Pathway-Dependent Regulation of Sleep Dynamics in a Network Model of the Sleep–Wake Cycle

Sleep is a fundamental homeostatic process within the animal kingdom. Although various brain areas and cell types are involved in the regulation of the sleep–wake cycle, it is still unclear how different pathways between neural populations contribute to its regulation. Here we address this issue by...

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Main Authors: Charlotte Héricé, Shuzo Sakata
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-12-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnins.2019.01380/full
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author Charlotte Héricé
Shuzo Sakata
author_facet Charlotte Héricé
Shuzo Sakata
author_sort Charlotte Héricé
collection DOAJ
description Sleep is a fundamental homeostatic process within the animal kingdom. Although various brain areas and cell types are involved in the regulation of the sleep–wake cycle, it is still unclear how different pathways between neural populations contribute to its regulation. Here we address this issue by investigating the behavior of a simplified network model upon synaptic weight manipulations. Our model consists of three neural populations connected by excitatory and inhibitory synapses. Activity in each population is described by a firing-rate model, which determines the state of the network. Namely wakefulness, rapid eye movement (REM) sleep or non-REM (NREM) sleep. By systematically manipulating the synaptic weight of every pathway, we show that even this simplified model exhibits non-trivial behaviors: for example, the wake-promoting population contributes not just to the induction and maintenance of wakefulness, but also to sleep induction. Although a recurrent excitatory connection of the REM-promoting population is essential for REM sleep genesis, this recurrent connection does not necessarily contribute to the maintenance of REM sleep. The duration of NREM sleep can be shortened or extended by changes in the synaptic strength of the pathways from the NREM-promoting population. In some cases, there is an optimal range of synaptic strengths that affect a particular state, implying that the amount of manipulations, not just direction (i.e., activation or inactivation), needs to be taken into account. These results demonstrate pathway-dependent regulation of sleep dynamics and highlight the importance of systems-level quantitative approaches for sleep–wake regulatory circuits.
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spelling doaj.art-9a266642cc72409e9e7b3fae6b7e69372022-12-22T01:09:30ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2019-12-011310.3389/fnins.2019.01380497195Pathway-Dependent Regulation of Sleep Dynamics in a Network Model of the Sleep–Wake CycleCharlotte HéricéShuzo SakataSleep is a fundamental homeostatic process within the animal kingdom. Although various brain areas and cell types are involved in the regulation of the sleep–wake cycle, it is still unclear how different pathways between neural populations contribute to its regulation. Here we address this issue by investigating the behavior of a simplified network model upon synaptic weight manipulations. Our model consists of three neural populations connected by excitatory and inhibitory synapses. Activity in each population is described by a firing-rate model, which determines the state of the network. Namely wakefulness, rapid eye movement (REM) sleep or non-REM (NREM) sleep. By systematically manipulating the synaptic weight of every pathway, we show that even this simplified model exhibits non-trivial behaviors: for example, the wake-promoting population contributes not just to the induction and maintenance of wakefulness, but also to sleep induction. Although a recurrent excitatory connection of the REM-promoting population is essential for REM sleep genesis, this recurrent connection does not necessarily contribute to the maintenance of REM sleep. The duration of NREM sleep can be shortened or extended by changes in the synaptic strength of the pathways from the NREM-promoting population. In some cases, there is an optimal range of synaptic strengths that affect a particular state, implying that the amount of manipulations, not just direction (i.e., activation or inactivation), needs to be taken into account. These results demonstrate pathway-dependent regulation of sleep dynamics and highlight the importance of systems-level quantitative approaches for sleep–wake regulatory circuits.https://www.frontiersin.org/article/10.3389/fnins.2019.01380/fullsleep regulatory circuitscomputational modelbrain statesleep/wake cyclePython programing language
spellingShingle Charlotte Héricé
Shuzo Sakata
Pathway-Dependent Regulation of Sleep Dynamics in a Network Model of the Sleep–Wake Cycle
Frontiers in Neuroscience
sleep regulatory circuits
computational model
brain state
sleep/wake cycle
Python programing language
title Pathway-Dependent Regulation of Sleep Dynamics in a Network Model of the Sleep–Wake Cycle
title_full Pathway-Dependent Regulation of Sleep Dynamics in a Network Model of the Sleep–Wake Cycle
title_fullStr Pathway-Dependent Regulation of Sleep Dynamics in a Network Model of the Sleep–Wake Cycle
title_full_unstemmed Pathway-Dependent Regulation of Sleep Dynamics in a Network Model of the Sleep–Wake Cycle
title_short Pathway-Dependent Regulation of Sleep Dynamics in a Network Model of the Sleep–Wake Cycle
title_sort pathway dependent regulation of sleep dynamics in a network model of the sleep wake cycle
topic sleep regulatory circuits
computational model
brain state
sleep/wake cycle
Python programing language
url https://www.frontiersin.org/article/10.3389/fnins.2019.01380/full
work_keys_str_mv AT charlotteherice pathwaydependentregulationofsleepdynamicsinanetworkmodelofthesleepwakecycle
AT shuzosakata pathwaydependentregulationofsleepdynamicsinanetworkmodelofthesleepwakecycle