Scientific Understanding of Consciousness
Gamma Oscillations in Somatosensory Cortex
PLoS Biol 5(5): e133. doi:10.1371/journal.pbio.0050133
Gamma Oscillations in Human Primary Somatosensory Cortex Reflect Pain Perception
Joachim Gross1, Alfons Schnitzler1,3, Lars Timmermann1, Markus Ploner1,4
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
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.
Within the continuous flow of sensory information, a huge number of events compete for neural representation and perception. This sensory overflow requires the selection and preferential processing of relevant information in order to optimize the utilization of cerebral processing resources. Recently, induced neuronal oscillations in the gamma frequency range (about 40–100 Hz) have been suggested to represent one mechanism of the selection and preferred processing of sensory information. These induced gamma oscillations represent event-related modulations of neuronal oscillations, are often observed in early sensory cortices and differ from evoked neuronal responses in a lack of phase locking to the sensory stimulus. Functionally, the association between induced gamma oscillations, and selection and preferred processing of sensory stimuli suggests that these responses may not only be related to the physical stimulus attributes, but also related particularly to the subjectively weighted percept of a sensory event.
Painful stimuli signal threats and are therefore of utmost behavioral relevance. Thus, we hypothesized that painful stimuli induce gamma oscillations in somatosensory cortices. Moreover, we speculated that these pain-induced gamma oscillations may not only relate to the objective attributes of painful stimuli, but may also particularly reflect the subjective experience of pain. To address this issue, we used magnetoencephalography to record neural responses to noxious stimuli in healthy human subjects. We investigated the effects of noxious stimuli on neuronal activity in the gamma band and related these effects to objective stimulus intensity and subjectively perceived pain intensity. Our results show that pain induces gamma oscillations in the contralateral primary somatosensory cortex. Amplitudes of pain-induced gamma oscillations increase with objective stimulus intensity and subjective pain intensity. However, around pain threshold, perceived stimuli induce significantly stronger gamma oscillations than unperceived stimuli of equal stimulus intensity. These observations provide direct evidence for a close association between induced gamma oscillations and the conscious and subjective perception of behaviorally relevant sensory events.
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