Dual-site TMS demonstrates causal functional connectivity between the left and right posterior temporal sulci during facial expression recognition

Abstract

<jats:title>Abstract</jats:title><jats:sec><jats:title>Background</jats:title><jats:p>Neuroimaging studies suggest that facial expression recognition is processed in the bilateral posterior superior temporal sulcus (pSTS). Our recent repetitive transcranial magnetic stimulation (rTMS) study demonstrates that the bilateral pSTS is causally involved in expression recognition, although involvement of the right pSTS is greater than involvement of the left pSTS.</jats:p></jats:sec><jats:sec><jats:title>Objective/Hypothesis</jats:title><jats:p>In this study, we used a dual-site TMS to investigate whether the left pSTS is functionally connected to the right pSTS during expression recognition. We predicted that if this connection exists, simultaneous TMS disruption of the bilateral pSTS would impair expression recognition to a greater extent than unilateral stimulation of the right pSTS.</jats:p></jats:sec><jats:sec><jats:title>Methods</jats:title><jats:p>Participants attended two TMS sessions. In Session 1, participants performed an expression recognition task while rTMS was delivered to the face-sensitive right pSTS (experimental site), object-sensitive right lateral occipital complex (control site) or no rTMS was delivered (behavioural control). In Session 2, the same experimental design was used except that continuous theta-burst stimulation (cTBS) was delivered to the left pSTS immediately before behavioural testing. Session order was counter-balanced across participants.</jats:p></jats:sec><jats:sec><jats:title>Results</jats:title><jats:p>In Session 1, rTMS to the rpSTS impaired performance accuracy compared to the control conditions. Crucially in Session 2, the size of this impairment effect doubled after cTBS was delivered to the left pSTS.</jats:p></jats:sec><jats:sec><jats:title>Conclusions</jats:title><jats:p>Our results provide evidence for a causal functional connection between the left and right pSTS during expression recognition. In addition, this study further demonstrates the utility of the dual-site TMS for investigating causal functional links between brain regions.</jats:p></jats:sec>

TMS disruption of the lateral prefrontal cortex increases neural activity in the default mode network when naming facial expressions

“…The lack of an interaction (that would have shown a greater impairment in selected face-selective areas than others) suggests that all five ROIs in both hemispheres are causally connected to the IFG during facial expression naming. This is consistent with patient and TMS studies showing that the IFG (Jastorff et al, 2016), pSTS (Pitcher, 2014;Sliwinska, Elson, et al, 2020), FFA (Rezlescu et al, 2012), OFA (Pitcher et al, 2008) and the amygdala (Adolphs et al, 1994) are all causally involved in facial expression recognition. Our findings reveal that IFG is directly or indirectly connected to all other regions in the face network.…”

“…In addition to the experimental task, we also ran a functional localizer to identify face-selective areas in each participant. Stimuli were 3-second movie clips of faces and objects that we have used in prior studies (Küçük et al, 2022;Sliwinska, Elson, et al, 2020;Sliwinska et al, 2022). There were sixty movie clips for each category in which distinct exemplars appeared multiple times.…”

Face Processing and TMS

“…This pattern of results is consistent with the hypothesis that changeable face information can reach the pSTS via cortico-cortical connections from early visual cortex that are independent of the OFA (O'Toole et al, 2002). This conclusion is consistent with a neuropsychological study of a prosopagnosic patient with a right ventral occipitotemporal lesion (Sliwinska et al, 2020a). The neural response in the patients right pSTS was comparable with control participants while the responses in his right OFA and FFA were impaired.…”

“…This is, at least partly, because many of the brain areas involved in processing expressions are located on the lateral brain surface and can be directly stimulated with TMS. TMS studies of expression processing have targeted the OFA (Pitcher et al, 2008), the posterior STS (Pourtois et al, 2004, Sliwinska and Pitcher, 2018, Sliwinska et al, 2020b, premotor cortex (Balconi et al, 2014), the face area in the somatosensory cortex (Pitcher et al, 2008), medial prefrontal cortex (Mattavelli et al, 2013), dorsolateral prefrontal cortex (Zwanzger et al, 2014) and the cerebellum (Ferrari et al, 2018). The fact that expressions are processed across so many areas distributed across the brain demonstrates the saliency of the face when conveying emotion.…”