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
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