Valence opponency in peripheral olfactory processing.
Valence opponency in peripheral olfactory processing.
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DOI：
10.1073/pnas.2120134119
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发表时间：
2022-02-01
影响因子：
11.1
通讯作者：
Su CY
中科院分区：
文献类型：
--
作者：
Wu ST;Chen JY;Martin V;Ng R;Zhang Y;Grover D;Greenspan RJ;Aljadeff J;Su CY
嗅觉感受器神经元(ON)是否以功能上有意义的方式排列，以促进信息处理？在这里，我们通过揭示果蝇嗅觉外围的价图来解决这个长期存在的问题。在感觉毛发中，我们发现相邻的Orn对行为进行了对抗性的调节：根据其特有的尖峰幅度，传统上将大尖峰和小尖峰区分开来，分别促进或抑制相同类型的行为。系统的光遗传和热遗传分析--覆盖了触角感受器的大部分--突出了价-对手组织。关键的是，气味混合行为实验表明，拮抗的Orns之间的侧抑制调节了对抵消线索的反应的稳健的行为决定。计算模型预测，行为输出的稳健性取决于气味混合比率。复杂感觉系统的一个特点是将神经元组织成有功能意义的地图，允许通过侧抑制对平行输入进行比较和对比。然而，目前还不清楚这种映射是否存在于嗅觉中。在这里，我们通过确定果蝇感觉毛发中嗅觉感受器神经元(ON)刻板配对的组织原理来解决这个问题，其中分隔的神经元通过触觉耦合相互抑制。系统的行为分析表明，大多数配对的兽人对抗性地控制着同一类型的行为。在关键的行为背景下，包括位置偏好、产卵和求爱，这种价态的对抗是相关的。混合气味实验表明，触觉抑制为评估和塑造传递到高级大脑中枢的抵消线索提供了一种外围手段。此外，计算模型表明，这种组织可能对气味混合物中的处理比率信息做出贡献。这种嗅觉价图可能已经进化成快速处理具有行为学意义的气味混合，而不涉及昂贵的突触计算。
Are olfactory receptor neurons (ORNs) arranged in a functionally meaningful manner to facilitate information processing? Here, we address this long-standing question by uncovering a valence map in the olfactory periphery of Drosophila. Within sensory hairs, we find that neighboring ORNs antagonistically regulate behaviors: stereotypically compartmentalized large- and small-spike ORNs, recognized by their characteristic spike amplitudes, either promote or inhibit the same type of behavior, respectively. Systematic optogenetic and thermogenetic assays—covering the majority of antennal sensilla—highlight a valence-opponent organization. Critically, odor-mixture behavioral experiments show that lateral inhibition between antagonistic ORNs mediates robust behavioral decisions in response to countervailing cues. Computational modeling predicts that the robustness of behavioral output depends on odor mixture ratios. A hallmark of complex sensory systems is the organization of neurons into functionally meaningful maps, which allow for comparison and contrast of parallel inputs via lateral inhibition. However, it is unclear whether such a map exists in olfaction. Here, we address this question by determining the organizing principle underlying the stereotyped pairing of olfactory receptor neurons (ORNs) in Drosophila sensory hairs, wherein compartmentalized neurons inhibit each other via ephaptic coupling. Systematic behavioral assays reveal that most paired ORNs antagonistically regulate the same type of behavior. Such valence opponency is relevant in critical behavioral contexts including place preference, egg laying, and courtship. Odor-mixture experiments show that ephaptic inhibition provides a peripheral means for evaluating and shaping countervailing cues relayed to higher brain centers. Furthermore, computational modeling suggests that this organization likely contributes to processing ratio information in odor mixtures. This olfactory valence map may have evolved to swiftly process ethologically meaningful odor blends without involving costly synaptic computation.
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