Bee gustatory neurons encode sugar concentration as a coherent temporal pattern of spiking

Abstract

Individual peripheral gustatory neurons in insects encode stimulus category (e.g. sweet, bitter) and concentration as a tonic rate of spiking that adapts with prolonged stimulation. While individual chemosensory neurons have been shown to interact through mutual inhibition, this interaction does not affect stimulus coding by the activated neuron. Here, I report the first evidence of a coherent, temporal pattern of spiking produced by the interaction of the gustatory receptor neurons (GRNs) within sensilla present on the mouthparts of bumblebees (Bombus terrestris) that encodes information about sugar concentration. Stimulation of gustatory sensilla with sucrose concentrations >10 mM elicited bursts of spikes riding on an oscillation in voltage of ~20 Hz. The concentration response function of spiking and bursting was sugar-identity specific, and only concentrations that produced bursting in the GRNs elicited the bee’s feeding reflex. Bursting bee GRNs exhibited a low rate of adaptation (0.002 s adaptation after 1 s of stimulation) compared to rates measured from other insect species’ GRNs. These data are the first to show that primary chemosensory neurons encode stimulus features such as concentration as a coherent temporal pattern of spiking produced as an interaction between two neurons. I propose that 1) the silent period between bursts is driven by the spike after-hyperpolarization of one neuron, which inhibits spiking of its neighboring neuron through an inhibitory lateral interaction, and 2) bursting is a novel mechanism evolved to allow persistent high frequency spiking during fluid consumption. Finally, I show that neural activity can be monitored from the bee’s central nervous system, which allows future experiments to question the function of this coherent and structured GRN activity in driving post-synaptic responses.