title: Neural substrate for higher-order learning in an insect: Mushroom bodies are necessary for configural discriminations.
abstract: Learning theories distinguish elemental from configural learning based on their different complexity. Although the former relies on simple and unambiguous links between the learned events, the latter deals with ambiguous discriminations in which conjunctive representations of events are learned as being different from their elements. In mammals, configural learning is mediated by brain areas that are either dispensable or partially involved in elemental learning. We studied whether the insect brain follows the same principles and addressed this question in the honey bee, the only insect in which configural learning has been demonstrated. We used a combination of conditioning protocols, disruption of neural activity, and optophysiological recording of olfactory circuits in the bee brain to determine whether mushroom bodies (MBs), brain structures that are essential for memory storage and retrieval, are equally necessary for configural and elemental olfactory learning. We show that bees with anesthetized MBs distinguish odors and learn elemental olfactory discriminations but not configural ones, such as positive and negative patterning. Inhibition of GABAergic signaling in the MB calyces, but not in the lobes, impairs patterning discrimination, thus suggesting a requirement of GABAergic feedback neurons from the lobes to the calyces for nonelemental learning. These results uncover a previously unidentified role for MBs besides memory storage and retrieval: namely, their implication in the acquisition of ambiguous discrimination problems. Thus, in insects as in mammals, specific brain regions are recruited when the ambiguity of learning tasks increases, a fact that reveals similarities in the neural processes underlying the elucidation of ambiguous tasks across species.
authors.affiliation: Research Center on Animal Cognition, Université de Toulouse, UPS, 31062 Toulouse Cedex 9, France; Research Center on Animal Cognition, CNRS, 31062 Toulouse Cedex 9, France; Groupement de Recherche 2905 "Neurosciences de la Mémoire," CNRS, France; jean-marc.devaud@univ-tlse3.fr.
authors.forename: Jean-Marc
authors.initials: JM
authors.lastname: Devaud
authors.affiliation: Research Center on Animal Cognition, Université de Toulouse, UPS, 31062 Toulouse Cedex 9, France; Research Center on Animal Cognition, CNRS, 31062 Toulouse Cedex 9, France; Groupement de Recherche 2905 "Neurosciences de la Mémoire," CNRS, France;
authors.forename: Thomas
authors.initials: T
authors.lastname: Papouin
authors.affiliation: Evolution, Genomes, Behavior and Ecology, CNRS, Université Paris-Sud, Institut de Recherche pour le Développement (UMR 9191), 91198 Gif-sur-Yvette, France;
authors.forename: Julie
authors.initials: J
authors.lastname: Carcaud
authors.affiliation: Evolution, Genomes, Behavior and Ecology, CNRS, Université Paris-Sud, Institut de Recherche pour le Développement (UMR 9191), 91198 Gif-sur-Yvette, France;
authors.forename: Jean-Christophe
authors.initials: JC
authors.lastname: Sandoz
authors.affiliation: Arbeitsgruppe Neurobiologie, Institut für Biologie, Freie Universität Berlin, 14195 Berlin, Germany.
authors.forename: Bernd
authors.initials: B
authors.lastname: Grünewald
authors.affiliation: Research Center on Animal Cognition, Université de Toulouse, UPS, 31062 Toulouse Cedex 9, France; Research Center on Animal Cognition, CNRS, 31062 Toulouse Cedex 9, France; Groupement de Recherche 2905 "Neurosciences de la Mémoire," CNRS, France;
authors.forename: Martin
authors.initials: M
authors.lastname: Giurfa
mesh_terms: D000818:Animals; D007313:Insecta / Q000502:physiology*; D007858:Learning; D024521:Mushroom Bodies / Q000187:drug effects / Q000502:physiology*; D009812:Odorants; D011343:Procaine / Q000494:pharmacology; D005680:gamma-Aminobutyric Acid / Q000378:metabolism
chemical_list: D011343:Procaine; D005680:gamma-Aminobutyric Acid
keywords: Apis mellifera; configural learning; honey bee; learning; mushroom bodies