Department of Neuroscience, The Scripps Research Institute, Jupiter, United States.
Chinese Institute for Brain Research, Beijing, China.
Elife. 2022 Mar 14;11:e76712. doi: 10.7554/eLife.76712.
Anatomical and physiological compartmentalization of neurons is a mechanism to increase the computational capacity of a circuit, and a major question is what role axonal compartmentalization plays. Axonal compartmentalization may enable localized, presynaptic plasticity to alter neuronal output in a flexible, experience-dependent manner. Here, we show that olfactory learning generates compartmentalized, bidirectional plasticity of acetylcholine release that varies across the longitudinal compartments of mushroom body (MB) axons. The directionality of the learning-induced plasticity depends on the valence of the learning event (aversive vs. appetitive), varies linearly across proximal to distal compartments following appetitive conditioning, and correlates with learning-induced changes in downstream mushroom body output neurons (MBONs) that modulate behavioral action selection. Potentiation of acetylcholine release was dependent on the Ca2.1 calcium channel subunit . In addition, contrast between the positive conditioned stimulus and other odors required the inositol triphosphate receptor, which maintained responsivity to odors upon repeated presentations, preventing adaptation. Downstream from the MB, a set of MBONs that receive their input from the γ3 MB compartment were required for normal appetitive learning, suggesting that they represent a key node through which reward learning influences decision-making. These data demonstrate that learning drives valence-correlated, compartmentalized, bidirectional potentiation, and depression of synaptic neurotransmitter release, which rely on distinct mechanisms and are distributed across axonal compartments in a learning circuit.
神经元的解剖和生理分区是增加电路计算能力的一种机制，而一个主要问题是轴突分区的作用是什么。轴突分区可能允许局部的、突触前的可塑性以灵活的、依赖经验的方式改变神经元的输出。在这里，我们表明嗅觉学习产生了乙酰胆碱释放的分区、双向可塑性，这种可塑性在蘑菇体（MB）轴突的纵向分区中有所不同。学习诱导的可塑性的方向性取决于学习事件的效价（厌恶型 vs. 奖赏型），在奖赏条件作用后沿近到远的分区线性变化，并且与学习诱导的下游蘑菇体输出神经元（MBON）的变化相关，这些神经元调节行为动作选择。乙酰胆碱释放的增强依赖于 Ca2.1 钙通道亚基。此外，正条件刺激与其他气味之间的对比需要三磷酸肌醇受体，该受体在重复呈现时保持对气味的反应性，防止适应。在 MB 的下游，一组从 γ3 MB 分区接收输入的 MBON 对于正常的奖赏学习是必需的，这表明它们代表了一个关键节点，通过这个节点，奖赏学习影响决策。这些数据表明，学习驱动了与效价相关的、分区的、双向的突触神经递质释放的增强和抑制，这些增强和抑制依赖于不同的机制，并在学习电路的轴突分区中分布。
