Frequency dependent emotion differentiation and directional coupling in amygdala, orbitofrontal and medial prefrontal cortex network with intracranial recordings
The amygdala, orbitofrontal cortex (OFC) and medial prefrontal cortex (mPFC) form a crucial part of the emotion circuit, yet their emotion induced responses and interactions have been poorly investigated with direct intracranial recordings. Such high-fidelity signals can uncover precise spectral dyn...
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Veröffentlicht in: | Molecular psychiatry 2023-04, Vol.28 (4), p.1636-1646 |
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creator | Sonkusare, Saurabh Qiong, Ding Zhao, Yijie Liu, Wei Yang, Ruoqi Mandali, Alekhya Manssuer, Luis Zhang, Chencheng Cao, Chunyan Sun, Bomin Zhan, Shikun Voon, Valerie |
description | The amygdala, orbitofrontal cortex (OFC) and medial prefrontal cortex (mPFC) form a crucial part of the emotion circuit, yet their emotion induced responses and interactions have been poorly investigated with direct intracranial recordings. Such high-fidelity signals can uncover precise spectral dynamics and frequency differences in valence processing allowing novel insights on neuromodulation. Here, leveraging the unique spatio-temporal advantages of intracranial electroencephalography (iEEG) from a cohort of 35 patients with intractable epilepsy (with 71 contacts in amygdala, 31 in OFC and 43 in mPFC), we assessed the spectral dynamics and interactions between the amygdala, OFC and mPFC during an emotional picture viewing task. Task induced activity showed greater broadband gamma activity in the negative condition compared to positive condition in all the three regions. Similarly, beta activity was increased in the negative condition in the amygdala and OFC while decreased in mPFC. Furthermore, beta activity of amygdala showed significant negative association with valence ratings. Critically, model-based computational analyses revealed unidirectional connectivity from mPFC to the amygdala and bidirectional communication between OFC-amygdala and OFC-mPFC. Our findings provide direct neurophysiological evidence for a much-posited model of top-down influence of mPFC over amygdala and a bidirectional influence between OFC and the amygdala. Altogether, in a relatively large sample size with human intracranial neuronal recordings, we highlight valence-dependent spectral dynamics and dyadic coupling within the amygdala-mPFC-OFC network with implications for potential targeted neuromodulation in emotion processing. |
doi_str_mv | 10.1038/s41380-022-01883-2 |
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Such high-fidelity signals can uncover precise spectral dynamics and frequency differences in valence processing allowing novel insights on neuromodulation. Here, leveraging the unique spatio-temporal advantages of intracranial electroencephalography (iEEG) from a cohort of 35 patients with intractable epilepsy (with 71 contacts in amygdala, 31 in OFC and 43 in mPFC), we assessed the spectral dynamics and interactions between the amygdala, OFC and mPFC during an emotional picture viewing task. Task induced activity showed greater broadband gamma activity in the negative condition compared to positive condition in all the three regions. Similarly, beta activity was increased in the negative condition in the amygdala and OFC while decreased in mPFC. Furthermore, beta activity of amygdala showed significant negative association with valence ratings. Critically, model-based computational analyses revealed unidirectional connectivity from mPFC to the amygdala and bidirectional communication between OFC-amygdala and OFC-mPFC. Our findings provide direct neurophysiological evidence for a much-posited model of top-down influence of mPFC over amygdala and a bidirectional influence between OFC and the amygdala. Altogether, in a relatively large sample size with human intracranial neuronal recordings, we highlight valence-dependent spectral dynamics and dyadic coupling within the amygdala-mPFC-OFC network with implications for potential targeted neuromodulation in emotion processing.</description><identifier>ISSN: 1359-4184</identifier><identifier>EISSN: 1476-5578</identifier><identifier>DOI: 10.1038/s41380-022-01883-2</identifier><identifier>PMID: 36460724</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/378 ; 631/443 ; 9/30 ; Amygdala ; Amygdala - physiology ; Behavioral Sciences ; Biological Psychology ; Brain ; EEG ; Electroencephalography ; Emotions ; Emotions - physiology ; Epilepsy ; Frontal Lobe ; Humans ; Medical imaging ; Medicine ; Medicine & Public Health ; Neural networks ; Neural Pathways - physiology ; Neuroimaging ; Neuromodulation ; Neurosciences ; Neurosurgery ; Pharmacotherapy ; Prefrontal cortex ; Prefrontal Cortex - physiology ; Psychiatry ; Temporal lobe ; Visual stimuli</subject><ispartof>Molecular psychiatry, 2023-04, Vol.28 (4), p.1636-1646</ispartof><rights>The Author(s) 2022</rights><rights>2022. The Author(s).</rights><rights>The Author(s) 2022. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). 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Such high-fidelity signals can uncover precise spectral dynamics and frequency differences in valence processing allowing novel insights on neuromodulation. Here, leveraging the unique spatio-temporal advantages of intracranial electroencephalography (iEEG) from a cohort of 35 patients with intractable epilepsy (with 71 contacts in amygdala, 31 in OFC and 43 in mPFC), we assessed the spectral dynamics and interactions between the amygdala, OFC and mPFC during an emotional picture viewing task. Task induced activity showed greater broadband gamma activity in the negative condition compared to positive condition in all the three regions. Similarly, beta activity was increased in the negative condition in the amygdala and OFC while decreased in mPFC. Furthermore, beta activity of amygdala showed significant negative association with valence ratings. Critically, model-based computational analyses revealed unidirectional connectivity from mPFC to the amygdala and bidirectional communication between OFC-amygdala and OFC-mPFC. Our findings provide direct neurophysiological evidence for a much-posited model of top-down influence of mPFC over amygdala and a bidirectional influence between OFC and the amygdala. Altogether, in a relatively large sample size with human intracranial neuronal recordings, we highlight valence-dependent spectral dynamics and dyadic coupling within the amygdala-mPFC-OFC network with implications for potential targeted neuromodulation in emotion processing.</description><subject>631/378</subject><subject>631/443</subject><subject>9/30</subject><subject>Amygdala</subject><subject>Amygdala - physiology</subject><subject>Behavioral Sciences</subject><subject>Biological Psychology</subject><subject>Brain</subject><subject>EEG</subject><subject>Electroencephalography</subject><subject>Emotions</subject><subject>Emotions - physiology</subject><subject>Epilepsy</subject><subject>Frontal Lobe</subject><subject>Humans</subject><subject>Medical imaging</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Neural networks</subject><subject>Neural Pathways - physiology</subject><subject>Neuroimaging</subject><subject>Neuromodulation</subject><subject>Neurosciences</subject><subject>Neurosurgery</subject><subject>Pharmacotherapy</subject><subject>Prefrontal cortex</subject><subject>Prefrontal Cortex - 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physiology</topic><topic>Behavioral Sciences</topic><topic>Biological Psychology</topic><topic>Brain</topic><topic>EEG</topic><topic>Electroencephalography</topic><topic>Emotions</topic><topic>Emotions - physiology</topic><topic>Epilepsy</topic><topic>Frontal Lobe</topic><topic>Humans</topic><topic>Medical imaging</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Neural networks</topic><topic>Neural Pathways - physiology</topic><topic>Neuroimaging</topic><topic>Neuromodulation</topic><topic>Neurosciences</topic><topic>Neurosurgery</topic><topic>Pharmacotherapy</topic><topic>Prefrontal cortex</topic><topic>Prefrontal Cortex - physiology</topic><topic>Psychiatry</topic><topic>Temporal lobe</topic><topic>Visual stimuli</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sonkusare, Saurabh</creatorcontrib><creatorcontrib>Qiong, Ding</creatorcontrib><creatorcontrib>Zhao, Yijie</creatorcontrib><creatorcontrib>Liu, Wei</creatorcontrib><creatorcontrib>Yang, Ruoqi</creatorcontrib><creatorcontrib>Mandali, Alekhya</creatorcontrib><creatorcontrib>Manssuer, Luis</creatorcontrib><creatorcontrib>Zhang, Chencheng</creatorcontrib><creatorcontrib>Cao, Chunyan</creatorcontrib><creatorcontrib>Sun, Bomin</creatorcontrib><creatorcontrib>Zhan, Shikun</creatorcontrib><creatorcontrib>Voon, Valerie</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest Pharma Collection</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Psychology Database</collection><collection>Biological Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular psychiatry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sonkusare, Saurabh</au><au>Qiong, Ding</au><au>Zhao, Yijie</au><au>Liu, Wei</au><au>Yang, Ruoqi</au><au>Mandali, Alekhya</au><au>Manssuer, Luis</au><au>Zhang, Chencheng</au><au>Cao, Chunyan</au><au>Sun, Bomin</au><au>Zhan, Shikun</au><au>Voon, Valerie</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Frequency dependent emotion differentiation and directional coupling in amygdala, orbitofrontal and medial prefrontal cortex network with intracranial recordings</atitle><jtitle>Molecular psychiatry</jtitle><stitle>Mol Psychiatry</stitle><addtitle>Mol Psychiatry</addtitle><date>2023-04-01</date><risdate>2023</risdate><volume>28</volume><issue>4</issue><spage>1636</spage><epage>1646</epage><pages>1636-1646</pages><issn>1359-4184</issn><eissn>1476-5578</eissn><abstract>The amygdala, orbitofrontal cortex (OFC) and medial prefrontal cortex (mPFC) form a crucial part of the emotion circuit, yet their emotion induced responses and interactions have been poorly investigated with direct intracranial recordings. Such high-fidelity signals can uncover precise spectral dynamics and frequency differences in valence processing allowing novel insights on neuromodulation. Here, leveraging the unique spatio-temporal advantages of intracranial electroencephalography (iEEG) from a cohort of 35 patients with intractable epilepsy (with 71 contacts in amygdala, 31 in OFC and 43 in mPFC), we assessed the spectral dynamics and interactions between the amygdala, OFC and mPFC during an emotional picture viewing task. Task induced activity showed greater broadband gamma activity in the negative condition compared to positive condition in all the three regions. Similarly, beta activity was increased in the negative condition in the amygdala and OFC while decreased in mPFC. Furthermore, beta activity of amygdala showed significant negative association with valence ratings. Critically, model-based computational analyses revealed unidirectional connectivity from mPFC to the amygdala and bidirectional communication between OFC-amygdala and OFC-mPFC. Our findings provide direct neurophysiological evidence for a much-posited model of top-down influence of mPFC over amygdala and a bidirectional influence between OFC and the amygdala. Altogether, in a relatively large sample size with human intracranial neuronal recordings, we highlight valence-dependent spectral dynamics and dyadic coupling within the amygdala-mPFC-OFC network with implications for potential targeted neuromodulation in emotion processing.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>36460724</pmid><doi>10.1038/s41380-022-01883-2</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0001-5931-2197</orcidid><orcidid>https://orcid.org/0000-0001-9206-7613</orcidid><orcidid>https://orcid.org/0000-0003-4472-4134</orcidid><orcidid>https://orcid.org/0000-0002-4439-0579</orcidid><orcidid>https://orcid.org/0000-0001-6790-1776</orcidid><orcidid>https://orcid.org/0000-0002-2202-8376</orcidid><orcidid>https://orcid.org/0000-0001-8769-8760</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | 631/378 631/443 9/30 Amygdala Amygdala - physiology Behavioral Sciences Biological Psychology Brain EEG Electroencephalography Emotions Emotions - physiology Epilepsy Frontal Lobe Humans Medical imaging Medicine Medicine & Public Health Neural networks Neural Pathways - physiology Neuroimaging Neuromodulation Neurosciences Neurosurgery Pharmacotherapy Prefrontal cortex Prefrontal Cortex - physiology Psychiatry Temporal lobe Visual stimuli |
title | Frequency dependent emotion differentiation and directional coupling in amygdala, orbitofrontal and medial prefrontal cortex network with intracranial recordings |
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