Sleep is required to consolidate odor memory and remodel olfactory synapses

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.

doi:10.1016/j.cell.2023.05.006

Cited by 19 publications

(9 citation statements)

References 109 publications

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“…In contrast, and in agreement with previous studies (Chandra et al, 2023), we found that 3 hours after training, the calcium response of the AIY interneurons to butanone (sensed by the AWC neurons) is reduced in trained animals only when pre-treated with lithium. Importantly, the memory trace was evident only in the soma of the AIY neurons, but not in the axonal area known as zone 2 ( Figure 6G ), where many pre- and post-synaptic partners of AIY connect, including AWC (Colón-Ramos et al, 2007; Hawk et al, 2018).…”

Section: Resultssupporting

confidence: 93%

“…When we examined the worms 3 hours after training, in search for a “memory trace” ( Figure 6D-G ), we did not detect a significant difference in the calcium response of the AWC neurons between trained and untrained animals, or between lithium-treated and untreated worms ( Figure 6F ). Interestingly, it was observed that also another assay of olfactory training does not result in long term changes to the AWC sensory neuron activity (Chandra et al, 2023).…”

Section: Resultsmentioning

confidence: 99%

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A Tunable and Druggable Mechanism to Delay Forgetting of Olfactory Memories inC. elegans

Berliner,

Goldstein,

Teichman

et al. 2024

Preprint

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The poet W.B Yeats wrote that "All that is personal soon rots, it must be packed in ice or salt". Here we show that in Caenorhabditis elegans nematodes, simple animals with just 302 neurons, memories are preserved on ice and in lithium salt. C. elegans nematodes can form associative memories, which are typically forgotten quickly. We discovered that when placed on ice, worms delay forgetting of specific olfactory memories by at least 8-fold. Delayed forgetting was canceled completely when the worms were gradually adapted to low temperatures, owing to a genetically-encoded program that turns acclimated worms cold-tolerant. RNA-seq, mutant analyses, and pharmacological assays revealed that regulation of membrane properties switches cold-induced delayed forgetting ON and OFF, and, remarkably, that lithium delays forgetting only in cold-sensitive but not cold-tolerant worms. We found that downregulation of the diacylglycerol pathway in the AWC sensory neurons is essential for lithium-mediated delayed forgetting, and using neuronal activity recordings located the memory trace to the downstream AIY interneurons. We suggest that the awesome genetic tractability of C. elegans might be harnessed to study the effects of lithium and cold temperatures on the brain, why it influences psychiatric disorders, and even more fundamentally how memory is stored and lost.

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Section: Resultssupporting

confidence: 93%

Section: Resultsmentioning

confidence: 99%

A Tunable and Druggable Mechanism to Delay Forgetting of Olfactory Memories inC. elegans

Berliner,

Goldstein,

Teichman

et al. 2024

Preprint

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“…Sleep is essential, as demonstrated by deprivation experiments. Sleep functions include memory consolidation [ 68 , 69 ] and metabolic processes including waste removal [ 70 , 71 ]. Since sleep-like states are reported in jellyfish and C. elegans , before the evolution of endothermy [ 71 , 72 ], the specific contributions of a lower Tb to endotherm sleep physiology are unclear.…”

Section: Discussionmentioning

confidence: 99%

Beyond day and night: The importance of ultradian rhythms in mouse physiology

Škop,

Liu,

Xiao

et al. 2024

Molecular Metabolism

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“…With these advances over the years, the C. elegans community has built a growing, but still very limited, collection of synaptic reporters. These reporters have been instrumental in studying synapse biology in abundant paradigms including, but not restricted to, synaptogenesis (Mizumoto, Jin, and Bessereau, 2023; Kurshan and Shen, 2019; Jin, 2005), sexual dimorphism (Pechuk et al, 2022; Salzberg et al, 2020; Bayer et al, 2020, 2018; Cook et al, 2019; Hart and Hobert, 2018; Weinberg et al, 2018; Oren-Suissa, Bayer, and Hobert, 2016), and experience-dependent plasticity (Chandra et al, 2023; Bhattacharya et al, 2019; Bayer et al, 2018; Hart and Hobert, 2018). A toolkit of novel reporters is presented in this paper as a resource for the C. elegans community ( Figure 1B, Supplementary table 1 ).…”

Section: Introductionmentioning

confidence: 99%

Toolkits for detailed and high-throughput interrogation of synapses inC. elegans

Majeed,

Han,

Zhang

et al. 2023

Preprint

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Visualizing synaptic connectivity has traditionally relied on time-consuming electron microscopy-based imaging approaches. To scale the analysis of synaptic connectivity, fluorescent protein-based techniques have been established, ranging from the labeling of specific pre- or postsynaptic components of chemical or electrical synapses to transsynaptic proximity labeling technology such as GRASP and iBLINC. In this paper, we describe WormPsyQi, a generalizable image analysis pipeline that automatically quantifies synaptically localized fluorescent signals in a high-throughput and robust manner, with reduced human bias. We also present a resource of 30 transgenic strains that label chemical or electrical synapses throughout the nervous system of the nematodeC. elegans, using CLA-1, RAB-3, GRASP (chemical synapses), or innexin (electrical synapse) reporters. We show that WormPsyQi captures synaptic structures in spite of substantial heterogeneity in neurite morphology, fluorescence signal, and imaging parameters. We use these toolkits to quantify multiple obvious and subtle features of synapses - such as number, size, intensity, and spatial distribution of synapses - in datasets spanning various regions of the nervous system, developmental stages, and sexes. Although the pipeline is described in the context of synapses, it may be utilized for other ‘punctate’ signals, such as fluorescently-tagged neurotransmitter receptors and cell adhesion molecules, as well as proteins in other subcellular contexts. By overcoming constraints on time, sample size, cell morphology, and phenotypic space, this work represents a powerful resource for further analysis of synapse biology inC. elegans.

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Sleep is required to consolidate odor memory and remodel olfactory synapses

Cited by 19 publications

References 109 publications

A Tunable and Druggable Mechanism to Delay Forgetting of Olfactory Memories inC. elegans

A Tunable and Druggable Mechanism to Delay Forgetting of Olfactory Memories inC. elegans

Beyond day and night: The importance of ultradian rhythms in mouse physiology

Toolkits for detailed and high-throughput interrogation of synapses inC. elegans

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