Early Integration of Temperature and Humidity Stimuli in the Drosophila Brain

Abstract

Summary The Drosophila antenna contains receptor neurons for mechanical, olfactory, thermal and humidity stimuli. Neurons expressing the ionotropic receptor IR40a have been implicated in the selection of an appropriate humidity range [1, 2], but while previous work indicates that insect hygroreceptors may be made up by a ‘triad’ of neurons (with a dry- a cold- and a humid-air responding cell [3]), IR40a expression included only cold- and dry-air cells. Here, we report the identification of the humid-responding neuron that completes the hygrosensory triad in the Drosophila antenna. This cell type expresses the Ir68a gene, and Ir68a mutation perturbs humidity preference. Next, we follow the projections of Ir68a neurons to the brain, and show that they form a distinct glomerulus in the posterior antennal lobe (PAL). In the PAL, a simple sensory map represents related features of the external environment with adjacent ‘hot’, ‘cold’, ‘dry’, and ‘humid’ glomeruli -an organization that allows for both unique and combinatorial sampling by central relay neurons. Indeed, flies avoided dry heat more robustly than humid heat, and this modulation was abolished by silencing dry-air receptors. Consistently, at least one projection neuron type received direct synaptic input from both temperature and dry air glomeruli. Our results further our understanding of humidity sensing in the Drosophila antenna, uncover a neuronal substrate for early sensory integration of temperature and humidity in the brain, and illustrate the logic of how ethologically relevant combinations of sensory cues can be processed together to produce adaptive behavioral responses

Connectomics analysis reveals first, second, and third order thermosensory and hygrosensory neurons in the adultDrosophilabrain

“…Fast-adapting thermosensory PNs take the lateral antennal lobe tract (lALT) to target the posterior lateral protocerebrum (PLP) and posterior slope (PS) [29,30]. One PN innervating several VP glomeruli takes the medial antennal lobe tract (mALT) to the PLP [23]. These studies indicate that thermo-and hygrosensory pathways project to multiple brain regions and suggest that these inputs are integrated at the level of the antennal lobe PNs.…”

“…In particular, Chamber I contains 5 -7 poreless basiconic sensilla, each housing two or three sensory neurons, and Chamber II contains 9 -10 poreless coeloconic sensilla, each housing three sensory neurons [19]. Consistent with sensilla morphology, dry-responsive neurons have been identified in chambers I and II [20,21] and humidresponsive neurons in Chamber II [22,23].…”

“…At the molecular level, in the arista, heating-activated neurons detect temperature via the gustatory receptor isoform Gr28b.d [24] and cooling-activated neurons via the ionotropic receptor Ir21a, which requires co-receptors Ir25a and Ir93a [17]. Ionotropic receptors are also expressed in the sacculus, with Ir40a mediating dry sensation [20][21][22] and Ir68a humid sensation [22,23], in both cases with Ir25a and Ir93a [20][21][22], suggesting widespread dependence on ionotropic receptor signalling.…”

“…In particular, Chamber I contains 5 -7 poreless basiconic sensilla, each housing two or three sensory neurons, and Chamber II contains 9 -10 poreless coeloconic sensilla, each housing three sensory neurons [19]. Consistent with sensilla morphology, dry-responsive neurons have been identified in chambers I and II [20,21] and humidresponsive neurons in Chamber II [22,23].At the molecular level, in the arista, heating-activated neurons detect temperature via the gustatory receptor isoform Gr28b.d [24] and cooling-activated neurons via the ionotropic receptor Ir21a, which requires co-receptors Ir25a and Ir93a [17]. Ionotropic receptors are also expressed in the sacculus, with Ir40a mediating dry sensation [20][21][22] and Ir68a humid sensation [22,23], in both cases with Ir25a and Ir93a [20][21][22], suggesting widespread dependence on ionotropic receptor signalling.At the circuit level, the funicular thermosensory and hygrosensory neurons primarily innervate ventroposterior (VP) antennal lobe glomeruli.…”

“…Aristal thermosensory neuron axons arborise unilaterally in either VP2 (warming) or VP3 (cooling) [16,25]. The saccular Ir40aexpressing, dry air-responsive neurons innervate VP4 (the "arm") [20,21,26], in both antennal lobes, and Ir68a-expressing, humid air-responsive neurons project ipsilaterally to VP5 [22,23]. In addition, putative thermosensors in Chamber II, which also express Ir40a, project to VP1 (the "column") [20,21,26] (Fig 1A).…”