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Burst Firing in Bee Gustatory Neurons Prevents Adaptation

Lookup NU author(s): Dr Ashwin Miriyala, Sebastien Kessler, Dr Claire Rind, Professor Geraldine Wright

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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License (CC BY-NC 4.0).


Abstract

© 2018 Elsevier Ltd Animals detect changes in the environment using modality-specific, peripheral sensory neurons. The insect gustatory system encodes tastant identity and concentration through the independent firing of gustatory receptor neurons (GRNs) that spike rapidly at stimulus onset and quickly adapt. Here, we show the first evidence that concentrated sugar evokes a temporally structured burst pattern of spiking involving two GRNs within the gustatory sensilla of bumblebees. Bursts of spikes resulted when a sucrose-activated GRN was inhibited by another GRN at a frequency of ∼22 Hz during the first 1 s of stimulation. Pharmacological blockade of gap junctions abolished bursting, indicating that bee GRNs have electrical synapses that produce a temporal pattern of spikes when one GRN is activated by a sugar ligand. Bursting permitted bee GRNs to maintain a high rate of spiking and to exhibit the slowest rate of adaptation of any insect species. Feeding bout duration correlated with coherent bursting; only sugar concentrations that produced bursting evoked the bumblebee's feeding reflex. Volume of solution imbibed was a direct function of time in contact with food. We propose that gap junctions among GRNs enable a sustained rate of GRN spiking that is necessary to drive continuous feeding by the bee proboscis. Miriyala et al. discover that galeal sensilla on the bumblebee's proboscis (mouthparts) have two gustatory receptor neurons (GRNs) that exhibit bursts of spikes in response to stimulation with sucrose. Bursting in these neurons depends on sugar value, is facilitated by gap junctions, and permits these neurons to resist sensory adaptation.


Publication metadata

Author(s): Miriyala A, Kessler S, Rind FC, Wright GA

Publication type: Article

Publication status: Published

Journal: Current Biology

Year: 2018

Volume: 28

Issue: 10

Pages: 1585-1594.e3

Print publication date: 21/05/2018

Online publication date: 10/05/2018

Acceptance date: 29/03/2018

Date deposited: 27/03/2018

ISSN (print): 0960-9822

ISSN (electronic): 1879-0445

Publisher: Cell Press

URL: https://doi.org/10.1016/j.cub.2018.03.070

DOI: 10.1016/j.cub.2018.03.070


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