Individualistic reward-seeking strategies that predict response to nicotine emerge among isogenic male mice living in a micro-society.

IF 9.8 1区 生物学 Q1 Agricultural and Biological Sciences PLoS Biology Pub Date : 2024-10-24 eCollection Date: 2024-10-01 DOI:10.1371/journal.pbio.3002850
Sophie L Fayad, Lauren M Reynolds, Nicolas Torquet, Stefania Tolu, Sarah Mondoloni, Claire Nguyen, Amy Siriphanh, Robin Justo, Steve Didienne, Nicolas Debray, Cécile Viollet, Louis Raynaud, Yasmine Layadi, Coralie Fouquet, Bernadette Hannesse, Ana-Marta Capaz, Thomas Topilko, Nicolas Renier, Alexandre Mourot, Fabio Marti, Philippe Faure
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Abstract

Individual animals differ in their traits and preferences, which shape their social interactions, survival, and susceptibility to disease, including addiction. Nicotine use is highly heterogenous and has been linked to the expression of personality traits. Although these relationships are well documented, we have limited understanding of the neurophysiological mechanisms that give rise to distinct behavioral profiles and their connection to nicotine susceptibility. To address this question, we conducted a study using a semi-natural and social environment called "Souris-City" to observe the long-term behavior of individual male mice. Souris-City provided both a communal living area and a separate test area where mice engaged in a reward-seeking task isolated from their peers. Mice developed individualistic reward-seeking strategies when choosing between water and sucrose in the test compartment, which, in turn, predicted how they adapted to the introduction of nicotine as a reinforcer. Moreover, the profiles mice developed while isolated in the test area correlated with their behavior within the social environment, linking decision-making strategies to the expression of behavioral traits. Neurophysiological markers of adaptability within the dopamine system were apparent upon nicotine challenge and were associated with specific profiles. Our findings suggest that environmental adaptations influence behavioral traits and sensitivity to nicotine by acting on dopaminergic reactivity in the face of nicotine exposure, potentially contributing to addiction susceptibility. These results further emphasize the importance of understanding interindividual variability in behavior to gain insight into the mechanisms of decision-making and addiction.

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生活在微型社会中的同源雄性小鼠出现了可预测对尼古丁反应的个体化奖励追求策略。
动物个体的特质和偏好各不相同,这些特质和偏好决定了它们的社会互动、生存以及对疾病(包括成瘾)的易感性。尼古丁的使用具有高度的异质性,并且与人格特质的表达有关。虽然这些关系都有据可查,但我们对导致不同行为特征的神经生理机制及其与尼古丁易感性的联系了解有限。为了解决这个问题,我们利用名为 "苏里斯城 "的半自然社会环境进行了一项研究,以观察雄性小鼠个体的长期行为。苏里斯城 "既提供了一个公共生活区,也提供了一个独立的测试区,让小鼠在该测试区进行与同伴隔离的奖励寻求任务。当小鼠在测试区的水和蔗糖之间做出选择时,它们形成了个体化的奖励寻求策略,这反过来又预测了它们如何适应尼古丁作为强化剂的引入。此外,小鼠在测试区隔离时形成的特征与它们在社会环境中的行为相关,这将决策策略与行为特征的表达联系了起来。尼古丁挑战时,多巴胺系统内适应性的神经生理学标记明显,并且与特定的特征相关。我们的研究结果表明,面对尼古丁暴露,环境适应性通过作用于多巴胺能反应性来影响行为特征和对尼古丁的敏感性,从而可能导致成瘾易感性。这些结果进一步强调了了解行为的个体间变异性以深入了解决策和成瘾机制的重要性。
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来源期刊
PLoS Biology
PLoS Biology BIOCHEMISTRY & MOLECULAR BIOLOGY-BIOLOGY
CiteScore
15.40
自引率
2.00%
发文量
359
审稿时长
3-8 weeks
期刊介绍: PLOS Biology is the flagship journal of the Public Library of Science (PLOS) and focuses on publishing groundbreaking and relevant research in all areas of biological science. The journal features works at various scales, ranging from molecules to ecosystems, and also encourages interdisciplinary studies. PLOS Biology publishes articles that demonstrate exceptional significance, originality, and relevance, with a high standard of scientific rigor in methodology, reporting, and conclusions. The journal aims to advance science and serve the research community by transforming research communication to align with the research process. It offers evolving article types and policies that empower authors to share the complete story behind their scientific findings with a diverse global audience of researchers, educators, policymakers, patient advocacy groups, and the general public. PLOS Biology, along with other PLOS journals, is widely indexed by major services such as Crossref, Dimensions, DOAJ, Google Scholar, PubMed, PubMed Central, Scopus, and Web of Science. Additionally, PLOS Biology is indexed by various other services including AGRICOLA, Biological Abstracts, BIOSYS Previews, CABI CAB Abstracts, CABI Global Health, CAPES, CAS, CNKI, Embase, Journal Guide, MEDLINE, and Zoological Record, ensuring that the research content is easily accessible and discoverable by a wide range of audiences.
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