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Dynamical Mechanism Underlying Scale-Free Network Reorganization in Low Acetylcholine States Corresponding to Slow Wave Sleep.

ABSTRACT: Sleep is indispensable for most animals' cognitive functions, and is hypothesized to be a major factor in memory consolidation. Although we do not fully understand the mechanisms of network reorganisation driving memory consolidation, available data suggests that sleep-associated neurochemical changes may be important for such processes. In particular, global acetylcholine levels change across the sleep/wake cycle, with high cholinergic tone during wake and REM sleep and low cholinergic tone during slow wave sleep. Furthermore, experimental perturbation of cholinergic tone has been shown to impact memory storage. Through in silico modeling of neuronal networks, we show how spiking dynamics change in highly heterogenous networks under varying levels of cholinergic tone, with neuronal networks under high cholinergic modulation firing asynchronously and at high frequencies, while those under low cholinergic modulation exhibit synchronous patterns of activity. We further examined the network's dynamics and its reorganization mediated via changing levels of acetylcholine within the context of different scale-free topologies, comparing network activity within the hub cells, a small group of neurons having high degree connectivity, and with the rest of the network. We show a dramatic, state-dependent change in information flow throughout the network, with highly active hub cells integrating information in a high-acetylcholine state, and transferring it to rest of the network in a low-acetylcholine state. This result is experimentally corroborated by frequency-dependent frequency changes observed in vivo experiments. Together, these findings provide insight into how new neurons are recruited into memory traces during sleep, a mechanism which may underlie system memory consolidation.

SUBMITTER: Czarnecki P

PROVIDER: S-EPMC9249096 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThere is evidence that slow wave sleep (SWS) promotes the consolidation of memories that are subserved by mediotemporal- and hippocampo-cortical neural networks. In contrast to implicit memories, explicit memories are accompanied by conscious (attentive and controlled) processing. Awareness at pre-sleep encoding has been recognized as critical for the off-line memory consolidation. The present study elucidated the role of task-dependent cortical activation guided by attentional control at pre-sleep encoding for the consolidation of hippocampus-dependent memories during sleep.MethodologyA task with a hidden regularity was used (Number Reduction Task, NRT), in which the responses that can be implicitly predicted by the hidden regularity activate hippocampo-cortical networks more strongly than responses that cannot be predicted. Task performance was evaluated before and after early-night sleep, rich in SWS, and late-night sleep, rich in rapid eye movement (REM) sleep. In implicit conditions, slow cortical potentials (SPs) were analyzed to reflect the amount of controlled processing and the localization of activated neural task representations.Principal findingsDuring implicit learning before sleep, the amount of controlled processing did not differ between unpredictable and predictable responses, nor between early- and late-night sleep groups. A topographic re-distribution of SPs indicating a spatial reorganization occurred only after early, not after late sleep, and only for predictable responses. These SP changes correlated with the amount of SWS and were covert because off-line RT decrease did not differentiate response types or sleep groups.ConclusionsIt is concluded that SWS promotes the neural reorganization of task representations that rely on the hippocampal system despite absence of conscious access to these representations.SignificanceOriginal neurophysiologic evidence is provided for the role of SWS in the consolidation of memories encoded with hippocampo-cortical interaction before sleep. It is demonstrated that this SWS-mediated mechanism does not depend critically on explicitness at learning nor on the amount of controlled executive processing during pre-sleep encoding.

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Dynamical Mechanism Underlying Scale-Free Network Reorganization in Low Acetylcholine States Corresponding to Slow Wave Sleep.

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