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Effect of GABAergic inhibition on odorant concentration coding in mushroom body intrinsic neurons of the honeybee

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Abstract

Kenyon cells, the intrinsic neurons of the insect mushroom body, have the intriguing property of responding in a sparse way to odorants. Sparse neuronal codes are often invariant to changes in stimulus intensity and duration, and sparse coding often depends on global inhibition. We tested if this is the case for honeybees’ Kenyon cells, too, and used in vivo Ca2+ imaging to record their responses to different odorant concentrations. Kenyon cells responded not only to the onset of odorant stimuli (ON responses), but also to their termination (OFF responses). Both, ON and OFF responses increased with increasing odorant concentration. ON responses were phasic and invariant to the duration of odorant stimuli, while OFF responses increased with increasing odorant duration. Pharmacological blocking of GABA receptors in the brain revealed that ionotropic GABAA and metabotropic GABAB receptors attenuate Kenyon cells’ ON responses without changing their OFF responses. Ionotropic GABAA receptors attenuated Kenyon cell ON responses more strongly than metabotropic GABAB receptors. However, the response dynamic, temporal resolution and paired-pulse depression did not depend on GABAA transmission. These data are discussed in the context of mechanisms leading to sparse coding in Kenyon cells.

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Abbreviations

GABA:

γ-Aminobutyric acid

cKC:

Clawed Kenyon cell

MB:

Mushroom body

PCT:

Protocerebral-calycal tract

BMI:

Bicuculline methiodide

PTX:

Picrotoxin

CGP:

CGP54626

ROI:

Region of interest

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Acknowledgments

We are grateful to Drs. Silke Sachse, Melanie Haehnel and Nobuhiro Yamagata for their help and advice during the experiments. The work was supported by a grant of the Deutsche Forschungsgemeinschaft (Me 365/31-1).

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Authors and Affiliations

  1. Institut für Neurobiologie, Freie Universität Berlin, Königin Luise-Str. 28/30, 14195, Berlin, Germany

    Anja Froese & Randolf Menzel

  2. Department of Biology, Neurobiology, University of Konstanz, Universitätsstraße 10, 78457, Constance, Germany

    Paul Szyszka

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  1. Anja Froese
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  2. Paul Szyszka
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  3. Randolf Menzel
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Correspondence to Randolf Menzel.

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Froese, A., Szyszka, P. & Menzel, R. Effect of GABAergic inhibition on odorant concentration coding in mushroom body intrinsic neurons of the honeybee. J Comp Physiol A 200, 183–195 (2014). https://doi.org/10.1007/s00359-013-0877-8

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  • DOI: https://doi.org/10.1007/s00359-013-0877-8

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