GABAA receptor availability relates to emotion-induced BOLD responses in the medial prefrontal cortex: simultaneous fMRI/PET with [11C]flumazenil

IntroductionThe fMRI BOLD response to emotional stimuli highlighting the role of the medial prefrontal cortex (MPFC) has been thoroughly investigated. Recently, the relationship between emotion processing and GABA levels has been studied using MPFC proton magnetic resonance spectroscopy (1H-MRS). Ho...

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Main Authors: Alexander Heinzel, Jörg Mauler, Hans Herzog, Frank Boers, Felix M. Mottaghy, Karl-Josef Langen, Jürgen Scheins, Christoph Lerche, Bernd Neumaier, Georg Northoff, N. Jon Shah
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-09-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2023.1027697/full
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author Alexander Heinzel
Alexander Heinzel
Alexander Heinzel
Jörg Mauler
Hans Herzog
Frank Boers
Felix M. Mottaghy
Felix M. Mottaghy
Karl-Josef Langen
Karl-Josef Langen
Jürgen Scheins
Christoph Lerche
Bernd Neumaier
Georg Northoff
N. Jon Shah
N. Jon Shah
N. Jon Shah
N. Jon Shah
author_facet Alexander Heinzel
Alexander Heinzel
Alexander Heinzel
Jörg Mauler
Hans Herzog
Frank Boers
Felix M. Mottaghy
Felix M. Mottaghy
Karl-Josef Langen
Karl-Josef Langen
Jürgen Scheins
Christoph Lerche
Bernd Neumaier
Georg Northoff
N. Jon Shah
N. Jon Shah
N. Jon Shah
N. Jon Shah
author_sort Alexander Heinzel
collection DOAJ
description IntroductionThe fMRI BOLD response to emotional stimuli highlighting the role of the medial prefrontal cortex (MPFC) has been thoroughly investigated. Recently, the relationship between emotion processing and GABA levels has been studied using MPFC proton magnetic resonance spectroscopy (1H-MRS). However, the role of GABAA receptors in the MPFC during emotion processing remains unexplored.MethodsUsing [11C]flumazenil PET, we investigated the relationship between the binding potential of GABAA receptors and emotion processing as measured using simultaneous fMRI BOLD. We hypothesized a correlation between the percent signal change in the BOLD signal and the binding potential of GABAA receptors in the MPFC. In a combined simultaneous fMRI and [11C]flumazenil-PET study, we analyzed the data from 15 healthy subjects using visual emotional stimuli. Our task comprised two types of emotional processing: passive viewing and appraisal. Following the administration of a bolus plus infusion protocol, PET and fMRI data were simultaneously acquired in a hybrid 3 T MR-BrainPET.ResultsWe found a differential correlation of BOLD percent signal change with [11C]flumazenil binding potential in the MPFC. Specifically, [11C]flumazenil binding potential in the ventromedial prefrontal cortex (vMPFC) correlated with passive viewing of emotionally valenced pictures. In contrast, the [11C]flumazenil binding potential and the BOLD signal induced by picture appraisal did show a correlation in the paracingulate gyrus.ConclusionOur data deliver first evidence for a relationship between MPFC GABAA receptors and emotion processing in the same region. Moreover, we observed that GABAA receptors appear to play different roles in emotion processing in the vMPFC (passive viewing) and paracingulate gyrus (appraisal).
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spelling doaj.art-c2b612de1ab24b5e9897b2637fc65bbc2023-09-12T17:33:35ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2023-09-011710.3389/fnins.2023.10276971027697GABAA receptor availability relates to emotion-induced BOLD responses in the medial prefrontal cortex: simultaneous fMRI/PET with [11C]flumazenilAlexander Heinzel0Alexander Heinzel1Alexander Heinzel2Jörg Mauler3Hans Herzog4Frank Boers5Felix M. Mottaghy6Felix M. Mottaghy7Karl-Josef Langen8Karl-Josef Langen9Jürgen Scheins10Christoph Lerche11Bernd Neumaier12Georg Northoff13N. Jon Shah14N. Jon Shah15N. Jon Shah16N. Jon Shah17Institute of Neuroscience and Medicine – 4, Forschungszentrum Jülich, Jülich, GermanyDepartment of Nuclear Medicine, Medical Faculty RWTH Aachen, Aachen, GermanyDepartment of Nuclear medicine, University Hospital Halle, Halle (Saale), GermanyInstitute of Neuroscience and Medicine – 4, Forschungszentrum Jülich, Jülich, GermanyInstitute of Neuroscience and Medicine – 4, Forschungszentrum Jülich, Jülich, GermanyInstitute of Neuroscience and Medicine – 4, Forschungszentrum Jülich, Jülich, GermanyDepartment of Nuclear Medicine, Medical Faculty RWTH Aachen, Aachen, GermanyDepartment of Radiology and Nuclear Medicine, Maastricht University Medical Centre, Maastricht, NetherlandsInstitute of Neuroscience and Medicine – 4, Forschungszentrum Jülich, Jülich, GermanyDepartment of Nuclear Medicine, Medical Faculty RWTH Aachen, Aachen, GermanyInstitute of Neuroscience and Medicine – 4, Forschungszentrum Jülich, Jülich, GermanyInstitute of Neuroscience and Medicine – 4, Forschungszentrum Jülich, Jülich, GermanyInstitute of Neuroscience and Medicine – 5, Forschungszentrum Jülich, Jülich, GermanyMind, Brain Imaging and Neuroethics Research Unit, Institute of Mental Health, Royal Ottawa Mental Health Centre and University of Ottawa, Ottawa, ON, CanadaInstitute of Neuroscience and Medicine – 4, Forschungszentrum Jülich, Jülich, GermanyInstitute of Neuroscience and Medicine – 11, Forschungszentrum Jülich, Jülich, GermanyJARA – BRAIN – Translational Medicine, Aachen, GermanyDepartment of Neurology, RWTH Aachen University, Aachen, GermanyIntroductionThe fMRI BOLD response to emotional stimuli highlighting the role of the medial prefrontal cortex (MPFC) has been thoroughly investigated. Recently, the relationship between emotion processing and GABA levels has been studied using MPFC proton magnetic resonance spectroscopy (1H-MRS). However, the role of GABAA receptors in the MPFC during emotion processing remains unexplored.MethodsUsing [11C]flumazenil PET, we investigated the relationship between the binding potential of GABAA receptors and emotion processing as measured using simultaneous fMRI BOLD. We hypothesized a correlation between the percent signal change in the BOLD signal and the binding potential of GABAA receptors in the MPFC. In a combined simultaneous fMRI and [11C]flumazenil-PET study, we analyzed the data from 15 healthy subjects using visual emotional stimuli. Our task comprised two types of emotional processing: passive viewing and appraisal. Following the administration of a bolus plus infusion protocol, PET and fMRI data were simultaneously acquired in a hybrid 3 T MR-BrainPET.ResultsWe found a differential correlation of BOLD percent signal change with [11C]flumazenil binding potential in the MPFC. Specifically, [11C]flumazenil binding potential in the ventromedial prefrontal cortex (vMPFC) correlated with passive viewing of emotionally valenced pictures. In contrast, the [11C]flumazenil binding potential and the BOLD signal induced by picture appraisal did show a correlation in the paracingulate gyrus.ConclusionOur data deliver first evidence for a relationship between MPFC GABAA receptors and emotion processing in the same region. Moreover, we observed that GABAA receptors appear to play different roles in emotion processing in the vMPFC (passive viewing) and paracingulate gyrus (appraisal).https://www.frontiersin.org/articles/10.3389/fnins.2023.1027697/fullsimultaneous fMRI/PETGABAA receptoremotion[11C]flumazenilBOLD signalbinding potential
spellingShingle Alexander Heinzel
Alexander Heinzel
Alexander Heinzel
Jörg Mauler
Hans Herzog
Frank Boers
Felix M. Mottaghy
Felix M. Mottaghy
Karl-Josef Langen
Karl-Josef Langen
Jürgen Scheins
Christoph Lerche
Bernd Neumaier
Georg Northoff
N. Jon Shah
N. Jon Shah
N. Jon Shah
N. Jon Shah
GABAA receptor availability relates to emotion-induced BOLD responses in the medial prefrontal cortex: simultaneous fMRI/PET with [11C]flumazenil
Frontiers in Neuroscience
simultaneous fMRI/PET
GABAA receptor
emotion
[11C]flumazenil
BOLD signal
binding potential
title GABAA receptor availability relates to emotion-induced BOLD responses in the medial prefrontal cortex: simultaneous fMRI/PET with [11C]flumazenil
title_full GABAA receptor availability relates to emotion-induced BOLD responses in the medial prefrontal cortex: simultaneous fMRI/PET with [11C]flumazenil
title_fullStr GABAA receptor availability relates to emotion-induced BOLD responses in the medial prefrontal cortex: simultaneous fMRI/PET with [11C]flumazenil
title_full_unstemmed GABAA receptor availability relates to emotion-induced BOLD responses in the medial prefrontal cortex: simultaneous fMRI/PET with [11C]flumazenil
title_short GABAA receptor availability relates to emotion-induced BOLD responses in the medial prefrontal cortex: simultaneous fMRI/PET with [11C]flumazenil
title_sort gabaa receptor availability relates to emotion induced bold responses in the medial prefrontal cortex simultaneous fmri pet with 11c flumazenil
topic simultaneous fMRI/PET
GABAA receptor
emotion
[11C]flumazenil
BOLD signal
binding potential
url https://www.frontiersin.org/articles/10.3389/fnins.2023.1027697/full
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