Parallel encoding of sensory history and behavioral preference during Caenorhabditis elegans olfactory learning

Sensory experience modifies behavior through both associative and non-associative learning. In Caenorhabditis elegans, pairing odor with food deprivation results in aversive olfactory learning, and pairing odor with food results in appetitive learning. Aversive learning requires nuclear translocatio...

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Bibliographic Details
Published in:eLife 2016-07, Vol.5
Main Authors: Cho, Christine E, Brueggemann, Chantal, L'Etoile, Noelle D, Bargmann, Cornelia I
Format: Article
Language:English
Subjects:
1-Phosphatidylinositol 3-kinase
adaptation
Animals
Associative learning
Behavior
Behavior, Animal
Caenorhabditis elegans
Caenorhabditis elegans - physiology
Cyclic GMP
Dietary restrictions
Food
Gene expression
Insulin
Interneurons
Kinases
Learning
Localization
Nematodes
Neural circuitry
neural circuits
Neurons
Neurons - physiology
Neuroscience
Nuclear transport
Odor
olfaction
Olfactory discrimination learning
Olfactory neurons
Olfactory pathways
Olfactory Perception
Physiological aspects
Protein kinase
Protein kinase G
Protein transport
Proteins
Scripts
Sensory evaluation
Signal transduction
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Summary:Sensory experience modifies behavior through both associative and non-associative learning. In Caenorhabditis elegans, pairing odor with food deprivation results in aversive olfactory learning, and pairing odor with food results in appetitive learning. Aversive learning requires nuclear translocation of the cGMP-dependent protein kinase EGL-4 in AWC olfactory neurons and an insulin signal from AIA interneurons. Here we show that the activity of neurons including AIA is acutely required during aversive, but not appetitive, learning. The AIA circuit and AGE-1, an insulin-regulated PI3 kinase, signal to AWC to drive nuclear enrichment of EGL-4 during conditioning. Odor exposure shifts the AWC dynamic range to higher odor concentrations regardless of food pairing or the AIA circuit, whereas AWC coupling to motor circuits is oppositely regulated by aversive and appetitive learning. These results suggest that non-associative sensory adaptation in AWC encodes odor history, while associative behavioral preference is encoded by altered AWC synaptic activity.
ISSN:2050-084X
2050-084X
DOI:10.7554/elife.14000