Mapping causal circuit dynamics in stroke using simultaneous electroencephalography and transcranial magnetic stimulation

Camarin E Rolle,Russell Toll,Hersh Trivedi,Wei Wu,Fiona M Baumer,Ketura Berry,Madelleine Garcia,Maarten Lansberg,Joshua T Jordan,Amit Etkin,Marion S Buckwalter,Karen Monusko

doi:10.1186/s12883-021-02319-0

Abstract

BackgroundMotor impairment after stroke is due not only to direct tissue loss but also to disrupted connectivity within the motor network. Mixed results from studies attempting to enhance motor recovery with Transcranial Magnetic Stimulation (TMS) highlight the need for a better understanding of both connectivity after stroke and the impact of TMS on this connectivity. This study used TMS-EEG to map the causal information flow in the motor network of healthy adult subjects and define how stroke alters these circuits.MethodsFourteen stroke patients and 12 controls received TMS to two sites (bilateral primary motor cortices) during two motor tasks (paretic/dominant hand movement vs. rest) while EEG measured the cortical response to TMS pulses. TMS-EEG based connectivity measurements were derived for each hemisphere and the change in connectivity (ΔC) between the two motor tasks was calculated. We analyzed if ΔC for each hemisphere differed between the stroke and control groups or across TMS sites, and whether ΔC correlated with arm function in stroke patients.ResultsRight hand movement increased connectivity in the left compared to the right hemisphere in controls, while hand movement did not significantly change connectivity in either hemisphere in stroke. Stroke patients with the largest increase in healthy hemisphere connectivity during paretic hand movement had the best arm function.ConclusionsTMS-EEG measurements are sensitive to movement-induced changes in brain connectivity. These measurements may characterize clinically meaningful changes in circuit dynamics after stroke, thus providing specific targets for trials of TMS in post-stroke rehabilitation.

Highlights

Motor impairment after stroke is due to direct tissue loss and to disrupted connectivity within the motor network
State‐dependent connectivity The change in connectivity elicited by hand movement (ΔC) significantly differs between Experimental Conditions (F(3,90) = 3.15, p = 0.03), but not between stroke patients and controls (F(1,90) = 1.53, p = 0.22); there is no significant interaction between group and Experimental Condition (F(3,90) = 0.53, p = 0.66)
We find that Transcranial Magnetic Stimulation (TMS)-EEG detects connectivity changes elicited by hand movement selectively when the task motor cortex is stimulated: with this stimulation, connectivity within the active hemisphere increases while connectivity within the passive hemisphere decreases

Summary

Introduction

Motor impairment after stroke is due to direct tissue loss and to disrupted connectivity within the motor network. Several studies using fMRI [8,9,10] and transcranial magnetic stimulation (TMS) [11, 12] have examined the interactions between the two hemispheres after stroke. The TMS-fMRI work of Bestmann et al [5] suggests that in the most severely affected chronic stroke patients, the ipsilateral, healthy hemisphere may facilitate paretic hand movement (for review, see [17, 18]). These complex and patient-specific interactions highlight a need for better tools to measure bihemispheric dynamics after stroke and the influence of therapy on them

Methods

Results

Conclusion