A tyrosine-hydroxylase characterization of dopaminergic neurons in the honey bee brain

Stevanus R. Tedjakumala, Jacques Rouquette, Marie Laure Boizeau, Karen A. Mesce, Lucie Hotier, Isabelle Massou, Martin Giurfa

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Abstract

Dopamine (DA) plays a fundamental role in insect behavior as it acts both as a general modulator of behavior and as a value system in associative learning where it mediates the reinforcing properties of unconditioned stimuli (US). Here we aimed at characterizing the dopaminergic neurons in the central nervous system of the honey bee, an insect that serves as an established model for the study of learning and memory. We used tyrosine hydroxylase (TH) immunoreactivity (ir) to ensure that the neurons detected synthesize DA endogenously. We found three main dopaminergic clusters, C1–C3, which had been previously described; the C1 cluster is located in a small region adjacent to the esophagus (ES) and the antennal lobe (AL); the C2 cluster is situated above the C1 cluster, between the AL and the vertical lobe (VL) of the mushroom body (MB); the C3 cluster is located below the calyces (CA) of the MB. In addition, we found a novel dopaminergic cluster, C4, located above the dorsomedial border of the lobula, which innervates the visual neuropils of the bee brain. Additional smaller processes and clusters were found and are described. The profuse dopaminergic innervation of the entire bee brain and the specific connectivity of DA neurons, with visual, olfactory and gustatory circuits, provide a foundation for a deeper understanding of how these sensory modules are modulated by DA, and the DA-dependent value-based associations that occur during associative learning.

Original languageEnglish (US)
Article number47
JournalFrontiers in Systems Neuroscience
Volume11
DOIs
StatePublished - Jul 10 2017

Bibliographical note

Funding Information:
Thanks are due to three anonymous reviewers for comments and suggestions, and to Hiromu Tanimoto and Axel Borst (Max Planck Institute of Neurobiology, Munich) for institutional support to SRT. Manon Marque provided help for some experiments. This work was possible thanks to the support received by MG from the French National Research Agency (ANR, award no. MINICOG), the Human Frontier Science Program (HFSP, award no. RGP0022), the Institut Universitaire de France (IUF), the Centre National de la Recherche Scientifique (CNRS) and the University of Toulouse. KAM thanks the University of Minnesota Agricultural Experiment Station for support. SRT was supported by the Bayerische Forschungsstiftung. A prior version of this article was included as a chapter in the PhD Thesis of SRT, which granted him the title of Dr. of the University of Toulouse. This thesis is accessible online (http://thesesups.ups-tlse.fr/2529/) and is the only medium in which this prior version has appeared (Tedjakumala, 2014).

Publisher Copyright:
© 2017 Tedjakumala, Rouquette, Boizeau, Mesce, Hotier, Massou and Giurfa.

Keywords

  • Apis mellifera
  • Dopamine
  • Dopaminergic signaling
  • Neural circuits
  • Neural clusters

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