Olfactory responses of Drosophila are encoded in the organization of projection neurons

The projection neurons (PNs), reconstructed from electron microscope (EM) images of the Drosophila olfactory system, offer a detailed view of neuronal anatomy, providing glimpses into information flow in the brain. About 150 uPNs constituting 58 glomeruli in the antennal lobe (AL) are bundled togeth...

Full description

Bibliographic Details
Main Authors: Kiri Choi, Won Kyu Kim, Changbong Hyeon
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-09-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/77748
_version_ 1811246368881115136
author Kiri Choi
Won Kyu Kim
Changbong Hyeon
author_facet Kiri Choi
Won Kyu Kim
Changbong Hyeon
author_sort Kiri Choi
collection DOAJ
description The projection neurons (PNs), reconstructed from electron microscope (EM) images of the Drosophila olfactory system, offer a detailed view of neuronal anatomy, providing glimpses into information flow in the brain. About 150 uPNs constituting 58 glomeruli in the antennal lobe (AL) are bundled together in the axonal extension, routing the olfactory signal received at AL to mushroom body (MB) calyx and lateral horn (LH). Here we quantify the neuronal organization in terms of the inter-PN distances and examine its relationship with the odor types sensed by Drosophila. The homotypic uPNs that constitute glomeruli are tightly bundled and stereotyped in position throughout the neuropils, even though the glomerular PN organization in AL is no longer sustained in the higher brain center. Instead, odor-type dependent clusters consisting of multiple homotypes innervate the MB calyx and LH. Pheromone-encoding and hygro/thermo-sensing homotypes are spatially segregated in MB calyx, whereas two distinct clusters of food-related homotypes are found in LH in addition to the segregation of pheromone-encoding and hygro/thermo-sensing homotypes. We find that there are statistically significant associations between the spatial organization among a group of homotypic uPNs and certain stereotyped olfactory responses. Additionally, the signals from some of the tightly bundled homotypes converge to a specific group of lateral horn neurons (LHNs), which indicates that homotype (or odor type) specific integration of signals occurs at the synaptic interface between PNs and LHNs. Our findings suggest that before neural computation in the inner brain, some of the olfactory information are already encoded in the spatial organization of uPNs, illuminating that a certain degree of labeled-line strategy is at work in the Drosophila olfactory system.
first_indexed 2024-04-12T14:52:31Z
format Article
id doaj.art-5c40cea8975b4bac8e834640cbddae37
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-12T14:52:31Z
publishDate 2022-09-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-5c40cea8975b4bac8e834640cbddae372022-12-22T03:28:22ZengeLife Sciences Publications LtdeLife2050-084X2022-09-011110.7554/eLife.77748Olfactory responses of Drosophila are encoded in the organization of projection neuronsKiri Choi0https://orcid.org/0000-0002-0156-8410Won Kyu Kim1https://orcid.org/0000-0002-6286-0925Changbong Hyeon2https://orcid.org/0000-0002-4844-7237School of Computational Sciences, Korea Institute for Advanced Study, Seoul, Republic of KoreaSchool of Computational Sciences, Korea Institute for Advanced Study, Seoul, Republic of KoreaSchool of Computational Sciences, Korea Institute for Advanced Study, Seoul, Republic of KoreaThe projection neurons (PNs), reconstructed from electron microscope (EM) images of the Drosophila olfactory system, offer a detailed view of neuronal anatomy, providing glimpses into information flow in the brain. About 150 uPNs constituting 58 glomeruli in the antennal lobe (AL) are bundled together in the axonal extension, routing the olfactory signal received at AL to mushroom body (MB) calyx and lateral horn (LH). Here we quantify the neuronal organization in terms of the inter-PN distances and examine its relationship with the odor types sensed by Drosophila. The homotypic uPNs that constitute glomeruli are tightly bundled and stereotyped in position throughout the neuropils, even though the glomerular PN organization in AL is no longer sustained in the higher brain center. Instead, odor-type dependent clusters consisting of multiple homotypes innervate the MB calyx and LH. Pheromone-encoding and hygro/thermo-sensing homotypes are spatially segregated in MB calyx, whereas two distinct clusters of food-related homotypes are found in LH in addition to the segregation of pheromone-encoding and hygro/thermo-sensing homotypes. We find that there are statistically significant associations between the spatial organization among a group of homotypic uPNs and certain stereotyped olfactory responses. Additionally, the signals from some of the tightly bundled homotypes converge to a specific group of lateral horn neurons (LHNs), which indicates that homotype (or odor type) specific integration of signals occurs at the synaptic interface between PNs and LHNs. Our findings suggest that before neural computation in the inner brain, some of the olfactory information are already encoded in the spatial organization of uPNs, illuminating that a certain degree of labeled-line strategy is at work in the Drosophila olfactory system.https://elifesciences.org/articles/77748labeled-line designodor-type dependent arrangementsecond-order neuronsinter-neuronal organizationinformation processingsynaptic connectivity
spellingShingle Kiri Choi
Won Kyu Kim
Changbong Hyeon
Olfactory responses of Drosophila are encoded in the organization of projection neurons
eLife
labeled-line design
odor-type dependent arrangement
second-order neurons
inter-neuronal organization
information processing
synaptic connectivity
title Olfactory responses of Drosophila are encoded in the organization of projection neurons
title_full Olfactory responses of Drosophila are encoded in the organization of projection neurons
title_fullStr Olfactory responses of Drosophila are encoded in the organization of projection neurons
title_full_unstemmed Olfactory responses of Drosophila are encoded in the organization of projection neurons
title_short Olfactory responses of Drosophila are encoded in the organization of projection neurons
title_sort olfactory responses of drosophila are encoded in the organization of projection neurons
topic labeled-line design
odor-type dependent arrangement
second-order neurons
inter-neuronal organization
information processing
synaptic connectivity
url https://elifesciences.org/articles/77748
work_keys_str_mv AT kirichoi olfactoryresponsesofdrosophilaareencodedintheorganizationofprojectionneurons
AT wonkyukim olfactoryresponsesofdrosophilaareencodedintheorganizationofprojectionneurons
AT changbonghyeon olfactoryresponsesofdrosophilaareencodedintheorganizationofprojectionneurons