Focal uncaging of GABA reveals a temporally defined role for GABAergic inhibition during appetitive associative olfactory conditioning in honeybees

  1. Uli Mueller1,3
  1. 1Department 8.3 Biosciences Zoology/Physiology–Neurobiology, ZHMB (Center of Human and Molecular Biology), Faculty 8–Natural Science and Technology III, Saarland University, D-66041 Saarbrücken, Germany
    • 2 Present address: Department of Cellular & Molecular Physiology, Yale School of Medicine, New Haven, Connecticut 06520, USA

    Abstract

    Throughout the animal kingdom, the inhibitory neurotransmitter γ-aminobutyric acid (GABA) is a key modulator of physiological processes including learning. With respect to associative learning, the exact time in which GABA interferes with the molecular events of learning has not yet been clearly defined. To address this issue, we used two different approaches to activate GABA receptors during appetitive olfactory conditioning in the honeybee. Injection of GABA-A receptor agonist muscimol 20 min before but not 20 min after associative conditioning affects memory performance. These memory deficits were attenuated by additional training sessions. Muscimol has no effect on sensory perception, odor generalization, and nonassociative learning, indicating a specific role of GABA during associative conditioning. We used photolytic uncaging of GABA to identify the GABA-sensitive time window during the short pairing of the conditioned stimulus (CS) and the unconditioned stimulus (US) that lasts only seconds. Either uncaging of GABA in the antennal lobes or the mushroom bodies during the CS presentation of the CS–US pairing impairs memory formation, while uncaging GABA during the US phase has no effect on memory. Uncaging GABA during the CS presentation in memory retrieval also has no effect. Thus, in honeybee appetitive olfactory learning GABA specifically interferes with the integration of CS and US during associative conditioning and exerts a modulatory role in memory formation depending on the training strength.

    Footnotes

    • 3 Corresponding author

      E-mail uli.mueller{at}mx.uni-saarland.de

    • Received December 22, 2012.
    • Accepted May 14, 2013.

    This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first 12 months after the full-issue publication date (see http://learnmem.cshlp.org/site/misc/terms.xhtml). After 12 months, it is available under a Creative Commons License (Attribution-NonCommercial 3.0 Unported), as described at http://creativecommons.org/licenses/by-nc/3.0/.

    | Table of Contents