Thetaburst TMS to the posterior superior temporal sulcus decreases resting-state fMRI connectivity across the face processing network

Abstract

<jats:title>Abstract</jats:title><jats:p>Humans process faces using a network of face-selective regions distributed across the brain. Neuropsychological patient studies demonstrate that focal damage to nodes in this network can impair face recognition, but such patients are rare. We approximated the effects of damage to the face network in neurologically normal human participants using thetaburst transcranial magnetic stimulation (TBS). Multi-echo functional magnetic resonance imaging (fMRI) resting-state data were collected pre- and post-TBS delivery over the face-selective right superior temporal sulcus (rpSTS), or a control site in the right motor cortex. Results showed that TBS delivered over the rpSTS reduced resting-state connectivity across the extended face-processing network. This connectivity reduction was observed not only between the rpSTS and other face-selective areas, but also between non-stimulated face-selective areas across the ventral, medial and lateral brain surfaces (e.g. between the right amygdala and bilateral fusiform face areas and occipital face areas). TBS delivered over the motor cortex did not produce significant changes in resting-state connectivity across the face-processing network. These results demonstrate that, even without task-induced fMRI signal changes, disrupting a single node in a brain network can decrease the functional connectivity between nodes in that network that have not been directly stimulated.</jats:p><jats:sec><jats:title>Author Summary</jats:title><jats:p>Human behavior is dependent on brain networks that perform different cognitive functions. We combined thetaburst transcranial magnetic stimulation (TBS) with resting-state fMRI to study the face processing network. Disruption of the face-selective right posterior superior temporal sulcus (rpSTS) reduced fMRI connectivity across the face network. This impairment in connectivity was observed not only between the rpSTS and other face-selective areas, but also between non-stimulated face-selective areas on the ventral and medial brain surfaces (e.g. between the right amygdala and bilateral fusiform face areas and occipital face areas). Thus, combined TBS/fMRI can be used to approximate and measure the effects of focal brain damage on brain networks, and suggests such an approach may be useful for mapping intrinsic network organization.</jats:p></jats:sec><jats:sec><jats:title>Technical Terms</jats:title><jats:sec><jats:title>TBS vs TMS</jats:title><jats:p>Transcranial magnetic stimulation (TMS) is a method that induces current in neural tissue by using a rapidly changing magnetic field. The pattern of magnetic field changes can vary. Thetaburst TMS (TBS) is a type of TMS where the same stimulation pattern fluctuates at around a 5Hz cycle.</jats:p></jats:sec><jats:sec><jats:title>Multi-echo fMRI</jats:title><jats:p>During typical fMRI, protons are excited and there is a delay, the echo time, before data are collected. That delay is typically designed to result in a high contrast for blood oxygenation differences. In multi-echo fMRI, data are collected at several echo times each time protons are excited. This results in data that have different levels of contrast for blood oxygenation differences. This added information can be used to empirically decrease noise.</jats:p></jats:sec><jats:sec><jats:title>Face network</jats:title><jats:p>A group of brain regions that show significant activity changes in response to visual face stimuli. While these regions have been defined using univariate analyses with task-based fMRI, they often significantly correlate with each other at rest. In this manuscript, the following regions were a priori defined as part of the face network: posterior superior temporal sulcus (pSTS), amygdala, fusiform face area (FFA), and occipital face area (OFA).</jats:p></jats:sec><jats:sec><jats:title>Matrix based analysis (MBA)</jats:title><jats:p>A recent approach that uses a Bayesian multilevel modeling framework to identify pairs of ROIs where a decrease in correlation magnitude was larger than expected along with a measure of statistical evidence. With this approach, correlations between all pairs of ROIs are assessed as part of a single model rather than many independent statistical tests.</jats:p></jats:sec></jats:sec>

Face Processing and TMS

“…The current chapter covers forty papers, demonstrating the growth of this area. Moreover, the past ten years have also seen studies that have combined TMS with EEG (Sadeh et al, 2011, Mattavelli et al, 2019 and TMS with fMRI (Pitcher, 2014, Pitcher et al, 2017, Handwerker et al, 2020 to study disruption across the extended face network. It is hoped that future TMS studies will continue to produce exciting and innovative insights into face processing in the coming years.221…”

“…Neural activity can be measured across the face network using fMRI before and after lateral face-selective areas such as the OFA or pSTS are stimulated. The remote effects of this stimulation can then be measured in remote areas such as the FFA (Pitcher, 2014) and the amygdala (Pitcher et al, 2017, Handwerker et al, 2020.…”

“…More recently a similar approach was used to study what effect TBS delivered over the rpSTS would have the functional connectivity of the extended face processing network (Handwerker et al, 2020). Participants were scanned using resting-state fMRI (rsfMRI) before, and after, TBS was delivered over the rpSTS or the right motor cortex.…”

“…identify or facial expression discrimination). TMS has also been combined with fMRI to measure how transient disruption of a targeted face-selective region impacts other faceselective regions , Pitcher et al, 2017, Handwerker et al, 2020. (Pitcher et al, 2011a).…”

Theta-burst TMS of lateral occipital cortex reduces BOLD responses across category-selective areas in ventral temporal cortex

“…In particular, recent work has explored this question with respect to the face-selective network using consecutive TMS/fMRI (Pitcher et al, 2014(Pitcher et al, , 2017Handwerker et al, 2020). Here, it was shown that TMS of the occipital face area (OFA; Gauthier et al, 2000) led to a local reduction in the response to faces within the OFA itself.…”