Abstract

Non-invasive brain stimulation is a promising approach to study the causal relationship between brain function and behavior. However, it is difficult to interpret behavioral null results as dynamic brain network changes have the potential to prevent stimulation from affecting behavior, ultimately compensating for the stimulation. The present study investigated local and remote changes in brain activity via functional magnetic resonance imaging (fMRI) after offline disruption of the inferior parietal lobule (IPL) or the vertex in human participants via 1 Hz repetitive transcranial magnetic stimulation (rTMS). Since the IPL acts as a multimodal hub of several networks, we implemented two experimental conditions in order to robustly engage task-positive networks, such as the fronto-parietal control network (on-task condition) and the default mode network (off-task condition). The condition-dependent neural after-effects following rTMS applied to the IPL were dynamic in affecting post-rTMS BOLD activity depending on the exact time-window. More specifically, we found that 1 Hz rTMS applied to the right IPL led to a delayed activity increase in both, the stimulated and the contralateral IPL, as well as in other brain regions of a task-positive network. This was markedly more pronounced in the on-task condition suggesting a condition-related delayed upregulation. Thus together, our results revealed a dynamic compensatory reorganization including upregulation and intra-network compensation which may explain mixed findings after low-frequency offline TMS.

Highlights

  • Over the past decades, a plethora of studies have investigated behavioral changes after transcranial magnetic stimulation (TMS, for reviews see e.g., Pascual-Leone et al, 2000; Rushworth and Taylor, 2006; Koch and Rothwell, 2009; Rossini et al, 2010; Crivelli and Balconi, 2017; Klaus and Schutter, 2018)

  • There are a number of possible explanations for TMS null results ranging from the stimulated brain region not being causally involved in the tested behavior (Rossi et al, 2006; Gohil et al, 2016) to dynamic brain network changes compensating for the stimulation (Lee et al, 2003; O’Shea et al, 2007; Zanto et al, 2013; Hartwigsen, 2018)

  • Administering a 20 min train of 1 Hz repetitive transcranial magnetic stimulation (rTMS) over right inferior parietal lobule (IPL) did not lead to behavioral impairments, which is in line with previous behavioral null results after low-frequency rTMS administered to IPL regions (Rossi et al, 2006; Riemer et al, 2016)

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Summary

Introduction

A plethora of studies have investigated behavioral changes after transcranial magnetic stimulation (TMS, for reviews see e.g., Pascual-Leone et al, 2000; Rushworth and Taylor, 2006; Koch and Rothwell, 2009; Rossini et al, 2010; Crivelli and Balconi, 2017; Klaus and Schutter, 2018). There are a number of possible explanations for TMS null results ranging from the stimulated brain region not being causally involved in the tested behavior (Rossi et al, 2006; Gohil et al, 2016) to dynamic brain network changes compensating for the stimulation (Lee et al, 2003; O’Shea et al, 2007; Zanto et al, 2013; Hartwigsen, 2018). The heuristic that low-frequency rTMS generally inhibits cortical excitability (Pascual-Leone et al, 1998) is not undebated (Beynel et al, 2020) in light of studies combining rTMS and fMRI that reported (compensatory) excitatory after-effects after lowfrequency stimulation on remote brain areas (Lee et al, 2003; O’Shea et al, 2007; Beynel et al, 2020; Castrillon et al, 2020). Stimulation effects seem to depend on several further factors e.g., the stimulated brain region (Castrillon et al, 2020), the post-stimulation task or condition (Lee et al, 2003; O’Shea et al, 2007) and the time passed after stimulation (O’Shea et al, 2007)

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