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Neural synchrony indexes impaired motor slowing after errors and novelty following white matter damage

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Obrig,  Hellmuth
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
Clinic for Cognitive Neurology, University of Leipzig, Germany;

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Villringer,  Arno
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
Leipzig Research Center for Civilization Diseases (LIFE), University of Leipzig, Germany;
Consortium for Frontotemporal Lobar Degeneration, Ulm, Germany;

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Quinque,  Eva Maria
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;

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Schroeter,  Matthias L.
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
Clinic for Cognitive Neurology, University of Leipzig, Germany;
Leipzig Research Center for Civilization Diseases (LIFE), University of Leipzig, Germany;
Consortium for Frontotemporal Lobar Degeneration, Ulm, Germany;

Bretschneider,  Katharina J.
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;

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Arélin,  Katrin
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
Clinic for Cognitive Neurology, University of Leipzig, Germany;
Leipzig Research Center for Civilization Diseases (LIFE), University of Leipzig, Germany;

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Roggenhofer,  Elisabeth
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
Clinic for Cognitive Neurology, University of Leipzig, Germany;
Laboratoire de Recherche en Neuroimagerie (LREN), Centre hospitalier universitaire vaudois, Lausanne, Switzerland;

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Frisch,  Stefan
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
Department of Neurology, Goethe University, Frankfurt, Germany;

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Klein,  Tilmann A.
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
Leipzig Research Center for Civilization Diseases (LIFE), University of Leipzig, Germany;

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Citation

Wessel, J. R., Ullsperger, M., Obrig, H., Villringer, A., Quinque, E. M., Schroeter, M. L., et al. (2016). Neural synchrony indexes impaired motor slowing after errors and novelty following white matter damage. Neurobiology of Aging, 38, 205-213. doi:10.1016/j.neurobiolaging.2015.10.014.


Cite as: http://hdl.handle.net/11858/00-001M-0000-002B-22F7-0
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.