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

Abstract 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....

Full description

Bibliographic Details
Main Authors: Seth R. Odell, David Clark, Nicholas Zito, Roshni Jain, Hui Gong, Kendall Warnock, Ricardo Carrion-Lopez, Coral Maixner, Lucia Prieto-Godino, Dennis Mathew
Format: Article
Language:English
Published: Nature Portfolio 2022-09-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-022-20147-1
_version_ 1828175472131833856
author Seth R. Odell
David Clark
Nicholas Zito
Roshni Jain
Hui Gong
Kendall Warnock
Ricardo Carrion-Lopez
Coral Maixner
Lucia Prieto-Godino
Dennis Mathew
author_facet Seth R. Odell
David Clark
Nicholas Zito
Roshni Jain
Hui Gong
Kendall Warnock
Ricardo Carrion-Lopez
Coral Maixner
Lucia Prieto-Godino
Dennis Mathew
author_sort Seth R. Odell
collection DOAJ
description Abstract 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.
first_indexed 2024-04-12T04:28:35Z
format Article
id doaj.art-1e9d2e0f4bf8497094536a9bae30a1fb
institution Directory Open Access Journal
issn 2045-2322
language English
last_indexed 2024-04-12T04:28:35Z
publishDate 2022-09-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj.art-1e9d2e0f4bf8497094536a9bae30a1fb2022-12-22T03:48:00ZengNature PortfolioScientific Reports2045-23222022-09-0112111410.1038/s41598-022-20147-1Internal state affects local neuron function in an early sensory processing center to shape olfactory behavior in Drosophila larvaeSeth R. Odell0David Clark1Nicholas Zito2Roshni Jain3Hui Gong4Kendall Warnock5Ricardo Carrion-Lopez6Coral Maixner7Lucia Prieto-Godino8Dennis Mathew9Integrative Neuroscience Program, University of NevadaIntegrative Neuroscience Program, University of NevadaIntegrative Neuroscience Program, University of NevadaMolecular Biosciences Program, University of NevadaThe Francis Crick InstituteDepartment of Biology, University of NevadaNSF-REU (BioSoRo) Program, University of NevadaNSF-REU (BioSoRo) Program, University of NevadaThe Francis Crick InstituteIntegrative Neuroscience Program, University of NevadaAbstract 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.https://doi.org/10.1038/s41598-022-20147-1
spellingShingle Seth R. Odell
David Clark
Nicholas Zito
Roshni Jain
Hui Gong
Kendall Warnock
Ricardo Carrion-Lopez
Coral Maixner
Lucia Prieto-Godino
Dennis Mathew
Internal state affects local neuron function in an early sensory processing center to shape olfactory behavior in Drosophila larvae
Scientific Reports
title Internal state affects local neuron function in an early sensory processing center to shape olfactory behavior in Drosophila larvae
title_full Internal state affects local neuron function in an early sensory processing center to shape olfactory behavior in Drosophila larvae
title_fullStr Internal state affects local neuron function in an early sensory processing center to shape olfactory behavior in Drosophila larvae
title_full_unstemmed Internal state affects local neuron function in an early sensory processing center to shape olfactory behavior in Drosophila larvae
title_short Internal state affects local neuron function in an early sensory processing center to shape olfactory behavior in Drosophila larvae
title_sort internal state affects local neuron function in an early sensory processing center to shape olfactory behavior in drosophila larvae
url https://doi.org/10.1038/s41598-022-20147-1
work_keys_str_mv AT sethrodell internalstateaffectslocalneuronfunctioninanearlysensoryprocessingcentertoshapeolfactorybehaviorindrosophilalarvae
AT davidclark internalstateaffectslocalneuronfunctioninanearlysensoryprocessingcentertoshapeolfactorybehaviorindrosophilalarvae
AT nicholaszito internalstateaffectslocalneuronfunctioninanearlysensoryprocessingcentertoshapeolfactorybehaviorindrosophilalarvae
AT roshnijain internalstateaffectslocalneuronfunctioninanearlysensoryprocessingcentertoshapeolfactorybehaviorindrosophilalarvae
AT huigong internalstateaffectslocalneuronfunctioninanearlysensoryprocessingcentertoshapeolfactorybehaviorindrosophilalarvae
AT kendallwarnock internalstateaffectslocalneuronfunctioninanearlysensoryprocessingcentertoshapeolfactorybehaviorindrosophilalarvae
AT ricardocarrionlopez internalstateaffectslocalneuronfunctioninanearlysensoryprocessingcentertoshapeolfactorybehaviorindrosophilalarvae
AT coralmaixner internalstateaffectslocalneuronfunctioninanearlysensoryprocessingcentertoshapeolfactorybehaviorindrosophilalarvae
AT luciaprietogodino internalstateaffectslocalneuronfunctioninanearlysensoryprocessingcentertoshapeolfactorybehaviorindrosophilalarvae
AT dennismathew internalstateaffectslocalneuronfunctioninanearlysensoryprocessingcentertoshapeolfactorybehaviorindrosophilalarvae