Connectomics Analysis Reveals First-, Second-, and Third-Order Thermosensory and Hygrosensory Neurons in the Adult Drosophila Brain

Elizabeth C Marin,Laurin Büld,Maria Theiss,Tatevik Sarkissian,Ruairí J.V Roberts,Robert Turnbull,Imaan F.M Tamimi,Markus W Pleijzier,Willem J Laursen,Nik Drummond,Philipp Schlegel,Alexander S Bates,Feng Li,Matthias Landgraf,Marta Costa,Davi D Bock,Paul A Garrity,Gregory S.X.E Jefferis

doi:10.1016/j.cub.2020.06.028

Abstract

SummaryAnimals exhibit innate and learned preferences for temperature and humidity—conditions critical for their survival and reproduction. Leveraging a whole-brain electron microscopy volume, we studied the adult Drosophila melanogaster circuitry associated with antennal thermo- and hygrosensory neurons. We have identified two new target glomeruli in the antennal lobe, in addition to the five known ones, and the ventroposterior projection neurons (VP PNs) that relay thermo- and hygrosensory information to higher brain centers, including the mushroom body and lateral horn, seats of learned and innate behavior. We present the first connectome of a thermo- and hygrosensory neuropil, the lateral accessory calyx (lACA), by reconstructing neurons downstream of heating- and cooling-responsive VP PNs. A few mushroom body-intrinsic neurons solely receive thermosensory input from the lACA, while most receive additional olfactory and thermo- and/or hygrosensory PN inputs. Furthermore, several classes of lACA-associated neurons form a local network with outputs to other brain neuropils, suggesting that the lACA serves as a hub for thermo- and hygrosensory circuitry. For example, DN1a neurons link thermosensory PNs in the lACA to the circadian clock via the accessory medulla. Finally, we survey strongly connected downstream partners of VP PNs across the protocerebrum; these include a descending neuron targeted by dry-responsive VP PNs, meaning that just two synapses might separate hygrosensory inputs from motor circuits. These data provide a comprehensive first- and second-order layer analysis of Drosophila thermo- and hygrosensory systems and an initial survey of third-order neurons that could directly modulate behavior.

Highlights

Temperature and humidity are interrelated environmental variables with dramatic effects on animal physiology and survival
Morphological clustering with NBLAST [31] paired the simpler VP3 receptor neurons (RNs) on each side with one another, within the larger VP3 RN group (Figure S2A), implying that they are of the same type and distinct from the complex VP3 RNs
The simpler VP3 RN provided most of the input to the righthand side (RHS) slow-cool VP3 Projection neurons (PNs), whereas the others targeted distinct VP3 PNs (Figure S2B)

Summary

Introduction

Temperature and humidity are interrelated environmental variables with dramatic effects on animal physiology and survival. Hygro- and thermosensory neurons have been found on the antennae of diverse species, with individual sensilla often containing pairs of cooling- and heating-responsive neurons or triads of cold-, dry-, and humid-responsive neurons [8]. These neurons (like olfactory sensory neurons) project from the antennae to the antennal lobe (AL) in the brain, where they innervate stereotyped glomerular subcompartments [9]. Projection neurons (PNs) relay information from these glomeruli to higher brain regions including the mushroom body calyx (CA) and lateral horn (LH) of the protocerebrum [10], respectively involved in learned and innate olfactory behaviors [11]

Methods

Results

Discussion

Conclusion