Kavli Affiliate: Cornelia Bargmann
| Authors: Du Cheng, James Lee, Maximillian Brown, Margaret S. Ebert, Masahiro Tomioka, Yuichi Iino and Cornelia I Bargmann
| Summary:
Information flow through neural circuits is continuously modified by context-dependent learning. In the nematode Caenorhabditis elegans, pairing specific odors with food deprivation results in aversion to the odor. Here we identify cell-specific mechanisms of insulin/IGF receptor signaling that integrate sensory information with food context during aversive olfactory learning. Using FLP::FRT recombination of an endogenously targeted locus, we show that aversive learning to butanone, an odor sensed only by the AWCON olfactory neuron, requires the insulin/IGF receptor DAF-2 in AWCON. Learning requires an axonally-localized DAF-2c isoform and the insulin receptor substrate (IRS) protein IST-1, and is partly independent of the FoxO transcription factor DAF-16. Food deprivation, the unconditioned stimulus for learning, increases DAF-2 expression post-transcriptionally through an insulin- and ist-1-dependent process. Aversive learning suppresses odor-regulated glutamate release from the AWCON axon in wild-type animals but not in ist-1 mutants, suggesting that insulin signaling drives presynaptic depression to generate an aversive memory.