Alpha Phase Synchronization of Parietal Areas Reflects Switch-Specific Activity During Mental Rotation: An EEG Study

Abstract

Action selection is typically influenced by the history of previously selected actions (the immediate motor history), which is apparent when a selected action is switched from a previously selected one to a new one. This history dependency of the action selection is even observable during a mental hand rotation task. Thus, we hypothesized that the history-dependent interaction of actions might share the same neural mechanisms among different types of action switching tasks. An alternative hypothesis is that the history dependency of the mental hand rotation task might involve a distinctive neural mechanism from the general action selection tasks so that the reported observation with the mental hand rotation task in the previously published literature might lack generality. To refute this possibility, we compared neural activity during action switching in the mental hand rotation with the general action switching task which is triggered by a simple visual stimulus. In the experiment, to focus on temporal changes in whole brain oscillatory activity, we recorded electroencephalographic (EEG) signals while 25 healthy subjects performed the two tasks. For analysis, we examined functional connectivity reflected in EEG phase synchronization and analyzed temporal changes in brain activity when subjects switched from a previously selected action to a new action. Using a clustering-based method to identify functional connectivity reflected in time-varying phase synchronization, we identified alpha-power inter-parietal synchronization that appears only during switching of the selected action, regardless of the hand laterality in the presented image. Moreover, the current study revealed that for both tasks the extent of this alpha-power inter-parietal synchronization was altered by the history of the selected actions. These findings suggest that alpha-power inter-parietal synchronization is engaged as a form of switching-specific functional connectivity, and that switching-related activity is independent of the task paradigm.

Keywords: action switching; dynamic time warping; electroencephalography; functional connectivity; mental rotation; parietal cortex; phase synchronization; weighted phase-lag index.

Figure 1

Experimental settings. (A) Experimental environment. Subjects were instructed to judge the hand laterality of an image presented on a monitor. (B) Channel location. Fifteen standard scalp electrodes, specifically, Fp1, Fpz, Fp1, F3, Fz, F4, C3, Cz, C4, P3, Pz, P4, O1, Oz, and O2, were selected using the International 10–20 system. (C) Rotating pattern of presented stimuli for the mental hand rotation task. (D) Experimental procedures for the mental hand rotation task. Images of a left or right hand were randomly presented on the computer monitor and shown until the subject made a response. To report the response, subjects were required to press the pedal with the foot corresponding to the laterality of the presented stimuli. After the response, the stimulus was replaced by a fixation cross, which was shown for 1 s until the next stimulus was presented. (E) Experimental procedures for the command-to-response task. Left or right angle brackets were randomly presented on the computer monitor and shown until the subject made a response. To report the response, subjects were required to press the pedal with the foot corresponding to the laterality of the presented stimuli. After the response, the stimulus was replaced by a fixation cross, which was shown for 1 s until the next stimulus was presented. (F,G) Definition of the trial-type (switch or repeat) for each task.

Figure 2

Estimation of functional connectivity. First, we computed the z-scored wPLI for each channel pair (105 pairs), then calculated the group-averaged values. Second, we evaluated the distance matrix using the DTW algorithm (see Materials and Methods section for detail). Finally, applying hierarchical clustering, we visualized the functional structures and cluster-averaged time-course of z-scored wPLIs for each identified cluster. These procedures were applied to each trial condition (switch or right) depending on the laterality condition (left or right).

Figure 3

Behavioral results. (A) Mean RTs for all subjects for each presented angle (red: repeat trial, blue: switch trial). (B) Comparison of RTs between the two tasks for each trial type. MR task and CR task refer to the mental hand rotation task and command-to-response task, respectively. Asterisks (*) indicate p < 0.05 by paired t-test with FDR correction. Error bars indicate the standard error of the mean.

Figure 4

Estimated clusters and functional connectivity based on time series matching of z-scored wPLIs using DTW (MR task: switch trial, alpha band). (A) Estimated significant clusters of functional connectivity for left switch trials. Six of eight clusters were estimated to be significant. (B) Estimated significant clusters of functional connectivity for right switch trials. Six of eight clusters were estimated to be significant. Marker size of the electrodes for each topographical location corresponds with the node degree of connectivity. (C,D) Cluster-averaged z-scored wPLIs for each hand in the switch trials (upper panels: stimulus-locked average; lower panels: response-locked average). Bold black lines indicate a significant level of temporal changes in cluster-averaged phase-synchronization values (p < 0.05 with FDR correction).

Figure 5

Estimated clusters and functional connectivity based on time series matching of z-scored wPLIs using DTW (MR task: repeat trial, alpha band). (A) Estimated significant clusters of functional connectivity for left repeat trials. Three of five clusters were estimated to be significant. (B) Estimated significant clusters of functional connectivity for right repeat trials. All four clusters were estimated to be significant. Marker size of the electrodes for each topographical location corresponds to the node degree of connectivity. (C,D) Cluster-averaged z-scored wPLIs for each hand in the repeat trials (upper panels: stimulus-locked average; lower panels: response-locked average). Bold black lines indicate a significant level of temporal changes in cluster-averaged value of phase-synchronization (p < 0.05 with FDR correction).

Figure 6

Comparison of the cluster-by-cluster similarity of the connectivity patterns (switch trials). (A) A matrix indicating the cluster-by-cluster similarity between left and right hand in the mental hand rotation task for the switch trials. (B) Pairs of most similar clusters between the two laterality conditions in the mental hand rotation task for switch trials and comparison of the temporal responses. (C,D) These also show the results of the cluster-by-cluster similarity analysis of the connectivity patterns in the command-to-response task for the switch trials.

Figure 7

Comparison of the cluster-by-cluster similarity of the connectivity patterns (switch trials; mental hand rotation task vs. command-to-response task). (A) A matrix indicating the cluster-by-cluster similarity between the mental hand rotation and command-to-response task for the left condition in the switch trials. (B) Pairs of most similar clusters between the two tasks for the left conditions in the switch trials and comparison of the temporal responses. (C,D) These also show the results of the cluster-by-cluster similarity analysis of the connectivity patterns between the two tasks for the right condition in the switch trials. MR and CR indicate the mental hand rotation and command-to-response task, respectively.