Early alterations in the MCH system link aberrant neuronal activity and sleep disturbances in a mouse model of Alzheimer’s disease

Sara Calafate*, Gökhan Özturan, Nicola Thrupp, Jeroen Vanderlinden, Luísa Santa-Marinha, Rafaela Morais-Ribeiro, Antonella Ruggiero, Ivan Bozic, Thomas Rusterholz, Blanca Lorente-Echeverría, Marcelo Dias, Wei Ting Chen, Mark Fiers, Ashley Lu, Ine Vlaeminck, Eline Creemers, Katleen Craessaerts, Joris Vandenbempt, Luuk van Boekholdt, Suresh PoovathingalKristofer Davie, Dietmar Rudolf Thal, Keimpe Wierda, Tiago Gil Oliveira, Inna Slutsky, Antoine Adamantidis, Bart De Strooper*, Joris de Wit*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

22 Scopus citations

Abstract

Early Alzheimer’s disease (AD) is associated with hippocampal hyperactivity and decreased sleep quality. Here we show that homeostatic mechanisms transiently counteract the increased excitatory drive to CA1 neurons in App NL-G-F mice, but that this mechanism fails in older mice. Spatial transcriptomics analysis identifies Pmch as part of the adaptive response in App NL-G-F mice. Pmch encodes melanin-concentrating hormone (MCH), which is produced in sleep–active lateral hypothalamic neurons that project to CA1 and modulate memory. We show that MCH downregulates synaptic transmission, modulates firing rate homeostasis in hippocampal neurons and reverses the increased excitatory drive to CA1 neurons in App NL-G-F mice. App NL-G-F mice spend less time in rapid eye movement (REM) sleep. App NL-G-F mice and individuals with AD show progressive changes in morphology of CA1-projecting MCH axons. Our findings identify the MCH system as vulnerable in early AD and suggest that impaired MCH-system function contributes to aberrant excitatory drive and sleep defects, which can compromise hippocampus-dependent functions.

Original languageEnglish
Pages (from-to)1021-1031
Number of pages11
JournalNature Neuroscience
Volume26
Issue number6
DOIs
StatePublished - Jun 2023

Funding

FundersFunder number
AARF
InfraMouse
VIB-KU
KU Leuven/Flemish Government
Stiftung Synapsis - Alzheimer Forschung Schweiz AFS
Fonds Wetenschappelijk Onderzoek
KU Leuven/Flemish
Stichting Alzheimer Onderzoek
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
Alzheimer’s Association Research Foundation
European Research Council ERC-CELLPHASE_AD834682
European Research Council
Inselspital, Universitätsspital BernCoG-725850
Horizon 2020 Framework Programme834682, 724866, 725850
Fundação para a Ciência e a TecnologiaPD/BD/150580/2020
SAO-FRA2020/017
KU Leuven-VIBZW09-03
University of BernG0F8516N, G065721N
Vlaamse regering2019/0013, G0H2818N

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