Insulin signaling plays a dual role in Caenorhabditis elegans memory acquisition and memory retrieval.
Insulin signaling plays a prominent role in regulation of dauer formation and longevity in Caenorhabditis elegans. Here, we show that insulin signaling also is required in benzaldehyde-starvation associative plasticity, in which worms pre-exposed to the odor attractant benzaldehyde in the absence of food subsequently demonstrate a conditioned aversion response toward the odorant. Animals with mutations in insulin-related 1 (ins-1), abnormal dauer formation 2 (daf-2), and aging alteration 1 (age-1), which encode the homolog of human insulin, insulin/IGF-1 receptor, and PIP3 kinase, respectively, demonstrated significant deficits in benzaldehyde-starvation associative plasticity. Using a conditional allele, we show that the behavioral roles of DAF-2 signaling in associative plasticity can be dissociated, with DAF-2 signaling playing a more significant role in the memory retrieval than in memory acquisition. We propose DAF-2 signaling acts as a learning-specific starvation signal in the memory acquisition phase of benzaldehyde-starvation associative plasticity but functions to switch benzaldehyde-sensing amphid wing C neurons into an avoidance signaling mode during memory retrieval.
Department of Molecular Genetics, University of Toronto, Toronto, Ontario M5S 1A8, Canada.
Chia Hsun Anthony
CH
Lin
Masahiro
M
Tomioka
Schreiber
S
Pereira
Laurie
L
Sellings
Yuichi
Y
Iino
Derek
D
van der Kooy
D000818:Animals; D001362:Avoidance Learning / Q000502:physiology*; D001547:Benzaldehydes / Q000737:chemistry; D017173:Caenorhabditis elegans / Q000378:metabolism* / Q000502:physiology; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism*; D003214:Conditioning, Classical / Q000502:physiology; D007328:Insulin / Q000378:metabolism*; D008568:Memory / Q000502:physiology*; D009154:Mutation; D009812:Odorants; D019869:Phosphatidylinositol 3-Kinases / Q000378:metabolism; D010716:Phosphatidylinositols / Q000378:metabolism; D017526:Receptor, IGF Type 1 / Q000378:metabolism; D011972:Receptor, Insulin / Q000378:metabolism; D015398:Signal Transduction / Q000502:physiology*; D013217:Starvation
D001547:Benzaldehydes; D029742:Caenorhabditis elegans Proteins; D007328:Insulin; D010716:Phosphatidylinositols; C424903:ins-1 protein, C elegans; D019869:Phosphatidylinositol 3-Kinases; C100662:AGE-1 protein, C elegans; C107483:DAF-2 protein, C elegans; D017526:Receptor, IGF Type 1; D011972:Receptor, Insulin; C032175:benzaldehyde