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      Gamma Oscillations in Human Primary Somatosensory Cortex Reflect Pain Perception

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Successful behavior requires selection and preferred processing of relevant sensory information. The cortical representation of relevant sensory information has been related to neuronal oscillations in the gamma frequency band. Pain is of invariably high behavioral relevance and, thus, nociceptive stimuli receive preferred processing. Here, by using magnetoencephalography, we show that selective nociceptive stimuli induce gamma oscillations between 60 and 95 Hz in primary somatosensory cortex. Amplitudes of pain-induced gamma oscillations vary with objective stimulus intensity and subjective pain intensity. However, around pain threshold, perceived stimuli yielded stronger gamma oscillations than unperceived stimuli of equal stimulus intensity. These results show that pain induces gamma oscillations in primary somatosensory cortex that are particularly related to the subjective perception of pain. Our findings support the hypothesis that gamma oscillations are related to the internal representation of behaviorally relevant stimuli that should receive preferred processing.

          Author Summary

          Pain is a highly subjective sensation of inherent behavioral importance and is therefore expected to receive enhanced processing in relevant brain regions. We show that painful stimuli induce high-frequency oscillations in the electrical activity of the human primary somatosensory cortex. Amplitudes of these pain-induced gamma oscillations were more closely related to the subjective perception of pain than to the objective stimulus attributes. They correlated with participants' ratings of pain and were stronger for laser stimuli that caused pain, compared with the same stimuli when no pain was perceived. These findings indicate that gamma oscillations may represent an important mechanism for processing behaviorally relevant sensory information.

          Abstract

          Magnetoencephalography reveals that gamma oscillations in the somatosensory cortex correlate with the subjective rating of pain and are stronger for laser stimuli that cause pain, compared with the same stimuli when no pain is perceived.

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          Most cited references31

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          Neuronal synchrony: a versatile code for the definition of relations?

          W. Singer (1999)
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            Dynamic imaging of coherent sources: Studying neural interactions in the human brain.

            Functional connectivity between cortical areas may appear as correlated time behavior of neural activity. It has been suggested that merging of separate features into a single percept ("binding") is associated with coherent gamma band activity across the cortical areas involved. Therefore, it would be of utmost interest to image cortico-cortical coherence in the working human brain. The frequency specificity and transient nature of these interactions requires time-sensitive tools such as magneto- or electroencephalography (MEG/EEG). Coherence between signals of sensors covering different scalp areas is commonly taken as a measure of functional coupling. However, this approach provides vague information on the actual cortical areas involved, owing to the complex relation between the active brain areas and the sensor recordings. We propose a solution to the crucial issue of proceeding beyond the MEG sensor level to estimate coherences between cortical areas. Dynamic imaging of coherent sources (DICS) uses a spatial filter to localize coherent brain regions and provides the time courses of their activity. Reference points for the computation of neural coupling may be based on brain areas of maximum power or other physiologically meaningful information, or they may be estimated starting from sensor coherences. The performance of DICS is evaluated with simulated data and illustrated with recordings of spontaneous activity in a healthy subject and a parkinsonian patient. Methods for estimating functional connectivities between brain areas will facilitate characterization of cortical networks involved in sensory, motor, or cognitive tasks and will allow investigation of pathological connectivities in neurological disorders.
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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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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                pbio
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                May 2007
                24 April 2007
                : 5
                : 5
                : e133
                Affiliations
                [1 ] Department of Neurology, Heinrich-Heine-University, Düsseldorf, Germany
                [2 ] Centre for Cognitive Neuroimaging, Department of Psychology, University of Glasgow, United Kingdom
                [3 ] Wolfson Centre for Clinical and Cognitive Neuroscience, School of Psychology, University of Wales, Bangor, United Kingdom
                [4 ] Department of Neurology, Technical University Munich, Munich, Germany
                F. C. Donders Centre for Cognitive Neuroimaging, The Netherlands
                Author notes
                * To whom correspondence should be addressed. E-mail: schnitza@ 123456uni-duesseldorf.de
                Article
                06-PLBI-RA-1755R3 plbi-05-05-24
                10.1371/journal.pbio.0050133
                1854914
                17456008
                fb32fd45-9da6-494b-876f-233150463ba1
                Copyright: © 2007 Gross et al. 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
                : 20 September 2006
                : 12 March 2007
                Page count
                Pages: 6
                Categories
                Research Article
                Neuroscience
                Homo (Human)
                Custom metadata
                Gross J, Schnitzler A, Timmermann L, Ploner M (2007) Gamma oscillations in human primary somatosensory cortex reflect pain perception. PLoS Biol 5(5): e133. doi: 10.1371/journal.pbio.0050133

                Life sciences
                Life sciences

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