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      Changes of Spontaneous Oscillatory Activity to Tonic Heat Pain

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      1 , 2 , 3 , 1 , *
      PLoS ONE
      Public Library of Science

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          Abstract

          Transient painful stimuli could induce suppression of alpha oscillatory activities and enhancement of gamma oscillatory activities that also could be greatly modulated by attention. Here, we attempted to characterize changes in cortical activities during tonic heat pain perception and investigated the influence of directed/distracted attention on these responses. We collected 5-minute long continuous Electroencephalography (EEG) data from 38 healthy volunteers during four conditions presented in a counterbalanced order: (A) resting condition; (B) innoxious-distracted condition; (C) noxious-distracted condition; (D) noxious-attended condition. The effects of tonic heat pain stimulation and selective attention on oscillatory activities were investigated by comparing the EEG power spectra among the four experimental conditions and assessing the relationship between spectral power difference and subjective pain intensity. The change of oscillatory activities in condition D was characterized by stable and persistent decrease of alpha oscillation power over contralateral-central electrodes and widespread increase of gamma oscillation power, which were even significantly correlated with subjective pain intensity. Since EEG responses in the alpha and gamma frequency band were affected by attention in different manners, they are likely related to different aspects of the multidimensional sensory experience of pain. The observed contralateral-central alpha suppression (conditions D vs. B and D vs. C) may reflect primarily a top-down cognitive process such as attention, while the widespread gamma enhancement (conditions D vs. A) may partly reflect tonic pain processing, representing the summary effects of bottom-up stimulus-related and top-down subject-driven cognitive processes.

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          Most cited references47

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          Dynamic predictions: oscillations and synchrony in top-down processing.

          Classical theories of sensory processing view the brain as a passive, stimulus-driven device. By contrast, more recent approaches emphasize the constructive nature of perception, viewing it as an active and highly selective process. Indeed, there is ample evidence that the processing of stimuli is controlled by top-down influences that strongly shape the intrinsic dynamics of thalamocortical networks and constantly create predictions about forthcoming sensory events. We discuss recent experiments indicating that such predictions might be embodied in the temporal structure of both stimulus-evoked and ongoing activity, and that synchronous oscillations are particularly important in this process. Coherence among subthreshold membrane potential fluctuations could be exploited to express selective functional relationships during states of expectancy or attention, and these dynamic patterns could allow the grouping and selection of distributed neuronal responses for further processing.
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            Oscillatory gamma activity in humans and its role in object representation.

            We experience objects as whole, complete entities irrespective of whether they are perceived by our sensory systems or are recalled from memory. However, it is also known that many of the properties of objects are encoded and processed in different areas of the brain. How then, do coherent representations emerge? One theory suggests that rhythmic synchronization of neural discharges in the gamma band (around 40 Hz) may provide the necessary spatial and temporal links that bind together the processing in different brain areas to build a coherent percept. In this article we propose that this mechanism could also be used more generally for the construction of object representations that are driven by sensory input or internal, top-down processes. The review will focus on the literature on gamma oscillatory activities in humans and will describe the different types of gamma responses and how to analyze them. Converging evidence that suggests that one particular type of gamma activity (induced gamma activity) is observed during the construction of an object representation will be discussed.
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              New vistas for alpha-frequency band oscillations.

              The amplitude of alpha-frequency band (8-14 Hz) activity in the human electroencephalogram is suppressed by eye opening, visual stimuli and visual scanning, whereas it is enhanced during internal tasks, such as mental calculation and working memory. alpha-Frequency band oscillations have hence been thought to reflect idling or inhibition of task-irrelevant cortical areas. However, recent data on alpha-amplitude and, in particular, alpha-phase dynamics posit a direct and active role for alpha-frequency band rhythmicity in the mechanisms of attention and consciousness. We propose that simultaneous alpha-, beta- (14-30 Hz) and gamma- (30-70 Hz) frequency band oscillations are required for unified cognitive operations, and hypothesize that cross-frequency phase synchrony between alpha, beta and gamma oscillations coordinates the selection and maintenance of neuronal object representations during working memory, perception and consciousness.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                6 March 2014
                : 9
                : 3
                : e91052
                Affiliations
                [1 ]Department of Orthopaedics and Traumatology, The University of Hong Kong, Pokfulam, Hong Kong
                [2 ]Key Laboratory of Cognition and Personality (Ministry of Education) and School of Psychology, Southwest University, Chongqing, China
                [3 ]Department of Electrical and Electronic Engineering, The University of Hong Kong, Pokfulam, Hong Kong
                Institute of Psychology, Chinese Academy of Sciences, China
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: WP LH YH. Performed the experiments: WP LH. Analyzed the data: WP ZZ YH. Contributed reagents/materials/analysis tools: LH YH. Wrote the paper: WP LH ZZ YH.

                Article
                PONE-D-13-43692
                10.1371/journal.pone.0091052
                3946288
                24603703
                322128c6-e450-4d10-a7ba-5d40812be75a
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 25 October 2013
                : 7 February 2014
                Page count
                Pages: 11
                Funding
                This research was supported by Seed Funding for Basic Research from The University of Hong Kong. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Neuroscience
                Cognitive Neuroscience
                Pain
                Neurophysiology
                Central Nervous System
                Neuropsychology
                Medicine
                Diagnostic Medicine
                Clinical Neurophysiology
                Electroencephalography
                Mental Health
                Psychology
                Behavior
                Attention (Behavior)
                Sensory Perception
                Neurology
                Cognitive Neurology
                Neuroimaging

                Uncategorized
                Uncategorized

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