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      Movement-Related Sensorimotor High-Gamma Activity Mainly Represents Somatosensory Feedback

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          Abstract

          Somatosensation plays pivotal roles in the everyday motor control of humans. During active movement, there exists a prominent high-gamma (HG >50 Hz) power increase in the primary somatosensory cortex (S1), and this provides an important feature in relation to the decoding of movement in a brain-machine interface (BMI). However, one concern of BMI researchers is the inflation of the decoding performance due to the activation of somatosensory feedback, which is not elicited in patients who have lost their sensorimotor function. In fact, it is unclear as to how much the HG component activated in S1 contributes to the overall sensorimotor HG power during voluntary movement. With regard to other functional roles of HG in S1, recent findings have reported that these HG power levels increase before the onset of actual movement, which implies neural activation for top-down movement preparation or sensorimotor interaction, i.e., an efference copy. These results are promising for BMI applications but remain inconclusive. Here, we found using electrocorticography (ECoG) from eight patients that HG activation in S1 is stronger and more informative than it is in the primary motor cortex (M1) regardless of the type of movement. We also demonstrate by means of electromyography (EMG) that the onset timing of the HG power in S1 is later (49 ms) than that of the actual movement. Interestingly, we show that the HG power fluctuations in S1 are closely related to subtle muscle contractions, even during the pre-movement period. These results suggest the following: (1) movement-related HG activity in S1 strongly affects the overall sensorimotor HG power, and (2) HG activity in S1 during voluntary movement mainly represents cortical neural processing for somatosensory feedback.

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          Most cited references28

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          Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band.

          N Crone (1998)
          It has been shown in animals that neuronal activity in the 'gamma band' (>30 Hz) is associated with cortical activation and may play a role in multi-regional and multi-modal integration of cortical processing. Studies of gamma activity in human scalp EEG have typically focused on event-related synchronization (ERS) in the 40 Hz band. To assess further the gamma band ERS further, as an index of cortical activation and as a tool for human functional brain mapping, we recorded subdural electrocorticographic (ECoG) signals in five clinical subjects while they performed visual-motor decision tasks designed to activate the representations of different body parts in sensorimotor cortex. ECoG spectral analysis utilized a mixed-effects analysis of variance model in which within-trial temporal dependencies were accounted for. Taking an exploratory approach, we studied gamma ERS in 10-Hz-wide bands (overlapping by 5 Hz) ranging from 30 to 100 Hz, and compared these findings with changes in the alpha (8-13 Hz) and beta (15-25 Hz) bands. Gamma ERS (observed in three out of subjects) occurred in two broad bands-'low gamma' included the 35-45 and 40-50 Hz bands, and 'high gamma' the 75-85, 80-90, 85-95 and 90-100 Hz bands. The temporal and spatial characteristics of low and high gamma ERS were distinct, suggesting relatively independent neurophysiological mechanisms. Low gamma ERS often began after onset of the motor response and was sustained through much of it, in parallel with event-related desynchronization (ERD) in the alpha band. High gamma ERS often began during, or slightly before, the motor response and was transient, ending well before completion of the motor response. These temporal differences in low and high gamma suggest different functional associations with motor performance. Compared with alpha and beta ERD, the topographical patterns of low and high gamma ERS were more discrete and somatotopically specific and only occurred over contralateral sensorimotor cortex during unilateral limb movements (alpha and beta ERD were also observed ipsilaterally). Maps of sensorimotor function inferred from gamma ERS were consistent with maps generated by cortical electrical stimulation for clinical purposes. In addition, different task conditions in one subject produced consistent differences in both motor response latencies and onset latency of gamma ERS, particularly high gamma ERS. Compared with alpha and beta ERD, the topography of gamma ERS is more consistent with traditional maps of sensorimotor functional anatomy. In addition, gamma ERS may provide complementary information about cortical neurophysiology that is useful for mapping brain function in humans.
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            Spectral changes in cortical surface potentials during motor movement.

            In the first large study of its kind, we quantified changes in electrocorticographic signals associated with motor movement across 22 subjects with subdural electrode arrays placed for identification of seizure foci. Patients underwent a 5-7 d monitoring period with array placement, before seizure focus resection, and during this time they participated in the study. An interval-based motor-repetition task produced consistent and quantifiable spectral shifts that were mapped on a Talairach-standardized template cortex. Maps were created independently for a high-frequency band (HFB) (76-100 Hz) and a low-frequency band (LFB) (8-32 Hz) for several different movement modalities in each subject. The power in relevant electrodes consistently decreased in the LFB with movement, whereas the power in the HFB consistently increased. In addition, the HFB changes were more focal than the LFB changes. Sites of power changes corresponded to stereotactic locations in sensorimotor cortex and to the results of individual clinical electrical cortical mapping. Sensorimotor representation was found to be somatotopic, localized in stereotactic space to rolandic cortex, and typically followed the classic homunculus with limited extrarolandic representation.
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              Gamma-band synchronization in visual cortex predicts speed of change detection.

              Our capacity to process and respond behaviourally to multiple incoming stimuli is very limited. To optimize the use of this limited capacity, attentional mechanisms give priority to behaviourally relevant stimuli at the expense of irrelevant distractors. In visual areas, attended stimuli induce enhanced responses and an improved synchronization of rhythmic neuronal activity in the gamma frequency band (40-70 Hz). Both effects probably improve the neuronal signalling of attended stimuli within and among brain areas. Attention also results in improved behavioural performance and shortened reaction times. However, it is not known how reaction times are related to either response strength or gamma-band synchronization in visual areas. Here we show that behavioural response times to a stimulus change can be predicted specifically by the degree of gamma-band synchronization among those neurons in monkey visual area V4 that are activated by the behaviourally relevant stimulus. When there are two visual stimuli and monkeys have to detect a change in one stimulus while ignoring the other, their reactions are fastest when the relevant stimulus induces strong gamma-band synchronization before and after the change in stimulus. This enhanced gamma-band synchronization is also followed by shorter neuronal response latencies on the fast trials. Conversely, the monkeys' reactions are slowest when gamma-band synchronization is high in response to the irrelevant distractor. Thus, enhanced neuronal gamma-band synchronization and shortened neuronal response latencies to an attended stimulus seem to have direct effects on visually triggered behaviour, reflecting an early neuronal correlate of efficient visuo-motor integration.
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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
                14 July 2017
                2017
                : 11
                : 408
                Affiliations
                [1] 1Interdisciplinary Program in Neuroscience, Seoul National University College of Natural Sciences Seoul, South Korea
                [2] 2Department of Brain and Cognitive Sciences, Seoul National University College of Natural Sciences Seoul, South Korea
                [3] 3Department of Neurosurgery, Seoul National University College of Medicine Seoul, South Korea
                Author notes

                Edited by: Sung Chan Jun, Gwangju Institute of Science and Technology, South Korea

                Reviewed by: Douglas Owen Cheyne, Hospital for Sick Children, Canada; Gareth Barnes, Wellcome Trust Centre for Neuroimaging (WT), United Kingdom

                *Correspondence: June Sic Kim jskim@ 123456hbf.re.kr

                This article was submitted to Brain Imaging Methods, a section of the journal Frontiers in Neuroscience

                Article
                10.3389/fnins.2017.00408
                5509940
                b2c06e26-8681-4640-b17c-a7e8654125a4
                Copyright © 2017 Ryun, Kim, Jeon and Chung.

                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) or licensor 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
                : 27 April 2017
                : 30 June 2017
                Page count
                Figures: 6, Tables: 2, Equations: 0, References: 34, Pages: 10, Words: 7129
                Categories
                Neuroscience
                Original Research

                Neurosciences
                voluntary movement,primary somatosensory cortex,primary motor cortex,high-gamma activity,somatosensory feedback,electrocorticography (ecog),brain-machine interface (bmi)

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