Sleep is required to consolidate odor memory and remodel olfactory synapses

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 colla...

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Published in:Cell 2023-06, Vol.186 (13), p.2911-2928.e20
Main Authors: Chandra, Rashmi, Farah, Fatima, Muñoz-Lobato, Fernando, Bokka, Anirudh, Benedetti, Kelli L., Brueggemann, Chantal, Saifuddin, Mashel Fatema A., Miller, Julia M., Li, Joy, Chang, Eric, Varshney, Aruna, Jimenez, Vanessa, Baradwaj, Anjana, Nassif, Cibelle, Alladin, Sara, Andersen, Kristine, Garcia, Angel J., Bi, Veronica, Nordquist, Sarah K., Dunn, Raymond L., Garcia, Vanessa, Tokalenko, Kateryna, Soohoo, Emily, Briseno, Fabiola, Kaur, Sukhdeep, Harris, Malcolm, Guillen, Hazel, Byrd, Decklin, Fung, Brandon, Bykov, Andrew E., Odisho, Emma, Tsujimoto, Bryan, Tran, Alan, Duong, Alex, Daigle, Kevin C., Paisner, Rebekka, Zuazo, Carlos E., Lin, Christine, Asundi, Aarati, Churgin, Matthew A., Fang-Yen, Christopher, Bremer, Martina, Kato, Saul, VanHoven, Miri K., L’Étoile, Noëlle D.
Format: Article
Language:English
Subjects:
Animals
behavior
C. elegans
Caenorhabditis elegans - physiology
circuit
memory
memory consolidation
Odorants
plasticity
single cell
sleep
Sleep - physiology
Smell
synapse
Synapses - physiology
systems consolidation
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Summary: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. [Display omitted] •Repeated, spaced odor training induces sleep in Caenorhabditis elegans•Sleep promoted by the ALA neuron is necessary for long-lasting memory•Memory consolidation requires AIY interneurons, which function in odor seeking•Sleep and training are required to reduce AWC olfactory neuron synapses with AIYs A sleep-like state is required for memory consolidation and synaptic remodeling, even in organisms with relatively small nervous systems, such as C. elegans, in which it is possible to examine how sleep affects individual neurons and their connections.
ISSN:0092-8674
1097-4172
DOI:10.1016/j.cell.2023.05.006