iScience (Feb 2024)
Adolescents’ pain-related ontogeny shares a neural basis with adults’ chronic pain in basothalamo-cortical organization
- Nils Jannik Heukamp,
- Tobias Banaschewski,
- Arun L.W. Bokde,
- Sylvane Desrivières,
- Antoine Grigis,
- Hugh Garavan,
- Penny Gowland,
- Andreas Heinz,
- Mina Kandić,
- Rüdiger Brühl,
- Jean-Luc Martinot,
- Marie-Laure Paillère Martinot,
- Eric Artiges,
- Dimitri Papadopoulos Orfanos,
- Herve Lemaitre,
- Martin Löffler,
- Luise Poustka,
- Sarah Hohmann,
- Sabina Millenet,
- Juliane H. Fröhner,
- Michael N. Smolka,
- Katrin Usai,
- Nilakshi Vaidya,
- Henrik Walter,
- Robert Whelan,
- Gunter Schumann,
- Herta Flor,
- Frauke Nees
Affiliations
- Nils Jannik Heukamp
- Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig-Holstein, Kiel University, Kiel, Germany; Corresponding author
- Tobias Banaschewski
- Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159 Mannheim, Germany
- Arun L.W. Bokde
- Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland
- Sylvane Desrivières
- Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology & Neuroscience, SGDP Centre, King’s College London, London, UK
- Antoine Grigis
- NeuroSpin, CEA, Université Paris-Saclay, 91191 Gif-sur-Yvette, France
- Hugh Garavan
- Departments of Psychiatry and Psychology, University of Vermont, Burlington, Vermont 05405, USA
- Penny Gowland
- Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, UK
- Andreas Heinz
- Department of Psychiatry and Psychotherapy CCM, Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
- Mina Kandić
- Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, Germany
- Rüdiger Brühl
- Physikalisch-Technische Bundesanstalt (PTB), Braunschweig, Berlin, Germany
- Jean-Luc Martinot
- Institut National de la Santé et de la Recherche Médicale, INSERM U A10 ''Trajectoires développementales en psychiatrie'', Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS, Centre Borelli, Gif-sur-Yvette, France
- Marie-Laure Paillère Martinot
- Institut National de la Santé et de la Recherche Médicale, INSERM U A10 ''Trajectoires développementales en psychiatrie'', Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS, Centre Borelli, Gif-sur-Yvette, France; AP-HP, Sorbonne Université, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, Paris, France
- Eric Artiges
- Institut National de la Santé et de la Recherche Médicale, INSERM U A10 ''Trajectoires développementales en psychiatrie'', Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS, Centre Borelli, Gif-sur-Yvette, France; Psychiatry Department, EPS Barthélémy Durand, Etampes, France
- Dimitri Papadopoulos Orfanos
- NeuroSpin, CEA, Université Paris-Saclay, 91191 Gif-sur-Yvette, France
- Herve Lemaitre
- NeuroSpin, CEA, Université Paris-Saclay, 91191 Gif-sur-Yvette, France; Institut des Maladies Neurodégénératives, UMR 5293, CNRS, CEA, Université de Bordeaux, 33076 Bordeaux, France
- Martin Löffler
- Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, Germany; Clinical Psychology, Department of Experimental Psychology, Heinrich Heine University Düsseldorf, Düsseldorf, Germany; Integrative Spinal Research Group, Department of Chiropractic Medicine, University Hospital Balgrist, University of Zurich, Zurich, Switzerland
- Luise Poustka
- Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, von-Siebold-Str. 5, 37075 Göttingen, Germany
- Sarah Hohmann
- Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159 Mannheim, Germany
- Sabina Millenet
- Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159 Mannheim, Germany
- Juliane H. Fröhner
- Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany
- Michael N. Smolka
- Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany
- Katrin Usai
- Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, Germany
- Nilakshi Vaidya
- Centre for Population Neuroscience and Stratified Medicine (PONS), Department of Psychiatry and Neuroscience, Charité Universitätsmedizin, Berlin, Germany
- Henrik Walter
- Department of Psychiatry and Psychotherapy CCM, Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
- Robert Whelan
- School of Psychology and Global Brain Health Institute, Trinity College Dublin, Berlin, Ireland
- Gunter Schumann
- Centre for Population Neuroscience and Stratified Medicine (PONS), Department of Psychiatry and Neuroscience, Charité Universitätsmedizin, Berlin, Germany; Centre for Population Neuroscience and Precision Medicine (PONS), Institute for Science and Technology of Brain-inspired Intelligence (ISTBI), Fudan University, Shanghai, China
- Herta Flor
- Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, Germany; Department of Psychology, School of Social Sciences, University of Mannheim, 68131 Mannheim, Germany
- Frauke Nees
- Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig-Holstein, Kiel University, Kiel, Germany; Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159 Mannheim, Germany; Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, Germany; Corresponding author
- Journal volume & issue
-
Vol. 27,
no. 2
p. 108954
Abstract
Summary: During late adolescence, the brain undergoes ontogenic organization altering subcortical-cortical circuitry. This includes regions implicated in pain chronicity, and thus alterations in the adolescent ontogenic organization could predispose to pain chronicity in adulthood - however, evidence is lacking. Using resting-state functional magnetic resonance imaging from a large European longitudinal adolescent cohort and an adult cohort with and without chronic pain, we examined links between painful symptoms and brain connectivity. During late adolescence, thalamo-, caudate-, and red nucleus-cortical connectivity were positively and subthalamo-cortical connectivity negatively associated with painful symptoms. Thalamo-cortical connectivity, but also subthalamo-cortical connectivity, was increased in adults with chronic pain compared to healthy controls. Our results indicate a shared basis in basothalamo-cortical circuitries between adolescent painful symptomatology and adult pain chronicity, with the subthalamic pathway being differentially involved, potentially due to a hyperconnected thalamo-cortical pathway in chronic pain and ontogeny-driven organization. This can inform neuromodulation-based prevention and early intervention.
