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      Auricular Transcutaneous Vagus Nerve Stimulation Diminishes Alpha-Band–Related Inhibitory Gating Processes During Conflict Monitoring in Frontal Cortices

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          Abstract

          Background

          Pursuing goals is compromised when being confronted with interfering information. In such situations, conflict monitoring is important. Theoretical considerations on the neurobiology of response selection and control suggest that auricular transcutaneous vagus nerve stimulation (atVNS) should modulate conflict monitoring. However, the neurophysiological-functional neuroanatomical underpinnings are still not understood.

          Methods

          AtVNS was applied in a randomized crossover study design (n = 45). During atVNS or sham stimulation, conflict monitoring was assessed using a Flanker task. EEG data were recorded and analyzed with focus on theta and alpha band activity. Beamforming was applied to examine functional neuroanatomical correlates of atVNS-induced EEG modulations. Moreover, temporal EEG signal decomposition was applied to examine different coding levels in alpha and theta band activity.

          Results

          AtVNS compromised conflict monitoring processes when it was applied at the second appointment in the crossover study design. On a neurophysiological level, atVNS exerted specific effects because only alpha-band activity was modulated. Alpha-band activity was lower in middle and superior prefrontal regions during atVNS stimulation and thus lower when there was also a decline in task performance. The same direction of alpha-band modulations was evident in fractions of the alpha-band activity coding stimulus-related processes, stimulus-response translation processes, and motor response–related processes.

          Conclusions

          The combination of prior task experience and atVNS compromises conflict monitoring processes. This is likely due to reduction of the alpha-band–associated inhibitory gating process on interfering information in frontal cortices. Future research should pay considerable attention to boundary conditions affecting the direction of atVNS effects.

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          Most cited references84

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          An integrative theory of prefrontal cortex function.

          The prefrontal cortex has long been suspected to play an important role in cognitive control, in the ability to orchestrate thought and action in accordance with internal goals. Its neural basis, however, has remained a mystery. Here, we propose that cognitive control stems from the active maintenance of patterns of activity in the prefrontal cortex that represent goals and the means to achieve them. They provide bias signals to other brain structures whose net effect is to guide the flow of activity along neural pathways that establish the proper mappings between inputs, internal states, and outputs needed to perform a given task. We review neurophysiological, neurobiological, neuroimaging, and computational studies that support this theory and discuss its implications as well as further issues to be addressed
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            Conflict monitoring and cognitive control.

            A neglected question regarding cognitive control is how control processes might detect situations calling for their involvement. The authors propose here that the demand for control may be evaluated in part by monitoring for conflicts in information processing. This hypothesis is supported by data concerning the anterior cingulate cortex, a brain area involved in cognitive control, which also appears to respond to the occurrence of conflict. The present article reports two computational modeling studies, serving to articulate the conflict monitoring hypothesis and examine its implications. The first study tests the sufficiency of the hypothesis to account for brain activation data, applying a measure of conflict to existing models of tasks shown to engage the anterior cingulate. The second study implements a feedback loop connecting conflict monitoring to cognitive control, using this to simulate a number of important behavioral phenomena.
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              An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance.

              Historically, the locus coeruleus-norepinephrine (LC-NE) system has been implicated in arousal, but recent findings suggest that this system plays a more complex and specific role in the control of behavior than investigators previously thought. We review neurophysiological and modeling studies in monkey that support a new theory of LC-NE function. LC neurons exhibit two modes of activity, phasic and tonic. Phasic LC activation is driven by the outcome of task-related decision processes and is proposed to facilitate ensuing behaviors and to help optimize task performance (exploitation). When utility in the task wanes, LC neurons exhibit a tonic activity mode, associated with disengagement from the current task and a search for alternative behaviors (exploration). Monkey LC receives prominent, direct inputs from the anterior cingulate (ACC) and orbitofrontal cortices (OFC), both of which are thought to monitor task-related utility. We propose that these frontal areas produce the above patterns of LC activity to optimize utility on both short and long timescales.
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                Author and article information

                Contributors
                Journal
                Int J Neuropsychopharmacol
                Int J Neuropsychopharmacol
                ijnp
                International Journal of Neuropsychopharmacology
                Oxford University Press (US )
                1461-1457
                1469-5111
                June 2022
                05 February 2022
                05 February 2022
                : 25
                : 6
                : 457-467
                Affiliations
                Cognitive Neurophysiology, Department of Child and Adolescent Psychiatry, Faculty of Medicine , TU Dresden, Germany
                University Neuropsychology Centre, Faculty of Medicine , TU Dresden, Germany
                Cognitive Neurophysiology, Department of Child and Adolescent Psychiatry, Faculty of Medicine , TU Dresden, Germany
                University Neuropsychology Centre, Faculty of Medicine , TU Dresden, Germany
                Faculty of Psychology, Shandong Normal University , Jinan, China
                Cognitive Neurophysiology, Department of Child and Adolescent Psychiatry, Faculty of Medicine , TU Dresden, Germany
                University Neuropsychology Centre, Faculty of Medicine , TU Dresden, Germany
                Cognitive Neurophysiology, Department of Child and Adolescent Psychiatry, Faculty of Medicine , TU Dresden, Germany
                University Neuropsychology Centre, Faculty of Medicine , TU Dresden, Germany
                Faculty of Psychology, Shandong Normal University , Jinan, China
                Author notes
                Correspondence: Christian Beste, PhD, Faculty of Medicine Carl Gustav Carus, TU Dresden, Department of Child and Adolescent Psychiatry, Fetscherstrasse 74, 01307 Dresden, Germany ( Christian.beste@ 123456ukdd.de ).

                M.M. and C.B. shared senior authorship.

                Author information
                https://orcid.org/0000-0002-2989-9561
                Article
                pyac013
                10.1093/ijnp/pyac013
                9211011
                35137108
                7d5dbb87-8312-4d3b-aae0-dd160cf3342d
                © The Author(s) 2022. Published by Oxford University Press on behalf of CINP.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License ( https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

                History
                : 29 July 2021
                : 11 January 2022
                : 01 February 2022
                : 25 February 2022
                Page count
                Pages: 11
                Funding
                Funded by: 100 Talent Grant of the Province of Shandong;
                Funded by: Deutsche Forschungsgemeinschaft, DOI 10.13039/501100001659;
                Award ID: BE4045/43-1
                Award ID: TRR 265
                Categories
                Regular Research Articles
                AcademicSubjects/MED00415
                AcademicSubjects/SCI01870

                Pharmacology & Pharmaceutical medicine
                auricular transcutaneous vagus nerve stimulation (atvns),conflict monitoring,eeg,theta band,alpha band,beamforming

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