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      An event‐based magnetoencephalography study of simulated driving: Establishing a novel paradigm to probe the dynamic interplay of executive and motor function

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          Abstract

          Magnetoencephalography (MEG) is particularly well‐suited to the study of human motor cortex oscillatory rhythms and motor control. However, the motor tasks studied to date are largely overly simplistic. This study describes a new approach: a novel event‐based simulated drive made operational via MEG compatible driving simulator hardware, paired with differential beamformer methods to characterize the neural correlates of realistic, complex motor activity. We scanned 23 healthy individuals aged 16–23 years (mean age = 19.5, SD = 2.5; 18 males and 5 females, all right‐handed) who completed a custom‐built repeated trials driving scenario. MEG data were recorded with a 275‐channel CTF, and a volumetric magnetic resonance imaging scan was used for MEG source localization. To validate this paradigm, we hypothesized that pedal‐use would elicit expected modulation of primary motor responses beta‐event‐related desynchronization (B‐ERD) and movement‐related gamma synchrony (MRGS). To confirm the added utility of this paradigm, we hypothesized that the driving task could also probe frontal cognitive control responses (specifically, frontal midline theta [FMT]). Three of 23 participants were removed due to excess head motion (>1.5 cm/trial), confirming feasibility. Nonparametric group analysis revealed significant regions of pedal‐use related B‐ERD activity (at left precentral foot area, as well as bilateral superior parietal lobe: p < .01 corrected), MRGS (at medial precentral gyrus: p < .01 corrected), and FMT band activity sustained around planned braking (at bilateral superior frontal gyrus: p < .01 corrected). This paradigm overcomes the limits of previous efforts by allowing for characterization of the neural correlates of realistic, complex motor activity in terms of brain regions, frequency bands and their dynamic temporal interplay.

          Abstract

          This study describes a new approach: a novel event‐based simulated drive made operational via magnetoencephalography compatible driving simulator hardware, paired with differential beamformer methods to characterize the neural correlates of realistic, complex motor activity. This paradigm is validated by expected primary beta and gamma motor responses. Demonstrating added utility, increased task demands were revealed in frontal midline theta cognitive control activity, and motor cortex gamma power decreased with habituation/learning over trials.

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          Frontal theta as a mechanism for cognitive control.

          Recent advancements in cognitive neuroscience have afforded a description of neural responses in terms of latent algorithmic operations. However, the adoption of this approach to human scalp electroencephalography (EEG) has been more limited, despite the ability of this methodology to quantify canonical neuronal processes. Here, we provide evidence that theta band activities over the midfrontal cortex appear to reflect a common computation used for realizing the need for cognitive control. Moreover, by virtue of inherent properties of field oscillations, these theta band processes may be used to communicate this need and subsequently implement such control across disparate brain regions. Thus, frontal theta is a compelling candidate mechanism by which emergent processes, such as 'cognitive control', may be biophysically realized. Copyright © 2014 Elsevier Ltd. All rights reserved.
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            Voluntary orienting is dissociated from target detection in human posterior parietal cortex.

            Human ability to attend to visual stimuli based on their spatial locations requires the parietal cortex. One hypothesis maintains that parietal cortex controls the voluntary orienting of attention toward a location of interest. Another hypothesis emphasizes its role in reorienting attention toward visual targets appearing at unattended locations. Here, using event-related functional magnetic resonance (ER-fMRI), we show that distinct parietal regions mediated these different attentional processes. Cortical activation occurred primarily in the intraparietal sulcus when a location was attended before visual-target presentation, but in the right temporoparietal junction when the target was detected, particularly at an unattended location.
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              Signal processing in magnetoencephalography.

              The subject of this article is detection of brain magnetic fields, or magnetoencephalography (MEG). The brain fields are many orders of magnitude smaller than the environmental magnetic noise and their measurement represent a significant metrological challenge. The only detectors capable of resolving such small fields and at the same time handling the large dynamic range of the environmental noise are superconducting quantum interference devices (or SQUIDs). The SQUIDs are coupled to the brain magnetic fields using combinations of superconducting coils called flux transformers (primary sensors). The environmental noise is attenuated by a combination of shielding, primary sensor geometry, and synthetic methods. One of the most successful synthetic methods for noise elimination is synthetic higher-order gradiometers. How the gradiometers can be synthesized is shown and examples of their noise cancellation effectiveness are given. The MEG signals measured on the scalp surface must be interpreted and converted into information about the distribution of currents within the brain. This task is complicated by the fact that such inversion is nonunique. Additional mathematical simplifications, constraints, or assumptions must be employed to obtain useful source images. Methods for the interpretation of the MEG signals include the popular point current dipole, minimum norm methods, spatial filtering, beamformers, MUSIC, and Bayesian techniques. The use of synthetic aperture magnetometry (a class of beamformers) is illustrated in examples of interictal epileptic spiking and voluntary hand-motor activity. Copyright 2001 Elsevier Science.
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                Author and article information

                Contributors
                gaetzw@chop.edu
                Journal
                Hum Brain Mapp
                Hum Brain Mapp
                10.1002/(ISSN)1097-0193
                HBM
                Human Brain Mapping
                John Wiley & Sons, Inc. (Hoboken, USA )
                1065-9471
                1097-0193
                08 January 2023
                1 April 2023
                : 44
                : 5 ( doiID: 10.1002/hbm.v44.5 )
                : 2109-2121
                Affiliations
                [ 1 ] Center for Injury Research and Prevention Children's Hospital of Philadelphia Philadelphia Pennsylvania USA
                [ 2 ] Lurie Family Foundations' MEG Imaging Center, Department of Radiology Children's Hospital of Philadelphia Philadelphia Pennsylvania USA
                [ 3 ] Department of Radiology Perelman School of Medicine, University of Pennsylvania Philadelphia Pennsylvania USA
                [ 4 ] Department of Pediatrics Perelamn School of Medicine, University of Pennysylvania Philadelphia Pennsylvania USA
                [ 5 ] Annenberg Public Policy Center University of Pennsylvania Philadelphia Pennsylvania USA
                Author notes
                [*] [* ] Correspondence

                William Gaetz, Lurie Family Foundations' MEG Imaging Center, Department of Radiology, Children's Hospital of Philadelphia, 34th St. and Civic Center Boulevard, Philadelphia, PA 19104, USA.

                Email: gaetzw@ 123456chop.edu

                Author information
                https://orcid.org/0000-0002-0466-4272
                Article
                HBM26197
                10.1002/hbm.26197
                9980886
                36617993
                fa26d5af-735d-4521-8dda-3246e4e85071
                © 2023 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

                History
                : 27 October 2022
                : 19 July 2022
                : 10 December 2022
                Page count
                Figures: 7, Tables: 0, Pages: 13, Words: 10874
                Funding
                Funded by: National Institute of Health
                Award ID: NIH‐R21 5R21NS118410‐02
                Funded by: Children's Hospital of Philadelphia (CHOP) Foerderer Award , doi 10.13039/100006458;
                Funded by: Center for Child Injury Prevention Studies
                Funded by: Center for Injury Research and Prevention at CHOP
                Funded by: Annenberg Public Policy Center at the University of Pennsylvania
                Categories
                Research Article
                Research Articles
                Custom metadata
                2.0
                April 1, 2023
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.2.5 mode:remove_FC converted:02.03.2023

                Neurology
                beta event‐related desynchronization,driving simulator,frontal midline theta,magnetoencephalography,motor control,movement‐related gamma synchrony

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