Alejandro Pan-Vazquez, Yoel Sanchez Araujo, Brenna McMannon, Miranta Louka, Akhil Bandi, Laura Haetzel, Mayo Faulkner, Jonathan W Pillow, Nathaniel D Daw, Ilana B Witten
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Although animals can learn to perform complex tasks that involve arbitrary associations between stimuli, actions, and rewards,<sup>1</sup><sup>,</sup><sup>2</sup><sup>,</sup><sup>3</sup><sup>,</sup><sup>4</sup><sup>,</sup><sup>5</sup><sup>,</sup><sup>6</sup> a consistent and striking result across varied experimental paradigms is that in initially acquiring such tasks, large differences between individuals are apparent in the learning process.<sup>7</sup><sup>,</sup><sup>8</sup><sup>,</sup><sup>9</sup><sup>,</sup><sup>10</sup><sup>,</sup><sup>11</sup><sup>,</sup><sup>12</sup> What neural mechanisms contribute to initial task acquisition, and why do some individuals learn a new task much more quickly than others? To address these questions, we recorded longitudinally from dopaminergic (DA) axon terminals in mice learning a visual decision-making task.<sup>7</sup> Across striatum, DA responses tracked idiosyncratic and side-specific learning trajectories, consistent with widespread reward prediction error coding across DA terminals. However, even before any rewards were delivered, contralateral-side-specific visual responses were present in DA terminals, primarily in the dorsomedial striatum (DMS). These pre-existing responses predicted the extent of learning for contralateral stimuli. Moreover, activation of these terminals improved contralateral performance. Thus, the initial conditions of a projection-specific and feature-specific DA signal help explain individual learning trajectories. More broadly, this work suggests that functional heterogeneity across DA projections may serve to bias target regions toward learning about different subsets of task features, providing a potential mechanism to address the dimensionality of the initial task learning problem.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":" ","pages":"5349-5358.e6"},"PeriodicalIF":8.1000,"publicationDate":"2024-11-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11579926/pdf/","citationCount":"0","resultStr":"{\"title\":\"Pre-existing visual responses in a projection-defined dopamine population explain individual learning trajectories.\",\"authors\":\"Alejandro Pan-Vazquez, Yoel Sanchez Araujo, Brenna McMannon, Miranta Louka, Akhil Bandi, Laura Haetzel, Mayo Faulkner, Jonathan W Pillow, Nathaniel D Daw, Ilana B Witten\",\"doi\":\"10.1016/j.cub.2024.09.045\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>A key challenge of learning a new task is that the environment is high dimensional-there are many different sensory features and possible actions, with typically only a small reward-relevant subset. 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引用次数: 0
摘要
学习新任务的一个主要挑战是环境的高维性--有许多不同的感官特征和可能的行动,通常只有一小部分与奖励相关。尽管动物可以学习完成涉及刺激、行动和奖励之间任意关联的复杂任务,1,2,3,4,5,6 但在不同的实验范式中,一个一致而惊人的结果是,在最初获得此类任务时,个体之间在学习过程中存在明显的巨大差异。7,8,9,10,11,12 是什么神经机制促成了最初任务的获得,以及为什么有些个体比其他个体更快地学会一项新任务?为了解决这些问题,我们纵向记录了正在学习视觉决策任务的小鼠的多巴胺能(DA)轴突末端。7 在整个纹状体中,DA反应追踪了特异性和侧面特异性的学习轨迹,这与DA末端广泛的奖励预测错误编码是一致的。然而,甚至在任何奖励被传递之前,DA 末端(主要是背内侧纹状体(DMS))就已经出现了对侧特异性视觉反应。这些预先存在的反应预示着对对侧刺激的学习程度。此外,激活这些末端可改善对侧的表现。因此,投射特异性和特征特异性 DA 信号的初始条件有助于解释个体的学习轨迹。更广泛地说,这项研究表明,DA投射的功能异质性可能会使目标区域偏向于学习不同的任务特征子集,从而为解决初始任务学习问题的维度提供了一种潜在机制。
Pre-existing visual responses in a projection-defined dopamine population explain individual learning trajectories.
A key challenge of learning a new task is that the environment is high dimensional-there are many different sensory features and possible actions, with typically only a small reward-relevant subset. Although animals can learn to perform complex tasks that involve arbitrary associations between stimuli, actions, and rewards,1,2,3,4,5,6 a consistent and striking result across varied experimental paradigms is that in initially acquiring such tasks, large differences between individuals are apparent in the learning process.7,8,9,10,11,12 What neural mechanisms contribute to initial task acquisition, and why do some individuals learn a new task much more quickly than others? To address these questions, we recorded longitudinally from dopaminergic (DA) axon terminals in mice learning a visual decision-making task.7 Across striatum, DA responses tracked idiosyncratic and side-specific learning trajectories, consistent with widespread reward prediction error coding across DA terminals. However, even before any rewards were delivered, contralateral-side-specific visual responses were present in DA terminals, primarily in the dorsomedial striatum (DMS). These pre-existing responses predicted the extent of learning for contralateral stimuli. Moreover, activation of these terminals improved contralateral performance. Thus, the initial conditions of a projection-specific and feature-specific DA signal help explain individual learning trajectories. More broadly, this work suggests that functional heterogeneity across DA projections may serve to bias target regions toward learning about different subsets of task features, providing a potential mechanism to address the dimensionality of the initial task learning problem.
期刊介绍:
Current Biology is a comprehensive journal that showcases original research in various disciplines of biology. It provides a platform for scientists to disseminate their groundbreaking findings and promotes interdisciplinary communication. The journal publishes articles of general interest, encompassing diverse fields of biology. Moreover, it offers accessible editorial pieces that are specifically designed to enlighten non-specialist readers.