Insulin signaling represents a gating mechanism between different memory phases in Drosophila larvae
| Autor: | Eschment, Melanie, Franz, Hanna R., Güllü, Nazlı, Hölscher, Luis G., Huh, Ko-Eun, Widmann, Annekathrin |
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| Jazyk: | angličtina |
| Rok vydání: | 2020 |
| Předmět: |
Sucrose
Life Cycles Physiology Social Sciences Protein Synthesis QH426-470 Disaccharides Biochemistry Larvae Cognition Learning and Memory Endocrinology Medicine and Health Sciences Insulin Psychology Organic Compounds Drosophila Melanogaster Eukaryota Chemical Synthesis Animal Models Insects Chemistry Experimental Organism Systems Larva Physical Sciences Drosophila Sensory Perception Signal Transduction Research Article Memory Long-Term animal structures Sensory Receptor Cells Arthropoda Biosynthetic Techniques education Carbohydrates Research and Analysis Methods Model Organisms Memory ddc:570 Genetics Animals Mushroom Bodies Diabetic Endocrinology Endocrine Physiology Cold-Shock Response Organic Chemistry Insulin Signaling fungi Chemical Compounds Organisms Cognitive Psychology Biology and Life Sciences Proteins Invertebrates Hormones Protein Biosynthesis Animal Studies Cognitive Science Perception Energy Metabolism Zoology Entomology Drosophila melanogaster Protein synthesis Insulin signaling Sensory perception Developmental Biology Neuroscience |
| Zdroj: | PLoS Genetics PLoS Genetics, Vol 16, Iss 10, p e1009064 (2020) |
| Popis: | The ability to learn new skills and to store them as memory entities is one of the most impressive features of higher evolved organisms. However, not all memories are created equal; some are short-lived forms, and some are longer lasting. Formation of the latter is energetically costly and by the reason of restricted availability of food or fluctuations in energy expanses, efficient metabolic homeostasis modulating different needs like survival, growth, reproduction, or investment in longer lasting memories is crucial. Whilst equipped with cellular and molecular pre-requisites for formation of a protein synthesis dependent long-term memory (LTM), its existence in the larval stage of Drosophila remains elusive. Considering it from the viewpoint that larval brain structures are completely rebuilt during metamorphosis, and that this process depends completely on accumulated energy stores formed during the larval stage, investing in LTM represents an unnecessary expenditure. However, as an alternative, Drosophila larvae are equipped with the capacity to form a protein synthesis independent so-called larval anaesthesia resistant memory (lARM), which is consolidated in terms of being insensitive to cold-shock treatments. Motivated by the fact that LTM formation causes an increase in energy uptake in Drosophila adults, we tested the idea of whether an energy surplus can induce the formation of LTM in the larval stage. Suprisingly, increasing the metabolic state by feeding Drosophila larvae the disaccharide sucrose directly before aversive olfactory conditioning led to the formation of a protein synthesis dependent longer lasting memory. Moreover, formation of this memory component is accompanied by the suppression of lARM. We ascertained that insulin receptors (InRs) expressed in the mushroom body Kenyon cells suppresses the formation of lARM and induces the formation of a protein synthesis dependent longer lasting memory in Drosophila larvae. Given the numerical simplicity of the larval nervous system this work offers a unique prospect to study the impact of insulin signaling on the formation of protein synthesis dependent memories on a molecular level. Author summary Memories enable organisms to deal with novelties and unpredictable complexities in an ever-changing environment by allowing past experiences to influence future behaviors. However, every memory has an energetic cost; some more, some less. In Drosophila, two long-lasting and mutually exclusive memory phases can be distinguished: anaesthesia-resistant memory (ARM) and long-term memory (LTM). The protein synthesis dependent formation of LTM is accompanied by a drastic increase in energy uptake and is disabled after reduced food availability. To understand the molecular underpinnings of how the brain disables LTM, we used a reductionistic approach. Drosophila larvae are equipped with the cellular and molecular pre-requisites of forming different memory component. However, the existence of LTM in the larval stage of Drosophila remains elusive. Theoretically, the emerging costs of a protein synthesis dependent LTM in larvae exceed the potential benefit since learned information becomes obsolete through metamorphosis. With this in mind, we tested whether an energy surplus can induce the formation of a protein synthesis dependent longer lasting memory in Drosophila larvae, and correlate this with molecular events in identifiable neurons. Indeed, an energy surplus prior to aversive Pavlovian conditioning successfully leads to the formation of a protein synthesis dependent memory and to the inhibition of ARM. We further demonstrate that this state-dependent switch between different types of memories is reliant on the activity of the rutabaga-encoded adenylate cyclase and insulin receptors expressed in the mushroom body Kenyon cells. |
| Databáze: | OpenAIRE |
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