The Coding of Temperature in the Drosophila Brain

Gallio, Marco; Ofstad, Tyler; Macpherson, Lindsey J.; Wang, Jing W.; Zuker, Charles S.

doi:10.1016/j.cell.2011.01.028

Cited by 255 publications

(392 citation statements)

References 58 publications

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“…Similarly, our attempts to construct a functional reporter for IR21a, which is expressed in neurons in the arista and sacculus (Benton et al, 2009), were unsuccessful (data not shown). However, these cells may correspond to those labeled by an enhancer trap near the brivido1 gene [encoding a transient receptor potential (TRP) channel] that-consistent with previous backfill studies (Stocker et al, 1983)-project to the VP3 glomerulus at the posterior of the antennal lobe (also referred to as the proximal antennal protocerebrum) (Gallio et al, 2011). Finally, the neurons expressing two IR coreceptors, IR8a and IR25a, as well as IR76b, which is expressed in one cell in each coeloconic sensillum class (Fig.…”

Section: Peripheral and Central Spatial Maps Of Ir Olfactory Sensorymentioning

confidence: 90%

Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

Silbering¹,

Rytz²,

Grosjean³

et al. 2011

J. Neurosci.

464

749

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To sense myriad environmental odors, animals have evolved multiple, large families of divergent olfactory receptors. How and why distinct receptor repertoires and their associated circuits are functionally and anatomically integrated is essentially unknown. We have addressed these questions through comprehensive comparative analysis of the Drosophila olfactory subsystems that express the ionotropic receptors (IRs) and odorant receptors (ORs). We identify ligands for most IR neuron classes, revealing their specificity for select amines and acids, which complements the broader tuning of ORs for esters and alcohols. IR and OR sensory neurons exhibit glomerular convergence in segregated, although interconnected, zones of the primary olfactory center, but these circuits are extensively interdigitated in higher brain regions. Consistently, behavioral responses to odors arise from an interplay between IR-and OR-dependent pathways. We integrate knowledge on the different phylogenetic and developmental properties of these receptors and circuits to propose models for the functional contributions and evolution of these distinct olfactory subsystems.

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Section: Peripheral and Central Spatial Maps Of Ir Olfactory Sensorymentioning

confidence: 90%

Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

Silbering¹,

Rytz²,

Grosjean³

et al. 2011

J. Neurosci.

464

749

View full text Add to dashboard Cite

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“…We subjected immobilized animals to sinusoidal temperature variations (1.5°C amplitude, 18°C mean temperature, 60-s period) that would evoke cool avoidance in behaving animals. Multineuronal calcium dynamics were imaged by driving GCaMP expression throughout the dorsal organ by using the panneuronal elav promoter, or a large subset of DOG neurons by using the NP4486 promoter, which had previously been shown to drive expression in cold-sensing neurons in the adult fly (9). Calcium imaging revealed three neurons in each dorsal organ that exhibited strong intracellular calcium dynamics coupled to the temperature waveform ( Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Substantial progress has been made in understanding circuits for thermotaxis in the adult fly (3). Distinct peripheral sensory pathways for warm and cold avoidance that start in the fly antenna and project to the adult central brain, also to a region ventral to the antennal lobe, have now been identified (9,37), as well as a distinct internal sensory pathway involving the anterior cell warmth sensors in the fly brain (10). The molecules, cells, and circuits for negative thermotaxis in Drosophila larva remain poorly understood, except at noxious temperatures (18,38), and we have not yet identified circuits for negative thermotaxis (warm avoidance).…”

Section: Discussionmentioning

confidence: 99%

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Sensory determinants of behavioral dynamics in Drosophila thermotaxis

Klein

Afonso

Vonner

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

152

206

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Complex animal behaviors are built from dynamical relationships between sensory inputs, neuronal activity, and motor outputs in patterns with strategic value. Connecting these patterns illuminates how nervous systems compute behavior. Here, we study Drosophila larva navigation up temperature gradients toward preferred temperatures (positive thermotaxis). By tracking the movements of animals responding to fixed spatial temperature gradients or random temperature fluctuations, we calculate the sensitivity and dynamics of the conversion of thermosensory inputs into motor responses. We discover three thermosensory neurons in each dorsal organ ganglion (DOG) that are required for positive thermotaxis. Random optogenetic stimulation of the DOG thermosensory neurons evokes behavioral patterns that mimic the response to temperature variations. In vivo calcium and voltage imaging reveals that the DOG thermosensory neurons exhibit activity patterns with sensitivity and dynamics matched to the behavioral response. Temporal processing of temperature variations carried out by the DOG thermosensory neurons emerges in distinct motor responses during thermotaxis. N avigation toward environmental conditions that improve survival and fitness is of near-universal importance in motile biological organisms. Quantitative analysis of such animal behaviors to defined sensory inputs is a powerful approach to elucidate how behavior is encoded in underlying neurons and circuits. The advantage of studying navigation in small, optically transparent, genetically modifiable animals like Caenorhabditis elegans (1) or Drosophila larvae (2) is the opportunity to dissect sensory, neuronal, and behavioral dynamics in live animals by using optical neurophysiology and optogenetics throughout the nervous system.The Drosophila melanogaster larva navigates gradients of many sensory cues, including light, temperature, odors, and tastes, but with fewer neurons in its sensory periphery and brain than the adult. Moreover, the simpler body plan and crawling movements of the larva facilitate the precise quantification of behavioral dynamics. Poikilotherms like C. elegans or Drosophila use sensitive thermosensory mechanisms to navigate moderate temperature ranges, thereby enabling them to use their environments to regulate their own body temperatures (3, 4). Here, we study sensory and behavioral dynamics during positive thermotaxis (i.e., cool avoidance) by the Drosophila larva. Tracking the movements of Drosophila exploring temperature, olfactory, or gaseous gradients has shown that their navigation is generated by a sequence of two alternating motor programs: runs involving peristaltic forward movement that are interrupted by turns involving probing side-to-side head sweeps until the initiation of a new run (5-8). Larvae negotiating temperature gradients stochastically transition between runs and turns by strategies that cause runs pointed in favorable directions to be more frequent and longer than runs pointed in unfavorable directions. These transitions b...

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“…In 1905, Thunberg (10) proposed that humidity may be perceived in humans as the synthesis of mechanical distension associated with changes in skin hydration, along with temperature signals from the rate of evaporative cooling. This old idea might apply to other animals as well; for instance, the hygrosensitive organs in cockroach and Drosophila also house thermosensitive neurons (8,11). Whether paired thermosensitive neurons are required for hygrosensation in insects or, for that matter, whether any animal (including humans) senses humidity via this mechanism, remains unknown.…”

mentioning

confidence: 99%

Humidity sensation requires both mechanosensory and thermosensory pathways in Caenorhabditis elegans

Russell

Vidal-Gadea

Makay

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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All terrestrial animals must find a proper level of moisture to ensure their health and survival. The cellular-molecular basis for sensing humidity is unknown in most animals, however. We used the model nematode Caenorhabditis elegans to uncover a mechanism for sensing humidity. We found that whereas C. elegans showed no obvious preference for humidity levels under standard culture conditions, worms displayed a strong preference after pairing starvation with different humidity levels, orienting to gradients as shallow as 0.03% relative humidity per millimeter. Cell-specific ablation and rescue experiments demonstrate that orientation to humidity in C. elegans requires the obligatory combination of distinct mechanosensitive and thermosensitive pathways. The mechanosensitive pathway requires a conserved DEG/ENaC/ ASIC mechanoreceptor complex in the FLP neuron pair. Because humidity levels influence the hydration of the worm's cuticle, our results suggest that FLP may convey humidity information by reporting the degree that subcuticular dendritic sensory branches of FLP neurons are stretched by hydration. The thermosensitive pathway requires cGMP-gated channels in the AFD neuron pair. Because humidity levels affect evaporative cooling, AFD may convey humidity information by reporting thermal flux. Thus, humidity sensation arises as a metamodality in C. elegans that requires the integration of parallel mechanosensory and thermosensory pathways. This hygrosensation strategy, first proposed by Thunberg more than 100 y ago, may be conserved because the underlying pathways have cellular and molecular equivalents across a wide range of species, including insects and humans. mechanosensation | thermosensation M oisture is essential for life. As such, many animals have adapted different behavioral mechanisms to migrate toward their preferred moisture level (hygrotaxis) (1-6). For instance, Drosophila avoid high humidity that impedes flight, whereas green frogs orient toward high humidity to maintain hydration (5, 6). Animals also sense moisture levels to determine important information about their environment; for example, moths detect humidity levels around flowers to deduce which ones might be damaged and contain less nectar (7). These behaviors are often critical to keep an animal within its niche and regulate essential processes such as growth and reproduction. Thus, it is surprising that the molecular basis for how different humidity levels are detected and encoded by the nervous system (hygrosensation) remains unknown in most animals.The search for humidity receptors has achieved the most progress in insects. For instance, distinct sets of hygrosensitive neurons have been found in dome-shaped organs on the antenna of the giant cockroach (8). One set activates with moist air, and the other set responds to dry air. Similar moist and dry receptive neurons have been detected in the branched arista subsegment of the antennae in adult Drosophila (9). Removal of the arista or deletion of any one of three TRP channels expres...

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The Coding of Temperature in the Drosophila Brain

Cited by 255 publications

References 58 publications

Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

Sensory determinants of behavioral dynamics in Drosophila thermotaxis

Humidity sensation requires both mechanosensory and thermosensory pathways in Caenorhabditis elegans

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