Distinct subpopulations of mechanosensory chordotonal organ neurons elicit grooming of the fruit fly antennae

Abstract

Diverse mechanosensory neurons detect different mechanical forces that can impact animal behavior. Yet our understanding of the anatomical and physiological diversity of these neurons and the behaviors that they influence is limited. We previously discovered that grooming of the Drosophila melanogaster antennae is elicited by an antennal mechanosensory chordotonal organ, the Johnston's organ (JO) (Hampel et al., 2015). Here, we describe anatomically and physiologically distinct JO mechanosensory neuron subpopulations that each elicit antennal grooming. We show that the subpopulations project to different, discrete zones in the brain and differ in their responses to mechanical stimulation of the antennae. Although activation of each subpopulation elicits antennal grooming, distinct subpopulations also elicit the additional behaviors of wing flapping or backward locomotion. Our results provide a comprehensive description of the diversity of mechanosensory neurons in the JO, and reveal that distinct JO subpopulations can elicit both common and distinct behavioral responses.

Descending neurons coordinate anterior grooming behavior in Drosophila

“…JOs detect diverse types of mechanical forces and send their projections into discrete zones in the AMMC. 30 EM reconstruction showed that the majority of JOs that connect to JO-in belong to the JO-E subtype, which are thought to detect static deflection of the antenna. 31,32 Since the JO-E neurons were previously shown to connect directly or indirectly to aDNs and their activation induces antennal grooming 14,23 (Figure S4B), we were puzzled to find them upstream of the DNg11 neurons that induce the competing behavior of front leg rubbing.…”

Drosophila gustatory projections are segregated by taste modality and connectivity

“…GRNs from the proboscis labellum send axons through the labial nerve to the SEZ (Figure 1A). The labial nerve is a compound nerve, carrying sensory axons from the labellum, maxillary palp, and eye, as well as motor axons innervating proboscis musculature (Hampel et al 2020, Hartenstein et al 2018, Miyazaki & Ito 2010, Nayak & Singh 1983, Rajashekhar & Singh 1994). Different sensory afferents occupy different domains in the SEZ, with labellar gustatory axons terminating in the anterior central sensory center (ACSC) (Hartenstein et al 2018, Miyazaki & Ito 2010, Thorne et al 2004, Wang et al 2004).…”

“…In the adult olfactory system, approximately 40% of the input onto olfactory receptor neurons (ORNs) comes from other ORNs projecting to the same olfactory glomerulus (Horne et al 2018, Schlegel et al 2021, Tobin et al 2017). Similarly, mechanosensory projections from the Johnston’s Organ of the same submodality are anatomically segregated and synaptically connected (Hampel et al 2020). In Drosophila larvae, 25% of gustatory neuron inputs are from other GRNs, although functional classes were not resolved (Miroschnikow et al 2018).…”

“…To identify second order neurons, random presynapses of skeleton 7349219 were chosen using the reconstruction sampler function of CATMAID and downstream partners were reconstructed. Skeletons were traced to completion either entirely manually or using a combination of an automated segmentation (Li et al 2020b) and manual tracing as previously described (Hampel et al 2020). Chemical synapses were annotated manually using criteria previously described (Zheng et al 2018).…”

“…GRN projections were identified based on their extension into the labial nerve and localization to characteristic neural tracts in the SEZ. Skeletons were traced to completion either entirely manually or using a combination of an automated segmentation (Li et al 2020b) and manual tracing as previously described (Hampel et al 2020). Chemical synapses were annotated manually and neurons were traced to synaptic completion, using criteria previously described (Zheng et al 2018).…”