Chronic nicotine increases midbrain dopamine neuron activity and biases individual strategies towards reduced exploration in mice

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 in mice the impact of ch...

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Published inNature communications Vol. 12; no. 1; pp. 6945 - 15
Main Authors Dongelmans, Malou, Durand-de Cuttoli, Romain, Nguyen, Claire, Come, Maxime, Duranté, Etienne K., Lemoine, Damien, Brito, Raphaël, Ahmed Yahia, Tarek, Mondoloni, Sarah, Didienne, Steve, Bousseyrol, Elise, Hannesse, Bernadette, Reynolds, Lauren M., Torquet, Nicolas, Dalkara, Deniz, Marti, Fabio, Mourot, Alexandre, Naudé, Jérémie, Faure, Philippe
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 26.11.2021
Nature Publishing Group
Nature Portfolio
Subjects
631/378/116/2396
631/378/1788
631/378/3920
9/30
Animals
Behavior, Animal - drug effects
Behavior, Animal - physiology
Decision analysis
Decision making
Dopamine
Dopamine - metabolism
Dopamine receptors
Dopaminergic Neurons - drug effects
Dopaminergic Neurons - metabolism
Exploitation
Exploration
Exploratory behavior
Exploratory Behavior - drug effects
Exploratory Behavior - physiology
Exposure
Genetics
Humanities and Social Sciences
Information processing
Intracranial self-stimulation
Life Sciences
Male
Mesencephalon
Mesencephalon - cytology
Mesencephalon - drug effects
Mesencephalon - metabolism
Mice
Models, Animal
multidisciplinary
Neurons
Neurons and Cognition
Nicotine
Nicotine - administration & dosage
Nicotine - adverse effects
Optics
Optogenetics
Phenotypes
Prejudice
Reinforcement
Reward
Science
Science (multidisciplinary)
Self Administration
Self stimulation
Stereotaxic Techniques
Tradeoffs
Online AccessGet full text

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Abstract 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 in mice the impact of chronic nicotine on midbrain dopamine neuron activity and its consequence on the trade-off between exploitation and exploration. Model-based and archetypal analysis revealed substantial inter-individual variability in decision-making strategies, with mice passively exposed to nicotine shifting toward a more exploitative profile compared to non-exposed animals. We then mimicked the effect of chronic nicotine on the tonic activity of dopamine neurons using optogenetics, and found that photo-stimulated mice adopted a behavioral phenotype similar to that of mice exposed to chronic nicotine. Our results reveal a key role of tonic midbrain dopamine in the exploration/exploitation trade-off and highlight a potential mechanism by which nicotine affects the exploration/exploitation balance and decision-making. Chronic nicotine exposure impacts various components of decision-making processes, such as exploratory behaviors. Here, the authors identify the cellular mechanism and show that chronic nicotine exposure increases the tonic activity of VTA dopaminergic neurons and reduces exploration in mice.
AbstractList 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 in mice the impact of chronic nicotine on midbrain dopamine neuron activity and its consequence on the trade-off between exploitation and exploration. Model-based and archetypal analysis revealed substantial inter-individual variability in decision-making strategies, with mice passively exposed to nicotine shifting toward a more exploitative profile compared to non-exposed animals. We then mimicked the effect of chronic nicotine on the tonic activity of dopamine neurons using optogenetics, and found that photo-stimulated mice adopted a behavioral phenotype similar to that of mice exposed to chronic nicotine. Our results reveal a key role of tonic midbrain dopamine in the exploration/exploitation trade-off and highlight a potential mechanism by which nicotine affects the exploration/exploitation balance and decision-making.
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 in mice the impact of chronic nicotine on midbrain dopamine neuron activity and its consequence on the trade-off between exploitation and exploration. Model-based and archetypal analysis revealed substantial inter-individual variability in decision-making strategies, with mice passively exposed to nicotine shifting toward a more exploitative profile compared to non-exposed animals. We then mimicked the effect of chronic nicotine on the tonic activity of dopamine neurons using optogenetics, and found that photo-stimulated mice adopted a behavioral phenotype similar to that of mice exposed to chronic nicotine. Our results reveal a key role of tonic midbrain dopamine in the exploration/exploitation trade-off and highlight a potential mechanism by which nicotine affects the exploration/exploitation balance and decision-making. Chronic nicotine exposure impacts various components of decision-making processes, such as exploratory behaviors. Here, the authors identify the cellular mechanism and show that chronic nicotine exposure increases the tonic activity of VTA dopaminergic neurons and reduces exploration in mice.
Chronic nicotine exposure impacts various components of decision-making processes, such as exploratory behaviors. Here, the authors identify the cellular mechanism and show that chronic nicotine exposure increases the tonic activity of VTA dopaminergic neurons and reduces exploration in mice.
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 in mice the impact of chronic nicotine on midbrain dopamine neuron activity and its consequence on the trade-off between exploitation and exploration. Model-based and archetypal analysis revealed substantial inter-individual variability in decision-making strategies, with mice passively exposed to nicotine shifting toward a more exploitative profile compared to non-exposed animals. We then mimicked the effect of chronic nicotine on the tonic activity of dopamine neurons using optogenetics, and found that photo-stimulated mice adopted a behavioral phenotype similar to that of mice exposed to chronic nicotine. Our results reveal a key role of tonic midbrain dopamine in the exploration/exploitation trade-off and highlight a potential mechanism by which nicotine affects the exploration/exploitation balance and decision-making.Chronic nicotine exposure impacts various components of decision-making processes, such as exploratory behaviors. Here, the authors identify the cellular mechanism and show that chronic nicotine exposure increases the tonic activity of VTA dopaminergic neurons and reduces exploration in mice.
ArticleNumber 6945
Author Naudé, Jérémie
Ahmed Yahia, Tarek
Bousseyrol, Elise
Lemoine, Damien
Mondoloni, Sarah
Dongelmans, Malou
Mourot, Alexandre
Hannesse, Bernadette
Dalkara, Deniz
Come, Maxime
Duranté, Etienne K.
Didienne, Steve
Reynolds, Lauren M.
Brito, Raphaël
Torquet, Nicolas
Durand-de Cuttoli, Romain
Nguyen, Claire
Marti, Fabio
Faure, Philippe
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SSID ssj0000391844
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Snippet Long-term exposure to nicotine alters brain circuits and induces profound changes in decision-making strategies, affecting behaviors both related and unrelated...
Chronic nicotine exposure impacts various components of decision-making processes, such as exploratory behaviors. Here, the authors identify the cellular...
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Open Access Repository
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Publisher
StartPage 6945
SubjectTerms 631/378/116/2396
631/378/1788
631/378/3920
9/30
Animals
Behavior, Animal - drug effects
Behavior, Animal - physiology
Decision analysis
Decision making
Dopamine
Dopamine - metabolism
Dopamine receptors
Dopaminergic Neurons - drug effects
Dopaminergic Neurons - metabolism
Exploitation
Exploration
Exploratory behavior
Exploratory Behavior - drug effects
Exploratory Behavior - physiology
Exposure
Genetics
Humanities and Social Sciences
Information processing
Intracranial self-stimulation
Life Sciences
Male
Mesencephalon
Mesencephalon - cytology
Mesencephalon - drug effects
Mesencephalon - metabolism
Mice
Models, Animal
multidisciplinary
Neurons
Neurons and Cognition
Nicotine
Nicotine - administration & dosage
Nicotine - adverse effects
Optics
Optogenetics
Phenotypes
Prejudice
Reinforcement
Reward
Science
Science (multidisciplinary)
Self Administration
Self stimulation
Stereotaxic Techniques
Tradeoffs
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Title Chronic nicotine increases midbrain dopamine neuron activity and biases individual strategies towards reduced exploration in mice
URI https://link.springer.com/article/10.1038/s41467-021-27268-7
https://www.ncbi.nlm.nih.gov/pubmed/34836948
https://www.proquest.com/docview/2602863870
https://hal.science/hal-03839427
https://pubmed.ncbi.nlm.nih.gov/PMC8635406
https://doaj.org/article/ad5caf779392407fa4039e76c1116fb7
Volume 12
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