Plasticity in inhibitory networks improves pattern separation in early olfactory processing

Abstract Distinguishing between nectar and non-nectar odors is challenging for animals due to shared compounds and varying ratios in complex mixtures. Changes in nectar production throughout the day and over the animal’s lifetime add to the complexity. The honeybee olfactory system, containing fewer...

Full description

Saved in:
Bibliographic Details
Main Authors: Shruti Joshi, Seth Haney, Zhenyu Wang, Fernando Locatelli, Hong Lei, Yu Cao, Brian Smith, Maxim Bazhenov
Format: Article
Language:English
Published: Nature Portfolio 2025-04-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-025-07879-2
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850184449490157568
author Shruti Joshi
Seth Haney
Zhenyu Wang
Fernando Locatelli
Hong Lei
Yu Cao
Brian Smith
Maxim Bazhenov
author_facet Shruti Joshi
Seth Haney
Zhenyu Wang
Fernando Locatelli
Hong Lei
Yu Cao
Brian Smith
Maxim Bazhenov
author_sort Shruti Joshi
collection DOAJ
description Abstract Distinguishing between nectar and non-nectar odors is challenging for animals due to shared compounds and varying ratios in complex mixtures. Changes in nectar production throughout the day and over the animal’s lifetime add to the complexity. The honeybee olfactory system, containing fewer than 1000 principal neurons in the early olfactory relay, the antennal lobe (AL), must learn to associate diverse volatile blends with rewards. Previous studies identified plasticity in the AL circuits, but its role in odor learning remains poorly understood. Using a biophysical computational model, tuned by in vivo electrophysiological data, and live imaging of the honeybee’s AL, we explored the neural mechanisms of plasticity in the AL. Our findings revealed that when trained with a set of rewarded and unrewarded odors, the AL inhibitory network suppresses responses to shared chemical compounds while enhancing responses to distinct compounds. This results in improved pattern separation and a more concise neural code. Our calcium imaging data support these predictions. Analysis of a graph convolutional neural network performing an odor categorization task revealed a similar mechanism for contrast enhancement. Our study provides insights into how inhibitory plasticity in the early olfactory network reshapes the coding for efficient learning of complex odors.
format Article
id doaj-art-f0e8d51a139f4a4bab84d1c4c9d8f9c3
institution OA Journals
issn 2399-3642
language English
publishDate 2025-04-01
publisher Nature Portfolio
record_format Article
series Communications Biology
spelling doaj-art-f0e8d51a139f4a4bab84d1c4c9d8f9c32025-08-20T02:17:02ZengNature PortfolioCommunications Biology2399-36422025-04-018111710.1038/s42003-025-07879-2Plasticity in inhibitory networks improves pattern separation in early olfactory processingShruti Joshi0Seth Haney1Zhenyu Wang2Fernando Locatelli3Hong Lei4Yu Cao5Brian Smith6Maxim Bazhenov7Department of Electrical and Computer Engineering, University of California San DiegoDepartment of Medicine, University of California San DiegoDepartment of Electrical, Computer and Energy Engineering, Arizona State UniversityFacultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Instituto de Fisiología, Biología Molecular y Neurociencias, CONICETSchool of Life Science, Arizona State UniversityDepartment of Electrical and Computer Engineering, University of MinnesotaSchool of Life Science, Arizona State UniversityDepartment of Medicine, University of California San DiegoAbstract Distinguishing between nectar and non-nectar odors is challenging for animals due to shared compounds and varying ratios in complex mixtures. Changes in nectar production throughout the day and over the animal’s lifetime add to the complexity. The honeybee olfactory system, containing fewer than 1000 principal neurons in the early olfactory relay, the antennal lobe (AL), must learn to associate diverse volatile blends with rewards. Previous studies identified plasticity in the AL circuits, but its role in odor learning remains poorly understood. Using a biophysical computational model, tuned by in vivo electrophysiological data, and live imaging of the honeybee’s AL, we explored the neural mechanisms of plasticity in the AL. Our findings revealed that when trained with a set of rewarded and unrewarded odors, the AL inhibitory network suppresses responses to shared chemical compounds while enhancing responses to distinct compounds. This results in improved pattern separation and a more concise neural code. Our calcium imaging data support these predictions. Analysis of a graph convolutional neural network performing an odor categorization task revealed a similar mechanism for contrast enhancement. Our study provides insights into how inhibitory plasticity in the early olfactory network reshapes the coding for efficient learning of complex odors.https://doi.org/10.1038/s42003-025-07879-2
spellingShingle Shruti Joshi
Seth Haney
Zhenyu Wang
Fernando Locatelli
Hong Lei
Yu Cao
Brian Smith
Maxim Bazhenov
Plasticity in inhibitory networks improves pattern separation in early olfactory processing
Communications Biology
title Plasticity in inhibitory networks improves pattern separation in early olfactory processing
title_full Plasticity in inhibitory networks improves pattern separation in early olfactory processing
title_fullStr Plasticity in inhibitory networks improves pattern separation in early olfactory processing
title_full_unstemmed Plasticity in inhibitory networks improves pattern separation in early olfactory processing
title_short Plasticity in inhibitory networks improves pattern separation in early olfactory processing
title_sort plasticity in inhibitory networks improves pattern separation in early olfactory processing
url https://doi.org/10.1038/s42003-025-07879-2
work_keys_str_mv AT shrutijoshi plasticityininhibitorynetworksimprovespatternseparationinearlyolfactoryprocessing
AT sethhaney plasticityininhibitorynetworksimprovespatternseparationinearlyolfactoryprocessing
AT zhenyuwang plasticityininhibitorynetworksimprovespatternseparationinearlyolfactoryprocessing
AT fernandolocatelli plasticityininhibitorynetworksimprovespatternseparationinearlyolfactoryprocessing
AT honglei plasticityininhibitorynetworksimprovespatternseparationinearlyolfactoryprocessing
AT yucao plasticityininhibitorynetworksimprovespatternseparationinearlyolfactoryprocessing
AT briansmith plasticityininhibitorynetworksimprovespatternseparationinearlyolfactoryprocessing
AT maximbazhenov plasticityininhibitorynetworksimprovespatternseparationinearlyolfactoryprocessing