Neural correlates of human fear conditioning and sources of variability in 2199 individuals
Abstract Pavlovian fear conditioning is a fundamental process in both health and disease. We investigate its neural correlates and sources of variability using harmonized functional magnetic resonance imaging data from 2199 individuals across nine countries, including 1888 healthy individuals and 31...
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2025-08-01
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| author | Joaquim Radua Hannah S. Savage Enric Vilajosana Alec Jamieson Birgit Abler Fredrik Åhs Tom Beckers Narcís Cardoner Josh M. Cisler Juliana B. Diniz Dominik R. Bach Sigrid Elsenbruch Steven G. Greening Daphne J. Holt Antonia N. Kaczkurkin Andreas Keil Merel Kindt Kathrin Koch Kevin S. LaBar Charlene L. Lam Christine L. Larson Tina B. Lonsdorf Christian J. Merz Katie A. McLaughlin Yuval Neria Daniel S. Pine Carien M. van Reekum Alexander J. Shackman Carles Soriano-Mas Victor I. Spoormaker Daniel M. Stout Benjamin Straube Thomas Straube Lauri Tuominen Renée M. Visser Laura Ahumada Volker Arolt Marcelo C. Batistuzzo Paulo R. Bazán Emma E. Biggs Marta Cano Pamela Chavarría-Elizondo Samuel E. Cooper Udo Dannlowski Víctor de la Peña-Arteaga Stephanie N. DeCross Katharina Domschke Mana R. Ehlers John L. Graner Alfons O. Hamm Martin J. Herrmann Ashley A. Huggins Adriane Icenhour Asier Juaneda-Seguí Markus Junghoefer Tilo Kircher Katja Koelkebeck Manuel Kuhn Franziska Labrenz Shmuel M. Lissek Martin Lotze Ulrike Lueken Jürgen Margraf Ignacio Martínez-Zalacaín Robert Moeck Jayne Morriss María Ortuño Andre Pittig Daniel Porta-Casteras Jan Richter Isabelle C. Ridderbusch Winfried Rief Kati Roesmann Jörgen Rosén Alena N. Rußmann Rachel Sjouwerman Jennifer Spohrs Andreas Ströhle Benjamin Suarez-Jimenez Martin Ulrich Hans-Ulrich Wittchen Xi Zhu Lea Waller Henrik Walter Paul M. Thompson Janna Marie Bas-Hoogendam Nynke A. Groenewold Dan J. Stein Nic J. Van der Wee Joseph E. Dunsmoor Andre F. Marquand Ben J. Harrison Miquel A. Fullana |
| author_facet | Joaquim Radua Hannah S. Savage Enric Vilajosana Alec Jamieson Birgit Abler Fredrik Åhs Tom Beckers Narcís Cardoner Josh M. Cisler Juliana B. Diniz Dominik R. Bach Sigrid Elsenbruch Steven G. Greening Daphne J. Holt Antonia N. Kaczkurkin Andreas Keil Merel Kindt Kathrin Koch Kevin S. LaBar Charlene L. Lam Christine L. Larson Tina B. Lonsdorf Christian J. Merz Katie A. McLaughlin Yuval Neria Daniel S. Pine Carien M. van Reekum Alexander J. Shackman Carles Soriano-Mas Victor I. Spoormaker Daniel M. Stout Benjamin Straube Thomas Straube Lauri Tuominen Renée M. Visser Laura Ahumada Volker Arolt Marcelo C. Batistuzzo Paulo R. Bazán Emma E. Biggs Marta Cano Pamela Chavarría-Elizondo Samuel E. Cooper Udo Dannlowski Víctor de la Peña-Arteaga Stephanie N. DeCross Katharina Domschke Mana R. Ehlers John L. Graner Alfons O. Hamm Martin J. Herrmann Ashley A. Huggins Adriane Icenhour Asier Juaneda-Seguí Markus Junghoefer Tilo Kircher Katja Koelkebeck Manuel Kuhn Franziska Labrenz Shmuel M. Lissek Martin Lotze Ulrike Lueken Jürgen Margraf Ignacio Martínez-Zalacaín Robert Moeck Jayne Morriss María Ortuño Andre Pittig Daniel Porta-Casteras Jan Richter Isabelle C. Ridderbusch Winfried Rief Kati Roesmann Jörgen Rosén Alena N. Rußmann Rachel Sjouwerman Jennifer Spohrs Andreas Ströhle Benjamin Suarez-Jimenez Martin Ulrich Hans-Ulrich Wittchen Xi Zhu Lea Waller Henrik Walter Paul M. Thompson Janna Marie Bas-Hoogendam Nynke A. Groenewold Dan J. Stein Nic J. Van der Wee Joseph E. Dunsmoor Andre F. Marquand Ben J. Harrison Miquel A. Fullana |
| author_sort | Joaquim Radua |
| collection | DOAJ |
| description | Abstract Pavlovian fear conditioning is a fundamental process in both health and disease. We investigate its neural correlates and sources of variability using harmonized functional magnetic resonance imaging data from 2199 individuals across nine countries, including 1888 healthy individuals and 311 with anxiety-related or depressive disorders. Using mega-analysis and normative modeling, we show that fear conditioning consistently engages brain regions within the “central autonomic–interoceptive” or “salience” network. Several task variables strongly modulate activity in these regions, contributing to variability in neural responses. Additionally, brain activation patterns differ between healthy individuals and those with anxiety-related or depressive disorders, with distinct profiles characterizing specific disorders such as post-traumatic stress disorder and obsessive-compulsive disorder. While the neural correlates of fear conditioning are highly generalizable at the population level, variability arises from differences in task design and clinical status, highlighting the importance of methodological diversity in capturing fear learning mechanisms. |
| format | Article |
| id | doaj-art-5ec627ee76cd43008786e3e54ca76f35 |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-08-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-5ec627ee76cd43008786e3e54ca76f352025-08-24T11:37:57ZengNature PortfolioNature Communications2041-17232025-08-0116111810.1038/s41467-025-63078-xNeural correlates of human fear conditioning and sources of variability in 2199 individualsJoaquim Radua0Hannah S. Savage1Enric Vilajosana2Alec Jamieson3Birgit Abler4Fredrik Åhs5Tom Beckers6Narcís Cardoner7Josh M. Cisler8Juliana B. Diniz9Dominik R. Bach10Sigrid Elsenbruch11Steven G. Greening12Daphne J. Holt13Antonia N. Kaczkurkin14Andreas Keil15Merel Kindt16Kathrin Koch17Kevin S. LaBar18Charlene L. Lam19Christine L. Larson20Tina B. Lonsdorf21Christian J. Merz22Katie A. McLaughlin23Yuval Neria24Daniel S. Pine25Carien M. van Reekum26Alexander J. Shackman27Carles Soriano-Mas28Victor I. Spoormaker29Daniel M. Stout30Benjamin Straube31Thomas Straube32Lauri Tuominen33Renée M. Visser34Laura Ahumada35Volker Arolt36Marcelo C. Batistuzzo37Paulo R. Bazán38Emma E. Biggs39Marta Cano40Pamela Chavarría-Elizondo41Samuel E. Cooper42Udo Dannlowski43Víctor de la Peña-Arteaga44Stephanie N. DeCross45Katharina Domschke46Mana R. Ehlers47John L. Graner48Alfons O. Hamm49Martin J. Herrmann50Ashley A. Huggins51Adriane Icenhour52Asier Juaneda-Seguí53Markus Junghoefer54Tilo Kircher55Katja Koelkebeck56Manuel Kuhn57Franziska Labrenz58Shmuel M. Lissek59Martin Lotze60Ulrike Lueken61Jürgen Margraf62Ignacio Martínez-Zalacaín63Robert Moeck64Jayne Morriss65María Ortuño66Andre Pittig67Daniel Porta-Casteras68Jan Richter69Isabelle C. Ridderbusch70Winfried Rief71Kati Roesmann72Jörgen Rosén73Alena N. Rußmann74Rachel Sjouwerman75Jennifer Spohrs76Andreas Ströhle77Benjamin Suarez-Jimenez78Martin Ulrich79Hans-Ulrich Wittchen80Xi Zhu81Lea Waller82Henrik Walter83Paul M. Thompson84Janna Marie Bas-Hoogendam85Nynke A. Groenewold86Dan J. Stein87Nic J. Van der Wee88Joseph E. Dunsmoor89Andre F. Marquand90Ben J. Harrison91Miquel A. Fullana92Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS)Donders Institute of Brain, Cognition and Behaviour, Radboud UniversityInstitut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS)Department of Psychiatry, The University of MelbourneDepartment of Psychiatry and Psychotherapy III, Ulm University ClinicDepartment of Psychology and Social Work, Mid Sweden UniversityFaculty of Psychology and Educational SciencesSant Pau Mental Health Group, Institut d’Investigació Biomèdica Sant Pau (IBB-Sant Pau)Department of Psychiatry and Behavioral Sciences, Dell Medical School, University of Texas at AustinDepartment of Psychiatry, Faculdade de Medicina, Universidade de São PauloUniversity of Bonn, Transdisciplinary Research Area “Life and Health”, Hertz Chair for Artificial Intelligence and Neuroscience, Institute of Computer Science, Medical Faculty, Institute of Experimental Epileptology and Cognition ResearchDepartment of Medical Psychology and Medical Sociology, Medical Faculty, Ruhr UniversityBrain & Cognitive Sciences, Department of Psychology, University of ManitobaDepartment of Psychiatry, Massachusetts General HospitalDepartment of Psychology, Vanderbilt UniversityDepartment of Psychology, University of FloridaDepartment of Psychology, University of AmsterdamSchool of Medicine and Health, Technical University of MunichCenter for Cognitive Neuroscience, Duke UniversityLaboratory of Clinical Psychology & Affective Neuroscience, Department of Psychology, University of Hong KongUniversity of Wisconsin-Milwaukee, Department of PsychologyBiological Psychology and Cognitive Neuroscience, Bielefeld UniversityDepartment of Cognitive Psychology, Institute of Cognitive Neuroscience, Ruhr University BochumDepartment of Psychology, Harvard UniversityDepartment of Psychiatry, Columbia University Irving Medical CenterSection on Development and Affective Neuroscience, National Institute of Mental HealthSchool of Psychology and Clinical Language Sciences, University of ReadingDepartment of Psychology, Neuroscience and Cognitive Science Program, University of MarylandCentro de Investigación Biomédica en Red de Salud Mental (CIBERSAM), Instituto de Salud Carlos III (ISCIII)Max Planck Institute of PsychiatryUniversity of CaliforniaDepartment of Psychiatry and Psychotherapy, University of MarburgInstitute of Medical Psychology and Systems Neuroscience, University of MuensterUniversity of Ottawa Institute of Mental Health Research at the RoyalDepartment of Psychology, University of AmsterdamDepartment of Psychology, University of FloridaInstitute for Translational Psychiatry, University of MünsterDepartment of Psychiatry, Faculdade de Medicina, Universidade de São PauloRadiology Institute, Faculdade de Medicina, Universidade de São PauloFaculty of Psychology and Educational SciencesSant Pau Mental Health Group, Institut d’Investigació Biomèdica Sant Pau (IBB-Sant Pau)Psychiatry and Mental Health Group, Neuroscience Program, Institut d’Investigació Biomèdica de Bellvitge - IDIBELLDepartment of Psychiatry and Behavioral Sciences, University of Texas at AustinInstitute for Translational Psychiatry, University of MünsterSant Pau Mental Health Group, Institut d’Investigació Biomèdica Sant Pau (IBB-Sant Pau)Department of Psychology, Harvard UniversityDepartment of Psychiatry and Psychotherapy, Medical Center - University of Freiburg, Faculty of Medicine, University of FreiburgBiological Psychology and Cognitive Neuroscience, Bielefeld UniversityCenter for Cognitive Neuroscience, Duke UniversityDepartment of Psychology, University of GreifswaldDepartment of Psychiatry, Psychosomatics and Psychotherapy, University of WürzburgDepartment of Psychology, University of ArizonaDepartment of Medical Psychology and Medical Sociology, Medical Faculty, Ruhr UniversityPsychiatry and Mental Health Group, Neuroscience Program, Institut d’Investigació Biomèdica de Bellvitge - IDIBELLOtto-Creutzfeld-Center of Cognitive Neuroscience, University of MünsterDepartment of Psychiatry and Psychotherapy, University of MarburgBielefeld University, Medical School and University Medical Center OWL, Protestant Hospital of the Bethel Foundation, Department of Psychiatry and PsychotherapyInstitute for Systems Neuroscience, University Medical Center Hamburg EppendorfDepartment of Medical Psychology and Medical Sociology, Medical Faculty, Ruhr UniversityDepartment of Psychology, University of MinnesotaDiagnostic Radiology, University Medicine GreifswaldGerman Center of Mental Health (DZPG), partner site Berlin/PotsdamMental Health Research and Treatment Center, Ruhr-University Bochum (FBZ) and German Center for Mental Health (DZPG), partner site Bochum/MarburgPsychiatry and Mental Health Group, Neuroscience Program, Institut d’Investigació Biomèdica de Bellvitge - IDIBELLInstitute of Medical Psychology and Systems Neuroscience, University of MuensterSchool of Psychology, Faculty of Environmental and Life Sciences, University of SouthamptonInstitut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS)Translational Psychotherapy, Institute for Psychology, University of GöttingenSant Pau Mental Health Group, Institut d’Investigació Biomèdica Sant Pau (IBB-Sant Pau)Department of Experimental Psychopathology, University of HildesheimDepartment of Psychiatry and Psychotherapy, University of MarburgDivision of Clinical Psychology and Psychotherapy, University of MarburgInstitute for Biomagnetism and Biosignal analysis, University of MünsterDepartment of Clinical Neuroscience, Karolinska InstitutetInstitute for Systems Neuroscience, University Medical Center Hamburg EppendorfInstitute for Systems Neuroscience, University Medical Center Hamburg EppendorfDepartment of Child and Adolescent Psychiatry and Psychotherapy, Ulm University Medical CentreDepartment of Psychiatry and Psychotherapy, Charité - Universitätsmedizin BerlinDepartment of Neuroscience, University of Rochester Medical CenterDepartment of Psychiatry and Psychotherapy III, Ulm University ClinicPsychiatric University Hospital, Ludwig-Maximilians-University MünchenDepartment of Psychiatry, Columbia University Irving Medical CenterDepartment of Psychiatry and Psychotherapy, Charité - Universitätsmedizin BerlinGerman Center of Mental Health (DZPG), partner site Berlin/PotsdamImaging Genetics Center, Stevens Neuroimaging & Informatics Institute, Keck School of Medicine, University of Southern CaliforniaDevelopmental and Educational Psychology, Institute of Psychology, Leiden UniversityDepartment of Psychiatry and Mental Health, Neuroscience Institute, University of Cape TownSAMRC Unit on Risk & Resilience in Mental Disorders, Department of Psychiatry and Mental Health, Neuroscience Institute, University of Cape TownLeiden Institute for Brain and Cognition, Leiden University Medical CenterDepartment of Neuroscience, University of Texas at AustinDonders Institute of Brain, Cognition and Behaviour, Radboud UniversityDepartment of Psychiatry, The University of MelbourneInstitut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS)Abstract Pavlovian fear conditioning is a fundamental process in both health and disease. We investigate its neural correlates and sources of variability using harmonized functional magnetic resonance imaging data from 2199 individuals across nine countries, including 1888 healthy individuals and 311 with anxiety-related or depressive disorders. Using mega-analysis and normative modeling, we show that fear conditioning consistently engages brain regions within the “central autonomic–interoceptive” or “salience” network. Several task variables strongly modulate activity in these regions, contributing to variability in neural responses. Additionally, brain activation patterns differ between healthy individuals and those with anxiety-related or depressive disorders, with distinct profiles characterizing specific disorders such as post-traumatic stress disorder and obsessive-compulsive disorder. While the neural correlates of fear conditioning are highly generalizable at the population level, variability arises from differences in task design and clinical status, highlighting the importance of methodological diversity in capturing fear learning mechanisms.https://doi.org/10.1038/s41467-025-63078-x |
| spellingShingle | Joaquim Radua Hannah S. Savage Enric Vilajosana Alec Jamieson Birgit Abler Fredrik Åhs Tom Beckers Narcís Cardoner Josh M. Cisler Juliana B. Diniz Dominik R. Bach Sigrid Elsenbruch Steven G. Greening Daphne J. Holt Antonia N. Kaczkurkin Andreas Keil Merel Kindt Kathrin Koch Kevin S. LaBar Charlene L. Lam Christine L. Larson Tina B. Lonsdorf Christian J. Merz Katie A. McLaughlin Yuval Neria Daniel S. Pine Carien M. van Reekum Alexander J. Shackman Carles Soriano-Mas Victor I. Spoormaker Daniel M. Stout Benjamin Straube Thomas Straube Lauri Tuominen Renée M. Visser Laura Ahumada Volker Arolt Marcelo C. Batistuzzo Paulo R. Bazán Emma E. Biggs Marta Cano Pamela Chavarría-Elizondo Samuel E. Cooper Udo Dannlowski Víctor de la Peña-Arteaga Stephanie N. DeCross Katharina Domschke Mana R. Ehlers John L. Graner Alfons O. Hamm Martin J. Herrmann Ashley A. Huggins Adriane Icenhour Asier Juaneda-Seguí Markus Junghoefer Tilo Kircher Katja Koelkebeck Manuel Kuhn Franziska Labrenz Shmuel M. Lissek Martin Lotze Ulrike Lueken Jürgen Margraf Ignacio Martínez-Zalacaín Robert Moeck Jayne Morriss María Ortuño Andre Pittig Daniel Porta-Casteras Jan Richter Isabelle C. Ridderbusch Winfried Rief Kati Roesmann Jörgen Rosén Alena N. Rußmann Rachel Sjouwerman Jennifer Spohrs Andreas Ströhle Benjamin Suarez-Jimenez Martin Ulrich Hans-Ulrich Wittchen Xi Zhu Lea Waller Henrik Walter Paul M. Thompson Janna Marie Bas-Hoogendam Nynke A. Groenewold Dan J. Stein Nic J. Van der Wee Joseph E. Dunsmoor Andre F. Marquand Ben J. Harrison Miquel A. Fullana Neural correlates of human fear conditioning and sources of variability in 2199 individuals Nature Communications |
| title | Neural correlates of human fear conditioning and sources of variability in 2199 individuals |
| title_full | Neural correlates of human fear conditioning and sources of variability in 2199 individuals |
| title_fullStr | Neural correlates of human fear conditioning and sources of variability in 2199 individuals |
| title_full_unstemmed | Neural correlates of human fear conditioning and sources of variability in 2199 individuals |
| title_short | Neural correlates of human fear conditioning and sources of variability in 2199 individuals |
| title_sort | neural correlates of human fear conditioning and sources of variability in 2199 individuals |
| url | https://doi.org/10.1038/s41467-025-63078-x |
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