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Differential neurophysiological correlates of bottom-up and top-down modulations of pain

Tiemann, Lauraa,b,*; May, Elisabeth S.a,b; Postorino, Martinaa,b; Schulz, Enricoa,b; Nickel, Moritz M.a,b; Bingel, Ulrikec; Ploner, Markusa,b

doi: 10.1097/01.j.pain.0000460309.94442.44
Research Paper
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The perception of pain is highly variable. It depends on bottom-up-mediated factors like stimulus intensity and top-down-mediated factors like expectations. In the brain, pain is associated with a complex pattern of neuronal responses including evoked potentials and induced responses at alpha and gamma frequencies. Although they all covary with stimulus intensity and pain perception, responses at gamma frequencies can be particularly closely related to the perception of pain. It is, however, unclear whether this association holds true across all types of pain modulation. Here, we used electroencephalography to directly compare bottom-up- and top-down-mediated modulations of pain, which were implemented by changes in stimulus intensity and placebo analgesia, respectively. The results show that stimulus intensity modulated pain-evoked potentials and pain-induced alpha and gamma responses. In contrast, placebo analgesia was associated with changes of evoked potentials, but not of alpha and gamma responses. These findings reveal that pain-related neuronal responses are differentially sensitive to bottom-up and top-down modulations of pain, indicating that they provide complementary information about pain perception. The results further show that pain-induced gamma oscillations do not invariably encode pain perception but may rather represent a marker of sensory processing whose influence on pain perception varies with behavioral context.

The close relationship between gamma oscillations and pain perception does not generalize to all types of pain modulation but varies with behavioral context.

aDepartment of Neurology, Technische Universität München, Munich, Germany

bTUM-Neuroimaging Center, Technische Universität München, Munich, Germany

cDepartment of Neurology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany

Corresponding author. Address: Department of Neurology, Klinikum rechts der Isar, Technische Universität München, Ismaninger Straße 22, 81675 Munich, Germany. Tel.: +49 89 4140 7664; fax: +49 89 4140 7681. E-mail address: tiemann@lrz.tu-muenchen.de (L. Tiemann).

Sponsorships or competing interests that may be relevant to content are disclosed at the end of this article.

Received July 03, 2014

Received in revised form October 13, 2014

Accepted November 14, 2014

© 2015 International Association for the Study of Pain
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