Elsevier

NeuroImage

Volume 51, Issue 2, June 2010, Pages 867-876
NeuroImage

Tactile expectation modulates pre-stimulus β-band oscillations in human sensorimotor cortex

https://doi.org/10.1016/j.neuroimage.2010.02.053Get rights and content

Abstract

Neuronal oscillations are postulated to play a fundamental role in top-down processes of expectation. We used magnetoencephalography (MEG) to investigate whether expectation of a tactile event involves a pre-stimulus modulation of neuronal oscillations in human somatosensory cortex. In a bimodal attention paradigm, participants were presented with a predictable spatio-temporal pattern of lateralized tactile stimulations and simultaneously occurring non-lateralized auditory stimuli. Before the onset of a series of such combined audio-tactile stimuli, a cue was presented that indicated the sensory stream that had to be attended. By investigating lateralized patterns of oscillatory activity, we were able to study both attentive (when the tactile stream was attended) and non-attentive (when the auditory stream was attended) tactile expectations. For both attention conditions, we observed a lateralized modulation of the amplitude of beta band oscillations prior to a predictable – and accordingly lateralized – tactile stimulus. As such, we show that anticipatory modulation of ongoing oscillatory activity is not restricted to attended sensory events. Attention did enlarge the size of this modulation. We argue that this modulation constitutes a suppression of beta oscillations that originate at least partly from primary somatosensory cortex (S1) contralateral to the expected stimulation. We discuss our results in the light of the hypothesis that ongoing beta oscillations over sensorimotor cortex reflect a brain state in which neuronal processing efficacy is low. Pre-stimulus suppression of these oscillations then prepares the system for future processing. This shows that perception is an active process that starts even prior to sensation.

Introduction

Perception is not mere registration of sensory input. Rather, it is an active process in which top-down mechanisms play important roles. Expectation constitutes one such top-down mechanism. Specifically, expectations about upcoming sensory events can be utilized to prepare sensory cortices by instantiating a neural context that allows for enhanced processing of the forthcoming event (Engel et al., 2001). Neuronal oscillations might define such a context, as they have been hypothesized to be involved in gating neuronal activity (Engel et al., 2001, Fries, 2005, Fries et al., 2001, Pfurtscheller and Lopes da Silva, 1999, Salinas and Sejnowski, 2001). In particular, because neuronal oscillations reflect rhythmic shifts of excitability they influence spike timing and synchronicity (Lampl and Yarom, 1993, Volgushev et al., 1998). Accordingly, pre-stimulus modulations of oscillatory activity may affect cortical information transfer of initial afferent input and are therefore considered a mechanism by which expectation can guide perception. Here we investigated whether expectation of a tactile event involves a pre-stimulus modulation of neuronal oscillations in human somatosensory cortex.

Because neuronal oscillations can be sustained in the absence of identifiable sensory input or motor output, they are likely to be involved in the neurophysiological mechanisms behind top-down influences such as expectation. These sustained neuronal oscillations can be identified because they are region and frequency specific (Hari and Salmelin, 1997). For instance, over posterior sites of the brain, alpha oscillations (8–12 Hz) are observed. This rhythm is affected by information processing, because its amplitude is modulated by visual input, as was already shown by Hans Berger (1929). Importantly, the alpha rhythm is also affected by top-down influences, as is demonstrated by the fact that its amplitude is modulated in anticipation of a visual stimulus (Foxe et al., 1998, Kelly et al., 2006, Rihs et al., 2007, Sauseng et al., 2005, Thut et al., 2006, Worden et al., 2000, Wyart and Tallon-Baudry, 2008). Similarly, over sensorimotor cortex, so-called mu (8–12 Hz) and beta (15–35 Hz) rhythms are observed, whose amplitudes are reduced over the contralateral hemisphere not only during, but also prior to voluntary movement (Jasper and Penfield, 1949, Nagamine et al., 1996, Pfurtscheller and Lopes da Silva, 1999, Taniguchi et al., 2000, Zhang et al., 2008a). It has further been shown that the sensorimotor mu rhythm is reduced in anticipation of nociceptive stimuli (Babiloni et al., 2003). The present paper provides evidence for another type of pre-stimulus modulation of an ongoing oscillation. Specifically, we show that the amplitude of beta oscillations over sensorimotor cortex is modulated by expectation of a tactile stimulus.

Because sensory afferents enter the cortex in the primary sensory cortices, this is the first neocortical terminal in which information can be gated. In studies measuring the BOLD-signal, expectation-related increases in regional blood flow have been observed in V1 (Kastner et al., 1999, McMains et al., 2007, Ress et al., 2000), S1 (Carlsson et al., 2000), early auditory cortices (Voisin et al., 2006) and even the LGN (O'Connor et al., 2002). Precise localizations on the basis of extra-cranial recordings of human electromagnetic brain activity are generally more problematic. Consequently, studies that implicate primary sensory cortices in anticipatory modulations of neuronal oscillations are rare. The human somatosensory system provides a unique system for investigating the role of primary sensory cortices in relation to expectation-induced modulation of neuronal activity. This is because, in the somatosensory system, only the primary sensory cortex (S1) receives (thalamic) input unilaterally (Burton, 1976, Hari et al., 1993). We made use of this fact by having participants expect either a left or right hand stimulation. Importantly, left and right hand stimulations are processed by the same S2 cortices, but different S1 cortices. By contrasting expected events with a different lateralization we could thus deduce the neuronal origin without the need for assumption-dependent source localization methods. As such, the present paper provides evidence for the involvement of S1 in oscillatory dynamics during expectation.

Empirically, effects of expectation have often been conflated with those of attention (Summerfield and Egner, 2009). For example, in the Posner cueing paradigm (a paradigm used in many of the abovementioned studies) expectation constitutes the primary source for the endogenously directed focus of attention. Anticipatory processes of expectation are, however, not necessarily confined to attended events. In the present study, we therefore examined whether the expectation-induced modulation of pre-stimulus oscillatory activity was restricted to task-relevant stimuli. For this, expectation was manipulated by a predictable spatio-temporal pattern of tactile stimulations. Because stimulus patterns are predictable regardless of their task-relevance, they allow for a dissociation between effects of attentive and non-attentive expectations. Interestingly, we provide evidence that the pre-stimulus modulation of beta oscillations is not restricted to task-relevant and therefore attended events.

Section snippets

Participants

A total of 22 healthy subjects voluntarily participated in the experiment (12 male, mean age: 24 y, range: 20–33 y). Four participants were excluded from the analysis due to excessive artifacts. Two participants returned for a follow-up session, about two months after their first session. All participants provided written consent and were paid in accordance with guidelines of the local ethics committee (CMO Committee on Research Involving Humans subjects, region Arnhem-Nijmegen, the Netherlands).

Behavioral performance

Average detection rates, expressed as the percentage of targets detected, were 69.7 (SD = 27.7) for tactile targets and 75.1 (SD = 24.3) for auditory targets. Few participants detected all targets in either sensory stream. All participants reported the task to be difficult and attention-demanding, consistent with the detection rate.

Pre-stimulus β-activity reflects tactile expectation (a representative participant)

Fig. 2 shows our main result for this single participant: an expectation-induced pre-stimulus modulation of oscillatory activity in the beta band. In Fig. 2A, a

Discussion

We set out to investigate whether expectation of an upcoming tactile event involves a pre-stimulus modulation of neuronal oscillatory activity in human somatosensory cortex, and primarily S1. Additionally, we set out to test whether such a modulation would be restricted to attended events. During expectation of a lateralized tactile event, we observed an accordingly lateralized modulation of neuronal oscillatory activity in the beta band. This modulation resembled the modulation observed

Conclusion

In the present paper we provided evidence that expectation of a tactile stimulation involves a pre-stimulus modulation of neuronal oscillatory activity in sensorimotor cortex. This modulation occurred in the beta band and most likely is produced by a contralateral suppression, originating at least partly from S1. We furthermore provided evidence that such an expectation-induced modulation is not restricted to attended events. We argue that the suppression of beta oscillations over the

Acknowledgments

The authors gratefully acknowledge the support of the BrainGain Smart Mix Programme of the Netherlands Ministry of Economic Affairs and the Netherlands Ministry of Education, Culture and Science. The authors want to thank Norbert Hermesdorf for designing and building the Braille tactile stimulation device, and Pascal de Water for designing and building the electronics of this device.

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