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. 2014 Jan;27(1):172-91.
doi: 10.1007/s10548-013-0277-y. Epub 2013 Mar 8.

Modulation of EEG functional connectivity networks in subjects undergoing repetitive transcranial magnetic stimulation

Mouhsin M Shafi  1 , M Brandon Westover, Lindsay Oberman, Sydney S Cash, Alvaro Pascual-Leone
Affiliations

Modulation of EEG functional connectivity networks in subjects undergoing repetitive transcranial magnetic stimulation

Mouhsin M Shafi et al. Brain Topogr. 2014 Jan.

Abstract

Transcranial magnetic stimulation (TMS) is a noninvasive brain stimulation technique that utilizes magnetic fluxes to alter cortical activity. Continuous theta-burst repetitive TMS (cTBS) results in long-lasting decreases in indices of cortical excitability, and alterations in performance of behavioral tasks. We investigated the effects of cTBS on cortical function via functional connectivity and graph theoretical analysis of EEG data. Thirty-one channel resting-state EEG recordings were obtained before and after 40 s of cTBS stimulation to the left primary motor cortex. Functional connectivity between nodes was assessed in multiple frequency bands using lagged max-covariance, and subsequently thresholded to construct undirected graphs. After cTBS, we find widespread decreases in functional connectivity in the alpha band. There are also simultaneous increases in functional connectivity in the high-beta bands, especially amongst anterior and interhemispheric connections. The analysis of the undirected graphs reveals that interhemispheric and interregional connections are more likely to be modulated after cTBS than local connections. There is also a shift in the topology of network connectivity, with an increase in the clustering coefficient after cTBS in the beta bands, and a decrease in clustering and increase in path length in the alpha band, with the alpha-band connectivity primarily decreased near the site of stimulation. cTBS produces widespread alterations in cortical functional connectivity, with resulting shifts in cortical network topology.

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Figures

Fig. 1
Fig. 1
Experimental setup and data processing for each subject. EEG was recorded for up to 30 min with the subject in the eyes-closed, awake, resting state. This was followed by administration of 40 s of continuous theta burst repetitive TMS (cTBS). Afterwards, an additional 10 min of EEG data was recorded with the subject in the eyes-closed, awake, resting state. The EEG data was subsequently processed offline. The data was downsampled to 512 Hz, re-referenced to an average reference, and then detrended. Segments of data with artifact were subsequently removed, and multiple continuous 3-second segments of artifact-free data identified. Lagged max-covariance (MC) analysis was done on these 3-second segments, then average max-covariance values for each electrode pair were obtained by averaging across the values for individual 3 s segments. Subsequently a MC matrix was built. The MC matrices were thresholded to produce undirected graphs. Electrodes were grouped by hemisphere (left; blue = left, pink = right, clear = midline) or anterior–posterior axis (right; blue = anterior, pink = posterior, clear = midline)
Fig. 2
Fig. 2
Functional connectivity changes after cTBS. EEG channels with a significant (Bonferroni adjusted p < 0.05) increase (red) or decrease (green) in functional connectivity, as measured via lagged max-correlation, in the broadband (4–30 Hz) frequency range, for each of the 12 subjects with significant changes in functional connectivity after cTBS (1 subject had no significant changes)
Fig. 3
Fig. 3
Max-correlation matrices and average functional connectivity changes. a shows the mean max-correlation matrices averaged across all subjects in the 4–30 Hz (broadband) frequency range before (left) and after (right) cTBS. The order of the electrodes is: Fp1, F7, F3, FC5, FC1, T7, C5, C3, C1, CP5, CP1, P7, P3, O1, Fz, Cz, Pz, Oz, Fp2, F8, F4, FC6, FC2, T8, C4, C2, CP6, CP2, P8, P4, O2. b shows the EEG channels with significant (unadjusted p < 0.0005) changes in functional connectivity after cTBS, across subjects, in each of the different frequency bands. Connections with increased connectivity are illustrated in red, connections with decreased connectivity are drawn in green
Fig. 4
Fig. 4
Frequency and region-specific changes in connection strength. a The average (across subjects) percentage of connections significantly changed after cTBS as a function of frequency band and region. b The average percentage of connections strengthened after cTBS. c The average percentage of connections weakened after cTBS. d The strengthening index (percentage of connections strengthened × 2/percentage of connections changed); A value greater than 1 indicates that more connections were strengthened than weakened, whereas a value less than 1 indicates that more connections were weakened. A = connection between two anterior electrodes, P = connection between two posterior electrodes, IR = interregional connection between an anterior and posterior electrode
Fig. 5
Fig. 5
Frequency and hemisphere-specific changes in connection strength. a The average percentage of connections significantly changed after cTBS as a function of frequency band and hemisphere. b The average percentage of connections strengthened after cTBS. c The average percentage of connections weakened after cTBS. d The strengthening index (defined in Fig. 4 legend)
Fig. 6
Fig. 6
Network topologies and cTBSin fixed-density networks. a Fixed-density networks for the average (across-subject) lagged max covariance data in different frequency bands. These graphs are constructed by applying a threshold to produce networks with a mean nodal connectivity degree of four (an average of four connections per node), with thresholds set independently in both the pre-cTBS and post-cTBS periods. Connections present both pre- and post-cTBS are depicted in black, connections present only prior to cTBS in green, and connections present only after cTBS are shown in red. b The percentage of broad-band connections that are present and stable (present both before and after rTMS) as a function of hemisphere and density. c The broad-band modulation index (percent of connections modified/percentage of connections present in either or both periods) as a function of hemisphere and density. d The percentage of broad-band connections that are present and stable as a function of region and density. e The broad-band modulation index as a function of region and density
Fig. 7
Fig. 7
Network topologies and cTBS in variable density networks. a Variable-density networks in different frequency bands. The thresholds used to construct these graphs are selected to produce networks with a mean nodal degree of four in the pre-cTBS period; the same threshold is then applied to the data from the post-cTBS period. Connections present both pre- and post-cTBS are depicted in black, connections present only prior to cTBS in green, and connections present only after cTBS are shown in red. b The strengthening index (percentage of connections strengthened × 2/percentage of connections changed) in the alpha band as a function of hemisphere and density. c The strengthening index in the alpha band as a function of region and density. d The strengthening index in the high-beta band as a function of hemisphere and density. e The strengthening index in the high-beta band as a function of region and density
Fig. 8
Fig. 8
Graph theory metrics. a Clustering coefficient pre- and post-cTBS as a function of density in the broad band in the fixed-density networks. b Clustering coefficient in the theta band in the fixed-density networks. c Clustering coefficient in the in the low-beta band in the fixed-density networks. d Channels with significant changes in node degree after cTBS in the variable-density networks. The green dots indicate electrodes with a significant decrease in node degree after rTMS, while the red dots indicate electrodes with a significant increase in node degree. No significant changes were seen in other frequency bands
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