Anticipation of somatosensory and motor events increases centro-parietal functional coupling: An EEG coherence study

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Abstract

Objective

Does functional coupling of centro-parietal EEG rhythms selectively increase during the anticipation of sensorimotor events composed by somatosensory stimulation and visuomotor task?

Methods

EEG data were recorded in (1) ‘simultaneous’ condition in which the subjects waited for somatosensory stimulation at left hand concomitant with a Go (or NoGo) visual stimulus triggering (50%) right hand movements and in (2) ‘sequential’ condition where the somatosensory stimulation was followed (+1.5 s) by a visuomotor Go/NoGo task. Centro-parietal functional coupling was modeled by spectral coherence. Spectral coherence was computed from Laplacian-transformed EEG data at delta–theta (2–7 Hz), alpha (8–14 Hz), beta 1 (15–21 Hz), beta 2 (22–33 Hz), and gamma (34–45 Hz) rhythms.

Results

Before ‘simultaneous’ sensorimotor events, centro-parietal coherence regions increased in both hemispheres and at all rhythms. In the ‘sequential’ condition, right centro-parietal coherence increased before somatosensory event (left hand), whereas left centro-parietal coherence increased before subsequent Go/NoGo event (right hand).

Conclusions

Anticipation of somatosensory and visuomotor events enhances contralateral centro-parietal coupling of slow and fast EEG rhythms.

Significance

Predictable somatosensory and visuomotor events are anticipated not only by synchronization of cortical pyramidal neurons generating EEG power in parietal and primary sensorimotor cortical areas (Babiloni C, Brancucci A, Capotosto P, Arendt-Nielsen L, Chen ACN, Rossini PM. Expectancy of pain is influenced by motor preparation: a high-resolution EEG study of cortical alpha rhythms. Behav. Neurosci. 2005a;119(2):503–511; Babiloni C, Brancucci A, Pizzella V, Romani G.L, Tecchio F, Torquati K, Zappasodi F, Arendt-Nielsen L, Chen ACN, Rossini PM. Contingent negative variation in the parasylvian cortex increases during expectancy of painful sensorimotor events: a magnetoencephalographic study. Behav. Neurosci. 2005b;119(2):491–502) but also by functional coordination of these areas.

Introduction

Sensorimotor events modulate the activity of centro-parietal areas not only during ongoing sensorimotor events but also during their anticipation. Recent studies have reported marked negative event-related potentials over posterior midline and bilateral central areas during the expectancy of painful (Babiloni et al., 2004b, Babiloni et al., 2004a) or non-painful (Babiloni et al., 2005c) sensorimotor interactions comprising somatosensory stimulations at the left arm and motor Go/NoGo task triggering right hand movements. In the case of painful sensorimotor interactions, the cortical potentials increase in amplitude at secondary somatosensory cortex also (Babiloni et al., 2005b). In parallel to the event-related potentials, the anticipation of the sensorimotor interactions modulates brain electroencephalographic (EEG) rhythms. In this respect, the alpha range (about 8–14 Hz) has been particularly investigated as alpha event-related desynchronization/synchronization (ERD/ERS; Pfurtscheller and Lopes da Silva, 1999). It has been shown that the anticipatory alpha ERD was higher in amplitude during painful sensorimotor events as compared to the alpha ERD preceding non-painful sensorimotor events or the simple pain anticipation (Babiloni et al., 2005a). The modulation of alpha rhythms has also been implicated during the expectancy of cognitive and visuomotor events (Babiloni et al., 2004a, Gomez et al., 2004, Klimesch, 1996, Klimesch, 1997, Klimesch, 1999, Klimesch et al., 1996, Klimesch et al., 1998). It has been shown that not only alpha but also slow (about 2–7 Hz), beta (about 15–33 Hz), and gamma (about 34–45 Hz) rhythms are modulated during cortical information processing related to a vast bulk of sensorimotor transformations (Pfurtscheller and Lopes da Silva, 1999).

The mentioned EEG studies suggest that a putative role of parietal areas is to integrate exteroceptive and proprioceptive information within a compatible reference frame (Tomberg and Desmedt, 1999). Together with central motor systems, parietal areas would also contribute to the transformation of sensory information into operative motor commands (Fogassi and Luppino, 2005). However, these studies have just disclosed the topographical distribution of the cortical activity, without testing whether the activity of the central and parietal areas was functionally interrelated by a functional coupling of their EEG rhythms. Keeping in mind these notions, the present study tested the working hypothesis that parietal and central cortical areas specifically increase the functional coupling of their EEG rhythms during the expectancy of contralateral somatosensory or motor events. For this aim, two conditions were included in the experimental design. In the ‘simultaneous’ condition, subjects expected parallel somatosensory stimulus to left hand and visual stimulus maybe triggering right hand movement. In the ‘sequential’ condition, they received that visual stimulus 1.5 s after the somatosensory stimulus. This design disentangled in time the specific preparatory processes for the somatosensory stimulus and for the visuomotor task. In the ‘sequential’ condition, 1 s period preceding the somatosensory stimulus could isolate the anticipatory somatosensory processes in the contralateral right hemisphere, while 1 s period preceding the visual stimulus could isolate the anticipatory visuomotor processes in the contralateral left hemisphere. To roughly pair the related attentional processes to the intrapersonal space, both conditions required that attention was focused on subject's hands. It should be remarked that the present EEG study did not aim at comparing functional centro-parietal cortical coupling during the expectancy of somatosensory stimuli vs. visuomotor demands. Indeed, there were unpaired modalities engaged in the two conditions. The somatosensory stimulus just activated the hand somatosensory systems, while the right hand movement implied the activation of both somatosensory (somatosensory reafferents) and motor systems.

In an attempt of addressing the working hypothesis, centro-parietal functional coupling was estimated by the analysis of EEG spectral coherence. In precedence, the EEG spectral coherence between electrode pairs has been interpreted as an evidence of functional coupling (Gerloff et al., 1998, Thatcher et al., 1986), mutual information exchange (Rappelsberger and Petsche, 1988), functional co-ordination (Gevins et al., 1998), and integrity of connection pathways (Locatelli et al., 1998). The basic idea of these definitions is that when the activity of two cortical areas is functionally coordinated, the EEG rhythms of these cortical areas show linear interrelatedness. This idea has been corroborated by several lines of evidence. It has been demonstrated that perceptive, cognitive, and motor processes are associated with the parallel functional coupling of slow (Serrien et al., 2004, Urbano et al., 1998), alpha (Sauseng et al., 2005), and beta (Serrien et al., 2004, Wheaton et al., 2005) EEG rhythms, as a function of the extension and kind of the neural networks engaged (Pfurtscheller and Lopes da Silva, 1999, von Stein and Sarnthein, 2000).

Section snippets

Materials and methods

Some procedures (experimental design, EEG recordings and preliminary data analysis) of the current investigation have been previously described in the context of a study with a completely different aim. In that study (Babiloni et al., 2005c), negative event-related potentials (i.e. contingent negative variation) preceding sensorimotor events were mapped. In contrast, the current investigation focused on the centro-parietal coupling of EEG rhythms before sensorimotor events, as revealed by

Functional coupling as revealed by spectral coherence between electrodes

Fig. 2 illustrates the grand average of coherence spectra at centro-parietal (C3–P3, C4–P4) electrode pairs during REST, PRE-somatosensory stimulus, and POST-somatosensory stimulus periods of the two conditions, namely the ‘Go/NoGo 0’ condition using ‘simultaneous’ sensorimotor events and the ‘Go/NoGo+1.5’ condition using ‘sequential’ sensorimotor events. In all periods and in both conditions, the absolute coherence values ranged from 0.3 to 0.5 for the left centro-parietal electrode pairs

Discussion

Is the anticipation of somatosensory or motor events related to an increase of centro-parietal functional coupling at the contralateral hemisphere (as revealed by EEG spectral coherence)? It was observed that the anticipation of the only somatosensory stimulation to the left hand just increased centro-parietal functional coupling in the contralateral right hemisphere. Conversely, the anticipation of the only right-hand movements just increased centro-parietal functional coupling in the

Acknowledgements

We thank Dr Paolo Capotosto for their helpful technical assist. We thank also Prof. Fabrizio Eusebi for his continuous support. The research was granted by Danish Technical Research Council and Association Fatebenefratelli for the Research (AFaR).

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