Long-range projection neurons in the taste circuit of Drosophila.

Heesoo Kim,Colleen Kirkhart,Kristin Scott

doi:10.7554/elife.23386

Abstract

Taste compounds elicit innate feeding behaviors and act as rewards or punishments to entrain other cues. The neural pathways by which taste compounds influence innate and learned behaviors have not been resolved. Here, we identify three classes of taste projection neurons (TPNs) in Drosophila melanogaster distinguished by their morphology and taste selectivity. TPNs receive input from gustatory receptor neurons and respond selectively to sweet or bitter stimuli, demonstrating segregated processing of different taste modalities. Activation of TPNs influences innate feeding behavior, whereas inhibition has little effect, suggesting parallel pathways. Moreover, two TPN classes are absolutely required for conditioned taste aversion, a learned behavior. The TPNs essential for conditioned aversion project to the superior lateral protocerebrum (SLP) and convey taste information to mushroom body learning centers. These studies identify taste pathways from sensory detection to higher brain that influence innate behavior and are essential for learned responses to taste compounds.

Highlights

The ability to detect nutrients and toxins is critical for survival
To identify novel second-order taste projection neurons (TPNs), we searched for neurons with arborizations near gustatory receptor neurons (GRNs) axons in a visual screen of more than 8000 images of Gal4 lines from existing collections (Dickson, unpublished; Gohl et al, 2011; Jenett et al, 2012)
TPN1, marked by R30A08-Gal4, has two bilaterally symmetric cell bodies in the metathoracic ganglia, contralateral dendrites in each leg ganglion, and axons that project from the ventral nerve cord (VNC) to terminate in the subesophageal zone (SEZ) (Figure 1B and Figure 1—figure supplement 1A,B)

Summary

Introduction

The ability to detect nutrients and toxins is critical for survival. In most animals, the gustatory system has evolved as a specialized sensory system to detect non-volatile chemicals in the environment. The pathways by which gustatory detection drive innate feeding behavior and learned associations have not been resolved. Fly gustatory receptor neurons (GRNs) are located on the proboscis labellum, internal mouthparts, legs, and wings (Stocker, 1994). Activation of sucroseresponsive taste neurons triggers behavioral subprograms associated with feeding, including inhibition of locomotion, extension of the fly proboscis, and ingestion (Gordon and Scott, 2009; Keene and Masek, 2012; Marella et al, 2006; Thoma et al, 2016). Activation of bitterresponsive sensory neurons triggers food rejection, including proboscis retraction (Keene and Masek, 2012; Marella et al, 2006). Taste cell activation elicits responses in mushroom body learning circuits for sensory associations (Burke et al, 2012; Kirkhart and Scott, 2015; Liu et al, 2012)

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