Journal of Neuroscience ( IF 4.4 ) Pub Date : 2024-08-28 , DOI: 10.1523/jneurosci.0120-24.2024 Masakazu Taira 1, 2 , Samuel J Millard 2 , Anna Verghese 2 , Lauren E DiFazio 2 , Ivy B Hoang 2 , Ruiting Jia 2 , Ana Sias 2 , Andrew Wikenheiser 2 , Melissa J Sharpe 1, 2
Dopamine release in the nucleus accumbens core (NAcC) is generally considered to be a proxy for phasic firing of the ventral tegmental area dopamine (VTADA) neurons. Thus, dopamine release in NAcC is hypothesized to reflect a unitary role in reward prediction error signaling. However, recent studies reveal more diverse roles of dopamine neurons, which support an emerging idea that dopamine regulates learning differently in distinct circuits. To understand whether the NAcC might regulate a unique component of learning, we recorded dopamine release in NAcC while male rats performed a backward conditioning task where a reward is followed by a neutral cue. We used this task because we can delineate different components of learning, which include sensory-specific inhibitory and general excitatory components. Furthermore, we have shown that VTADA neurons are necessary for both the specific and general components of backward associations. Here, we found that dopamine release in NAcC increased to the reward across learning while reducing to the cue that followed as it became more expected. This mirrors the dopamine prediction error signal seen during forward conditioning and cannot be accounted for temporal-difference reinforcement learning. Subsequent tests allowed us to dissociate these learning components and revealed that dopamine release in NAcC reflects the general excitatory component of backward associations, but not their sensory-specific component. These results emphasize the importance of examining distinct functions of different dopamine projections in reinforcement learning.
中文翻译:
伏隔核中的多巴胺释放编码学习的一般兴奋性成分
伏隔核 (NAcC) 中的多巴胺释放通常被认为是腹侧被盖区多巴胺 (VTADA) 神经元阶段性放电的代理。因此,假设 NAcC 中的多巴胺释放反映了奖励预测误差信号传导中的单一作用。然而,最近的研究揭示了多巴胺神经元更多样化的作用,这支持了一个新兴的观点,即多巴胺在不同回路中以不同的方式调节学习。为了了解 NAcC 是否可能调节学习的独特组成部分,我们在 NAcC 中记录了多巴胺的释放,而雄性大鼠执行向后条件反射任务,其中奖励后跟中性提示。我们之所以使用这个任务,是因为我们可以描述学习的不同组成部分,包括感觉特异性抑制和一般兴奋性成分。此外,我们已经表明 VTADA 神经元对于反向关联的特异性和一般成分都是必需的。在这里,我们发现 NAcC 中的多巴胺释放在学习过程中会增加奖励,而随着它变得更加预期,多巴胺释放会减少到随之而来的线索。这反映了在前向条件反射期间看到的多巴胺预测误差信号,不能解释时间差异强化学习。随后的测试使我们能够分离这些学习成分,并揭示 NAcC 中的多巴胺释放反映了向后联想的一般兴奋成分,而不是它们的感觉特异性成分。这些结果强调了在强化学习中检查不同多巴胺投射的不同功能的重要性。