Evoked potentials in large-scale cortical networks elicited by TMS of the visual cortex

Abstract

Single pulses of transcranial magnetic stimulation (TMS) result in distal and long-lasting oscillations, a finding directly challenging the virtual lesion hypothesis. Previous research supporting this finding has primarily come from stimulation of the motor cortex. We have used single-pulse TMS with simultaneous EEG to target seven brain regions, six of which belong to the visual system [left and right primary visual area V1, motion-sensitive human middle temporal cortex, and a ventral temporal region], as determined with functional MRI-guided neuronavigation, and a vertex "control" site to measure the network effects of the TMS pulse. We found the TMS-evoked potential (TMS-EP) over visual cortex consists mostly of site-dependent theta-and alphaband oscillations. These site-dependent oscillations extended beyond the stimulation site to functionally connected cortical regions and correspond to time windows where the EEG responses maximally diverge (40, 200, and 385 ms). Correlations revealed two site-independent oscillations ϳ350 ms after the TMS pulse: a theta-band oscillation carried by the frontal cortex, and an alpha-band oscillation over parietal and frontal cortical regions. A manipulation of stimulation intensity at one stimulation site (right hemisphere V1-V3) revealed sensitivity to the stimulation intensity at different regions of cortex, evidence of intensity tuning in regions distal to the site of stimulation. Together these results suggest that a TMS pulse applied to the visual cortex has a complex effect on brain function, engaging multiple brain networks functionally connected to the visual system with both invariant and site-specific spatiotemporal dynamics. With this characterization of TMS, we propose an alternative to the virtual lesion hypothesis. Rather than a technique that simulates lesions, we propose TMS generates natural brain signals and engages functional networks.

Continuous theta burst transcranial magnetic stimulation reduces resting state connectivity between visual areas

“…Our results on the influence of TMS on the resting state connectivity between separate brain regions extend previous research on the topic of distant aftereffects of TMS (Bestmann et al 2008;Chouinard et al 2003;Fox et al 2012;Garcia et al 2011;Hampson and Hoffman 2010;Ruff et al 2009;Zanto et al 2011). Previous research has shown that using conditioning pulses over distant areas such as the motion sensitive area MT (Pascual-Leone and Walsh 2001), parietal cortex (Silvanto et al 2009), or frontal eye fields (Silvanto et al 2006) can affect the propensity of a subsequent pulse over the occipital cortex to elicit phosphenes.…”

“…Such a possibility is in line with a number of recent studies that have demonstrated that the effect of TMS extends beyond the focus of stimulation, often to remote regions that are anatomically connected to the focal region (Bestmann et al 2008;Chouinard et al 2003;Fox et al 2012;Garcia et al 2011;Hampson and Hoffman 2010;Ruff et al 2009;Zanto et al 2011). …”

The contribution of TMS–EEG coregistration in the exploration of the human cortical connectome

“…Compelling evidence has also been found in the visual system. Garcia et al (2011) applied TMS to different areas of the visual system, including the left and right primary visual area, middle temporal cortex, and a ventral temporal region. Interestingly, both site-specific and site-invariant EEG responses were obtained.…”

“…At first, different nodes (site-specific responses) and eventually the same hubs are activated (site-invariant responses). The figure simulates results fromGarcia et al (2011). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.…”

Modulation of EEG Functional Connectivity Networks in Subjects Undergoing Repetitive Transcranial Magnetic Stimulation

“…For example, single-pulse TMS to the motor cortex produces immediate EEG changes in the region under the TMS coil, which spread over a few milliseconds to ipsilateral motor, premotor and parietal regions, and then several milliseconds later to the contralateral motor cortex (Ilmoniemi et al 1997; Komssi et al 2002). In one recent study, stimulation of different regions within visual cortex resulted in widespread, long-lasting oscillations, with the precise pattern of network activations containing both stimulation site-specific and site-invariant features (Garcia et al 2011). Similarly, a number of studies have demonstrated that rTMS produces alterations in activity in distributed networks.…”