Sleep is Required for Odor Exposure to Consolidate Memory and Remodel Olfactory Synapses

Chandra, Rashmi; Farah, Fatima; Muñoz-Lobato, Fernando; Bokka, Anirudh; Benedetti, Kelli L.; Brueggemann, Chantal; Saifuddin, Fatema A.; Miller, Julia M.; Li, Joy; Chang, Eric; Varshney, Aruna; Jiménez, Vanessa; Baradwaj, A; Nassif, Cibelle; Alladin, Sara; Andersen, Kristine; Bi, Veronica; Nordquist, Sarah K.; Dunn, Raymond L.; Tsujimoto, Bryan; Tran, Alan; Duong, Alex; Paisner, Rebekka; Zuazo, Carlos E.; Churgin, Matthew A.; Fang-Yen, Christopher; Bremer, Martina; Kato, Saul; L’Étoile, Noëlle D.; VanHoven, Miri

doi:10.2139/ssrn.4124635

Cited by 2 publications

(4 citation statements)

References 79 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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“…Therefore, we asked whether the CEPsh cells are modulated during a spaced the olfactory training paradigm in which animals learn to avoid the innately attractive odorant, butanone by repeatedly pairing the odor with starvation and exercise (Chandra et al, 2022; Kauffamnn et al, 2011). The memory from this training remains for at least 24 hours (Chandra et al, 2022). In particular, we asked whether the cephalic sheath (CEPsh) glia, the astrocyte equivalent in C. elegans , integrate information from outside the animal with the animal’s internal, physiological, state.…”

Section: Descriptionmentioning

confidence: 99%

“…Though the C. elegans’ sensory ensheathing glia (AMsh) have been shown to detect odorants and drive olfactory adaptation (Duan et al, 2020), it remains unknown if their astrocytes respond directly or indirectly to environmental stimuli. Therefore, we asked whether the CEPsh cells are modulated during a spaced the olfactory training paradigm in which animals learn to avoid the innately attractive odorant, butanone by repeatedly pairing the odor with starvation and exercise (Chandra et al, 2022; Kauffamnn et al, 2011). The memory from this training remains for at least 24 hours (Chandra et al, 2022).…”

Section: Descriptionmentioning

confidence: 99%

Astrocyte-like CEPsh glia respond to stress

Chien

Garcia

Chandra

et al. 2022

Preprint

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While astrocytes are known to be important for development and nourishment of the nervous system, the field is just beginning to explore how astrocytes respond to environmental stimuli. Using Caenorhabditis elegans and their astrocyte-equivalent, CEPsh, we asked whether astrocyte-like glia respond to odor exposure. We found day-old adult C. elegans decrease hlh-17 promoter (CEPsh glia marker) mediated fluorescent expression when trained with an innately attractive odor butanone. Moreover, the olfactory training paradigm itself affects phlh-17 expression, but in a different way. This suggests astrocyte-like CEPsh glia can integrate environmental information to respond to changes in the environment, which enhances survival.

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Sleep is Required for Odor Exposure to Consolidate Memory and Remodel Olfactory Synapses

Cited by 2 publications

References 79 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

Astrocyte-like CEPsh glia respond to stress

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