From preparation to post-processing: Insights into evoked and induced cortical activity during pre-cued motor reactions in children and adolescents

NeuroImage, vol. 297, pp. 120735

Abstract

INTRODUCTION: The motor system undergoes significant development throughout childhood and adolescence. The contingent negative variation (CNV), a brain response reflecting preparation for upcoming actions, offers valuable insights into these changes. However, previous CNV studies of motor preparation have primarily focused on adults, leaving a gap in our understanding of how cortical activity related to motor planning and execution matures in children and adolescents. METHODS: The study addresses this gap by investigating the maturation of motor preparation, pre-activation, and post-processing in 46 healthy, right-handed children and adolescents aged 5-16 years. To overcome the resolution limitations of previous studies, we combined 64-electrode high-density Electroencephalography (EEG) and advanced analysis techniques, such as event-related potentials (ERPs), mu-rhythm desynchronization as well as source localization approaches. The combined analyses provided an in-depth understanding of cortical activity during motor control. RESULTS: Our data showed that children exhibited prolonged reaction times, increased errors, and a distinct pattern of cortical activation compared to adolescents. The findings suggest that the supplementary motor area (SMA) plays a progressively stronger role in motor planning and response evaluation as children age. Additionally, we observe a decrease in sensory processing and post-movement activity with development, potentially reflecting increased efficiency. Interestingly, adolescent subjects, unlike young adults in previous studies, did not yet show contralateral activation of motor areas during the motor preparation phase (late CNV). CONCLUSION: The progressive increase in SMA activation and distinct cortical activation patterns in younger participants suggest immature motor areas. These immature regions might be a primary cause underlying the age-related increase in motor action control efficiency. Additionally, the study demonstrates a prolonged maturation of cortical motor areas, extending well into early adulthood, challenging the assumption that motor control is fully developed by late adolescence. This research, extending fundamental knowledge of motor control development, offers valuable insights that lay the foundation for understanding and treating motor control difficulties.

Authors 4

1. Julia Schmidgen corresponding

   University of Cologne · University Hospital Cologne

   Affiliation as printed

   Department of Child and Adolescent Psychiatry, University of Cologne, University Hospital Cologne, Germany. Electronic address: Julia.schmidgen@uk-koeln.de

   Department of Child and Adolescent Psychiatry, University of Cologne, University Hospital Cologne, Germany

2. Theresa Valentine Heinen Aachen Section Child Neuropsychology Department of Child and Adolescent Psychiatry JARA-Brain Institute II JARA-Brain Institute II

   Forschungszentrum Jülich · Universitätsklinikum Aachen · Jülich Aachen Research Alliance · RWTH Aachen University

   Affiliation as printed

   Section Child Neuropsychology, Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, RWTH, University Hospital, Aachen, Germany; JARA-BRAIN Institute II, Molecular Neuroscience and Neuroimaging, Forschungszentrum Jülich GmbH and RWTH Aachen University, Germany

   JARA-BRAIN Institute II, Molecular Neuroscience and Neuroimaging, Forschungszentrum Jülich GmbH and RWTH Aachen University, Germany

   Section Child Neuropsychology, Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, RWTH, University Hospital, Aachen, Germany

3. Kerstin Konrad Aachen Section Child Neuropsychology Department of Child and Adolescent Psychiatry JARA-Brain Institute II JARA-Brain Institute II

   Forschungszentrum Jülich · Universitätsklinikum Aachen · Jülich Aachen Research Alliance · RWTH Aachen University

   Affiliation as printed

   Section Child Neuropsychology, Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, RWTH, University Hospital, Aachen, Germany; JARA-BRAIN Institute II, Molecular Neuroscience and Neuroimaging, Forschungszentrum Jülich GmbH and RWTH Aachen University, Germany

   JARA-BRAIN Institute II, Molecular Neuroscience and Neuroimaging, Forschungszentrum Jülich GmbH and RWTH Aachen University, Germany

   Section Child Neuropsychology, Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, RWTH, University Hospital, Aachen, Germany

4. Stephan Bender

   University of Cologne · University Hospital Cologne

   Affiliation as printed

   Department of Child and Adolescent Psychiatry, University of Cologne, University Hospital Cologne, Germany