Maximino Caio, Araujo-Silva Heloysa, Cacela-Rodrigues Inês, Luchiari Ana C, Saraiva João L, Soares Marta C
Laboratory of Neurosciences and Behavior "Frederico Guilherme Graeff", Faculty of Psychology, Institute of Health and Biological Studies, Federal University of the South and Southeast of Pará, Marabá 68500-000, Brazil.
Research Group on Neurosciences, Behavior & Cognition, Federal University of the South and Southeast of Pará, Marabá 68500-000, Brazil.
Proc Biol Sci. 2025 Aug;292(2052):20251532. doi: 10.1098/rspb.2025.1532. Epub 2025 Aug 13.
According to the 'incentive salience hypothesis' reward processing involves two main components, including the motivation to obtain a reward (i.e. incentive salience or 'wanting') and the hedonic pleasure felt during its consumption (i.e. hedonic impact or 'liking'), which are dissociable. The processing of these hedonic mechanisms is suggested to be mediated by opioid neurotransmission; however, most evidence comes from humans and other mammals. Here we argue that, in mutualistic associations, client fish seek to interact with cleaner fish not only due to the immediate benefits of being cleaned but also because of the hedonic impact of tactile stimulation, modulated by the opioid system. We used a conditioned place preference (CPP) paradigm to test the hedonic dimension of motivation to be cleaned and found that de-parasitized client fish (the butterflyfish ) preferred the compartment paired with cleaner fish (). Treatment with the μ-opioid receptor agonist The µ-opioid receptor agonist 2-Ala-4-mephe-5-gly-enkephalin (DAMGO) dose-dependently increased preference, while treatment with the antagonist naloxone decreased it. To test for fish incentive salience, we used a detour task, with barriers being added after each trial to demand higher response strength to reach the target and found that client fish can circumvent barriers to reach a cleaner-adjacent compartment. Response strength (number of barriers added before 'giving up') was not affected by treatment with either naloxone or DAMGO. Our results show that cleaner-client interactions are hedonically positive for clients, an effect that is mediated by the opiodergic system. Visual contact with cleaners is sufficient to activate incentive salience programmes, but no evidence of participation of the opioidergic system in these programmes was found. Overall, we provide the first evidence confirming the participation of the opioidergic system in motivation to be cleaned in mutualistic associations.
根据“动机显著性假说”，奖赏处理涉及两个主要成分，包括获得奖赏的动机（即动机显著性或“欲求”）以及在消费奖赏过程中感受到的享乐愉悦（即享乐影响或“喜好”），这两者是可分离的。这些享乐机制的处理过程被认为是由阿片类神经传递介导的；然而，大多数证据来自人类和其他哺乳动物。在此我们认为，在互利共生关系中，寄主鱼寻求与清洁鱼互动，不仅是因为清洁带来的直接益处，还因为触觉刺激的享乐影响，这种影响由阿片系统调节。我们使用条件性位置偏好（CPP）范式来测试被清洁动机的享乐维度，发现去除寄生虫的寄主鱼（蝴蝶鱼）更喜欢与清洁鱼配对的隔室。用μ-阿片受体激动剂2-丙氨酸-4-甲硫氨酸-5-甘氨酸脑啡肽（DAMGO）处理后，偏好呈剂量依赖性增加，而用拮抗剂纳洛酮处理则降低了偏好。为了测试鱼类的动机显著性，我们使用了迂回任务，每次试验后增加障碍物，要求更高的反应强度才能到达目标，结果发现寄主鱼能够绕过障碍物到达与清洁鱼相邻的隔室。反应强度（“放弃”前增加的障碍物数量）不受纳洛酮或DAMGO处理的影响。我们的结果表明，清洁鱼与寄主鱼的互动对寄主鱼来说在享乐方面是积极的，这种效应由阿片能系统介导。与清洁鱼的视觉接触足以激活动机显著性程序，但未发现阿片能系统参与这些程序的证据。总体而言，我们提供了首个证据，证实了阿片能系统参与互利共生关系中被清洁的动机。
