Task-dependent changes in cortical excitability and effective connectivity: A combined TMS-EEG study

Department of Psychiatry, University of Wisconsin-Madison, 6001 Research Park Blvd., Madison, WI 53719, USA.
Journal of Neurophysiology (Impact Factor: 2.89). 02/2012; 107(9):2383-92. DOI: 10.1152/jn.00707.2011
Source: PubMed


The brain's electrical response to transcranial magnetic stimulation (TMS) is known to be influenced by exogenous factors such as the frequency and intensity of stimulation and the orientation and positioning of the stimulating coil. Less understood, however, is the influence of endogenous neural factors, such as global brain state, on the TMS-evoked response (TMS-ER). In the present study, we explored how changes in behavioral state affect the TMS-ER by perturbing the superior parietal lobule (SPL) with single pulses of TMS and measuring consequent differences in the frequency, strength, and spatial spread of TMS-evoked currents during the delay period of a spatial short-term memory task and during a period of passive fixation. Results revealed that task performance increased the overall strength of electrical currents induced by TMS, increased the spatial spread of TMS-evoked activity to distal brain regions, and increased the ability of TMS to reset the phase of ongoing broadband cortical oscillations. By contrast, task performance had little effect on the dominant frequency of the TMS-ER, both locally and at distal brain areas. These findings contribute to a growing body of work using combined TMS and neuroimaging methods to explore task-dependent changes in the functional organization of cortical networks implicated in task performance.

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Available from: Bradley R Postle, Aug 05, 2014
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    • "Variability in the effects of TMS have been reported across a wide variety of different stimulation protocols and locations [6]–[12]. Many factors have been proposed to contribute to this variability [5], and these can broadly be split into (1) static subject-specific variables (e.g., individuals’ age [12], genetic makeup [17], and variability in the activation of inhibitory interneurons of individuals [7]), and (2) fluctuating, site- or state-specific variables (e.g., previous physical activity [14], relationship between TMS and underlying electrophysiological fluctuations [8], [85], [86], geometry of underlying neural tissue [13], fluctuations in TMS thresholds across days and sites, and, in this study, variability in the time between TMS sessions). All of these factors could have contributed to the variability observed in our study. "
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    ABSTRACT: Transcranial Magnetic Stimulation (TMS) is an important tool for testing causal relationships in cognitive neuroscience research. However, the efficacy of TMS can be variable across individuals and difficult to measure. This variability is especially a challenge when TMS is applied to regions without well-characterized behavioral effects, such as in studies using TMS on multi-modal areas in intrinsic networks. Here, we examined whether perfusion fMRI recordings of Cerebral Blood Flow (CBF), a quantitative measure sensitive to slow functional changes, reliably index variability in the effects of stimulation. Twenty-seven participants each completed four combined TMS-fMRI sessions during which both resting state Blood Oxygen Level Dependent (BOLD) and perfusion Arterial Spin Labeling (ASL) scans were recorded. In each session after the first baseline day, continuous theta-burst TMS (TBS) was applied to one of three locations: left dorsolateral prefrontal cortex (L dlPFC), left anterior insula/frontal operculum (L aI/fO), or left primary somatosensory cortex (L S1). The two frontal targets are components of intrinsic networks and L S1 was used as an experimental control. CBF changes were measured both before and after TMS on each day from a series of interleaved resting state and perfusion scans. Although TBS led to weak selective increases under the coil in CBF measurements across the group, individual subjects showed wide variability in their responses. TBS-induced changes in rCBF were related to TBS-induced changes in functional connectivity of the relevant intrinsic networks measured during separate resting-state BOLD scans. This relationship was selective: CBF and functional connectivity of these networks were not related before TBS or after TBS to the experimental control region (S1). Furthermore, subject groups with different directions of CBF change after TBS showed distinct modulations in the functional interactions of targeted networks. These results suggest that CBF is a marker of individual differences in the effects of TBS.
    Full-text · Article · Jul 2014 · PLoS ONE
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    • "Theoretically, the level of output from the primary motor cortex in response to identical consecutive stimuli could be used as an indicator of connectivity strength and of short-term changes in the network governing M1 excitability , and the level of output could be largely indicative of changes in synaptic efficacy within network connections [Destexhe and Marder, 2004; Erchova and Diamond, 2004; Johnson et al., 2012; Steinke and Gal an, 2011]. Over the last 25 years, a number of specific methods have been developed to identify transient modifications in the functional coupling of distributed neuronal assemblies via electroencephalography (EEG) and magnetoencephalographic (MEG) recordings [Andrew and Pfurtscheller, 1996; Bressler et al., 1993; Lachaux et al., 1999; M€ a€ att€ a et al., 2010; Rodriguez et al., 1999; Vecchio et al., 2010; Zeitler et al., 2006] or by transcranial magnetic stimulation [TMS; Barker et al., 1985; Basso et al.,2006; Hallett, 2000; Kujirai et al., 1993; Rossini et al., 1994]. "
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    ABSTRACT: Motor evoked potentials (MEPs) elicited by a train of consecutive, individual transcranial magnetic stimuli demonstrate fluctuations in amplitude with respect to time when recorded from a relaxed muscle. The influence of time-varying, instantaneous modifications of the electroencephalography (EEG) properties immediately preceding the transcranial magnetic stimulation (TMS) has rarely been explored. The aim of this study was to investigate the influence of the pre-TMS motor cortex and related areas EEG profile on time variants of the MEPs amplitude. MRI-navigated TMS and multichannel TMS-compatible EEG devices were used. For each experimental subject, post-hoc analysis of the MEPs amplitude that was based on the 50th percentile of the MEPs amplitude distribution provided two subgroups corresponding to "high" (large amplitude) and "low" (small amplitude). The pre-stimulus EEG characteristics (coherence and spectral profile) from the motor cortex and related areas were analyzed separately for the "high" and "low" MEPs and were then compared. On the stimulated hemisphere, EEG coupling was observed more often in the high compared to the low MEP trials. Moreover, a paradigmatic pattern in which TMS was able to lead to significantly larger MEPs was found when the EEG of the stimulated motor cortex was coupled in the beta 2 band with the ipsilateral prefrontal cortex and in the delta band with the bilateral centro-parietal-occipital cortices. This data provide evidence for a statistically significant influence of time-varying and spatially patterned synchronization of EEG rhythms in determining cortical excitability, namely motor cortex excitability in response to TMS. Hum Brain Mapp, 2013. © 2013 Wiley Periodicals, Inc.
    Full-text · Article · May 2014 · Human Brain Mapping
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    • "The data from the 61-channel scalp EEG (and 1-channel eye-related potential) in all conditions were first segmented in epochs from 1,500 ms before and 1,000 ms after the target time, and all of the segmented data was bunched together for each subject. Next, an independent component (IC) analysis with extended infomax algorithm (Bell and Sejnowski, 1995; Lee et al., 1999) was applied to the EEG data in order to identify and remove the components reflecting TMS-related artifacts and eye-blink- and/or eye-movement-related activities (Jung et al., 2000a,b; Johnson et al., 2012). From the 62 extracted independent components (ICs), the TMS-related ICs were chosen mainly by their time courses; the variance value of the IC during a time period of 20 ms just after the TMS was 20 times larger than those during the rest of the time periods and during no-TMS trials. "
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    ABSTRACT: Transcranial magnetic stimulation (TMS) has often been used in conjunction with electroencephalography (EEG), which is effective for the direct demonstration of cortical reactivity and corticocortical connectivity during cognitive tasks through the spatio-temporal pattern of long-latency TMS-evoked potentials (TEPs). However, it remains unclear what pattern is associated with the inhibition of a planned motor response. Therefore, we performed TMS-EEG recording during a go/stop task, in which participants were instructed to click a computer mouse with a right index finger when an indicator that was moving with a constant velocity reached a target (go trial) or to avoid the click when the indicator randomly stopped just before it reached the target (stop trial). Single-pulse TMS to the left (contralateral) or right (ipsilateral) motor cortex was applied 500 ms before or just at the target time. TEPs related to motor execution and inhibition were obtained by subtractions between averaged EEG waveforms with and without TMS. As a result, in TEPs induced by both contralateral and ipsilateral TMS, small oscillations were followed by a prominent negative deflection around the TMS site peaking at approximately 100 ms post-TMS (N100), and a less pronounced later positive component (LPC) over the broad areas that was centered at the midline-central site in both go and stop trials. However, compared to the pattern in go and stop trials with TMS at 500 ms before the target time, N100 and LPC were differently modulated in the go and stop trials with TMS just at the target time. The amplitudes of both N100 and LPC decreased in go trials, while the amplitude of LPC decreased and the latency of LPC was delayed in both go and stop trials. These results suggested that TMS-induced neuronal reactions in the motor cortex and subsequent their propagation to surrounding cortical areas might change functionally according to task demand when executing and inhibiting a motor response.
    Full-text · Article · Nov 2013 · Frontiers in Human Neuroscience
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