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      A Systematic Review of Integrated Functional Near-Infrared Spectroscopy (fNIRS) and Transcranial Magnetic Stimulation (TMS) Studies

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          Abstract

          Background: The capacity for TMS to elicit neural activity and manipulate cortical excitability has created significant expectation regarding its use in both cognitive and clinical neuroscience. However, the absence of an ability to quantify stimulation effects, particularly outside of the motor cortex, has led clinicians and researchers to pair noninvasive brain stimulation with noninvasive neuroimaging techniques. fNIRS, as an optical and wearable neuroimaging technique, is an ideal candidate for integrated use with TMS. Together, TMS+fNIRS may offer a hybrid alternative to “blind” stimulation to assess NIBS in therapy and research.

          Objective: In this systematic review, the current body of research into the transient and prolonged effects of TMS on fNIRS-based cortical hemodynamic measures while at rest and during tasks are discussed. Additionally, studies investigating the relation of fNIRS to measures of cortical excitability as produced by TMS-evoked Motor-Evoked-Potential (MEP) are evaluated. The aim of this review is to outline the integrated use of TMS+fNIRS and consolidate findings related to use of fNIRS to monitor changes attributed to TMS and the relationship of fNIRS to cortical excitability itself.

          Methods: Key terms were searched in PubMed and Web-of-Science to identify studies investigating the use of both fNIRS and TMS. Works from Google-Scholar and referenced works in identified papers were also assessed for relevance. All published experimental studies using both fNIRS and TMS techniques in the study methodology were included.

          Results: A combined literature search of neuroimaging and neurostimulation studies identified 53 papers detailing the joint use of fNIRS and TMS. 22/53 investigated the immediate effects of TMS at rest in the DLPFC and M1 as measured by fNIRS. 21/22 studies reported a significant effect in [HbO] for 40/54 stimulation conditions with 14 resulting an increase and 26 in a decrease. While 15/22 studies also reported [HbR], only 5/37 conditions were significant. Task effects of fNIRS+TMS were detailed in 16 studies, including 10 with clinical populations. Most studies only reported significant changes in [HbO] related measures. Studies comparing fNIRS to changes in MEP-measured cortical excitability suggest that fNIRS measures may be spatially more diffuse but share similar traits.

          Conclusion: This review summarizes the progress in the development of this emerging hybrid neuroimaging & neurostimulation methodology and its applications. Despite encouraging progress and novel applications, a lack of replicated works, along with highly disparate methodological approaches, highlight the need for further controlled studies. Interpretation of current research directions, technical challenges of TMS+fNIRS, and recommendations regarding future works are discussed.

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          Most cited references84

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          NON-INVASIVE MAGNETIC STIMULATION OF HUMAN MOTOR CORTEX

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            Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS)

            A group of European experts was commissioned to establish guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS) from evidence published up until March 2014, regarding pain, movement disorders, stroke, amyotrophic lateral sclerosis, multiple sclerosis, epilepsy, consciousness disorders, tinnitus, depression, anxiety disorders, obsessive-compulsive disorder, schizophrenia, craving/addiction, and conversion. Despite unavoidable inhomogeneities, there is a sufficient body of evidence to accept with level A (definite efficacy) the analgesic effect of high-frequency (HF) rTMS of the primary motor cortex (M1) contralateral to the pain and the antidepressant effect of HF-rTMS of the left dorsolateral prefrontal cortex (DLPFC). A Level B recommendation (probable efficacy) is proposed for the antidepressant effect of low-frequency (LF) rTMS of the right DLPFC, HF-rTMS of the left DLPFC for the negative symptoms of schizophrenia, and LF-rTMS of contralesional M1 in chronic motor stroke. The effects of rTMS in a number of indications reach level C (possible efficacy), including LF-rTMS of the left temporoparietal cortex in tinnitus and auditory hallucinations. It remains to determine how to optimize rTMS protocols and techniques to give them relevance in routine clinical practice. In addition, professionals carrying out rTMS protocols should undergo rigorous training to ensure the quality of the technical realization, guarantee the proper care of patients, and maximize the chances of success. Under these conditions, the therapeutic use of rTMS should be able to develop in the coming years. Copyright © 2014 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
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              Functional near infrared spectroscopy (NIRS) signal improvement based on negative correlation between oxygenated and deoxygenated hemoglobin dynamics.

              Near infrared spectroscopy (NIRS) is a promising technology for functional brain imaging which measures hemodynamic signals from the cortex, similar to functional magnetic resonance imaging (fMRI), but does not require the participant to lie motionless in a confined space. NIRS can therefore be used for more naturalistic experiments, including face to face communication, or natural body movements, and is well suited for real-time applications that may require lengthy training. However, improving signal quality and reducing noise, especially noise induced by head motion, is challenging, particularly for real time applications. Here we study the properties of head motion induced noise, and find that motion noise causes the measured oxygenated and deoxygenated hemoglobin signals, which are typically strongly negatively correlated, to become more positively correlated. Next, we develop a method to reduce noise based on the principle that the concentration changes of oxygenated and deoxygenated hemoglobin should be negatively correlated. We show that despite its simplicity, this method is effective in reducing noise and improving signal quality, for both online and offline noise reduction. Copyright 2009 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Journal
                Front Neurosci
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                28 February 2019
                2019
                : 13
                : 84
                Affiliations
                [1] 1Drexel University, School of Biomedical Engineering, Science and Health Systems , Philadelphia, PA, United States
                [2] 2School of Biomedical Engineering, Shanghai Jiao Tong University , Shanghai, China
                [3] 3Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine , Shanghai, China
                [4] 4Department of Family and Community Health, University of Pennsylvania , Philadelphia, PA, United States
                [5] 5Center for Injury Research and Prevention, Children's Hospital of Philadelphia , Philadelphia, PA, United States
                Author notes

                Edited by: Mikhail Lebedev, Duke University, United States

                Reviewed by: Ali Yadollahpour, Ahvaz Jundishapur University of Medical Sciences, Iran; Daniel Richard Leff, Imperial College London, United Kingdom

                *Correspondence: Hasan Ayaz hasan.ayaz@ 123456drexel.edu

                This article was submitted to Neural Technology, a section of the journal Frontiers in Neuroscience

                Article
                10.3389/fnins.2019.00084
                6403189
                30872985
                9dd4c9d2-e902-4db2-a6f1-e5cabe83c6bd
                Copyright © 2019 Curtin, Tong, Sun, Wang, Onaral and Ayaz.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 05 October 2018
                : 25 January 2019
                Page count
                Figures: 5, Tables: 4, Equations: 0, References: 90, Pages: 23, Words: 19040
                Categories
                Neuroscience
                Systematic Review

                Neurosciences
                non-invasive brain stimulation (nibs),functional near-infrared spectroscopy (fnirs),transcranial magnetic stimulation (tms),neuromodulation,cognition,motor,functional neuroimaging,tms+fnirs

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