Simultaneous EEG-NIRS Measurement of the Inferior Parietal Lobule During a Reaching Task With Delayed Visual Feedback

Abstract

We investigated whether the inferior parietal lobule (IPL) responds in real-time to multisensory inconsistency during movement. The IPL is thought to be involved in both the detection of inconsistencies in multisensory information obtained during movement and that obtained during self-other discrimination. However, because of the limited temporal resolution of conventional neuroimaging techniques, it is difficult to distinguish IPL activity during movement from that during self-other discrimination. We simultaneously conducted electroencephalography (EEG) and near-infrared spectroscopy (NIRS) with the goal of examining IPL activity with a high spatiotemporal resolution during single reaching movements. Under a visual feedback-delay condition, gamma event-related synchronization (γ-ERS), i.e., an increase in gamma (31-47 Hz) EEG power occurred during reaching movements. This γ-ERS is considered to reflect processing of information about prediction errors. To integrate this temporal information with spatial information from the NIRS signals, we developed a new analysis technique that enabled estimation of the regions that show a hemodynamic response characterized by EEG fluctuation present in the visual feedback-delay condition. As a result, IPL activity was explained by γ-ERS specific to visual feedback delay during movements. Thus, we succeeded in demonstrating real-time activation of the IPL in response to multisensory inconsistency. However, we did not find any correlation between either IPL activity or γ-ERS with the sense of agency. Therefore, our results suggest that while the IPL is influenced by prediction error signals, it does not engage in direct processing underlying the conscious experience of making a movement, which is the foundation of self-other discrimination.

Keywords: electroencephalography; event-related (de)synchronization; inferior parietal lobule; near-infrared spectroscopy; psychophysiological interaction; simultaneous measurement; visual feedback delay.

FIGURE 1

Experimental setup and task procedure. Participants performed a reaching task using a tough panel display (Zama et al., 2017). They observed a moving image of their right hand that was projected onto a mirror. In the Delay condition, the feedback image was delayed to modulate the sense of agency with respect to their hand. Participants were instructed to swipe their right index finger across the touch panel display from the home position to left/right goal areas via a central square. They were instructed to perform the movements as quickly and accurately as possible after seeing the “go” cue.

FIGURE 2

Location of EEG electrodes and NIRS optodes arranged in the customized cap. Both sensors were placed over the frontoparietal areas that are important for visuomotor function.

FIGURE 3

Schematic chart of our ERS/D-based PPI analysis. In this technique, the hemodynamic response (explained variable X_i) in a region i is estimated as a superposition of impulse responses. The regression coefficient is calculated so that the error (e) between the estimated hemodynamic response (X_i) and the observed hemodynamic response is minimized. This analysis can be interpreted as estimating the area where the contribution from a certain ERS/D is increased by an event (psychological or experimental factor).

FIGURE 4

Behavioral results. All error bars represent the mean SE. (A) Trajectory error was significantly increased by the delay in visual feedback. (B) Endpoint error was also significantly increased by the delay. (C) SoA score dropped with the delay. (D) The duration of reaching movements was significantly larger in the Delay condition than in the Non-delay condition but did not affect task performance. Neither maximum reaching speed (E) nor response time (F) differed between conditions.

FIGURE 5

Sequential topological maps of EEG power. γ-ERS and α-ERD during movement differed significantly between conditions (p < 0.05, FDR corrected). The γ-ERS specific to the Delay condition occurred at the central area, while α-ERD occurred around the parietal area.

FIGURE 6

The results of cross-frequency coupling analysis between the alpha- and gamma-rhythms. The comparison between Delay and Non-delay conditions of phase-amplitude coupling (PAC, left) and phase-phase coupling (PPC, right). The dashed lines in each panel denote the threshold value (p < 0.05, Bonferroni corrected). At the C1 electrode, the PAC in the Delay condition was significantly larger than that in the Non-Delay condition.

FIGURE 7

The phase synchronization of alpha-rhythm between the central and the parietal area. The black dotted lines and red dashed lines in each panel denote the threshold values (p < 0.1 and p < 0.05, respectively). The increase in synchrony was marginally significant between the left central electrode (C1) and the right parietal electrode (P4) in either condition (p < 0.1, Bonferroni corrected).

FIGURE 8

Results of ERS/D-based PPI analysis. The result showed activation of right angular and supramarginal gyri, which was explained by the γ-ERS that occurred when visual feedback was delayed (p < 0.05). This delay-specific activity in the right IPL could not explained by α-ERD.

FIGURE 9

Results of the LM analysis. The areas identified by green dots represent activation areas common to both the Delay and Non-delay conditions. Several regions (blue dots) were activated only during the Delay condition.