CREBB repression of protein synthesis in mushroom body gates long-term memory formation in Drosophila

Author:

Lin Hsuan-Wen1,Chen Chun-Chao1,Jhang Ruei-Yu12ORCID,Chen Linyi12,de Belle J. Steven13456ORCID,Tully Tim1ORCID,Chiang Ann-Shyn178910ORCID

Affiliation:

1. Brain Research Center, National Tsing Hua University, Hsinchu 30013, Taiwan

2. Department of Medical Science and Institute of Molecular Medicine, National Tsing Hua University, Hsinchu 30013, Taiwan

3. School of Life Sciences, Arizona State University, Tempe, AZ, 85281

4. Department of Psychological Sciences, University of San Diego, San Diego, CA, 92110

5. School of Life Sciences, University of Nevada, Las Vegas, NV 89154

6. MnemOdyssey Limited Liability Corporation, Escondido CA 92027

7. Institute of Systems Neuroscience and Department of Life Science, National Tsing Hua University, Hsinchu 30013, Taiwan

8. Department of Biomedical Science and Environmental Biology, Kaohsiung Medical University, Kaohsiung 80708, Taiwan

9. Institute of Molecular and Genomic Medicine, National Health Research Institutes, Zhunan 35053, Taiwan

10. Graduate Institute of Clinical Medical Science, China Medical University, Taichung 40402, Taiwan

Abstract

Learned experiences are not necessarily consolidated into long-term memory (LTM) unless they are periodic and meaningful. LTM depends on de novo protein synthesis mediated by cyclic AMP response element-binding protein (CREB) activity. In Drosophila , two creb genes ( crebA , crebB ) and multiple CREB isoforms have reported influences on aversive olfactory LTM in response to multiple cycles of spaced conditioning. How CREB isoforms regulate LTM effector genes in various neural elements of the memory circuit is unclear, especially in the mushroom body (MB), a prominent associative center in the fly brain that has been shown to participate in LTM formation. Here, we report that i) spaced training induces crebB expression in MB α-lobe neurons and ii) elevating specific CREBB isoform levels in the early α/β subpopulation of MB neurons enhances LTM formation. By contrast, learning from weak training iii) induces 5-HT1A serotonin receptor synthesis, iv) activates 5-HT1A in early α/β neurons, and v) inhibits LTM formation. vi) LTM is enhanced when this inhibitory effect is relieved by down-regulating 5-HT1A or overexpressing CREBB. Our findings show that spaced training-induced CREBB antagonizes learning-induced 5-HT1A in early α/β MB neurons to modulate LTM consolidation.

Funder

MOST | Hsinchu Science Park Bureau, Ministry of Science and Technology, Taiwan

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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