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Parallel Reinforcement Pathways for Conditioned Food Aversions in the Honeybee

2010; Elsevier BV; Volume: 20; Issue: 24 Linguagem: Inglês

10.1016/j.cub.2010.11.040

1879-0445

Geraldine A. Wright, Julie A. Mustard, Nicola K. Simcock, Alexandra A.R. Ross-Taylor, Lewis D. McNicholas, Alexandra Luminita Popescu, Frédéric Marion‐Poll,

Neurobiology and Insect Physiology Research

Avoiding toxins in food is as important as obtaining nutrition. Conditioned food aversions have been studied in animals as diverse as nematodes and humans [1Reilly S. Central gustatory system lesions and conditioned taste aversion.in: Reilly S. Schachtman T.R. Conditioned Taste Aversion: Behavioral and Neural Processes. Oxford University Press, Oxford2009: 309-327Google Scholar, 2Zhang Y. Lu H. Bargmann C.I. Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans.Nature. 2005; 438: 179-184Crossref PubMed Scopus (538) Google Scholar], but the neural signaling mechanisms underlying this form of learning have been difficult to pinpoint. Honeybees quickly learn to associate floral cues with food [3Bitterman M.E. Menzel R. Fietz A. Schäfer S. Classical conditioning of proboscis extension in honeybees (Apis mellifera).J. Comp. Psychol. 1983; 97: 107-119Crossref PubMed Scopus (848) Google Scholar], a trait that makes them an excellent model organism for studying the neural mechanisms of learning and memory. Here we show that honeybees not only detect toxins but can also learn to associate odors with both the taste of toxins and the postingestive consequences of consuming them. We found that two distinct monoaminergic pathways mediate learned food aversions in the honeybee. As for other insect species conditioned with salt or electric shock reinforcers [4Honjo K. Furukubo-Tokunaga K. Distinctive neuronal networks and biochemical pathways for appetitive and aversive memory in Drosophila larvae.J. Neurosci. 2009; 29: 852-862Crossref PubMed Scopus (85) Google Scholar, 5Schwaerzel M. Monastirioti M. Scholz H. Friggi-Grelin F. Birman S. Heisenberg M. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila.J. Neurosci. 2003; 23: 10495-10502Crossref PubMed Google Scholar, 6Unoki S. Matsumoto Y. Mizunami M. Participation of octopaminergic reward system and dopaminergic punishment system in insect olfactory learning revealed by pharmacological study.Eur. J. Neurosci. 2005; 22: 1409-1416Crossref PubMed Scopus (173) Google Scholar, 7Unoki S. Matsumoto Y. Mizunami M. Roles of octopaminergic and dopaminergic neurons in mediating reward and punishment signals in insect visual learning.Eur. J. Neurosci. 2006; 24: 2031-2038Crossref PubMed Scopus (119) Google Scholar], learned avoidances of odors paired with bad-tasting toxins are mediated by dopamine. Our experiments are the first to identify a second, postingestive pathway for learned olfactory aversions that involves serotonin. This second pathway may represent an ancient mechanism for food aversion learning conserved across animal lineages.