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Requirements of Postnatal proBDNF in the Hippocampus for Spatial Memory Consolidation and Neural Function.

ABSTRACT: Mature brain-derived neurotrophic factor (BDNF) and its downstream signaling pathways have been implicated in regulating postnatal development and functioning of rodent brain. However, the biological role of its precursor pro-brain-derived neurotrophic factor (proBDNF) in the postnatal brain remains unknown. The expression of hippocampal proBDNF was blocked in postnatal weeks, and multiple behavioral tests, Western blot and morphological techniques, and neural recordings were employed to investigate how proBDNF played a role in spatial cognition in adults. The peak expression and its crucial effects were found in the fourth but not in the second or eighth postnatal week. Blocking proBDNF expression disrupted spatial memory consolidation rather than learning or memory retrieval. Structurally, blocking proBDNF led to the reduction in spine density and proportion of mature spines. Although blocking proBDNF did not affect N-methyl-D-aspartate (NMDA) receptor (NMDAR) and α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR) subunits, the learning-induced phosphorylation of the GluN2B subunit level declined significantly. Functionally, paired-pulse facilitation, post-low-frequency stimulation (LFS) transiently enhanced depression, and GluN2B-dependent short-lasting long-term depression in the Schaffer collateral-CA1 pathway were weakened. The firing rate of pyramidal neurons was significantly suppressed around the target region during the memory test. Furthermore, the activation of GluN2B-mediated signaling could effectively facilitate neural function and mitigate memory impairment. The findings were consistent with the hypothesis that postnatal proBDNF played an essential role in synaptic and cognitive functions.

SUBMITTER: Sun W

PROVIDER: S-EPMC8319730 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:It is known that sleep reshapes the neural representations that subtend the memories acquired while navigating in a virtual environment. However, navigation is not process-pure, as manifold learning components contribute to performance, notably the spatial and contextual memory constituents. In this context, it remains unclear whether post-training sleep globally promotes consolidation of all of the memory components embedded in virtual navigation, or rather favors the development of specific representations. Here, we investigated the effect of post-training sleep on the neural substrates of the consolidation of spatial and contextual memories acquired while navigating in a complex 3D, naturalistic virtual town. Using fMRI, we mapped regional cerebral activity during various tasks designed to tap either the spatial or the contextual memory component, or both, 72 h after encoding with or without sleep deprivation during the first post-training night. Behavioral performance was not dependent upon post-training sleep deprivation, neither in a natural setting that engages both spatial and contextual memory processes nor when looking more specifically at each of these memory representations. At the neuronal level however, analyses that focused on contextual memory revealed distinct correlations between performance and neuronal activity in frontal areas associated with recollection processes after post-training sleep, and in the parahippocampal gyrus associated with familiarity processes in sleep-deprived participants. Likewise, efficient spatial memory was associated with posterior cortical activity after sleep whereas it correlated with parahippocampal/medial temporal activity after sleep deprivation. Finally, variations in place-finding efficiency in a natural setting encompassing spatial and contextual elements were associated with caudate activity after post-training sleep, suggesting the automation of navigation. These data indicate that post-training sleep modulates the neural substrates of the consolidation of both the spatial and contextual memories acquired during virtual navigation.

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Requirements of Postnatal proBDNF in the Hippocampus for Spatial Memory Consolidation and Neural Function.

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