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Chronic nicotine increases midbrain dopamine neuron activity and biases individual strategies towards reduced exploration in a foraging task

Malou Dongelmans, View ORCID ProfileRomain Durand-de Cuttoli, View ORCID ProfileClaire Nguyen, Maxime Come, View ORCID ProfileEtienne K. Duranté, Damien Lemoine, Raphael Britto, Tarek Ahmed Yahia, View ORCID ProfileSarah Mondoloni, View ORCID ProfileSteve Didienne, View ORCID ProfileElise Bousseyrol, Bernadette Hannesse, View ORCID ProfileLauren M. Reynolds, View ORCID ProfileNicolas Torquet, View ORCID ProfileDeniz Dalkara, View ORCID ProfileFabio Marti, View ORCID ProfileAlexandre Mourot, View ORCID ProfileJérémie Naudé, View ORCID ProfilePhilippe Faure
doi: https://doi.org/10.1101/2021.01.29.428835
Malou Dongelmans
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
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Romain Durand-de Cuttoli
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
3Nash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY, USA
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Claire Nguyen
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
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Maxime Come
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
2Brain Plasticity Unit, CNRS, ESPCI Paris, PSL Research University, 75005 Paris, France
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Etienne K. Duranté
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
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  • ORCID record for Etienne K. Duranté
Damien Lemoine
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
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Raphael Britto
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
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Tarek Ahmed Yahia
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
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Sarah Mondoloni
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
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Steve Didienne
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
2Brain Plasticity Unit, CNRS, ESPCI Paris, PSL Research University, 75005 Paris, France
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Elise Bousseyrol
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
2Brain Plasticity Unit, CNRS, ESPCI Paris, PSL Research University, 75005 Paris, France
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Bernadette Hannesse
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
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Lauren M. Reynolds
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
2Brain Plasticity Unit, CNRS, ESPCI Paris, PSL Research University, 75005 Paris, France
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Nicolas Torquet
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
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Deniz Dalkara
4Sorbonne Université, INSERM, CNRS, Institut de la Vision, Paris, France
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Fabio Marti
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
2Brain Plasticity Unit, CNRS, ESPCI Paris, PSL Research University, 75005 Paris, France
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Alexandre Mourot
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
2Brain Plasticity Unit, CNRS, ESPCI Paris, PSL Research University, 75005 Paris, France
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Jérémie Naudé
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
2Brain Plasticity Unit, CNRS, ESPCI Paris, PSL Research University, 75005 Paris, France
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Philippe Faure
1Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine - Institut de Biologie Paris Seine (NPS - IBPS), 75005 Paris, France
2Brain Plasticity Unit, CNRS, ESPCI Paris, PSL Research University, 75005 Paris, France
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  • For correspondence: phfaure@gmail.com
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Summary

Long-term exposure to nicotine alters brain circuits and induces profound changes in decision-making strategies, affecting behaviors both related and unrelated to drug seeking and consumption. Using an intracranial self-stimulation reward-based foraging task, we investigated the impact of chronic nicotine on the trade-off between exploitation and exploration, and the role of ventral tegmental area (VTA) dopamine (DA) neuron activity in decision-making unrelated to nicotine-seeking. Model-based and archetypal analysis revealed a substantial inter-individual variability in decision-making strategies, with mice passively exposed to chronic nicotine visiting more frequently options associated with higher reward probability and therefore shifting toward a more exploitative profile compared to non-exposed animals. We then mimicked the effect of chronic nicotine on the tonic activity of VTA DA neurons using optogenetics, and found that photo-stimulated mice had a behavioral phenotype very close to that of mice exposed to nicotine, suggesting that the dopaminergic control of the exploration/exploitation balance is altered under nicotine exposure. Our results thus reveal a key role of tonic midbrain DA in the exploration/exploitation trade-off and highlight a potential mechanism by which nicotine affects decision-making.

Competing Interest Statement

The authors have declared no competing interest.

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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 February 01, 2021.
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Chronic nicotine increases midbrain dopamine neuron activity and biases individual strategies towards reduced exploration in a foraging task
Malou Dongelmans, Romain Durand-de Cuttoli, Claire Nguyen, Maxime Come, Etienne K. Duranté, Damien Lemoine, Raphael Britto, Tarek Ahmed Yahia, Sarah Mondoloni, Steve Didienne, Elise Bousseyrol, Bernadette Hannesse, Lauren M. Reynolds, Nicolas Torquet, Deniz Dalkara, Fabio Marti, Alexandre Mourot, Jérémie Naudé, Philippe Faure
bioRxiv 2021.01.29.428835; doi: https://doi.org/10.1101/2021.01.29.428835
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Chronic nicotine increases midbrain dopamine neuron activity and biases individual strategies towards reduced exploration in a foraging task
Malou Dongelmans, Romain Durand-de Cuttoli, Claire Nguyen, Maxime Come, Etienne K. Duranté, Damien Lemoine, Raphael Britto, Tarek Ahmed Yahia, Sarah Mondoloni, Steve Didienne, Elise Bousseyrol, Bernadette Hannesse, Lauren M. Reynolds, Nicolas Torquet, Deniz Dalkara, Fabio Marti, Alexandre Mourot, Jérémie Naudé, Philippe Faure
bioRxiv 2021.01.29.428835; doi: https://doi.org/10.1101/2021.01.29.428835

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