Different types of Drosophila dopaminergic neurons (DANs) reinforce memories of unique valence and provide state-dependent motivational control [1]. Prior studies suggest that the compartment architecture of the mushroom body (MB) is the relevant resolution for distinct DAN functions [2, 3]. Here we used a recent electron microscope volume of the fly brain [4] to reconstruct the fine anatomy of individual DANs within three MB compartments. We find the 20 DANs of the γ5 compartment, at least some of which provide reward teaching signals, can be clustered into 5 anatomical subtypes that innervate different regions within γ5. Reconstructing 821 upstream neurons reveals input selectivity, supporting the functional relevance of DAN sub-classification. Only one PAM-γ5 DAN subtype γ5(fb) receives direct recurrent feedback from γ5β′2a mushroom body output neurons (MBONs) and behavioral experiments distinguish a role for these DANs in memory revaluation from those reinforcing sugar memory. Other DAN subtypes receive major, and potentially reinforcing, inputs from putative gustatory interneurons or lateral horn neurons, which can also relay indirect feedback from MBONs. We similarly reconstructed the single aversively reinforcing PPL1-γ1pedc DAN. The γ1pedc DAN inputs mostly differ from those of γ5 DANs and they cluster onto distinct dendritic branches, presumably separating its established roles in aversive reinforcement and appetitive motivation [5, 6]. Tracing also identified neurons that provide broad input to γ5, β′2a, and γ1pedc DANs, suggesting that distributed DAN populations can be coordinately regulated. These connectomic and behavioral analyses therefore reveal further complexity of dopaminergic reinforcement circuits between and within MB compartments.

不同类型的果蝇多巴胺能神经元 (DAN) 增强了独特价的记忆，并提供了状态依赖的动机控制 [1]。先前的研究表明，蘑菇体 (MB) 的隔室结构是不同 DAN 功能的相关分辨率 [2, 3]。在这里，我们使用最近的电子显微镜体积的苍蝇大脑 [4] 来重建三个 MB 隔间内单个 DAN 的精细解剖结构。我们发现 γ5 隔室的 20 个 DAN，至少其中一些提供奖励教学信号，可以聚集成 5 个解剖亚型，支配 γ5 内的不同区域。重建 821 个上游神经元揭示了输入选择性，支持 DAN 子分类的功能相关性。只有一种 PAM-γ5 DAN 亚型 γ5(fb) 接收来自 γ5β'2a 蘑菇体输出神经元 (MBON) 的直接循环反馈，并且行为实验区分了这些 DAN 在记忆重估中的作用与那些增强糖记忆的作用。其他 DAN 亚型接收来自假定的味觉中间神经元或侧角神经元的主要且可能增强的输入，这些输入也可以传递来自 MBON 的间接反馈。我们同样重建了单个厌恶性增强的 PPL1-γ1pedc DAN。γ1pedc DAN 输入与 γ5 DAN 的输入大多不同，它们聚集在不同的树突分支上，可能将其在厌恶强化和食欲动机中的既定角色分开 [5, 6]。追踪还发现了为 γ5、β'2a 和 γ1pedc DAN 提供广泛输入的神经元，表明分布式 DAN 种群可以被协调调节。因此，这些连接组学和行为分析揭示了 MB 隔间之间和内部的多巴胺能增强回路的进一步复杂性。