Ionotropic Receptors Specify the Morphogenesis of Phasic Sensors Controlling Rapid Thermal Preference in Drosophila

Budelli, Gonzalo; Ni, Lina; Berciu, Cristina; Giesen, Lena van; Knecht, Zachary A.; Chang, Elaine; Kaminski, Benjamin Lucien; Silbering, Ana F.; Samuel, Aravi; Klein, Mason; Benton, Richard; Nicastro, Daniela; Garrity, Paul

doi:10.1016/j.neuron.2018.12.022

Cited by 95 publications

(140 citation statements)

References 47 publications

Supporting

Mentioning

129

Contrasting

Order By: Relevance

“…S2B). These results are consistent with reports of three or four pairs of heating-responsive and cooling-responsive aristal sensory neurons that project to VP2 and VP3, respectively [16,17], and primarily non-aristal cold input to the slow-cool VP3 PN [29].…”

Section: Sensory Neurons Define Two Novel Glomeruli In the Ventropostsupporting

confidence: 92%

“…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.…”

mentioning

confidence: 87%

“…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.…”

Section: Introductionmentioning

confidence: 99%

“…In flies, the third antennal segment (funiculus) features two structures housing thermo-and hygrosensory neurons: the arista and the sacculus [14,15]. The arista is a feathery protrusion containing three (sometimes four) pairs of phasic thermosensory neurons, one transiently activated by warming and the other by cooling [16,17]. The sacculus is a multichambered invagination [18] containing several types of sensilla, some of which resemble thermosensory or hygrosensory sensilla.…”

mentioning

confidence: 99%

See 3 more Smart Citations

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

Marin

Roberts

Büld

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

HIGHLIGHTS• Two novel thermo/hygrosensory glomeruli in the fly antennal lobe • First complete set of thermosensory and hygrosensory projection neurons • First connectome for a thermosensory centre, the lateral accessory calyx • Novel third order neurons, including a link to the circadian clock SUMMARY (250):Animals exhibit innate and learned preferences for temperature and humidity -conditions critical for their survival and reproduction. Here, we leveraged a whole adult brain electron microscopy volume to study the circuitry associated with antennal thermosensory and hygrosensory neurons, which target specific ventroposterior (VP) glomeruli in the Drosophila melanogaster antennal lobe. We have identified two new VP glomeruli, in addition to the five known ones, and the projection neurons (VP PNs) that relay VP information to higher brain centres, including the mushroom body and lateral horn, seats of learned and innate olfactory behaviours, respectively. Focussing on the mushroom body lateral accessory calyx (lACA), a known thermosensory neuropil, we present a comprehensive connectome by reconstructing neurons downstream of heating-and coolingresponsive VP PNs. We find that a few lACA-associated mushroom body intrinsic neurons (Kenyon cells) solely receive thermosensory inputs, while most receive additional olfactory and thermo-or hygrosensory PN inputs in the main calyx. Unexpectedly, we find several classes of lACA-associated neurons that form a local network with outputs to other brain neuropils, suggesting that the lACA serves as a general hub for thermosensory circuitry. For example, we find DN1 pacemaker neurons that link the lACA to the accessory medulla, likely mediating temperature-based entrainment of the circadian clock. Finally, we survey strongly connected downstream partners of VP PNs across the protocerebrum; these include a descending neuron that receives input mainly from dry-responsive VP PNs, meaning that just two synapses might separate hygrosensory inputs from motor neurons in the nerve cord. (249) KEYWORDSThermosensation, hygrosensation, connectomics, antennal lobe, projection neuron, lateral accessory calyx, circadian clock Temperature and humidity are two interrelated environmental variables with dramatic effects on animal physiology and survival. Animals exhibit intrinsic species-specific preferences for the temperature and humidity levels compatible with their survival and reproduction [1]. However, these preferences can be modulated by state and experience; vinegar flies prefer higher levels of relative humidity when dehydrated [2], and nematodes starved at low humidity subsequently prefer higher humidities, and vice versa [3]. Temperature and/or humidity also cue essential behavioural programmes; for example, female mosquitoes use heat and humidity to locate warmblooded hosts for blood feeding [4,5], and temperature entrains the circadian clock in organisms from molds to mammals to drive daily rhythms of physiology and behaviour [6,7]. Whilst fundamental for survival, the neuronal mec...

show abstract

Section: Sensory Neurons Define Two Novel Glomeruli In the Ventropostsupporting

confidence: 92%

mentioning

confidence: 87%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

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

Marin

Roberts

Büld

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…In addition to members of the IR family, an OBP, OBP59a, has also been implicated in humidity sensing (Sun et al, 2018). IR93a and IR25a, along with IR21a, also mediate temperature sensation and are expressed in thermosensory neurons in the arista (Enjin et al, 2016;Budelli et al, 2019). In addition, a member of the GR family, GR28b, has been identified as a peripheral thermosensor that responds to rapid warming (Ni et al, 2013).…”

Section: Box 1 Organization Of Olfactory Sensory Neurons In Drosophimentioning

confidence: 99%

Chemosensation and Evolution of Drosophila Host Plant Selection

Anholt

2020

iScience

View full text Add to dashboard Cite

Neuronal Compartmentalization: A Means to Integrate Sensory Input at the Earliest Stage of Information Processing?

2020

BioEssays

View full text Add to dashboard Cite

In numerous peripheral sense organs, external stimuli are detected by primary sensory neurons compartmentalized within specialized structures composed of cuticular or epithelial tissue. Beyond reflecting developmental constraints, such compartmentalization also provides opportunities for grouped neurons to functionally interact. Here, the authors review and illustrate the prevalence of these structural units, describe characteristics of compartmentalized neurons, and consider possible interactions between these cells. This article discusses instances of neuronal crosstalk, examples of which are observed in the vertebrate tastebuds and multiple types of arthropod chemosensory hairs. Particular attention is paid to insect olfaction, which presents especially well‐characterized mechanisms of functional, cross‐neuronal interactions. These examples highlight the potential impact of peripheral processing, which likely contributes more to signal integration than previously considered. In surveying a wide variety of structural units, it is hoped that this article will stimulate future research that determines whether grouped neurons in other sensory systems can also communicate to impact information processing.

show abstract

Ionotropic Receptors Specify the Morphogenesis of Phasic Sensors Controlling Rapid Thermal Preference in Drosophila

Cited by 95 publications

References 47 publications

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

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

Chemosensation and Evolution of Drosophila Host Plant Selection

Neuronal Compartmentalization: A Means to Integrate Sensory Input at the Earliest Stage of Information Processing?

Contact Info

Product

Resources

About