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Sleep is required to consolidate odor memory and remodel olfactory synapses.

ABSTRACT: Animals with complex nervous systems demand sleep for memory consolidation and synaptic remodeling. Here, we show that, although the Caenorhabditis elegans nervous system has a limited number of neurons, sleep is necessary for both processes. In addition, it is unclear if, in any system, sleep collaborates with experience to alter synapses between specific neurons and whether this ultimately affects behavior. C. elegans neurons have defined connections and well-described contributions to behavior. We show that spaced odor-training and post-training sleep induce long-term memory. Memory consolidation, but not acquisition, requires a pair of interneurons, the AIYs, which play a role in odor-seeking behavior. In worms that consolidate memory, both sleep and odor conditioning are required to diminish inhibitory synaptic connections between the AWC chemosensory neurons and the AIYs. Thus, we demonstrate in a living organism that sleep is required for events immediately after training that drive memory consolidation and alter synaptic structures.

SUBMITTER: Chandra R

PROVIDER: S-EPMC10354834 | biostudies-literature | 2023 Jun

REPOSITORIES: biostudies-literature

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Sleep is required to consolidate odor memory and remodel olfactory synapses.

Chandra Rashmi R Farah Fatima F Muñoz-Lobato Fernando F Bokka Anirudh A Benedetti Kelli L KL Brueggemann Chantal C Saifuddin Mashel Fatema A MFA Miller Julia M JM Li Joy J Chang Eric E Varshney Aruna A Jimenez Vanessa V Baradwaj Anjana A Nassif Cibelle C Alladin Sara S Andersen Kristine K Garcia Angel J AJ Bi Veronica V Nordquist Sarah K SK Dunn Raymond L RL Garcia Vanessa V Tokalenko Kateryna K Soohoo Emily E Briseno Fabiola F Kaur Sukhdeep S Harris Malcolm M Guillen Hazel H Byrd Decklin D Fung Brandon B Bykov Andrew E AE Odisho Emma E Tsujimoto Bryan B Tran Alan A Duong Alex A Daigle Kevin C KC Paisner Rebekka R Zuazo Carlos E CE Lin Christine C Asundi Aarati A Churgin Matthew A MA Fang-Yen Christopher C Bremer Martina M Kato Saul S VanHoven Miri K MK L'Étoile Noëlle D ND

Cell 20230602 13

Animals with complex nervous systems demand sleep for memory consolidation and synaptic remodeling. Here, we show that, although the Caenorhabditis elegans nervous system has a limited number of neurons, sleep is necessary for both processes. In addition, it is unclear if, in any system, sleep collaborates with experience to alter synapses between specific neurons and whether this ultimately affects behavior. C. elegans neurons have defined connections and well-described contributions to behavio ...[more]

PMID: 37269832

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Project description:UnlabelledNeural circuits that undergo reorganization by newborn interneurons in the olfactory bulb (OB) are necessary for odor detection and discrimination, olfactory memory, and innate olfactory responses, including predator avoidance and sexual behaviors. The OB possesses many interneurons, including various types of granule cells (GCs); however, the contribution that each type of interneuron makes to olfactory behavioral control remains unknown. Here, we investigated the in vivo functional role of oncofetal trophoblast glycoprotein 5T4, a regulator for dendritic arborization of 5T4-expressing GCs (5T4 GCs), the level of which is reduced in the OB of 5T4 knock-out (KO) mice. Electrophysiological recordings with acute OB slices indicated that external tufted cells (ETCs) can be divided into two types, bursting and nonbursting. Optogenetic stimulation of 5T4 GCs revealed their connection to both bursting and nonbursting ETCs, as well as to mitral cells (MCs). Interestingly, nonbursting ETCs received fewer inhibitory inputs from GCs in 5T4 KO mice than from those in wild-type (WT) mice, whereas bursting ETCs and MCs received similar inputs in both mice. Furthermore, 5T4 GCs received significantly fewer excitatory inputs in 5T4 KO mice. Remarkably, in olfactory behavior tests, 5T4 KO mice had higher odor detection thresholds than the WT, as well as defects in odor discrimination learning. Therefore, the loss of 5T4 attenuates inhibitory inputs from 5T4 GCs to nonbursting ETCs and excitatory inputs to 5T4 GCs, contributing to disturbances in olfactory behavior. Our novel findings suggest that, among the various types of OB interneurons, the 5T4 GC subtype is required for odor detection and discrimination behaviors.Significance statementNeuronal circuits in the brain include glutamatergic principal neurons and GABAergic interneurons. Although the latter is a minority cell type, they are vital for normal brain function because they regulate the activity of principal neurons. If interneuron function is impaired, brain function may be damaged, leading to behavior disorder. The olfactory bulb (OB) possesses various types of interneurons, including granule cells (GCs); however, the contribution that each type of interneuron makes to the control of olfactory behavior remains unknown. Here, we analyzed electrophysiologically and behaviorally the function of oncofetal trophoblast glycoprotein 5T4, a regulator for dendritic branching in OB GCs. We found that, among the various types of OB interneuron, the 5T4 GC subtype is required for odor detection and odor discrimination behaviors.

Dataset Information

Sleep is required to consolidate odor memory and remodel olfactory synapses.

Publications

Sleep is required to consolidate odor memory and remodel olfactory synapses.

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