The spontaneous fluctuation of the excitability of a single node modulates the internodes connectivity: a TMS-EEG study

Abstract

Brain effective connectivity can be tracked by cerebral recruitments evoked by transcranial magnetic stimulation (TMS), as measured by simultaneous electroencephalography (TMS-EEG). When TMS is targeting the primary motor area, motor evoked potentials (MEPs) can be collected from the "target" muscles. The aim of this study was to measure whether or not effective brain connectivity changes with the excitability level of the corticospinal motor pathway (CSMP) as parameterized by MEP amplitude. After averaging two subgroups of EEG-evoked responses corresponding to high and low MEP amplitudes, we calculated the individual differences between them and submitted the grand average to sLORETA algorithm obtaining localized regions of interest (RoIs). Statistical differences of RoI recruitment strength between low and high CSMP excitation was assessed in single subjects. Preceding the feedback arrival, neural recruitment for stronger CSMP activation were weaker at 6-10 ms of homotopic sensorimotor areas BA3/4/5 of the right nonstimulated hemisphere (trend), weaker at 18-25 ms of left parietal BA2/3/40, and stronger at 26-32 ms of bilateral frontal motor areas BA6/8. The proposed method enables the tracking of brain network connectivity during stimulation of one node by measuring the strength of the connected recruited node activations. Spontaneous increases of the excitation of the node originating the transmission within the hand control network gave rise to dynamic recruitment patterns with opposite behaviors, weaker in homotopic and parietal circuits, stronger in frontal ones. The effective connectivity within bilateral circuits orchestrating hand control appeared dynamically modulated in time even in resting state as probed by TMS.

Keywords: cerebral connectivity as localized cortical recruitment; spontaneous fluctuation of excitability; transcranial magnetic stimulation simultaneous to electroencephalographic recordings.

Figure 1

Experimental setup. Left neuronavigated TMS setup: the subject lies relaxed on a semireclined chair and the coil position is monitored throughout the session duration. The hand with surface electrodes for FDI muscle recordings is evidenced in the inset (white arch, ground symbol indicates belly‐tendon montage, while on the wrist dorsum is the ground electrode). Right EEG and EMG signals after artifact removal. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 2

Procedure to identify high and low motor pathway excitation levels. Left MEP peak‐to‐peak amplitude for each trial of a representative subject, with largest/smallest third (red/blue) of trials used to select the EEG epochs to obtain individual EEG_high and EEG_low averages. Right average of largest/smallest third (red/blue) MEPs in the [−10, 50] ms time window.

Figure 3

Cerebral areas recruited differently at low and high CSMP excitation levels by left M1‐TMS. Top superimposition in a butterfly plot of the TMS evoked potentials recorded at electrodes common to all subjects in the [−10, 100] ms time window, obtained from grand average of the differences between high and low CSMP. Bottom region of activation at corresponding latencies (ms), with color code referring to lower/higher (blue/red) activation corresponding to higher/lower CSMP excitation level, trends indicated by dashed lines and significant differences by solid lines.