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      Entwined engrams : The evolution of associative and non-associative learning

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          Abstract

          The nematode Caenorhabditis elegans displays a surprisingly sophisticated behavioral repertoire that includes the utilization of both associative and non-associative forms of learning. Elucidating the molecular basis of learning remains a fundamental, yet daunting, challenge of modern neuroscience. In Pereira and van der Kooy (ref. 2), we described the use of a two input—two output stimuli system to dissociate between associative and non-associative learning and between memory acquisition and retrieval processes. Briefly, one finding indicated that after training with the odorant isoamyl alcohol (IsoA), we could preferentially retrieve either associative or non-associative memory with a choice of either a benzaldehyde (Bnz) or IsoA retrieval stimulus, respectively. Here, we describe how that apparently enigmatic molecular cross wiring of the two forms of memory examined could represent an evolutionary relic of the ancient divergence between non-associative and associative learning. In addition, we extrapolate on the utility and subtleties of using such a system to dissociate and decipher the components of memory in C. elegans.

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          Most cited references14

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          Evolution and tinkering.

          F Jacob (1977)
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            The insulin/PI 3-kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans.

            The insulin-like signaling pathway is known to regulate fat metabolism, dauer formation, and longevity in Caenorhabditis elegans. Here, we report that this pathway is also involved in salt chemotaxis learning, in which animals previously exposed to a chemoattractive salt under starvation conditions start to show salt avoidance behavior. Mutants of ins-1, daf-2, age-1, pdk-1, and akt-1, which encode the homologs of insulin, insulin/IGF-I receptor, PI 3-kinase, phosphoinositide-dependent kinase, and Akt/PKB, respectively, show severe defects in salt chemotaxis learning. daf-2 and age-1 act in the ASER salt-sensing neuron, and the activity level of the DAF-2/AGE-1 pathway in this neuron determines the extent and orientation of salt chemotaxis. On the other hand, ins-1 acts in AIA interneurons, which receive direct synaptic inputs from sensory neurons and also send synaptic outputs to ASER. These results suggest that INS-1 secreted from AIA interneurons provides feedback to ASER to generate plasticity of chemotaxis.
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              Neuropeptide feedback modifies odor-evoked dynamics in C. elegans olfactory neurons

              Many neurons release classical transmitters together with neuropeptide cotransmitters whose functions are incompletely understood. Here we define the relationship between two transmitters in the olfactory system of Caenorhabditis elegans, showing that a neuropeptide-to-neuropeptide feedback loop alters sensory dynamics in primary olfactory neurons. The AWC olfactory neuron is glutamatergic and also expresses the peptide NLP-1. nlp-1 mutants have increased AWC-dependent behaviors, suggesting that NLP-1 limits the normal response. The receptor for NLP-1 is the G protein-coupled receptor NPR-11, which acts in postsynaptic AIA interneurons. Feedback from AIA interneurons modulates odor-evoked calcium dynamics in AWC olfactory neurons and requires INS-1, a neuropeptide released from AIA. The neuropeptide feedback loop dampens behavioral responses to odors on short and long timescales. Our results point to neuronal dynamics as a site of behavioral regulation and reveal the ability of neuropeptide feedback to remodel sensory networks on multiple timescales.
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                Author and article information

                Journal
                Worm
                Worm
                WORM
                Worm
                Landes Bioscience
                2162-4046
                2162-4054
                01 April 2013
                01 April 2013
                01 April 2013
                : 2
                : 2
                : e22725
                Affiliations
                Department of Molecular Genetics; and Donnelly Centre for Cellular and Biomolecular Research; University of Toronto; Toronto, ON Canada
                Author notes
                [* ]Correspondence to: Schrieber Pereira; Email: schreiber.pereira@ 123456mail.utoronto.ca
                Article
                2012WORM091R 22725
                10.4161/worm.22725
                3704443
                24058869
                14a4457e-78b7-44af-bbf8-ad4fc861473a
                Copyright © 2013 Landes Bioscience

                This is an open-access article licensed under a Creative Commons Attribution-NonCommercial 3.0 Unported License. The article may be redistributed, reproduced, and reused for non-commercial purposes, provided the original source is properly cited.

                History
                : 30 September 2012
                : 19 October 2012
                : 30 October 2012
                Categories
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                c. elegans behavior,associative learning,evolution of learning,habituation,olfactory adaptation

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