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A neural system that represents the association of odors with rewarded outcomes and promotes behavioral engagement

Marie A. Gadziola, Lucas A. Stetzik, Katherine N. Wright, Adrianna J. Milton, Keiko Arakawa, María del Mar Cortijo, Daniel W. Wesson
doi: https://doi.org/10.1101/617902
Marie A. Gadziola
1Department of Pharmacology & Therapeutics, University of Florida, 1200 Newell Dr. Gainesville, FL, 32610. U.S.A.
2Department of Neurosciences, Case Western Reserve University, 2109 Adelbert Rd., Cleveland, OH, 44106. U.S.A.
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Lucas A. Stetzik
1Department of Pharmacology & Therapeutics, University of Florida, 1200 Newell Dr. Gainesville, FL, 32610. U.S.A.
2Department of Neurosciences, Case Western Reserve University, 2109 Adelbert Rd., Cleveland, OH, 44106. U.S.A.
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Katherine N. Wright
1Department of Pharmacology & Therapeutics, University of Florida, 1200 Newell Dr. Gainesville, FL, 32610. U.S.A.
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Adrianna J. Milton
2Department of Neurosciences, Case Western Reserve University, 2109 Adelbert Rd., Cleveland, OH, 44106. U.S.A.
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Keiko Arakawa
2Department of Neurosciences, Case Western Reserve University, 2109 Adelbert Rd., Cleveland, OH, 44106. U.S.A.
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María del Mar Cortijo
1Department of Pharmacology & Therapeutics, University of Florida, 1200 Newell Dr. Gainesville, FL, 32610. U.S.A.
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Daniel W. Wesson
1Department of Pharmacology & Therapeutics, University of Florida, 1200 Newell Dr. Gainesville, FL, 32610. U.S.A.
2Department of Neurosciences, Case Western Reserve University, 2109 Adelbert Rd., Cleveland, OH, 44106. U.S.A.
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  • For correspondence: danielwesson@ufl.edu
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Summary

Learning strengthens the strong emotional and behavioral responses odors are well known for eliciting. Presumably subserving this, several brain regions display experience-dependent plasticity during odor learning, yet the specific cellular systems involved and the actual influence of these systems on odor-directed behavior are less understood. Here we investigated the transformation of odor information throughout the association of odors with rewards and also sought to link those neural systems with displays of reinforcement-based task engagement. First, we investigated the representation of odor-reward associations within two areas recipient of dense olfactory bulb input, the posterior piriform cortex (pPCX) and olfactory tubercle (OT), using simultaneous multi-site electrophysiological recordings from mice engaged in a reward-based olfactory learning task. As expected, neurons in both regions represented conditioned odors and did so with similar information content, yet both the proportion of neurons recruited by conditioned rewarded odors and the magnitudes and durations of their responses were greater in the OT. Using fiber photometry, we found that OT D1-type dopamine receptor expressing neurons flexibly represent odors based upon reward associations. In both the recordings and imaging, statistically meaningful changes in activity occurred soon after odor onset. Finally, using optogenetics we show that OT D1-receptor expressing neurons strongly influence behavior to promote task engagement. Together our results contribute to a model whereby OT D1 neurons support odor-guided motivated behaviors.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • New figure panels have been included and the structure of some figures modified. The title and abstract have been updated. Text sections in the Results, Introduction, and Discussion are updated.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted June 01, 2020.
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A neural system that represents the association of odors with rewarded outcomes and promotes behavioral engagement
Marie A. Gadziola, Lucas A. Stetzik, Katherine N. Wright, Adrianna J. Milton, Keiko Arakawa, María del Mar Cortijo, Daniel W. Wesson
bioRxiv 617902; doi: https://doi.org/10.1101/617902
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A neural system that represents the association of odors with rewarded outcomes and promotes behavioral engagement
Marie A. Gadziola, Lucas A. Stetzik, Katherine N. Wright, Adrianna J. Milton, Keiko Arakawa, María del Mar Cortijo, Daniel W. Wesson
bioRxiv 617902; doi: https://doi.org/10.1101/617902

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