Evidence for the cholinergic markers ChAT and vAChT in sensory cells of the developing antennal nervous system of the desert locust Schistocerca gregaria

Erica Ehrhardt,George Boyan

doi:10.1007/s10158-020-00252-4

Abstract

Sensory and motor systems in insects with hemimetabolous development must be ready to mediate adaptive behavior directly on hatching from the egg. For the desert locust S. gregaria, cholinergic transmission from antennal sensillae to olfactory or mechanosensory centers in the brain requires that choline acetyltransferase (ChAT) and the vesicular acetylcholine transporter (vAChT) already be present in sensory cells in the first instar. In this study, we used immunolabeling to demonstrate that ChAT and vAChT are both expressed in sensory cells from identifiable sensilla types in the immature antennal nervous system. We observed ChAT expression in dendrites, neurites and somata of putative basiconic-type sensillae at the first instar stage. We also detected vAChT in the sensory axons of these sensillae in a major antennal nerve tract. We then examined whether evidence for cholinergic transmission is present during embryogenesis. Immunolabeling confirms that vAChT is expressed in somata typical of campaniform sensillae, as well as in small sensory cell clusters typically associated with either a large basiconic or coeloconic sensilla, at 99% of embryogenesis. The vAChT is also expressed in the somata of these sensilla types in multiple antennal regions at 90% of embryogenesis, but not at earlier (70%) embryonic stages. Neuromodulators are known to appear late in embryogenesis in neurons of the locust central complex, and the cholinergic system of the antenna may also only reach maturity shortly before hatching.

Highlights

Acetylcholine is a ubiquitous neuromodulator with extensive roles in insect physiology and behavior (Heinrich et al 1997; Kunst et al 2011; Boppana et al 2017; Deshpande et al 2020; Showell et al 2020)
Invertebrate Neuroscience (2020) 20:19 system—choline acetyltransferase (ChAT) which catalyzes the synthesis of acetylcholine and the vesicular acetylcholine transporter which packs the transmitter into vesicles for synaptic release are present in sensory cells of the locust antenna at this first instar stage
Our results confirm the presence of the cholinergic markers choline acetyltransferase (ChAT) and the vesicular acetylcholine transporter in sensory cells of the developing antenna of the desert locust S. gregaria

Summary

Introduction

Acetylcholine is a ubiquitous neuromodulator with extensive roles in insect physiology and behavior (Heinrich et al 1997; Kunst et al 2011; Boppana et al 2017; Deshpande et al 2020; Showell et al 2020). For example, most chemosensory, olfactory, chordotonal, and auditory primary sensory neurons are cholinergic Components of cholinergic transmission including acetylcholinesterase, choline acetyltransferase, the high affinity choline transport system, and acetylcholine receptors are expressed throughout the adult CNS (see Homberg 2002 for review). In insects with a hemimetabolous mode of development, sensory and motor systems must contribute to adaptive behavior directly on hatching from the egg (Stevenson and Kutsch 1986). Cholinergic transmission in the antennal nervous system of the desert locust S. gregaria, for example, must be functional at this first instar stage for olfactory and mechanosensory information to reach regulatory centers in the brain (Gewecke 1972). Developmental data on cholinergic neurotransmission in this sensory system are lacking

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