μ-suppression during action observation and execution correlates with BOLD in dorsal premotor, inferior parietal, and SI cortices

Abstract

The discovery of mirror neurons in the monkey, that fire during both the execution and the observation of the same action, sparked great interest in studying the human equivalent. For over a decade, both functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) have been used to quantify activity in the human mirror neuron system (MNS)-yet, little is still known about how fMRI and EEG measures of the MNS relate to each other. To test the frequent assumption that regions of the MNS as evidenced by fMRI are the origin of the suppression of the EEG μ-rhythm during both action execution and observation, we recorded EEG and BOLD-fMRI signals simultaneously while participants observed and executed actions. We found that the suppression of the μ-rhythm in EEG covaried with BOLD activity in typical MNS regions, inferior parietal lobe (IPL), dorsal premotor (dPM) and primary somatosensory cortex (BA2), during both action observation and execution. In contrast, in BA44, only nonoverlapping voxels correlated with μ-suppression during observation and execution. These findings provide direct support for the notion that μ-suppression is a valid indicator of MNS activity in BA2, IPL, and dPM, but argues against the idea that mirror neurons in BA44 are the prime source of μ-suppression. These results shed light on the neural basis of μ-suppression and provide a basis for integrating more closely the flourishing but often separate literatures on the MNS using fMRI and EEG.

Figure 1.

A, Snapshots from the different experimental conditions. B, Percentage μ-power change relative to average baseline power in C3 while participants observed or performed actions within the scanner environment and while participants performed the Manipulate_EXE condition in the pilot experiment. *p < 0.05, **p < 0.01, ***p < 0.001. t tests against zero (= baseline) when over a bar or matched-sample t test when over square brackets. C, sVx fMRI localizer, i.e., voxels activated during action execution (Manipulate_EXE-Eye_EXE, punc<0.001, red), during action observation (Manipulate_OBS-Move_OBS, punc<0.01 and Manipulate_OBS-Static_OBS, punc<0.01, green) or both (white, sVx). D, Comparison of voxels significantly activated during Squeeze_EXE (black) and Manipulate_EXE (yellow). E, Voxels with μ-power correlating negatively with BOLD signal during OBS (p_unc < 0.001, all clusters survive p_FDR < 0.05). F, Same for Squeeze_EXE. G, sVx (white as in C), voxels correlating with μ-power suppression during observation and execution (i.e., overlap of E and F, blue), and their overlap (pink).