The hedonic impact of cleaner-client fish interactions is mediated by the opioid system

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 Chaetodon auriga) preferred the compartment paired with cleaner fish (Labroides dimidiatus). 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.