Fronto-temporal interactions are functionally relevant for semantic control in language processing

Abstract

Semantic cognition, i.e. processing of meaning is based on semantic representations and their controlled retrieval. Semantic control has been shown to be implemented in a network that consists of left inferior frontal (IFG), and anterior and posterior middle temporal gyri (a/pMTG). We aimed to disrupt semantic control processes with continuous theta burst stimulation (cTBS) over left IFG and pMTG and to study whether behavioral effects are moderated by induced alterations in resting-state functional connectivity. To this end, we applied real cTBS over left IFG and left pMTG as well as sham stimulation on 20 healthy participants in a within-subject design. Stimulation was followed by resting-state functional magnetic resonance imaging and a semantic priming paradigm. Resting-state functional connectivity of regions of interest in left IFG, pMTG and aMTG revealed highly interconnected left-lateralized fronto-temporal networks representing the semantic system. We did not find any significant direct modulation of either task performance or resting-state functional connectivity by effective cTBS. However, after sham cTBS, functional connectivity between IFG and pMTG correlated with task performance under high semantic control demands in the semantic priming paradigm. These findings provide evidence for the functional relevance of interactions between IFG and pMTG for semantic control processes. This interaction was functionally less relevant after cTBS over aIFG which might be interpretable in terms of an indirect disruptive effect of cTBS.

A systematic review of the neurobiological effects of theta-burst stimulation (TBS) as measured using functional magnetic resonance imaging (fMRI)

“…The IFG has also been a target of interest for the TBS research identified in this review. While some authors report no effects of iTBS (Anderkova et al 2018 ) nor cTBS (Wawrzyniak et al 2017 ; Anderkova et al 2018 ) to the IFG on rsFC, during task performance, the effects of both TBS protocols have been observed. Specifically, iTBS to the left IFG resulted in widespread increased network-wide activity and connectivity at frontal, occipital and cerebellar regions during phases of encoding in older adults (Vidal-Piñeiro et al 2014 ).…”

A systematic review of the neurobiological effects of theta-burst stimulation (TBS) as measured using functional magnetic resonance imaging (fMRI)

“…The IFG has also been a target of interest for the TBS research identified in this review. While some authors report no effects of iTBS (Anderkova et al, 2018) or cTBS (Anderkova et al, 2018;Wawrzyniak et al, 2017) to the IFG on rsFC, during task performance, the effects of both TBS protocols have been observed. Specifically, iTBS to the left IFG resulted in widespread increased network wide activity and connectivity at frontal, occipital and cerebellar regions during phases of encoding in older adults (Vidal-Piñeiro et al, 2014).…”

“…Similarly, functional connectivity within the visual network, acting as a control network, was not shown to be influenced by iTBS over M1 or the vertex, rather, stimulation effects remained within the stimulated motor network (Nettekoven et al, 2014). In contrast, others who have taken this approach report no significant TBS effects to either the target or control networks (Hermiller et al, 2019;Wawrzyniak et al, 2017). Hermiller et al (2019), however, reported a positive relationship between cTBS induced improvements in an offline behavioural memory task and increases in functional connectivity between the hippocampus and the target HCN, whereas a similar pattern of results was identified between the hippocampus and non-HCN regions for iTBS.…”

“…Several studies reviewed here targeted the vertex as an active (Agnew et al, 2018;Andoh et al, 2015;Andoh & Zatorre, 2013;Pitcher et al, 2017;Rahnev et al, 2013) or sham (Nettekoven et al, 2014;Nettekoven et al, 2015) control site, while others performed statistical comparisons between the target and a non-target network (Halko et al, 2014;Hermiller et al, 2019;Nettekoven et al, 2014;Rastogi et al, 2017;Wawrzyniak et al, 2017).…”

Neurocognitive correlates of category ambiguous verb processing: The single versus dual lexical entry hypotheses

“…Collectively, the literature suggests that left anterior IFG (BA 47; pars orbitalis) and posterior IFG (BA 45; pars triangularis) mediate top-down controlled retrieval and selection of lexical representations, respectively (see Lau, Phillips, & Poeppel, 2008). Left temporal areas, found to coactivate with the frontal cortex, also play a role in control processes during meaning retrieval in addition to lexical representation/activation (e.g., Badre, Poldrack, Paré-Blagoev, Insler, & Wagner, 2005; Kuperberg, Sitnikova, & Lakshmanan, 2008; Noppeney, Phillips, & Price, 2004; Thompson-Schill, D’Esposito, Aguirre, & Farah, 1997; Wagner, Pare-Blagoev, Clark, & Poldrack, 2001; Wawrzyniak et al, 2017). Moreover, Whitney, Jefferies, and Kircher (2011) identified a functional dissociation between processes related to semantic control and representation in posterior and inferior aspects of the temporal cortex during ambiguity processing.…”