Honeybee Kenyon cells are regulated by a tonic GABA receptor conductance

Mary J. Palmer (Lead / Corresponding author), Jenni Harvey

    Research output: Contribution to journalArticle

    4 Citations (Scopus)

    Abstract

    The higher cognitive functions of insects are dependent on their mushroom bodies (MBs), which are particularly large in social insects such as honeybees. MB Kenyon cells (KCs) receive multisensory input and are involved in associative learning and memory. In addition to receiving sensory input via excitatory nicotinic synapses, KCs receive inhibitory GABAergic input from MB feedback neurons. Cultured honeybee KCs exhibit ionotropic GABA receptor currents but the properties of GABA-mediated inhibition in intact MBs are currently unknown. Here, using whole-cell recordings from KCs in acutely-isolated honeybee brain, we show that KCs exhibit a tonic current that is inhibited by picrotoxin but not by bicuculline. Bath application of GABA (5 µM) and taurine (1 mM) activate a tonic current in KCs, but L-glutamate (0.1-0.5 mM) has no effect. The tonic current is strongly potentiated by the allosteric GABAA receptor modulator pentobarbital, and is reduced by inhibition of Ca(2+) channels with Cd(2+) or nifedipine. Noise analysis of the GABA-evoked current gives a single-channel conductance value for the underlying receptors of 27 ± 3 pS, similar to that of RDL receptors. The amount of injected current required to evoke action potential firing in KCs is significantly lower in the presence of picrotoxin. KCs recorded in an intact honeybee head preparation similarly exhibit a tonic GABA receptor conductance that reduces neuronal excitability, a property that is likely to contribute to the sparse coding of sensory information in insect MBs.
    Original languageEnglish
    Pages (from-to)2026-2035
    Number of pages10
    JournalJournal of Neurophysiology
    Volume112
    Issue number8
    DOIs
    Publication statusPublished - 15 Oct 2014

    Fingerprint

    GABA Receptors
    Mushroom Bodies
    gamma-Aminobutyric Acid
    Insects
    Picrotoxin
    Bicuculline
    Taurine
    Patch-Clamp Techniques
    Pentobarbital
    GABA-A Receptors
    Nifedipine
    Baths
    Synapses
    Cognition
    Action Potentials
    Noise
    Glutamic Acid
    Head
    Learning
    Neurons

    Cite this

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    title = "Honeybee Kenyon cells are regulated by a tonic GABA receptor conductance",
    abstract = "The higher cognitive functions of insects are dependent on their mushroom bodies (MBs), which are particularly large in social insects such as honeybees. MB Kenyon cells (KCs) receive multisensory input and are involved in associative learning and memory. In addition to receiving sensory input via excitatory nicotinic synapses, KCs receive inhibitory GABAergic input from MB feedback neurons. Cultured honeybee KCs exhibit ionotropic GABA receptor currents but the properties of GABA-mediated inhibition in intact MBs are currently unknown. Here, using whole-cell recordings from KCs in acutely-isolated honeybee brain, we show that KCs exhibit a tonic current that is inhibited by picrotoxin but not by bicuculline. Bath application of GABA (5 µM) and taurine (1 mM) activate a tonic current in KCs, but L-glutamate (0.1-0.5 mM) has no effect. The tonic current is strongly potentiated by the allosteric GABAA receptor modulator pentobarbital, and is reduced by inhibition of Ca(2+) channels with Cd(2+) or nifedipine. Noise analysis of the GABA-evoked current gives a single-channel conductance value for the underlying receptors of 27 ± 3 pS, similar to that of RDL receptors. The amount of injected current required to evoke action potential firing in KCs is significantly lower in the presence of picrotoxin. KCs recorded in an intact honeybee head preparation similarly exhibit a tonic GABA receptor conductance that reduces neuronal excitability, a property that is likely to contribute to the sparse coding of sensory information in insect MBs.",
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    Honeybee Kenyon cells are regulated by a tonic GABA receptor conductance. / Palmer, Mary J. (Lead / Corresponding author); Harvey, Jenni.

    In: Journal of Neurophysiology, Vol. 112, No. 8, 15.10.2014, p. 2026-2035.

    Research output: Contribution to journalArticle

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    T1 - Honeybee Kenyon cells are regulated by a tonic GABA receptor conductance

    AU - Palmer, Mary J.

    AU - Harvey, Jenni

    N1 - Copyright © 2014, Journal of Neurophysiology.

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    N2 - The higher cognitive functions of insects are dependent on their mushroom bodies (MBs), which are particularly large in social insects such as honeybees. MB Kenyon cells (KCs) receive multisensory input and are involved in associative learning and memory. In addition to receiving sensory input via excitatory nicotinic synapses, KCs receive inhibitory GABAergic input from MB feedback neurons. Cultured honeybee KCs exhibit ionotropic GABA receptor currents but the properties of GABA-mediated inhibition in intact MBs are currently unknown. Here, using whole-cell recordings from KCs in acutely-isolated honeybee brain, we show that KCs exhibit a tonic current that is inhibited by picrotoxin but not by bicuculline. Bath application of GABA (5 µM) and taurine (1 mM) activate a tonic current in KCs, but L-glutamate (0.1-0.5 mM) has no effect. The tonic current is strongly potentiated by the allosteric GABAA receptor modulator pentobarbital, and is reduced by inhibition of Ca(2+) channels with Cd(2+) or nifedipine. Noise analysis of the GABA-evoked current gives a single-channel conductance value for the underlying receptors of 27 ± 3 pS, similar to that of RDL receptors. The amount of injected current required to evoke action potential firing in KCs is significantly lower in the presence of picrotoxin. KCs recorded in an intact honeybee head preparation similarly exhibit a tonic GABA receptor conductance that reduces neuronal excitability, a property that is likely to contribute to the sparse coding of sensory information in insect MBs.

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