation of emotional arousal and weakening of emotional content relative to neutral content.

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Elucidating the role of protein synthesis in hippocampus-dependent memory consolidation across the day and night.

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