Sub-acute stroke demonstrates altered beta oscillation and connectivity pattern in working memory

Abstract

Introduction: Working memory (WM) is suggested to play a pivotal role in relearning and neural restoration during stroke rehabilitation. Using EEG, this study investigated the oscillatory mechanisms of WM in subacute stroke.

Methods: This study included 48 first subacute stroke patients (26 good-recovery, 22 poor-recovery, based on prognosis after a 4-week period) and 24 matched health controls. We examined the oscillatory characteristics and functional connectivity of the 0-back WM paradigm and assessed their associations with prognosis.

Results: Patients of poor recovery are characterised by a loss of significant beta rebound, beta-band connectivity, as well as impaired working memory speed and performances. Meanwhile, patients with good recovery have preserved these capacities to some extent. Our data further identified beta rebound to be closely associated with working memory speed and performances.

Conclusions: We provided novel findings that beta rebound and network connectivity as mechanistic evidence of impaired working memory in subacute stroke. These oscillatory features could potentially serve as a biomarker for brain stimulation technologies in stroke recovery.

Keywords: EEG; Oscillations; Prognosis; Stroke; Working memory.

Fig. 1

Flowchart for patient inclusion and exclusion

Fig. 2

Working memory task and performances. a) An example of non-target and target stimulus. b) Results of reaction time. Patients with poor recovery had longer reaction time compared to those with good recovery and healthy controls. There was no difference between patients with good-recovery and healthy controls. c). Results of d prime sensitivity. Healthy controls had higher d prime sensitivity compared to patients with good recovery and to those with poor recovery. There was no difference between patients with good recovery and with poor recovery (Pcorrected > 0.5). * denotes p < 0.05, ** denotes p < 0.01

Fig. 3

Event-related changes from baseline. a-c) All three groups demonstrated a decrease in beta power in the central regions (healthy controls: Pcorrected = 0.004, time range = 0.17–0.73 s; good-recovery: Pcorrected = 0.003, time range = 0.22–0.81 s; poor-recovery: Pcorrected = 0.000, time range = 0.20–0.97 s). There was also an increased late beta power in the frontal and parieto-occipital regions in the healthy controls and patients of good-recovery (healthy controls: Pcorrected = 0.000, time range = 0.88–1.80 s; good-recovery: Pcorrected = 0.014, time range = 1.33–1.78 s). This pattern of beta oscillation was not significant in patients with poor recovery (Pcorrected > 0.05). Tagged electrodes in each topolot indicated the significant channels revealed by cluster statistics. The time-frequency representations were plotted with the significant electrodes in the topoplot of (c), or the shared significant electrodes in the two topoplots in (a, b). X denotes p < 0.05. * denotes p < 0.01, dB = decibel

Fig. 4

Group comparisons EEG oscillations. a-b) Patients of poor-recovery demonstrated a larger decrease in early beta power in the frontal and parieto-occipital regions compared to healthy controls and to those of good-recovery (healthy controls: Pcorrected = 0.010, time range = 0.72–1.10 s; good-recovery: Pcorrected = 0.021, time range = 0.70–0.87 s). c-d) Healthy controls demonstrated a larger increase in late beta power in the frontal and parieto-occipital regions compared to patients of good-recovery and to those of poor-recovery (good-recovery: Pcorrected = 0.010, time range = 0.90–1.70 s; poor-recovery: Pcorrected = 0.003, time range = 0.81–1.78 s). Tagged electrodes in each topolot indicated the significant channels revealed by cluster statistics. The time-frequency representations were plotted with the significant electrodes in the topoplot. X denotes p < 0.05. * denotes p < 0.01, dB = decibel

Fig. 5

Correlation results. a-b) Increased beta power in the healthy controls and patients of good-recovery was associated with the faster reaction, as well as with higher d prime sensitivity. In contrast, decreased beta power in the early phase was not associated with either reaction time or d prime sensitivity. All EEG signals were extracted from the significant clusters in the event-related analysis

Fig. 6

EEG connectivity analysis. a) In healthy controls, EEG connectivity data demonstrated increased beta band WPLI (P_corrected = 0.048) between the frontal regions (F4, F8) and parieto-occipital regions (P7, O1). b) In the pooled dataset of healthy controls and good-recovery, EEG connectivity data indicated increased beta band WPLI (P_corrected = 0.013) between the frontal regions (AF3, FP1, FP2, F8) and parieto-occipital regions (O1, PO3), as well as increased interactions between parietal and occipital regions (P3, P7, PO3, O1). L and R denote left and right hemispheres respectively