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Cellular physiology of olfactory learning in the honeybee brain

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Abstract

The honeybee (Apis mellifera) is a model organism for the study of learning and memory formation and its underlying cellular mechanisms. The neuronal and molecular bases of olfactory associative learning have been intensively studied using the proboscis extension reflex. The neuronal pathway of the associative olfactory learning includes two main neuropils: the antennal lobes (AL) and the mushroom bodies (MB). Here, the excitatory olfactory and octopaminergic reward pathway converge together onto the AL neurons and MB intrinsic Kenyon cells (KCs). For learning-related neural plasticity to occur, the coincidence between the conditioned stimulus (CS) and the reward has to be reliably detected. Therefore, this review focusses on (1) the excitatory ionotropic nicotinic acetylcholine receptor (nAChR) and (2) the metabotropic octopamine receptor (OAR) which are located on the cell membrane in AL neurons as well as in KCs. For plasticity-dependent cellular mechanisms, we discuss the role of inhibition provided by GABAergic local interneurons in the ALs and feedback neurons in the MBs, as well as glutamatergic neurons in both neuropils. In our working model, we postulate two possible coincidence detector systems which may modulate further incoming olfactory stimuli: (1) an elevated intracellular Ca2+ concentration induced by the activation of the nAChR and OAR may result in the activation of Ca2+-dependent kinases. (2) Activation of a cAMP-dependent PKA may lead to phosphorylation of the nAChR and hence to learning-related intracellular changes.

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Acknowledgments

The authors thank Dr. Wolfgang Blenau for fruitful comments on the manuscript. The work was supported by the Stiftung Polytechnische Gesellschaft, Frankfurt am Main (scholarship to S.H.).

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  1. Institut für Bienenkunde, Polytechnische Gesellschaft, Frankfurt am Main; Fachbereich Biowissenschaften, Goethe-Universität Frankfurt am Main, Karl von Frisch Weg 2, 61440, Oberursel, Germany

    Sophie Himmelreich & Bernd Grünewald

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  1. Sophie Himmelreich
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Correspondence to Sophie Himmelreich.

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Manuscript editor: Yves Le Conte

Physiologie cellulaire de l’apprentissage olfactif dans le cerveau de l’abeille.

Apis mellifera / détection en coïncidence / récepteur acétylcholine / récepteur octopamine / lobe antennaire / corps pédonculé

Zellphysiologie des olfaktorischen Lernens der Honigbiene.

Apis mellifera / Koinzidenz-Detektion / Acetylcholinrezeptor / Oktopaminrezeptor / Antennallobus / Pilzkörper

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Himmelreich, S., Grünewald, B. Cellular physiology of olfactory learning in the honeybee brain. Apidologie 43, 308–321 (2012). https://doi.org/10.1007/s13592-012-0135-z

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