Yamagata Nobuhiro, Imanishi Yasuhito, Wu Hongyang, Kondo Shu, Sano Hiroko, Tanimoto Hiromu
Graduate School of Life Sciences, Tohoku University, Sendai, Japan.
Department of Biological Science and Technology, Faculty of Advanced Engineering, Tokyo University of Science, Tokyo, Japan.
Front Behav Neurosci. 2022 Oct 19;16:986064. doi: 10.3389/fnbeh.2022.986064. eCollection 2022.
CCHamide-2 (CCHa2) is a protostome excitatory peptide ortholog known for various arthropod species. In fruit flies, CCHa2 plays a crucial role in the endocrine system, allowing peripheral tissue to communicate with the central nervous system to ensure proper development and the maintenance of energy homeostasis. Since the formation of odor-sugar associative long-term memory (LTM) depends on the nutrient status in an animal, CCHa2 may play an essential role in linking memory and metabolic systems. Here we show that CCHa2 signals are important for consolidating appetitive memory by acting on the rewarding dopamine neurons. Genetic disruption of CCHa2 using mutant strains abolished appetitive LTM but not short-term memory (STM). A post-learning thermal suppression of CCHa2 expressing cells impaired LTM. In contrast, a post-learning thermal activation of CCHa2 cells stabilized STM induced by non-nutritious sugar into LTM. The receptor of CCHa2, CCHa2-R, was expressed in a subset of dopamine neurons that mediate reward for LTM. In accordance, the receptor expression in these dopamine neurons was required for LTM specifically. We thus concluded that CCHa2 conveys a sugar nutrient signal to the dopamine neurons for memory consolidation. Our finding establishes a direct interplay between brain reward and the putative endocrine system for long-term energy homeostasis.
CCH酰胺-2(CCHa2)是一种原口动物兴奋性肽直系同源物,在多种节肢动物物种中都有发现。在果蝇中,CCHa2在内分泌系统中发挥着关键作用,使外周组织能够与中枢神经系统进行通信,以确保正常发育和能量稳态的维持。由于气味-糖联想性长期记忆(LTM)的形成取决于动物的营养状况,CCHa2可能在连接记忆和代谢系统中发挥重要作用。在这里,我们表明CCHa2信号通过作用于产生奖赏效应的多巴胺能神经元,对巩固食欲记忆很重要。使用突变株对CCHa2进行基因破坏消除了食欲性LTM,但没有消除短期记忆(STM)。学习后对表达CCHa2的细胞进行热抑制会损害LTM。相反,学习后对CCHa2细胞进行热激活可将由无营养糖诱导的STM稳定为LTM。CCHa2的受体CCHa2-R在介导LTM奖赏的一部分多巴胺能神经元中表达。相应地,这些多巴胺能神经元中的受体表达对于LTM是特异性必需的。因此,我们得出结论,CCHa2将糖营养信号传递给多巴胺能神经元以进行记忆巩固。我们的发现确立了大脑奖赏与假定的内分泌系统之间为长期能量稳态而进行的直接相互作用。