title: Neural synchrony indexes impaired motor slowing after errors and novelty following white matter damage.
abstract: In humans, action errors and perceptual novelty elicit activity in a shared frontostriatal brain network, allowing them to adapt their ongoing behavior to such unexpected action outcomes. Healthy and pathologic aging reduces the integrity of white matter pathways that connect individual hubs of such networks and can impair the associated cognitive functions. Here, we investigated whether structural disconnection within this network because of small-vessel disease impairs the neural processes that subserve motor slowing after errors and novelty (post-error slowing, PES; post-novel slowing, PNS). Participants with intact frontostriatal circuitry showed increased right-lateralized beta-band (12-24 Hz) synchrony between frontocentral and frontolateral electrode sites in the electroencephalogram after errors and novelty, indexing increased neural communication. Importantly, this synchrony correlated with PES and PNS across participants. Furthermore, such synchrony was reduced in participants with frontostriatal white matter damage, in line with reduced PES and PNS. The results demonstrate that behavioral change after errors and novelty result from coordinated neural activity across a frontostriatal brain network and that such cognitive control is impaired by reduced white matter integrity.
authors.affiliation: Department of Psychological and Brain Sciences, University of Iowa, Iowa City, IA, USA; Department of Neurology, Carver College of Medicine, University of Iowa, Iowa City, IA, USA. Electronic address: jan-wessel@uiowa.edu.
authors.forename: Jan R
authors.initials: JR
authors.lastname: Wessel
authors.affiliation: Department of Neuropsychology, Otto von Guericke University, Magdeburg, Germany; Center for Behavioral Brain Sciences, Magdeburg, Germany; Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, the Netherlands.
authors.forename: Markus
authors.initials: M
authors.lastname: Ullsperger
authors.affiliation: Max Planck Institute for Cognitive and Brain Sciences, Leipzig, Germany; Day Clinic for Cognitive Neurology, University Clinic, Leipzig, Germany.
authors.forename: Hellmuth
authors.initials: H
authors.lastname: Obrig
authors.affiliation: Leipzig Research Center for Civilization Diseases, University of Leipzig, Leipzig, German; German Consortium for Frontotemporal Lobar Degeneration, Ulm, Germany.
authors.forename: Arno
authors.initials: A
authors.lastname: Villringer
authors.affiliation: Max Planck Institute for Cognitive and Brain Sciences, Leipzig, Germany.
authors.forename: Eva
authors.initials: E
authors.lastname: Quinque
authors.affiliation: Max Planck Institute for Cognitive and Brain Sciences, Leipzig, Germany; Day Clinic for Cognitive Neurology, University Clinic, Leipzig, Germany; Leipzig Research Center for Civilization Diseases, University of Leipzig, Leipzig, German; German Consortium for Frontotemporal Lobar Degeneration, Ulm, Germany.
authors.forename: Matthias L
authors.initials: ML
authors.lastname: Schroeter
authors.affiliation: Max Planck Institute for Cognitive and Brain Sciences, Leipzig, Germany.
authors.forename: Katharina J
authors.initials: KJ
authors.lastname: Bretschneider
authors.affiliation: Max Planck Institute for Cognitive and Brain Sciences, Leipzig, Germany; Day Clinic for Cognitive Neurology, University Clinic, Leipzig, Germany; Leipzig Research Center for Civilization Diseases, University of Leipzig, Leipzig, German.
authors.forename: Katrin
authors.initials: K
authors.lastname: Arelin
authors.affiliation: Max Planck Institute for Cognitive and Brain Sciences, Leipzig, Germany; Day Clinic for Cognitive Neurology, University Clinic, Leipzig, Germany; Laboratoire de Recherche en Neuroimagerie, Département des Neurosciences Cliniques, Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland.
authors.forename: Elisabeth
authors.initials: E
authors.lastname: Roggenhofer
authors.affiliation: Max Planck Institute for Cognitive and Brain Sciences, Leipzig, Germany; Department of Neurology, University Hospital Frankfurt/Goethe-University, Frankfurt am Main, Germany.
authors.forename: Stefan
authors.initials: S
authors.lastname: Frisch
authors.affiliation: Max Planck Institute for Cognitive and Brain Sciences, Leipzig, Germany; Day Clinic for Cognitive Neurology, University Clinic, Leipzig, Germany.
authors.forename: Tilmann A
authors.initials: TA
authors.lastname: Klein
mesh_terms: D001519:Behavior / Q000502:physiology; D003071:Cognition / Q000502:physiology; D058407:Electroencephalography Phase Synchronization / Q000502:physiology*; D056344:Executive Function / Q000502:physiology; D005260:Female; D006801:Humans; D008297:Male; D008875:Middle Aged; D009415:Nerve Net / Q000473:pathology / Q000503:physiopathology; D066127:White Matter / Q000473:pathology* / Q000503:physiopathology*
keywords: Cognitive control; EEG synchrony; Errors; Executive functions; Novelty; Small-vessel disease