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Modulatory effects of dynamic fMRI-based neurofeedback on emotion regulation networks in adolescent females
Research has shown that difficulties with emotion regulation abilities in childhood and adolescence increase the risk for developing symptoms of mental disorders, e.g anxiety. We investigated whether functional magnetic resonance imaging (fMRI)-based neurofeedback (NF) can modulate brain networks su...
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Published in: | NeuroImage (Orlando, Fla.) Fla.), 2020-10, Vol.220, p.117053-117053, Article 117053 |
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description | Research has shown that difficulties with emotion regulation abilities in childhood and adolescence increase the risk for developing symptoms of mental disorders, e.g anxiety. We investigated whether functional magnetic resonance imaging (fMRI)-based neurofeedback (NF) can modulate brain networks supporting emotion regulation abilities in adolescent females.
We performed three experiments (Experiment 1: N = 18; Experiment 2: N = 30; Experiment 3: N = 20). We first compared different NF implementations regarding their effectiveness of modulating prefrontal cortex (PFC)-amygdala functional connectivity (fc). Further we assessed the effects of fc-NF on neural measures, emotional/metacognitive measures and their associations. Finally, we probed the mechanism underlying fc-NF by examining concentrations of inhibitory and excitatory neurotransmitters.
Results showed that NF implementations differentially modulate PFC-amygdala fc. Using the most effective NF implementation we observed important relationships between neural and emotional/metacognitive measures, such as practice-related change in fc was related with change in thought control ability. Further, we found that the relationship between state anxiety prior to the MRI session and the effect of fc-NF was moderated by GABA concentrations in the PFC and anterior cingulate cortex.
To conclude, we were able to show that fc-NF can be used in adolescent females to shape neural and emotional/metacognitive measures underlying emotion regulation. We further show that neurotransmitter concentrations moderate fc–NF–effects.
•Neurofeedback implementations differentially modulate PFC-amygdala connectivity.•Functional connectivity neurofeedback affect measures of emotion regulation.•Neurotransmitter concentrations moderate neurofeedback effects. |
doi_str_mv | 10.1016/j.neuroimage.2020.117053 |
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We performed three experiments (Experiment 1: N = 18; Experiment 2: N = 30; Experiment 3: N = 20). We first compared different NF implementations regarding their effectiveness of modulating prefrontal cortex (PFC)-amygdala functional connectivity (fc). Further we assessed the effects of fc-NF on neural measures, emotional/metacognitive measures and their associations. Finally, we probed the mechanism underlying fc-NF by examining concentrations of inhibitory and excitatory neurotransmitters.
Results showed that NF implementations differentially modulate PFC-amygdala fc. Using the most effective NF implementation we observed important relationships between neural and emotional/metacognitive measures, such as practice-related change in fc was related with change in thought control ability. Further, we found that the relationship between state anxiety prior to the MRI session and the effect of fc-NF was moderated by GABA concentrations in the PFC and anterior cingulate cortex.
To conclude, we were able to show that fc-NF can be used in adolescent females to shape neural and emotional/metacognitive measures underlying emotion regulation. We further show that neurotransmitter concentrations moderate fc–NF–effects.
•Neurofeedback implementations differentially modulate PFC-amygdala connectivity.•Functional connectivity neurofeedback affect measures of emotion regulation.•Neurotransmitter concentrations moderate neurofeedback effects.</description><identifier>ISSN: 1053-8119</identifier><identifier>EISSN: 1095-9572</identifier><identifier>DOI: 10.1016/j.neuroimage.2020.117053</identifier><identifier>PMID: 32574803</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Adolescence ; Adolescent ; Amygdala ; Anxiety ; Biofeedback ; Brain ; Brain - diagnostic imaging ; Brain mapping ; Brain Mapping - methods ; Brain-computer-interface ; Child development ; Children ; Cognition - physiology ; Cognitive ability ; Connectivity ; Cortex (cingulate) ; Electroencephalography ; Emotion regulation ; Emotional Regulation - physiology ; Emotions ; Experiments ; Feedback ; Female ; Females ; Functional magnetic resonance imaging ; Humans ; Magnetic resonance imaging ; Magnetic Resonance Imaging - methods ; Magnetic resonance spectroscopy ; Mental disorders ; Metacognition ; Neural networks ; Neurofeedback ; Neurofeedback - methods ; Neuroimaging ; Neurotransmitters ; Prefrontal cortex ; Questionnaires ; Teenagers ; γ-Aminobutyric acid</subject><ispartof>NeuroImage (Orlando, Fla.), 2020-10, Vol.220, p.117053-117053, Article 117053</ispartof><rights>2020 The Author(s)</rights><rights>Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.</rights><rights>2020. The Author(s)</rights><rights>2020 The Author(s) 2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c573t-d2ccacb6fbf99e7698bec7c9996ba2fac7b6966a65af1bb05fecb85f3ce7ab8b3</citedby><cites>FETCH-LOGICAL-c573t-d2ccacb6fbf99e7698bec7c9996ba2fac7b6966a65af1bb05fecb85f3ce7ab8b3</cites><orcidid>0000-0002-3451-0696 ; 0000-0002-0705-9297 ; 0000-0002-0576-1525</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32574803$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zich, Catharina</creatorcontrib><creatorcontrib>Johnstone, Nicola</creatorcontrib><creatorcontrib>Lührs, Michael</creatorcontrib><creatorcontrib>Lisk, Stephen</creatorcontrib><creatorcontrib>Haller, Simone PW</creatorcontrib><creatorcontrib>Lipp, Annalisa</creatorcontrib><creatorcontrib>Lau, Jennifer YF</creatorcontrib><creatorcontrib>Kadosh, Kathrin Cohen</creatorcontrib><title>Modulatory effects of dynamic fMRI-based neurofeedback on emotion regulation networks in adolescent females</title><title>NeuroImage (Orlando, Fla.)</title><addtitle>Neuroimage</addtitle><description>Research has shown that difficulties with emotion regulation abilities in childhood and adolescence increase the risk for developing symptoms of mental disorders, e.g anxiety. We investigated whether functional magnetic resonance imaging (fMRI)-based neurofeedback (NF) can modulate brain networks supporting emotion regulation abilities in adolescent females.
We performed three experiments (Experiment 1: N = 18; Experiment 2: N = 30; Experiment 3: N = 20). We first compared different NF implementations regarding their effectiveness of modulating prefrontal cortex (PFC)-amygdala functional connectivity (fc). Further we assessed the effects of fc-NF on neural measures, emotional/metacognitive measures and their associations. Finally, we probed the mechanism underlying fc-NF by examining concentrations of inhibitory and excitatory neurotransmitters.
Results showed that NF implementations differentially modulate PFC-amygdala fc. Using the most effective NF implementation we observed important relationships between neural and emotional/metacognitive measures, such as practice-related change in fc was related with change in thought control ability. Further, we found that the relationship between state anxiety prior to the MRI session and the effect of fc-NF was moderated by GABA concentrations in the PFC and anterior cingulate cortex.
To conclude, we were able to show that fc-NF can be used in adolescent females to shape neural and emotional/metacognitive measures underlying emotion regulation. We further show that neurotransmitter concentrations moderate fc–NF–effects.
•Neurofeedback implementations differentially modulate PFC-amygdala connectivity.•Functional connectivity neurofeedback affect measures of emotion regulation.•Neurotransmitter concentrations moderate neurofeedback effects.</description><subject>Adolescence</subject><subject>Adolescent</subject><subject>Amygdala</subject><subject>Anxiety</subject><subject>Biofeedback</subject><subject>Brain</subject><subject>Brain - diagnostic imaging</subject><subject>Brain mapping</subject><subject>Brain Mapping - methods</subject><subject>Brain-computer-interface</subject><subject>Child development</subject><subject>Children</subject><subject>Cognition - physiology</subject><subject>Cognitive ability</subject><subject>Connectivity</subject><subject>Cortex (cingulate)</subject><subject>Electroencephalography</subject><subject>Emotion regulation</subject><subject>Emotional Regulation - physiology</subject><subject>Emotions</subject><subject>Experiments</subject><subject>Feedback</subject><subject>Female</subject><subject>Females</subject><subject>Functional magnetic resonance imaging</subject><subject>Humans</subject><subject>Magnetic resonance imaging</subject><subject>Magnetic Resonance Imaging - methods</subject><subject>Magnetic resonance spectroscopy</subject><subject>Mental disorders</subject><subject>Metacognition</subject><subject>Neural networks</subject><subject>Neurofeedback</subject><subject>Neurofeedback - methods</subject><subject>Neuroimaging</subject><subject>Neurotransmitters</subject><subject>Prefrontal cortex</subject><subject>Questionnaires</subject><subject>Teenagers</subject><subject>γ-Aminobutyric acid</subject><issn>1053-8119</issn><issn>1095-9572</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNqFUsFu1DAQjRCIloVfQJa4cMlix7FjX5CgomWlVkgIzpbtjBdnk7jYSav9e5ymFMqF04zGb97MPL-iQARvCSb8XbcdYY7BD3oP2wpXuUwazOiT4pRgyUrJmurpkjNaCkLkSfEipQ5jLEktnhcntGJNLTA9LQ5XoZ17PYV4ROAc2Cmh4FB7HPXgLXJXX3el0QladDfRAbRG2wMKI4IhTD7HCPuFYUlHmG5DPCTkR6Tb0EOyME7IwaBz_rJ45nSf4NV93BTfzz99O_tcXn652J19uCwta-hUtpW12hrujJMSGi6FAdtYKSU3unLaNoZLzjVn2hFjMMtbG8EctdBoIwzdFLuVtw26U9cxyxSPKmiv7goh7pWOk7c9KEqrSjaO15zzWjhmHNbGWYm5IwIIzlzvV67r2QzQLudE3T8iffwy-h9qH25Uk29hlGeCt_cEMfycIU1q8FmVvtcjhDmpqiZc1lTwKkPf_APtwhzHLFVG1ZIzhjPlphArysaQUgT3sAzBanGH6tQfd6jFHWp1R259_fcxD42_7ZABH1cA5O-58RBVsh5GC62P2RpZP___Kb8A_BHUKg</recordid><startdate>20201015</startdate><enddate>20201015</enddate><creator>Zich, Catharina</creator><creator>Johnstone, Nicola</creator><creator>Lührs, Michael</creator><creator>Lisk, Stephen</creator><creator>Haller, Simone PW</creator><creator>Lipp, Annalisa</creator><creator>Lau, Jennifer YF</creator><creator>Kadosh, Kathrin Cohen</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><general>Academic Press</general><general>Elsevier</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-3451-0696</orcidid><orcidid>https://orcid.org/0000-0002-0705-9297</orcidid><orcidid>https://orcid.org/0000-0002-0576-1525</orcidid></search><sort><creationdate>20201015</creationdate><title>Modulatory effects of dynamic fMRI-based neurofeedback on emotion regulation networks in adolescent females</title><author>Zich, Catharina ; Johnstone, Nicola ; Lührs, Michael ; Lisk, Stephen ; Haller, Simone PW ; Lipp, Annalisa ; Lau, Jennifer YF ; Kadosh, Kathrin Cohen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c573t-d2ccacb6fbf99e7698bec7c9996ba2fac7b6966a65af1bb05fecb85f3ce7ab8b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Adolescence</topic><topic>Adolescent</topic><topic>Amygdala</topic><topic>Anxiety</topic><topic>Biofeedback</topic><topic>Brain</topic><topic>Brain - diagnostic imaging</topic><topic>Brain mapping</topic><topic>Brain Mapping - methods</topic><topic>Brain-computer-interface</topic><topic>Child development</topic><topic>Children</topic><topic>Cognition - physiology</topic><topic>Cognitive ability</topic><topic>Connectivity</topic><topic>Cortex (cingulate)</topic><topic>Electroencephalography</topic><topic>Emotion regulation</topic><topic>Emotional Regulation - physiology</topic><topic>Emotions</topic><topic>Experiments</topic><topic>Feedback</topic><topic>Female</topic><topic>Females</topic><topic>Functional magnetic resonance imaging</topic><topic>Humans</topic><topic>Magnetic resonance imaging</topic><topic>Magnetic Resonance Imaging - methods</topic><topic>Magnetic resonance spectroscopy</topic><topic>Mental disorders</topic><topic>Metacognition</topic><topic>Neural networks</topic><topic>Neurofeedback</topic><topic>Neurofeedback - methods</topic><topic>Neuroimaging</topic><topic>Neurotransmitters</topic><topic>Prefrontal cortex</topic><topic>Questionnaires</topic><topic>Teenagers</topic><topic>γ-Aminobutyric acid</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zich, Catharina</creatorcontrib><creatorcontrib>Johnstone, Nicola</creatorcontrib><creatorcontrib>Lührs, Michael</creatorcontrib><creatorcontrib>Lisk, Stephen</creatorcontrib><creatorcontrib>Haller, Simone PW</creatorcontrib><creatorcontrib>Lipp, Annalisa</creatorcontrib><creatorcontrib>Lau, Jennifer YF</creatorcontrib><creatorcontrib>Kadosh, Kathrin Cohen</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</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>ProQuest - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>NeuroImage (Orlando, Fla.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zich, Catharina</au><au>Johnstone, Nicola</au><au>Lührs, Michael</au><au>Lisk, Stephen</au><au>Haller, Simone PW</au><au>Lipp, Annalisa</au><au>Lau, Jennifer YF</au><au>Kadosh, Kathrin Cohen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Modulatory effects of dynamic fMRI-based neurofeedback on emotion regulation networks in adolescent females</atitle><jtitle>NeuroImage (Orlando, Fla.)</jtitle><addtitle>Neuroimage</addtitle><date>2020-10-15</date><risdate>2020</risdate><volume>220</volume><spage>117053</spage><epage>117053</epage><pages>117053-117053</pages><artnum>117053</artnum><issn>1053-8119</issn><eissn>1095-9572</eissn><abstract>Research has shown that difficulties with emotion regulation abilities in childhood and adolescence increase the risk for developing symptoms of mental disorders, e.g anxiety. We investigated whether functional magnetic resonance imaging (fMRI)-based neurofeedback (NF) can modulate brain networks supporting emotion regulation abilities in adolescent females.
We performed three experiments (Experiment 1: N = 18; Experiment 2: N = 30; Experiment 3: N = 20). We first compared different NF implementations regarding their effectiveness of modulating prefrontal cortex (PFC)-amygdala functional connectivity (fc). Further we assessed the effects of fc-NF on neural measures, emotional/metacognitive measures and their associations. Finally, we probed the mechanism underlying fc-NF by examining concentrations of inhibitory and excitatory neurotransmitters.
Results showed that NF implementations differentially modulate PFC-amygdala fc. Using the most effective NF implementation we observed important relationships between neural and emotional/metacognitive measures, such as practice-related change in fc was related with change in thought control ability. Further, we found that the relationship between state anxiety prior to the MRI session and the effect of fc-NF was moderated by GABA concentrations in the PFC and anterior cingulate cortex.
To conclude, we were able to show that fc-NF can be used in adolescent females to shape neural and emotional/metacognitive measures underlying emotion regulation. We further show that neurotransmitter concentrations moderate fc–NF–effects.
•Neurofeedback implementations differentially modulate PFC-amygdala connectivity.•Functional connectivity neurofeedback affect measures of emotion regulation.•Neurotransmitter concentrations moderate neurofeedback effects.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>32574803</pmid><doi>10.1016/j.neuroimage.2020.117053</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-3451-0696</orcidid><orcidid>https://orcid.org/0000-0002-0705-9297</orcidid><orcidid>https://orcid.org/0000-0002-0576-1525</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adolescence Adolescent Amygdala Anxiety Biofeedback Brain Brain - diagnostic imaging Brain mapping Brain Mapping - methods Brain-computer-interface Child development Children Cognition - physiology Cognitive ability Connectivity Cortex (cingulate) Electroencephalography Emotion regulation Emotional Regulation - physiology Emotions Experiments Feedback Female Females Functional magnetic resonance imaging Humans Magnetic resonance imaging Magnetic Resonance Imaging - methods Magnetic resonance spectroscopy Mental disorders Metacognition Neural networks Neurofeedback Neurofeedback - methods Neuroimaging Neurotransmitters Prefrontal cortex Questionnaires Teenagers γ-Aminobutyric acid |
title | Modulatory effects of dynamic fMRI-based neurofeedback on emotion regulation networks in adolescent females |
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