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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.
Highlights
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
We have shown that decisions in reward-based foraging are modulated by the cholinergic neurotransmission of the ventral tegmental area (VTA), with a particular role of nicotinic acetylcholine receptors in directed exploration, driven by expected uncertainty[33]
Mouse choices depend on reward probability, uncertainty and on motor cost
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 in mice the impact of chronic nicotine on midbrain dopamine neuron activity and its consequence on the trade-off between exploitation and exploration. When faced with two alternatives, one with low and one with high probability of reward, animals do not purely exploit, they choose the less likely rewarded option a significant portion of the time The origin of such seemingly suboptimal choices remains poorly understood. Altered DA function is a promising candidate to link chronic nicotine exposure to changes in decision-making behavior This neuromodulator, which is at the crossroads of motivation, learning and decision-making, is hijacked, in the context of addiction, by most drugs of abuse[21,22,23]. Drug-induced alterations of DA transmission may modify behavioral choices, either positively or negatively depending on the environment and the specific type of DA manipulation
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