The Molecular Basis of Odor Coding in the Drosophila Larva

Kreher, Scott A.; Kwon, Jae Young; Carlson, John R.

doi:10.1016/j.neuron.2005.04.007

Cited by 290 publications

(393 citation statements)

References 51 publications

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“…3D and Movie S3). The rest of the DOG neurons-olfactory receptor neurons (ORNs) and a few gustatory receptor neurons-send their dendrites to a dome of cuticle perforated by pores (25). In contrast, the thermosensory neurons develop large membrane-rich dendritic bulbs that appear 60 ± 13% of the distance before reaching the dome (Fig.…”

Section: Resultsmentioning

confidence: 99%

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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Section: Resultsmentioning

confidence: 99%

Sensory determinants of behavioral dynamics in Drosophila thermotaxis

Klein

Afonso

Vonner

et al. 2014

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

152

206

View full text Add to dashboard Cite

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“…Thus, a learning index of zero indicated that no associations were formed, whereas a learning index significantly greater than zero indicated a positive association between conditioned stimuli and reward. PA and BUT were chosen, as they were unlikely to be odor equivalents; in larvae they are detected and processed by different combinations of peripheral and central structures (Kreher et al 2005). In addition, we found that larvae of the natural rover (for R ), sitter (for s ), and sitter mutant (for s2 ) strain, which was generated on a rover genetic background (de Belle et al 1989;Pereira and Sokolowski 1993), do not differ significantly in their response to these odors (below).…”

Section: Resultsmentioning

confidence: 99%

Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase

Kaun

Hendel²,

Gerber³

et al. 2007

Learn. Mem.

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Animals must be able to find and evaluate food to ensure survival. The ability to associate a cue with the presence of food is advantageous because it allows an animal to quickly identify a situation associated with a good, bad, or even harmful food. Identifying genes underlying these natural learned responses is essential to understanding this ability. Here, we investigate whether natural variation in the foraging (for) gene in Drosophila melanogaster larvae is important in mediating associations between either an odor or a light stimulus and food reward. We found that for influences olfactory conditioning and that the mushroom bodies play a role in this for-mediated olfactory learning. Genotypes associated with high activity of the product of for, cGMP-dependent protein kinase (PKG), showed greater memory acquisition and retention compared with genotypes associated with low activity of PKG when trained with three conditioning trials. Interestingly, increasing the number of training trials resulted in decreased memory retention only in genotypes associated with high PKG activity. The difference in the dynamics of memory acquisition and retention between variants of for suggests that the ability to learn and retain an association may be linked to the foraging strategies of the two variants.Learned associations such as identifying odors as indicators of food, or showing preferences for food-related odors, are conserved across diverse taxa from humans and mice to slugs, honeybees, and fruit flies (Ache and Young 2005). The fruit fly Drosophila melanogaster can use odors as cues for the presence of both a food reward and an aversive stimulus (Tempel et al. 1983;Scherer et al. 2003;Schwaerzel et al. 2003;Margulies et al. 2005;McGuire et al. 2005;Kim et al. 2007). Identifying genes underlying these natural learned responses is essential to understanding this ability. Here, we use classical reward conditioning to investigate how natural variation in the foraging (for) gene affects acquisition and decay of memory in D. melanogaster larvae.for encodes a cGMP-dependent protein kinase (PKG) (Osborne et al. 1997). In mammals, PKG is important for proper induction of long-term potentiation (LTP) and long-term depression (LTD) (Hartell 1994;Zhuo et al. 1994;Lev-Ram et al. 1997;Arancio et al. 2001;Fiel et al. 2003Fiel et al. , 2005Kleppisch et al. 2003;Hofmann et al. 2006). Although LTP and LTD are thought to be important mechanisms underlying learning and memory (Whitlock et al. 2006), few studies have shown a direct role for PKG in learning and memory. This study aims to do this by investigating how learning differs between allelic variants of for in Drosophila larvae.for is an ideal candidate to study how natural genetic variation can affect learning and memory, since natural for variants exist that have subtle but significant variations in PKG activity (Osborne et al. 1997). The rover variants of for (for R ) have higher for transcript levels and higher PKG activities compared with the sitter variants of for (for s ) (Osb...

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“…Indeed, the arbovirus vector mosquito Aedes aegypti expresses 24 odorant receptor (OR) genes in the larval antenna, 15 of which are larval specific (4). Elegant work in the Drosophila melanogaster model has detailed larval behavioral responses and characterized 25 ORs that are expressed in 21 olfactory receptor neurons (ORNs) in each of the two dorsal organs, which constitute the olfactory apparatus of the fly larva (5)(6)(7).…”

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confidence: 99%

The molecular and cellular basis of olfactory-driven behavior inAnopheles gambiaelarvae

Xia

Wang

Buscariollo

et al. 2008

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

140

211

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The mosquito Anopheles gambiae is the principal Afrotropical vector for human malaria. A central component of its vectorial capacity is the ability to maintain sufficient populations of adults. During both adult and preadult (larval) stages, the mosquitoes depend on the ability to recognize and respond to chemical cues that mediate feeding and survival. In this study, we used a behavioral assay to identify a range of odorant-specific responses of An. gambiae larvae that are dependent on the integrity of the larval antennae. Parallel molecular analyses have identified a subset of the An. gambiae odorant receptors (AgOrs) that are localized to discrete neurons within the larval antennae and facilitate odor-evoked responses in Xenopus oocytes that are consistent with the larval behavioral spectrum. These studies shed light on chemosensory-driven behaviors and represent molecular and cellular characterization of olfactory processes in mosquito larvae. These advances may ultimately enhance the development of vector control strategies, targeting olfactory pathways in larval-stage mosquitoes to reduce the catastrophic effects of malaria and other diseases.malaria ͉ olfaction ͉ signal transduction ͉ odorant receptors S ensitivity and the ability to respond to a wide range of olfactory cues are essential for many behavioral processes that mediate the vectorial capacity of Anopheles gambiae and other diseasecarrying mosquitoes (1). Although there is a growing body of knowledge of the adult An. gambiae olfactory system, there is a paucity of information as to the molecular and cellular basis of olfaction in larval stages, in which it may be of potential importance in disease control. Paradoxically, despite being one of the historically most successful strategies for mosquito control (2) and prevention of human malaria, the targeting of mosquito larvae or larval habitats around human dwellings is sparsely implemented in Africa and other malaria-endemic regions (3). Furthermore, the simplicity of insect larval olfactory systems makes them excellent models to study olfactory signal transduction and coding. Indeed, the arbovirus vector mosquito Aedes aegypti expresses 24 odorant receptor (OR) genes in the larval antenna, 15 of which are larval specific (4). Elegant work in the Drosophila melanogaster model has detailed larval behavioral responses and characterized 25 ORs that are expressed in 21 olfactory receptor neurons (ORNs) in each of the two dorsal organs, which constitute the olfactory apparatus of the fly larva (5-7).In this study, we designed and used a simple olfactory-based assay to carry out an initial characterization of An. gambiae larval behavioral responses to a range of natural and synthetic chemical stimuli. Consistent with olfactory function, ablation of the larval antennae specifically eliminated these behavioral responses, and molecular approaches identified a set of larval AgOrs, which were in some cases larval specific and the transcripts of which were mapped to a distinctive population of ORNs within th...

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The Molecular Basis of Odor Coding in the Drosophila Larva

Cited by 290 publications

References 51 publications

Sensory determinants of behavioral dynamics in Drosophila thermotaxis

Sensory determinants of behavioral dynamics in Drosophila thermotaxis

Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase

The molecular and cellular basis of olfactory-driven behavior inAnopheles gambiaelarvae

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