Identification of Dopaminergic Neurons That Can Both Establish Associative Memory and Acutely Terminate Its Behavioral Expression

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2020
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Schleyer, Michael
Weiglein, Aliće
Thoener, Juliane
Hartenstein, Volker
Kantar Weigelt, Melisa
Schuller, Sarah
Saumweber, Timo
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The Journal of neuroscience : the official journal of the Society for Neuroscience. Society for Neuroscience. 2020, 40(31), pp. 5990-6006. ISSN 0270-6474. eISSN 1529-2401. Available under: doi: 10.1523/JNEUROSCI.0290-20.2020
Zusammenfassung

An adaptive transition from exploring the environment in search of vital resources to exploiting these resources once the search was successful is important to all animals. Here we study the neuronal circuitry that allows larval Drosophila melanogaster of either sex to negotiate this exploration-exploitation transition. We do so by combining Pavlovian conditioning with high-resolution behavioral tracking, optogenetic manipulation of individually identified neurons, and EM data-based analyses of synaptic organization. We find that optogenetic activation of the dopaminergic neuron DAN-i1 can both establish memory during training and acutely terminate learned search behavior in a subsequent recall test. Its activation leaves innate behavior unaffected, however. Specifically, DAN-i1 activation can establish associative memories of opposite valence after paired and unpaired training with odor, and its activation during the recall test can terminate the search behavior resulting from either of these memories. Our results further suggest that in its behavioral significance DAN-i1 activation resembles, but does not equal, sugar reward. Dendrogram analyses of all the synaptic connections between DAN-i1 and its two main targets, the Kenyon cells and the mushroom body output neuron MBON-i1, further suggest that the DAN-i1 signals during training and during the recall test could be delivered to the Kenyon cells and to MBON-i1, respectively, within previously unrecognized, locally confined branching structures. This would provide an elegant circuit motif to terminate search on its successful completion.SIGNIFICANCE STATEMENT In the struggle for survival, animals have to explore their environment in search of food. Once food is found, however, it is adaptive to prioritize exploiting it over continuing a search that would now be as pointless as searching for the glasses you are wearing. This exploration-exploitation trade-off is important for animals and humans, as well as for technical search devices. We investigate which of the only 10,000 neurons of a fruit fly larva can tip the balance in this trade-off, and identify a single dopamine neuron called DAN-i1 that can do so. Given the similarities in dopamine neuron function across the animal kingdom, this may reflect a general principle of how search is terminated once it is successful.

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570 Biowissenschaften, Biologie
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dopamine; exploration-exploitation; mushroom body; optogenetics; reinforcement; search
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ISO 690SCHLEYER, Michael, Aliće WEIGLEIN, Juliane THOENER, Martin STRAUCH, Volker HARTENSTEIN, Melisa KANTAR WEIGELT, Sarah SCHULLER, Timo SAUMWEBER, Katharina EICHLER, Astrid ROHWEDDER, Dorit MERHOF, Marta ZLATIC, Andreas THUM, Bertram GERBER, 2020. Identification of Dopaminergic Neurons That Can Both Establish Associative Memory and Acutely Terminate Its Behavioral Expression. In: The Journal of neuroscience : the official journal of the Society for Neuroscience. Society for Neuroscience. 2020, 40(31), pp. 5990-6006. ISSN 0270-6474. eISSN 1529-2401. Available under: doi: 10.1523/JNEUROSCI.0290-20.2020
BibTex
@article{Schleyer2020-07-29Ident-50684,
  year={2020},
  doi={10.1523/JNEUROSCI.0290-20.2020},
  title={Identification of Dopaminergic Neurons That Can Both Establish Associative Memory and Acutely Terminate Its Behavioral Expression},
  number={31},
  volume={40},
  issn={0270-6474},
  journal={The Journal of neuroscience : the official journal of the Society for Neuroscience},
  pages={5990--6006},
  author={Schleyer, Michael and Weiglein, Aliće and Thoener, Juliane and Strauch, Martin and Hartenstein, Volker and Kantar Weigelt, Melisa and Schuller, Sarah and Saumweber, Timo and Eichler, Katharina and Rohwedder, Astrid and Merhof, Dorit and Zlatic, Marta and Thum, Andreas and Gerber, Bertram}
}
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