tracking-drosophila-larval-behavior-response-to-optogenetic

Tracking Drosophila Larval Behavior in Response to Optogenetic Stimulation of Olfactory Neurons

The ability of insects to navigate toward odor sources is based on the activities of their first-order olfactory receptor neurons (ORNs). While a ...

in-vivo-ex-vivo-calcium-imaging-an-olfactory-circuit-neuron-third

In-vivo and Ex-vivo Calcium Imaging of an Olfactory Circuit Neuron in the Third-Instar Drosophila melanogaster Larva

Calcium imaging is crucial for studying neural dynamics and brain function. However, current methods for imaging calcium in Drosophila larvae are ...

University of Nevada

University of Nevada, Reno

The ability of an animal to detect, discriminate, and respond to odors depends on the functions of its olfactory receptor neurons (ORNs). The extent to which each ORN, upon activation, contributes to chemotaxis is not well understood. We hypothesized that strong activation of each ORN elicits a different behavioral response in the Drosophila melanogaster larva by differentially affecting the composition of its navigational behavior. To test this hypothesis, we exposed Drosophila larvae to specific odorants to analyze the effect of individual ORN activity on chemotaxis. We used two different behavioral paradigms to analyze the chemotaxis response of larvae to odorants. When tested with five different odorants that elicit strong physiological responses from single ORNs, larval behavioral responses toward each odorant differed in the strength of attraction as well as in the composition of discrete navigational elements, such as runs and turns. Further, behavioral responses to odorants did not correlate with either the strength of odor gradients tested or the sensitivity of each ORN to its cognate odorant. Finally, we provide evidence that wild-type larvae with all ORNs intact exhibit higher behavioral variance than mutant larvae that have only a single pair of functional ORNs. We conclude that individual ORNs contribute differently to the olfactory circuit that instructs chemotactic responses. Our results, along with recent studies from other groups, suggest that ORNs are functionally nonequivalent units. These results have implications for understanding peripheral odor coding.

Differential Contributions of Olfactory Receptor Neurons in a Drosophila Olfactory Circuit.

Most animals depend upon olfaction to find food, mates, and to avoid predators. An animal's olfactory circuit helps it sense its olfactory environment and generate critical behavioral responses. The general architecture of the olfactory circuit, which is conserved across species, is made up of a few different neuronal types including first-order receptor neurons, second- and third-order neurons, and local interneurons. Each neuronal type differs in their morphology, physiology, and neurochemistry. However, several recent studies have suggested that there is intrinsic diversity even among neurons of the same type and that this diversity is important for neural function. In this review, we first examine instances of intrinsic diversity observed among individual types of olfactory neurons. Next, we review potential genetic and experience-based plasticity mechanisms that underlie this diversity. Finally, we consider the implications of intrinsic neuronal diversity for circuit function. Overall, we hope to highlight the importance of intrinsic diversity as a previously underestimated property of circuit function.

Strength in diversity: functional diversity among olfactory neurons of the same type.

We are immersed within an odorous sea of chemical currents that we parse into individual odors with complex structures. Odors have been posited as determined by the structural relation between the molecules that compose the chemical compounds and their interactions with the receptor site. But, naturally occurring smells are parsed from gaseous odor plumes. To give a comprehensive account of the nature of odors the chemosciences must account for these large distributed entities as well. We offer a focused review of what is known about the perception of odor plumes for olfactory navigation and tracking, which we then connect to what is known about the role odorants play as properties of the plume in determining odor identity with respect to odor quality. We end by motivating our central claim that more research needs to be conducted on the role that odorants play within the odor plume in determining odor identity.

Odors: from chemical structures to gaseous plumes.

Starvation enhances olfactory sensitivity that encourage animals to search for food. The molecular mechanisms that enable sensory neurons to remain flexible and adapt to a particular internal state remain poorly understood. Here, we study the roles of GABA and insulin signaling in starvation-dependent modulation of olfactory sensory neuron (OSN) function in the Drosophila larva. We show that GABA-receptor and insulin-receptor play important roles during OSN modulation. Using an OSN-specific gene expression analysis, we explore downstream targets of insulin signaling in OSNs. Our results suggest that insulin and GABA signaling pathways interact within OSNs and modulate OSN function by impacting olfactory information processing. We further show that manipulating these signaling pathways specifically in the OSNs impact larval feeding behavior and its body weight. These results challenge the prevailing model of OSN modulation and highlight opportunities to better understand OSN modulation mechanisms and their relationship to animal physiology.

Mechanism underlying starvation-dependent modulation of olfactory behavior in Drosophila larva.

Crawling insects, when starved, tend to have fewer head wavings and travel in straighter tracks in search of food. We used the Drosophila melanogaster larva to investigate whether this flexibility in the insect's navigation strategy arises during early olfactory processing and, if so, how. We demonstrate a critical role for Keystone-LN, an inhibitory local neuron in the antennal lobe, in implementing head-sweep behavior. Keystone-LN responds to odor stimuli, and its inhibitory output is required for a larva to successfully navigate attractive and aversive odor gradients. We show that insulin signaling in Keystone-LN likely mediates the starvation-dependent changes in head-sweep magnitude, shaping the larva's odor-guided movement. Our findings demonstrate how flexibility in an insect's navigation strategy can arise from context-dependent modulation of inhibitory neurons in an early sensory processing center. They raise new questions about modulating a circuit's inhibitory output to implement changes in a goal-directed movement.

Internal state affects local neuron function in an early sensory processing center to shape olfactory behavior in Drosophila larvae.

Individuals of many animal populations exhibit idiosyncratic behaviors. One measure of idiosyncratic behavior is a behavior syndrome, defined as the stability of one or more behavior traits in an individual across different situations. While behavior syndromes have been described in various animal systems, their properties and the circuit mechanisms that generate them are poorly understood. We thus have an incomplete understanding of how circuit properties influence animal behavior. Here, we characterize olfactory behavior syndromes in the Drosophila larva. We show that larvae exhibit idiosyncrasies in their olfactory behavior over short time scales. They are influenced by the larva's satiety state and odor environment. Additionally, we identified a group of antennal lobe local neurons that influence the larva's idiosyncratic behavior. These findings reveal previously unsuspected influences on idiosyncratic behavior. They further affirm the idea that idiosyncrasies are not simply statistical phenomena but manifestations of neural mechanisms. In light of these findings, we discuss more broadly the importance of idiosyncrasies to animal survival and how they might be studied.

Stability of olfactory behavior syndromes in the Drosophila larva.

Neonicotinoid pesticides are well-known for their sublethal effects on insect behavior and physiology. Recent work suggests neonicotinoids can impair insect olfactory processing, with potential downstream effects on behavior and possibly survival. However, it is unclear whether impairment occurs during peripheral olfactory detection, during information processing in central brain regions, or in both contexts. We used Drosophila melanogaster to explore the potential for neonicotinoids to disrupt olfaction by conducting electrophysiological analyses of single neurons and whole antennae of flies exposed to varying concentrations of the neonicotinoid imidacloprid (IMD) that were shown to cause relative differences in fly survival. Our results demonstrated that IMD exposure significantly reduced the activity of a single focal olfactory neuron and delayed the return to baseline activity of the whole antenna. To determine if IMD also impacts olfactory-guided behavior, we compared flies' relative preference for odor sources varying in ethanol content. Flies exposed to IMD had a greater relative preference for ethanol-laced pineapple juice than control flies, demonstrating that neuronal shifts induced by IMD that we observed are associated with changes in relative preference. Given the interest in the sensory impacts of agrochemical exposure on wild insect behavior and physiology, we highlight the potential of Drosophila as a tractable model for investigating the effects of pesticides at scales ranging from single-neuron physiology to olfactory-guided behavior.

ArticleTotal : 2	Year
Publication title Cited by 8	2018
Publication title	2025

Article	Year
Differential Contributions of Olfactory Receptor Neurons in a Drosophila Olfactory Circuit. eNeuro\| PubMed ID: 27570823	2016
Strength in diversity: functional diversity among olfactory neurons of the same type. Journal of bioenergetics and biomembranes\| PubMed ID: 30604088	2019
Odors: from chemical structures to gaseous plumes. Neuroscience and biobehavioral reviews\| PubMed ID: 31931034	2020
Mechanism underlying starvation-dependent modulation of olfactory behavior in Drosophila larva. Scientific reports\| PubMed ID: 32080342	2020
Internal state affects local neuron function in an early sensory processing center to shape olfactory behavior in Drosophila larvae. Scientific reports\| PubMed ID: 36131078	2022
Stability of olfactory behavior syndromes in the Drosophila larva. Scientific reports\| PubMed ID: 36765192	2023
A neonicotinoid pesticide alters Drosophila olfactory processing. Scientific reports\| PubMed ID: 37391495	2023

Dennis Mathew

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