An evolutionarily conserved cation channel tunes the sensitivity of gustatory neurons to ephaptic inhibition in Drosophila

• 成果类型: Article
• 署名作者: Lee, Minhyuk; Kim, Seon Yeong; Park, Taeim; Yoon, Sung-Eun; Kim, Young-Joon; Joo, Kyeung Min; Kwon, Jae Young; Kim, Kyuhyung; Kang, Kyeongjin
• 署名单位: Korea Brain Research Institute (KBRI); Sungkyunkwan University (SKKU); Samsung Medical Center; Sungkyunkwan University (SKKU); Daegu Gyeongbuk Institute of Science & Technology (DGIST); Gwangju Institute of Science & Technology (GIST)
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-15080
• DOI: 10.1073/pnas.2413134122
• 发表日期: 2025-01-15
• 关键词: taste mixture interactions; bitter taste; purkinje-cells; suppression; reveals; motoneurons; receptors; dendrites; avoidance; synapses

摘要

In ephaptic coupling, physically adjacent neurons influence one another's activity via the electric fields they generate. To date, the molecular mechanisms that mediate and modulate ephaptic coupling's effects remain poorly understood. Here, we show that the hyperpolarization-activated cyclic nucleotide-gated (HCN) channel lateralizes the potentially mutual ephaptic inhibition between Drosophila gustatory receptor neurons (GRNs). While sweet-sensing GRNs (sGRNs) engage in ephaptic suppression of the adjacent bitter-sensing GRNs (bGRNs), HCN expression in sGRNs enables them to resist ephaptic suppression from the bGRNs. This one-sided ephaptic inhibition confers sweetness dominance, facilitating ingestion of bitter-laced sweets. The role of fly HCN in this process can be replaced by human HCN2. Furthermore, unlike the mechanism in olfaction, gustatory ephaptic inhibition is independent of sensillum potential changes, suggesting that the compartmentalized arrangement of neighboring GRNs is dispensable for gustatory ephaptic inhibition. These findings indicate a role for the gating of ephaptic coding to ensure the intake of the essential nutrient despite bitter contaminants present in the feeding niche of Drosophila, and propose that studies in Drosophila gustation could reveal ephaptic principles conserved across diverse animals.