Department of Genetics, Leibniz Institute for Neurobiology, Magdeburg, Germany.
Institute of Biology, Otto von Guericke University Magdeburg, Germany.
J Comp Neurol. 2021 May 1;529(7):1553-1570. doi: 10.1002/cne.25037. Epub 2021 Jan 22.
Dopamine serves many functions, and dopamine neurons are correspondingly diverse. We use a combination of optogenetics, behavioral experiments, and high-resolution video-tracking to probe for the functional capacities of two single, identified dopamine neurons in larval Drosophila. The DAN-f1 and the DAN-d1 neuron were recently found to carry aversive teaching signals during Pavlovian olfactory learning. We enquire into a fundamental feature of these teaching signals, namely their temporal "fingerprint". That is, receiving punishment feels bad, whereas being relieved from it feels good, and animals and humans alike learn with opposite valence about the occurrence and the termination of punishment (the same principle applies in the appetitive domain, with opposite sign). We find that DAN-f1 but not DAN-d1 can mediate such timing-dependent valence reversal: presenting an odor before DAN-f1 activation leads to learned avoidance of the odor (punishment memory), whereas presenting the odor upon termination of DAN-f1 activation leads to learned approach (relief memory). In contrast, DAN-d1 confers punishment memory only. These effects are further characterized in terms of the impact of the duration of optogenetic activation, the temporal stability of the memories thus established, and the specific microbehavioral patterns of locomotion through which they are expressed. Together with recent findings in the appetitive domain and from adult Drosophila, our results suggest that heterogeneity in the temporal fingerprint of teaching signals might be a more general principle of reinforcement processing through dopamine neurons.
多巴胺具有多种功能,多巴胺神经元也相应地具有多样性。我们结合光遗传学、行为实验和高分辨率视频追踪,探究了两个单一、已鉴定的幼虫果蝇多巴胺神经元的功能能力。最近发现 DAN-f1 和 DAN-d1 神经元在巴甫洛夫嗅觉学习过程中携带厌恶教学信号。我们探究了这些教学信号的一个基本特征,即它们的时间“指纹”。也就是说,受到惩罚会感觉很糟糕,而摆脱惩罚会感觉很好,动物和人类都会根据惩罚的发生和结束以相反的效价进行学习(在食欲领域也适用,只是符号相反)。我们发现,只有 DAN-f1 而不是 DAN-d1 可以介导这种依赖时间的效价反转:在 DAN-f1 激活之前呈现气味会导致对该气味的学习回避(惩罚记忆),而在 DAN-f1 激活结束时呈现气味会导致对该气味的学习趋近(缓解记忆)。相比之下,DAN-d1 只能赋予惩罚记忆。我们根据光遗传学激活的持续时间、由此建立的记忆的时间稳定性以及它们表达的特定运动微行为模式,进一步描述了这些效应。结合最近在食欲领域和成年果蝇中的发现,我们的结果表明,教学信号的时间指纹的异质性可能是多巴胺神经元强化处理的更普遍原则。