Classification and genetic targeting of cell types in the primary taste and premotor center of the adult Drosophila brain.

Gabriella R Sterne,Kristin Scott,Barry J Dickson,Hideo Otsuna

doi:10.7554/elife.71679

Abstract

Neural circuits carry out complex computations that allow animals to evaluate food, select mates, move toward attractive stimuli, and move away from threats. In insects, the subesophageal zone (SEZ) is a brain region that receives gustatory, pheromonal, and mechanosensory inputs and contributes to the control of diverse behaviors, including feeding, grooming, and locomotion. Despite its importance in sensorimotor transformations, the study of SEZ circuits has been hindered by limited knowledge of the underlying diversity of SEZ neurons. Here, we generate a collection of split-GAL4 lines that provides precise genetic targeting of 138 different SEZ cell types in adult Drosophila melanogaster, comprising approximately one third of all SEZ neurons. We characterize the single-cell anatomy of these neurons and find that they cluster by morphology into six supergroups that organize the SEZ into discrete anatomical domains. We find that the majority of local SEZ interneurons are not classically polarized, suggesting rich local processing, whereas SEZ projection neurons tend to be classically polarized, conveying information to a limited number of higher brain regions. This study provides insight into the anatomical organization of the SEZ and generates resources that will facilitate further study of SEZ neurons and their contributions to sensory processing and behavior.

Highlights

Elucidating the neural architecture that underlies sensorimotor transformations for behavior requires the ability to resolve and manipulate neural circuits with single-c ell precision
The subesophageal zone (SEZ) contains four neuropil subregions: the gnathal ganglia (GNG), saddle (SAD), prow (PRW), and antennal mechanosensory and motor center (AMMC; Figure 1A and B; Ito et al, 2014). These SEZ subregions are composed of cells from the tritocerebral, mandibular, maxillary, and labial neuromeres, which are genetically defined by the expression of known homeobox-containing, neuromere-specific genes
To supplement our annotation of the presence of axons, dendrites, or both in each neuropil compartment and polarization strategy, we indicated whether each cell type is an interneuron, projection neuron, descending interneuron (DN), or sensory neuron (Figure 10, left)

Summary

Introduction

Elucidating the neural architecture that underlies sensorimotor transformations for behavior requires the ability to resolve and manipulate neural circuits with single-c ell precision. In Drosophila and other insects, the SEZ participates in many context-dependent motor actions, including feeding, grooming, and locomotion, with evidence suggesting that it is involved in action selection (Bidaye et al, 2020; Flood et al, 2013; Gordon and Scott, 2009; Hampel et al, 2017; Hampel et al, 2015; Mann et al, 2013; Manzo et al, 2012; Marella et al, 2006; Tastekin et al, 2015; Wang et al, 2004) It receives direct sensory input from axonal arbors of gustatory and mechanosensory peripheral neurons and indirect input

Methods

Results

Conclusion