Mushroom body subsets encode CREB2-dependent water-reward long-term memory in Drosophila
Autor: | Tony Wu, Wang Pao Lee, Tai Hsiang Chiu, Meng Hsuan Chiang, Tsai-Feng Fu, Hsueh Cheng Chiang, Ya-Lun Tsai, Li Yun Chang, Jhen Yi Lee, Chia-Lin Wu |
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Rok vydání: | 2020 |
Předmět: |
Cancer Research
Social Sciences Protein Synthesis QH426-470 Synaptic Transmission Biochemistry Animals Genetically Modified Cognition Learning and Memory 0302 clinical medicine Animal Cells Drosophila Proteins Psychology Cyclic AMP Response Element-Binding Protein Genetics (clinical) Neurons 0303 health sciences education.field_of_study Drosophila Melanogaster Chemical Synthesis Eukaryota Animal Models Calcium Imaging Activating transcription factor 2 Cell biology Smell Insects medicine.anatomical_structure Experimental Organism Systems Mushroom bodies Drosophila Cellular Types Research Article Memory Long-Term Biosynthetic Techniques Arthropoda Imaging Techniques Population Neuroimaging Biology Neurotransmission Research and Analysis Methods CREB Olfactory Receptor Neurons 03 medical and health sciences Model Organisms Calcium imaging Reward Memory Genetics medicine Biological neural network Animals education Molecular Biology Mushroom Bodies Ecology Evolution Behavior and Systematics 030304 developmental biology Behavior Organisms Water Biology and Life Sciences Proteins Afferent Neurons Cell Biology Invertebrates Protein Biosynthesis Cellular Neuroscience Trans-Activators Animal Studies biology.protein Cognitive Science Conditioned Response Calcium Neuron Zoology Entomology 030217 neurology & neurosurgery Neuroscience |
Zdroj: | PLoS Genetics, Vol 16, Iss 8, p e1008963 (2020) PLoS Genetics |
ISSN: | 1553-7404 |
Popis: | Long-term memory (LTM) formation depends on the conversed cAMP response element-binding protein (CREB)-dependent gene transcription followed by de novo protein synthesis. Thirsty fruit flies can be trained to associate an odor with water reward to form water-reward LTM (wLTM), which can last for over 24 hours without a significant decline. The role of de novo protein synthesis and CREB-regulated gene expression changes in neural circuits that contribute to wLTM remains unclear. Here, we show that acute inhibition of protein synthesis in the mushroom body (MB) αβ or γ neurons during memory formation using a cold-sensitive ribosome-inactivating toxin disrupts wLTM. Furthermore, adult stage-specific expression of dCREB2b in αβ or γ neurons also disrupts wLTM. The MB αβ and γ neurons can be further classified into five different neuronal subsets including αβ core, αβ surface, αβ posterior, γ main, and γ dorsal. We observed that the neurotransmission from αβ surface and γ dorsal neuron subsets is required for wLTM retrieval, whereas the αβ core, αβ posterior, and γ main are dispensable. Adult stage-specific expression of dCREB2b in αβ surface and γ dorsal neurons inhibits wLTM formation. In vivo calcium imaging revealed that αβ surface and γ dorsal neurons form wLTM traces with different dynamic properties, and these memory traces are abolished by dCREB2b expression. Our results suggest that a small population of neurons within the MB circuits support long-term storage of water-reward memory in Drosophila. Author summary Unlike short-term memory (STM), the formation of long-term memory (LTM) requires de novo protein synthesis and CREB-mediated gene transcription in many animals. To date, the mechanism underlying LTM formation remains poorly understood. Thirsty fruit flies can be trained to associate an odor with water to form a water-reward LTM (wLTM), which requires de novo protein synthesis and dCREB2 activity. In this study, we found that dCREB2 activity in the mushroom body (MB) αβ surface and γ dorsal neuron subsets is essential for wLTM formation. Neurotransmission from αβ surface and γ dorsal neurons is specifically required for retrieval, but not for acquisition or consolidation of wLTM. Moreover, wLTM traces are formed in the αβ surface and γ dorsal neurons with different neural dynamics, which require normal dCREB2 functions. These findings highlight that dCREB2-dependent wLTM is located within a specific brain circuitry in fruit flies. |
Databáze: | OpenAIRE |
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