Mesoscale functional connectivity of amygdala to the auditory and prefrontal cortex of macaque monkeys revealed by INS-fMRI

Mammals rely heavily on their auditory system to perceive environmental threats, socially communicate, and care for the young. As an extension of the multiple sensory system including the auditory system, the amygdala evaluates the emotional salience of acoustic stimuli, and mediates its impact on s...

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Main Authors: Qianbing Li, An Ping, Yuqi Feng, Bin Xu, Baorong Zhang, Anna Wang Roe, Lixia Gao, Xinjian Li
Format: Article
Language:English
Published: Elsevier 2025-09-01
Series:NeuroImage
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Online Access:http://www.sciencedirect.com/science/article/pii/S1053811925004094
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author Qianbing Li
An Ping
Yuqi Feng
Bin Xu
Baorong Zhang
Anna Wang Roe
Lixia Gao
Xinjian Li
author_facet Qianbing Li
An Ping
Yuqi Feng
Bin Xu
Baorong Zhang
Anna Wang Roe
Lixia Gao
Xinjian Li
author_sort Qianbing Li
collection DOAJ
description Mammals rely heavily on their auditory system to perceive environmental threats, socially communicate, and care for the young. As an extension of the multiple sensory system including the auditory system, the amygdala evaluates the emotional salience of acoustic stimuli, and mediates its impact on sensory, cognitive, and physiological aspects of emotional processing via the lateral amygdala (LA), basal amygdala (BA), and central amygdala (CeA) nuclei of the amygdala in acoustic domain. However, the functional connections of LA, BA, and CeA with the auditory cortex (AC) and the prefrontal cortex (PFC) remain unclear, particularly at the mesoscale level. Here we employed a novel method called INS-fMRI (Infrared Neural Stimulation combined with high-resolution functional magnetic resonance imaging) in Macaque monkeys, this method permits stimulation of multiple sites within single animals in vivo, so that the relative organization of auditory networks can be studied. We found that: (1) Focal INS stimulation of the amygdala elicited robust and reliable responses in both the AC and the PFC; (2) Amygdala stimulation mainly activated ipsilateral AC and PFC; (3) The stimulation of the amygdala mainly activated the secondary AC, and the dorsolateral PFC; (4) The connection between the amygdala and the cortex is mainly mediated by neurons in LA and BA connection area. Our study further revealed the functional connectivity among the amygdala subnucleus, the auditory cortex and the prefrontal cortex, and will shed light on the research for processing biologically meaningful complex sounds.
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spelling doaj-art-b7cae762a25448fea8d59bed75778e712025-08-20T04:02:09ZengElsevierNeuroImage1095-95722025-09-0131812140610.1016/j.neuroimage.2025.121406Mesoscale functional connectivity of amygdala to the auditory and prefrontal cortex of macaque monkeys revealed by INS-fMRIQianbing Li0An Ping1Yuqi Feng2Bin Xu3Baorong Zhang4Anna Wang Roe5Lixia Gao6Xinjian Li7Department of Neurology of the Second Affiliated Hospital, Interdisciplinary Institute of Neuroscience and Technology, Zhejiang University School of Medicine, Hangzhou 310020, China; Key Laboratory of Biomedical Engineering of Ministry of Education, College of Biomedical Engineering and Instrument Science, Zhejiang University, Hangzhou 310027, ChinaDepartment of Neurology of the Second Affiliated Hospital, Interdisciplinary Institute of Neuroscience and Technology, Zhejiang University School of Medicine, Hangzhou 310020, China; Department of Neurosurgery of the Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, ChinaDepartment of Neurology of the Second Affiliated Hospital, Interdisciplinary Institute of Neuroscience and Technology, Zhejiang University School of Medicine, Hangzhou 310020, China; Key Laboratory of Biomedical Engineering of Ministry of Education, College of Biomedical Engineering and Instrument Science, Zhejiang University, Hangzhou 310027, ChinaDepartment of Neurology of the Second Affiliated Hospital, Interdisciplinary Institute of Neuroscience and Technology, Zhejiang University School of Medicine, Hangzhou 310020, ChinaDepartment of Neurology, Second Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, Zhejiang, 310009, ChinaDepartment of Neurology of the Second Affiliated Hospital, Interdisciplinary Institute of Neuroscience and Technology, Zhejiang University School of Medicine, Hangzhou 310020, China; Nanhu Brain-computer Interface Institute, Hangzhou 311100, China; MOE Frontier Science Center for Brain Science and Brain-machine Integration, School of Brain Science and Brain Medicine, Zhejiang University, Hangzhou 310058, China; Key Laboratory of Biomedical Engineering of Ministry of Education, College of Biomedical Engineering and Instrument Science, Zhejiang University, Hangzhou 310027, China; NHC and CAMS Key Laboratory of Medical Neurobiology, Zhejiang University, Hangzhou 310058, China; Corresponding authors.Department of Neurology of the Second Affiliated Hospital, Interdisciplinary Institute of Neuroscience and Technology, Zhejiang University School of Medicine, Hangzhou 310020, China; Nanhu Brain-computer Interface Institute, Hangzhou 311100, China; MOE Frontier Science Center for Brain Science and Brain-machine Integration, School of Brain Science and Brain Medicine, Zhejiang University, Hangzhou 310058, China; Key Laboratory of Biomedical Engineering of Ministry of Education, College of Biomedical Engineering and Instrument Science, Zhejiang University, Hangzhou 310027, China; NHC and CAMS Key Laboratory of Medical Neurobiology, Zhejiang University, Hangzhou 310058, China; Corresponding authors.Department of Neurology of the Second Affiliated Hospital, Interdisciplinary Institute of Neuroscience and Technology, Zhejiang University School of Medicine, Hangzhou 310020, China; MOE Frontier Science Center for Brain Science and Brain-machine Integration, School of Brain Science and Brain Medicine, Zhejiang University, Hangzhou 310058, China; NHC and CAMS Key Laboratory of Medical Neurobiology, Zhejiang University, Hangzhou 310058, China; Key Laboratory of Medical Neurobiology of Zhejiang Province, Hangzhou 310020, China; State Key Laboratory of Transvascular Implantation Devices, Hangzhou 310009, China; Corresponding authors.Mammals rely heavily on their auditory system to perceive environmental threats, socially communicate, and care for the young. As an extension of the multiple sensory system including the auditory system, the amygdala evaluates the emotional salience of acoustic stimuli, and mediates its impact on sensory, cognitive, and physiological aspects of emotional processing via the lateral amygdala (LA), basal amygdala (BA), and central amygdala (CeA) nuclei of the amygdala in acoustic domain. However, the functional connections of LA, BA, and CeA with the auditory cortex (AC) and the prefrontal cortex (PFC) remain unclear, particularly at the mesoscale level. Here we employed a novel method called INS-fMRI (Infrared Neural Stimulation combined with high-resolution functional magnetic resonance imaging) in Macaque monkeys, this method permits stimulation of multiple sites within single animals in vivo, so that the relative organization of auditory networks can be studied. We found that: (1) Focal INS stimulation of the amygdala elicited robust and reliable responses in both the AC and the PFC; (2) Amygdala stimulation mainly activated ipsilateral AC and PFC; (3) The stimulation of the amygdala mainly activated the secondary AC, and the dorsolateral PFC; (4) The connection between the amygdala and the cortex is mainly mediated by neurons in LA and BA connection area. Our study further revealed the functional connectivity among the amygdala subnucleus, the auditory cortex and the prefrontal cortex, and will shed light on the research for processing biologically meaningful complex sounds.http://www.sciencedirect.com/science/article/pii/S1053811925004094INS-fMRIAmygdalaAuditory cortexPrefrontal cortexNon-human primate
spellingShingle Qianbing Li
An Ping
Yuqi Feng
Bin Xu
Baorong Zhang
Anna Wang Roe
Lixia Gao
Xinjian Li
Mesoscale functional connectivity of amygdala to the auditory and prefrontal cortex of macaque monkeys revealed by INS-fMRI
NeuroImage
INS-fMRI
Amygdala
Auditory cortex
Prefrontal cortex
Non-human primate
title Mesoscale functional connectivity of amygdala to the auditory and prefrontal cortex of macaque monkeys revealed by INS-fMRI
title_full Mesoscale functional connectivity of amygdala to the auditory and prefrontal cortex of macaque monkeys revealed by INS-fMRI
title_fullStr Mesoscale functional connectivity of amygdala to the auditory and prefrontal cortex of macaque monkeys revealed by INS-fMRI
title_full_unstemmed Mesoscale functional connectivity of amygdala to the auditory and prefrontal cortex of macaque monkeys revealed by INS-fMRI
title_short Mesoscale functional connectivity of amygdala to the auditory and prefrontal cortex of macaque monkeys revealed by INS-fMRI
title_sort mesoscale functional connectivity of amygdala to the auditory and prefrontal cortex of macaque monkeys revealed by ins fmri
topic INS-fMRI
Amygdala
Auditory cortex
Prefrontal cortex
Non-human primate
url http://www.sciencedirect.com/science/article/pii/S1053811925004094
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