Second-order threat conditioning in the amygdala-posterior piriform cortex network

Abstract Fear, while crucial for survival, is a component of a myriad of psychiatric illnesses in its extreme. Persistent fear memories can form through processes such as second-order conditioning (SOC), during which a second-order conditioned stimulus (CS2) acquires significance by associating with...

Full description

Saved in:
Bibliographic Details
Main Authors: Tayebeh Sepahvand, Tian Qin, Zia Hasan, Kyron D. Power, Samantha J. Carew, Negar Nazari, Alyssa M. Janes, Ali Salman, Yue Xia, Touati Benoukraf, Qi Yuan
Format: Article
Language:English
Published: Nature Portfolio 2025-06-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-025-08287-2
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850224189986832384
author Tayebeh Sepahvand
Tian Qin
Zia Hasan
Kyron D. Power
Samantha J. Carew
Negar Nazari
Alyssa M. Janes
Ali Salman
Yue Xia
Touati Benoukraf
Qi Yuan
author_facet Tayebeh Sepahvand
Tian Qin
Zia Hasan
Kyron D. Power
Samantha J. Carew
Negar Nazari
Alyssa M. Janes
Ali Salman
Yue Xia
Touati Benoukraf
Qi Yuan
author_sort Tayebeh Sepahvand
collection DOAJ
description Abstract Fear, while crucial for survival, is a component of a myriad of psychiatric illnesses in its extreme. Persistent fear memories can form through processes such as second-order conditioning (SOC), during which a second-order conditioned stimulus (CS2) acquires significance by associating with a first-order conditioned stimulus (CS1). The neural circuitry underlying SOC, particularly the roles of sensory cortices, remains poorly understood. Here we explore the mechanisms of olfactory SOC in rats, focusing on the basolateral amygdala (BLA) and posterior piriform cortex (pPC). Our results demonstrate that NMDAR-dependent plasticity in both regions is essential for SOC. The BLA mediates the CS2-CS1 association, while the pPC, receiving inputs from the locus coeruleus and BLA, is critical for memory acquisition and retrieval. Single-nucleus multiomics analysis of Fos + ensembles in both regions reveals distinct yet overlapping gene activation profiles in excitatory neurons, accompanied by global chromatin remodeling. These findings highlight the specific yet coordinated roles of these structures in supporting learning and memory.
format Article
id doaj-art-48a8909d2fef48e780a772ac2f8f2bea
institution OA Journals
issn 2399-3642
language English
publishDate 2025-06-01
publisher Nature Portfolio
record_format Article
series Communications Biology
spelling doaj-art-48a8909d2fef48e780a772ac2f8f2bea2025-08-20T02:05:42ZengNature PortfolioCommunications Biology2399-36422025-06-018111810.1038/s42003-025-08287-2Second-order threat conditioning in the amygdala-posterior piriform cortex networkTayebeh Sepahvand0Tian Qin1Zia Hasan2Kyron D. Power3Samantha J. Carew4Negar Nazari5Alyssa M. Janes6Ali Salman7Yue Xia8Touati Benoukraf9Qi Yuan10Biomedical Sciences, Faculty of Medicine, Memorial UniversityBiomedical Sciences, Faculty of Medicine, Memorial UniversityBiomedical Sciences, Faculty of Medicine, Memorial UniversityBiomedical Sciences, Faculty of Medicine, Memorial UniversityBiomedical Sciences, Faculty of Medicine, Memorial UniversityBiomedical Sciences, Faculty of Medicine, Memorial UniversityBiomedical Sciences, Faculty of Medicine, Memorial UniversityBiomedical Sciences, Faculty of Medicine, Memorial UniversityBiomedical Sciences, Faculty of Medicine, Memorial UniversityBiomedical Sciences, Faculty of Medicine, Memorial UniversityBiomedical Sciences, Faculty of Medicine, Memorial UniversityAbstract Fear, while crucial for survival, is a component of a myriad of psychiatric illnesses in its extreme. Persistent fear memories can form through processes such as second-order conditioning (SOC), during which a second-order conditioned stimulus (CS2) acquires significance by associating with a first-order conditioned stimulus (CS1). The neural circuitry underlying SOC, particularly the roles of sensory cortices, remains poorly understood. Here we explore the mechanisms of olfactory SOC in rats, focusing on the basolateral amygdala (BLA) and posterior piriform cortex (pPC). Our results demonstrate that NMDAR-dependent plasticity in both regions is essential for SOC. The BLA mediates the CS2-CS1 association, while the pPC, receiving inputs from the locus coeruleus and BLA, is critical for memory acquisition and retrieval. Single-nucleus multiomics analysis of Fos + ensembles in both regions reveals distinct yet overlapping gene activation profiles in excitatory neurons, accompanied by global chromatin remodeling. These findings highlight the specific yet coordinated roles of these structures in supporting learning and memory.https://doi.org/10.1038/s42003-025-08287-2
spellingShingle Tayebeh Sepahvand
Tian Qin
Zia Hasan
Kyron D. Power
Samantha J. Carew
Negar Nazari
Alyssa M. Janes
Ali Salman
Yue Xia
Touati Benoukraf
Qi Yuan
Second-order threat conditioning in the amygdala-posterior piriform cortex network
Communications Biology
title Second-order threat conditioning in the amygdala-posterior piriform cortex network
title_full Second-order threat conditioning in the amygdala-posterior piriform cortex network
title_fullStr Second-order threat conditioning in the amygdala-posterior piriform cortex network
title_full_unstemmed Second-order threat conditioning in the amygdala-posterior piriform cortex network
title_short Second-order threat conditioning in the amygdala-posterior piriform cortex network
title_sort second order threat conditioning in the amygdala posterior piriform cortex network
url https://doi.org/10.1038/s42003-025-08287-2
work_keys_str_mv AT tayebehsepahvand secondorderthreatconditioningintheamygdalaposteriorpiriformcortexnetwork
AT tianqin secondorderthreatconditioningintheamygdalaposteriorpiriformcortexnetwork
AT ziahasan secondorderthreatconditioningintheamygdalaposteriorpiriformcortexnetwork
AT kyrondpower secondorderthreatconditioningintheamygdalaposteriorpiriformcortexnetwork
AT samanthajcarew secondorderthreatconditioningintheamygdalaposteriorpiriformcortexnetwork
AT negarnazari secondorderthreatconditioningintheamygdalaposteriorpiriformcortexnetwork
AT alyssamjanes secondorderthreatconditioningintheamygdalaposteriorpiriformcortexnetwork
AT alisalman secondorderthreatconditioningintheamygdalaposteriorpiriformcortexnetwork
AT yuexia secondorderthreatconditioningintheamygdalaposteriorpiriformcortexnetwork
AT touatibenoukraf secondorderthreatconditioningintheamygdalaposteriorpiriformcortexnetwork
AT qiyuan secondorderthreatconditioningintheamygdalaposteriorpiriformcortexnetwork