Elsevier

NeuroImage

Volume 32, Issue 3, September 2006, Pages 1231-1236
NeuroImage

Oscillatory activity reflects the excitability of the human somatosensory system

https://doi.org/10.1016/j.neuroimage.2006.06.004Get rights and content

Abstract

The neuronal activity of the resting human brain is dominated by spontaneous oscillations in primary sensory and motor areas. These oscillations are thought to reflect the excitability of sensory and motor systems that can be modulated according to the actual behavioral demands. However, so far, evidence for an association between oscillatory activity and excitability has been inconsistent. Here, we used magnetoencephalography to reinvestigate the relationship between oscillatory activity and excitability in the somatosensory system on a single trial basis. Brief painful stimuli were applied to relate pain-induced suppressions of oscillatory activity to pain-induced increases in excitability. The analysis reveals a significant negative correlation between sensorimotor oscillatory activity, particularly in the α-band, and excitability of somatosensory cortices. Oscillatory activity outside the somatosensory system did not correlate with somatosensory excitability. These findings demonstrate that modulations of sensorimotor oscillatory activity specifically reflect modulations in excitability of the somatosensory system and thus provide direct evidence for the basic tenet of an association between oscillatory activity and cortical excitability.

Introduction

Spontaneous oscillatory activity represents a basic feature of the neuronal activity of the human brain. Particularly, spontaneous oscillations in the α-band (8–13 Hz) and β-band (14–30 Hz) are consistently observed in primary visual, somatosensory and motor cortices (Berger, 1929, Gastaut, 1952, Hari and Salmelin, 1997, Niedermeyer, 2005). These oscillations have been related to the functional state of sensory and motor systems (Hari and Salmelin, 1997, Pfurtscheller and Lopes da Silva, 2005). A higher amplitude of oscillatory activity has been associated with an idling state whereas a lower amplitude may signal activation of a system (Steriade and Llinas, 1988, Hari and Salmelin, 1997, Niedermeyer, 2005, Pfurtscheller and Lopes da Silva, 2005). Furthermore, oscillatory activity is thought to reflect the excitability of thalamocortical systems that can be modulated by exogenous or endogenous events (Steriade and Llinas, 1988). However, experimental evidence for this association between oscillatory activity and cortical excitability is sparse and inconsistent. Some studies showed a positive correlation between oscillations and excitability (Brandt et al., 1991, Arieli et al., 1996, Nikouline et al., 2000, Tamura et al., 2005), whereas others revealed a negative correlation (Brandt and Jansen, 1991, Rossini et al., 1991, Rahn and Basar, 1993a, Rahn and Basar, 1993b, Chen et al., 1999) or did not show any significant relationship (Simoes et al., 2004) between oscillations and excitability.

Therefore, we reinvestigated the relationship between excitability and oscillatory activity – termed mu-rhythm – in the human somatosensory system on a single trial basis. The mu-rhythm comprises two frequency components in the α- and β-band, which can be suppressed by exogenous or endogenous activation of the sensorimotor system. Particularly, painful stimuli have been shown to suppress the mu-rhythm (Mouraux et al., 2003, Ohara et al., 2004, Raij et al., 2004, Ploner et al., 2006) as well as to increase somatosensory excitability (Ploner et al., 2004). Here, we applied brief painful cutaneous laser stimuli in order to relate pain-induced suppressions of the mu-rhythm to pain-induced increases in cortical excitability. Using a conditioning test stimulus paradigm, cortical responses to tactile test stimuli applied 500 ms after the painful conditioning stimuli were used as a measure of somatosensory excitability. Our single trial-based analysis reveals an inverse correlation between oscillatory activity, particularly the α-component of the mu-rhythm, and the excitability of primary (S1) and secondary (S2) somatosensory cortices. Thus, these findings provide direct evidence for the basic tenet of an association between oscillatory activity and cortical excitability in humans.

Section snippets

Subjects

Eight healthy male subjects with a mean age of 31 years (range, 23–45 years) participated in the experiment. Informed consent was obtained from all subjects before participation. The study was approved by the local ethics committee and conducted in conformity with the declaration of Helsinki.

Procedure

The relationship between oscillatory activity and cortical excitability was studied using a conditioning test stimulus paradigm (Fig. 1A). Conditioning stimuli (CS) were brief painful laser stimuli, which

Results

In all subjects, conditioning stimuli consistently evoked slightly painful pinprick-like sensations and test stimuli elicited clear and consistent non-painful sensations.

Fig. 1B shows the time courses of the α- and β-components of the mu-rhythm with reference to a prestimulus baseline averaged across all subjects. The figure illustrates that painful conditioning stimuli induce a significant suppression of both components of the mu-rhythm (p < 0.01 for both components, two-tailed Wilcoxon signed

Discussion

In the present study, we investigated the relationship between oscillatory activity and excitability in the human somatosensory system. By using magnetoencephalography and applying a conditioning test stimulus paradigm, our results reveal an inverse linear correlation between pain-induced modulations of oscillatory activity and pain-induced modulations of cortical excitability in the somatosensory system. This correlation particularly applies to the α-component of the mu-rhythm, indicating that

Acknowledgments

The study was supported by the Research Committee of the Medical Faculty of the Heinrich-Heine-University (9772196), by the Deutsche Forschungsgemeinschaft (PO 806/2-1), and by the German Ministry of Education and Science (01GW0533).

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