Visualizing long-term memory formation in two neurons of the Drosophila brain.
Long-term memory (LTM) depends on the synthesis of new proteins. Using a temperature-sensitive ribosome-inactivating toxin to acutely inhibit protein synthesis, we screened individual neurons making new proteins after olfactory associative conditioning in Drosophila. Surprisingly, LTM was impaired after inhibiting protein synthesis in two dorsal-anterior-lateral (DAL) neurons but not in the mushroom body (MB), which is considered the adult learning and memory center. Using a photoconvertible fluorescent protein KAEDE to report de novo protein synthesis, we have directly visualized cyclic adenosine monophosphate (cAMP) response element-binding protein (CREB)-dependent transcriptional activation of calcium/calmodulin-dependent protein kinase II and period genes in the DAL neurons after spaced but not massed training. Memory retention was impaired by blocking neural output in DAL during retrieval but not during acquisition or consolidation. These findings suggest an extra-MB memory circuit in Drosophila: LTM consolidation (MB to DAL), storage (DAL), and retrieval (DAL to MB).
Institute of Biotechnology and Department of Life Science, National Tsing Hua University, Hsinchu 30013, Taiwan.
Chun-Chao
CC
Chen
Jie-Kai
JK
Wu
Hsuan-Wen
HW
Lin
Tsung-Pin
TP
Pai
Tsai-Feng
TF
Fu
Chia-Lin
CL
Wu
Tim
T
Tully
Ann-Shyn
AS
Chiang
D000818:Animals; D030801:Animals, Genetically Modified; D001369:Axons / Q000648:ultrastructure; D001921:Brain / Q000166:cytology / Q000502:physiology; D054732:Calcium-Calmodulin-Dependent Protein Kinase Type 2 / Q000096:biosynthesis / Q000235:genetics; D003213:Conditioning, Psychological; D056931:Cryptochromes / Q000096:biosynthesis / Q000235:genetics; D017362:Cyclic AMP Response Element-Binding Protein / Q000235:genetics / Q000378:metabolism; D004330:Drosophila / Q000166:cytology / Q000235:genetics / Q000502:physiology*; D029721:Drosophila Proteins / Q000096:biosynthesis* / Q000235:genetics / Q000378:metabolism; D020869:Gene Expression Profiling; D005786:Gene Expression Regulation; D017344:Genes, Insect; D008164:Luminescent Proteins / Q000096:biosynthesis / Q000235:genetics; D057567:Memory, Long-Term / Q000502:physiology*; D024521:Mushroom Bodies / Q000502:physiology*; D009474:Neurons / Q000502:physiology* / Q000648:ultrastructure; D009812:Odorants; D056950:Period Circadian Proteins / Q000096:biosynthesis / Q000235:genetics; D012276:Ricin / Q000494:pharmacology; D011984:Sensory Receptor Cells / Q000502:physiology; D012697:Serine Endopeptidases / Q000096:biosynthesis / Q000235:genetics; D015534:Trans-Activators / Q000235:genetics / Q000378:metabolism; D015533:Transcriptional Activation
C102181:CrebB protein, Drosophila; D056931:Cryptochromes; D017362:Cyclic AMP Response Element-Binding Protein; D029721:Drosophila Proteins; C513582:Kaede protein, Trachyphyllia geoffroyi; D008164:Luminescent Proteins; D056950:Period Circadian Proteins; D015534:Trans-Activators; D012276:Ricin; D054732:Calcium-Calmodulin-Dependent Protein Kinase Type 2; D012697:Serine Endopeptidases; C512782:Teq protein, Drosophila