Somatotopic organization among parallel sensory pathways that promote a grooming sequence inDrosophila

Abstract

Mechanosensory neurons located across the body surface respond to tactile stimuli and elicit diverse behavioral responses, from relatively simple stimulus location-aimed movements to complex movement sequences. How mechanosensory neurons and their postsynaptic circuits influence such diverse behaviors remains unclear. We previously discovered that Drosophila perform a body location-prioritized grooming sequence when mechanosensory neurons at different locations on the head and body are simultaneously stimulated by dust (Hampel et al., 2017; Seeds et al., 2014). Here, we identify nearly all mechanosensory neurons on the Drosophila head that individually elicit aimed grooming of specific head locations, while collectively eliciting a whole head grooming sequence. Different tracing methods were used to reconstruct the projections of these neurons from different locations on the head to their distinct arborizations in the brain. This provides the first synaptic resolution somatotopic map of a head, and defines the parallel-projecting mechanosensory pathways that elicit head grooming.

Neuronal wiring diagram of an adult brain

“…Almost 95% of these neurons were in the neck connective, antennal nerve, and maxillary-labial nerve. Although afferents are truncated in our reconstruction, Schlegel et al (Philipp Schlegel et al 2023) along with other community members (Eichler et al 2023;H. Kim et al 2020) were able to determine the sensory organs corresponding to 5,362 of the 5,495 non-visual sensory neurons (Fig.…”

“…Neurons in Drosophila are considered to be identifiable across hemispheres and individuals (Luan et al 2006;Pfeiffer et al 2010), enabling cell type classification of all neurons in FlyWire -such classification is useful for generating testable hypotheses about circuit function from the connectome. FlyWire community members, experts in diverse regions of the fly brain, have shared 91,649 annotations of 59,548 neurons (Supplemental Information 4), including the majority of sexually-dimorphic neurons (Deutsch et al, in prep), sensory neurons (Eichler et al 2023), as well as a diversity of cell types in the optic lobes and SEZ (Fig. 2f), two brain regions not covered in the hemibrain connectome.…”

“…Our connectome advances beyond the hemibrain in ways that are not simply numerical. It encompasses the subesophageal zone (SEZ) of the central brain, important for diverse functions such as gustation and mechanosensation (see companion paper Shiu et al (Shiu et al 2023) as well as Eichler et al (Eichler et al 2023)), and containing many of the processes of neurons that descend from the brain to the ventral nerve cord to drive motor behaviors. It includes annotations for nearly all sexually-dimorphic neurons, analyzed in a companion paper (Deutsch et al in prep).…”

Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster

“…We thank Clare Pilgrim, Alex McLachlan and David Osumi-Sutherland for incorporating our predictions into Virtual Fly Brain. Researchers 18 , 50 , 65 , 74 , 76 , 90 , 114 , 202 , 208 , 209 , 210 , 211 have already utilized our preprinted results to formulate neurobiological hypotheses. The most reliable predictions align across hemispheres, exhibit cohesion within a cell type, adhere to Lacin’s law and remain consistent across datasets.…”

Editorial: Neurobiology of Drosophila: the 19th NeuroFly-2022 meeting

“…Frontiers in Physiology frontiersin.org mechanosensory neurons that control grooming of head regions establish a somatotopic brain map (Eichler et al, 2023). Neurogenetic, imaging and behavioral studies identified mushroom body neurons that decode the value rather than the specificity of an odor (Das Chakraborty et al, 2022;Villar et al, 2022), whereas Mohamed et al uncovered neurons implicated in intensity-dependent odor discrimination learning.…”