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Striatal dopamine explains novelty-induced behavioral dynamics and individual variability in threat prediction

View ORCID ProfileKorleki Akiti, View ORCID ProfileIku Tsutsui-Kimura, View ORCID ProfileYudi Xie, Alexander Mathis, Jeffrey Markowitz, Rockwell Anyoha, View ORCID ProfileSandeep Robert Datta, View ORCID ProfileMackenzie Weygandt Mathis, View ORCID ProfileNaoshige Uchida, View ORCID ProfileMitsuko Watabe-Uchida
doi: https://doi.org/10.1101/2021.12.21.473723
Korleki Akiti
1Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, MA 02138, USA
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  • ORCID record for Korleki Akiti
Iku Tsutsui-Kimura
1Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, MA 02138, USA
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Yudi Xie
1Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, MA 02138, USA
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Alexander Mathis
1Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, MA 02138, USA
2The Rowland Institute at Harvard, Harvard University, Cambridge, MA, USA
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Jeffrey Markowitz
3Department of Neurobiology, Harvard Medical School, Boston, MA, USA
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Rockwell Anyoha
3Department of Neurobiology, Harvard Medical School, Boston, MA, USA
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Sandeep Robert Datta
3Department of Neurobiology, Harvard Medical School, Boston, MA, USA
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Mackenzie Weygandt Mathis
2The Rowland Institute at Harvard, Harvard University, Cambridge, MA, USA
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Naoshige Uchida
1Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, MA 02138, USA
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Mitsuko Watabe-Uchida
1Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, MA 02138, USA
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  • For correspondence: mitsuko@mcb.harvard.edu
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SUMMARY

Animals exhibit diverse behavioral responses, such as exploration and avoidance, to novel cues in the environment. However, it remains unclear how dopamine neuron-related novelty responses influence behavior. Here, we characterized dynamics of novelty exploration using multi-point tracking (DeepLabCut) and behavioral segmentation (MoSeq). Novelty elicits a characteristic sequence of behavior, starting with investigatory approach and culminating in object engagement or avoidance. Dopamine in the tail of striatum (TS) suppresses engagement, and dopamine responses were predictive of individual variability in behavior. Behavioral dynamics and individual variability were explained by a novel reinforcement learning (RL) model of threat prediction, in which behavior arises from a novelty-induced initial threat prediction (akin to “shaping bonus”), and a threat prediction that is learned through dopamine-mediated threat prediction errors. These results uncover an algorithmic similarity between reward- and threat-related dopamine sub-systems.

Highlights

  • Novelty-induced behaviors are analyzed using modern machine-learning methods

  • Novelty induces risk assessment which develops into engagement or avoidance

  • Dopamine in the tail of striatum correlates with individual behavioral variability

  • Reinforcement learning with shaping bonus and uncertainty explains the data

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted December 21, 2021.
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Striatal dopamine explains novelty-induced behavioral dynamics and individual variability in threat prediction
Korleki Akiti, Iku Tsutsui-Kimura, Yudi Xie, Alexander Mathis, Jeffrey Markowitz, Rockwell Anyoha, Sandeep Robert Datta, Mackenzie Weygandt Mathis, Naoshige Uchida, Mitsuko Watabe-Uchida
bioRxiv 2021.12.21.473723; doi: https://doi.org/10.1101/2021.12.21.473723
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Striatal dopamine explains novelty-induced behavioral dynamics and individual variability in threat prediction
Korleki Akiti, Iku Tsutsui-Kimura, Yudi Xie, Alexander Mathis, Jeffrey Markowitz, Rockwell Anyoha, Sandeep Robert Datta, Mackenzie Weygandt Mathis, Naoshige Uchida, Mitsuko Watabe-Uchida
bioRxiv 2021.12.21.473723; doi: https://doi.org/10.1101/2021.12.21.473723

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