Elsevier

Cortex

Volume 133, December 2020, Pages 149-160
Cortex

Special Issue “The Brain’s Brake”: Research Report
Modulating the influence of recent trial history on attentional capture via transcranial magnetic stimulation (TMS) of right TPJ

https://doi.org/10.1016/j.cortex.2020.09.009Get rights and content

Abstract

In visual search, salient yet task-irrelevant distractors in the stimulus array interfere with target selection. This is due to the unwanted shift of attention towards the salient stimulus-the so-called attentional capture effect, which delays deployment of attention onto the target. Although powerful and automatic, attentional capture by a salient distractor is nonetheless antagonized by distractor-filtering mechanisms and is further modulated by cross-trial contingencies: The distractor cost is typically more robust when no distraction has been experienced in the immediate past, compared to when a distractor was present on the immediately preceding trial. Here, we used transcranial magnetic stimulation (TMS) to shed light on the causal role of two crucial nodes of the ventral attention network, namely the Temporo-Parietal Junction (TPJ) and the Middle Frontal Gyrus (MFG), in the exogenous control of attention (i.e., attentional capture) and its history-dependent modulation. Participants were asked to discriminate the direction of a target arrow while ignoring a task-irrelevant salient distractor, when present. Immediately after display onset, 10 Hz triple-pulse TMS was delivered either to TPJ or MFG on the right hemisphere. Results demonstrated that stimulation of right TPJ–but not of right MFG, strongly modulated attentional capture as a function of the type of previous trial, by somewhat enhancing the distractor-related cost when the preceding trial was a distractor-absent trial and significantly decreasing the cost when the preceding trial was a distractor-present trial. These findings indicate that TMS of right TPJ exacerbates the effect of the recent history, likely reflecting enhanced updating of the predictive model that dynamically governs proactive distractor-filtering mechanisms. More generally, the results attest to a role of TPJ in mediating the history-dependent modulation of attentional capture.

Introduction

The ability to interact successfully with our rich visual environment depends on sophisticated and flexible visual selective attention mechanisms, which allow selecting relevant information while disregarding irrelevant stimuli (Chelazzi, Marini, Pascucci, & Turatto, 2019, 2011; Desimone & Duncan, 1995; Forster & Lavie, 2008; Jonides & Yantis, 1988; Marini, Chelazzi, & Maravita, 2013; Reynolds & Chelazzi, 2004; Yantis & Jonides, 1990). Salient, attention-grabbing stimuli involuntarily capture the participant's attention, interfering with the ongoing task, although a panoply of distractor-filtering mechanisms exist that try and counteract such unwanted capture of attention (for a review, see Chelazzi et al., 2019; Geng, Won, & Carlisle, 2019).

Distractor-filtering mechanisms may intervene proactively via top-down control whenever potential distraction is foreseen in order to limit the likely performance cost from distracting stimuli (i.e., before they are actually presented). Besides guidance via higher-level cognitive control, distraction-filtering may be the result of the engagement of lower-level and possibly automatic mechanisms. Indeed, attentional capture is known to be modulated by repeated exposure to a certain distractor (e.g., habituation of capture, see Neo & Chua, 2006; Pascucci & Turatto, 2015, Turatto, Bonetti, & Pascucci, 2017, 2018), as well as by the implicit manipulation of the spatial probability distribution of (targets and) distractors (Di Caro, Theeuwes, & Della Libera, 2019; Ferrante et al., 2018; Goschy, Bakos, Muller, & Zehetleitner, 2014; Sauter, Liesefeld, & Müller, 2019, 2018; Wang & Theeuwes, 2018b, 2018a) and by inter-trial priming (Geyer, Müller, & Krummenacher, 2008; Goschy et al., 2014; Müller et al., 2010).

Inter-trial contingency effects refer to the facilitation of distractor filtering if the distractor was present (versus absent) in the preceding, n-1 trial. Although the influence of inter-trial contingencies is a well-established phenomenon, the underlying mechanisms are not fully understood (Chelazzi et al., 2019). Likely, this facilitation is due to the fact that distractor-filtering mechanisms remain in a state of persistent activation (Marini et al., 2013, 2016). This is also in line with the observation that the influence of inter-trial contingencies is modulated by the context, decreasing with increasing overall distractor frequency across the experimental session. In particular, greater inter-trial effects have been observed under low overall distractor probability (i.e., when sustained proactive filtering mechanisms are less likely recruited), whereas a less consistent effect or no effect has been observed under higher distractor probability (i.e., when tonic proactive mechanism are active) (Geyer et al., 2008; Müller, Geyer, Zehetleitner, & Krummenacher, 2009).

The neural mechanisms that the brain can implement to limit or counteract distraction by salient, unexpected stimuli have received mounting interest in the recent years (Chelazzi et al., 2019; Geng, 2014; Geng et al., 2019). Numerous functional imaging studies demonstrated that attentional control in the presence of potential salient distraction is linked to the activation of the dorsal frontoparietal attention network, whose core regions include the frontal eye field (FEF) and the posterior parietal cortex, including tissue within the intraparietal sulcus (IPS), and the ventral frontoparietal network, whose core regions include the temporo-parietal junction (TPJ) and the middle-inferior frontal gyrus (IFG and MFG) (Corbetta & Shulman, 2002; de Fockert, Rees, Frith, & Lavie, 2004; de Fockert & Theeuwes, 2012; DiQuattro, Sawaki, & Geng, 2014; Leber, 2010; Lee & Geng, 2017; Marini, Demeter, Roberts, Chelazzi, & Woldorff, 2016; Melloni, Van Leeuwen, Alink, & Müller, 2012; Serences, Yantis, Culberson, & Awh, 2004, 2005; Talsma, Coe, Munoz, & Theeuwes, 2009). However, an inherent limitation of neuroimaging studies is the inability to reveal any causal organization in the described relationships between brain activity and behavioral performance. Furthermore, functional neuroimaging lacks the temporal resolution to establish whether and how each element of the network is causally involved in determining attentional capture and supporting any distractor filtering mechanism.

In a recent study (Lega et al., 2019), a systematic transcranial magnetic stimulation (TMS) approach was adopted to comparatively assess the causal role of both FEF and IPS in the dorsal attention network on either side of the brain. A substantial reduction of the distractor cost emerged following rTMS of right (but not left) FEF. This result suggested that the stimulation of the right FEF improved distractor suppression mechanisms by activating neural circuits involved in attentional regulation, therefore allowing for more successful inhibition of task-irrelevant information. Interestingly, right FEF stimulation also affected history-contingent modulation of attentional capture, by entirely eliminating the relative (extra) cost in performance when a distractor-present trial was preceded by a distractor-absent trial (of note, the latter result was similarly obtained by stimulating right IPS). Stimulation of right FEF thus seemed to be able to mimic the effect of having encountered a distractor on the preceding trial, perhaps by priming dedicated mechanisms for the filtering-out of distractors, when actually encountered.

Altogether, these findings demonstrated that it is possible to ignite cortical mechanisms that are responsible for distractor suppression by means of TMS. In the present study, we extended the investigation of putative mechanisms for distractor-filtering to the ventral attention network, by targeting two regions that are often involved in attentional processing, including distractor suppression, namely the TPJ and the MFG in the right hemisphere. The right MFG has been demonstrated to be a pivotal hub for proactively filtering distracting information and its activation correlates with behavioral indexes of distractor suppression (Demeter, Hernandez-Garcia, Sarter, & Lustig, 2011; Marini et al., 2016; Weissman, Roberts, Visscher, & Woldorff, 2006). Furthermore, neuropsychological evidence indicated the rMFG as a crucial node for regulating both top-down and bottom-up attention (see Japee, Holiday, Satyshur, Mukai, & Ungerleider, 2015). Congruently, resting-state analysis suggested that part of the ventrolateral frontal cortex, and specifically the right MFG, may link dorsal and ventral attention networks (Fox, Corbetta, Snyder, Vincent, & Raichle, 2006; He et al., 2007). Together with the right MFG, the right TPJ is traditionally considered to be a critical part of a right-lateralized ventral attentional network that re-orients attention toward the appearance of unexpected, but behaviorally relevant events in the environment (Corbetta, Patel, & Shulman, 2008; Corbetta & Shulman, 2002; Downar et al., 2002; Dugué, Merriam, Heeger, & Carrasco, 2018; Shomstein et al., 2012). Evidence for a role of right TPJ in attentional re-orienting came principally from studies using variants of the Posner task, where TPJ activation occurred predominantly in response to invalidly cued targets (i.e., when attentional re-orienting is required) (Corbetta, Kincade, Ollinger, McAvoy, & Shulman, 2000; Doricchi, Macci, Silvetti, & Macaluso, 2010; Indovina & Macaluso, 2007; Kincade, 2005; Natale, Marzi, & Macaluso, 2010; Vossel, Thiel, & Fink, 2006). However, more recent evidence suggested that TPJ activation may not be specific for stimulus-driven attentional re-orienting, but may instead reflect post-perceptual processes involved in contextual updating and adjustments of top-down expectations (DiQuattro et al., 2014; Geng & Vossel, 2013; Han & Marois, 2014; Mengotti, Dombert, Fink, & Vossel, 2017; Vossel, Mathys, Stephan, & Friston, 2015).

Building on these premises, the purpose of this study was twofold. First, we aimed at investigating the causal role of the right ventral attention network (TPJ and MFG) in the mechanisms involved in attentional capture and the filtering of salient but irrelevant distractors. Second, based on previous findings that established a role of the ventral attention network in proactive attentional processes and the contextual updating of predictive models, we tested the role of TPJ and MFG by means of TMS in the regulation of cross-trial dynamics of distractor-filtering.

Section snippets

Materials and methods

All relevant methodological details of the present study are reported in what follows, including how we determined our sample size, all data exclusions, all inclusion/exclusion criteria, whether inclusion/exclusion criteria were established prior to data analyses, all manipulations, and all variables measured in the study. No part of the study procedures, nor of the study analyses was pre-registered prior to the research being conducted. The datasets, the digital study materials and the

Effect of TMS: on-line effects on visual search performance

We tested the effect of TMS on attentional capture and distractor filtering mechanisms using a linear mixed model that predicted log-transformed RTs of correct-response trials. The experimental factors TMS (sham vs. MFG vs. TPJ), Distractor presence (present vs. absent) and their interaction were included as fixed effects. Random coefficients across participants were estimated for intercept and for the factors TMS and distractor presence. The analysis revealed a significant main effect of

Discussion

This study sought to ascertain the causal role of two key regions of the right ventral attention network, MFG and TPJ, in modulating attentional capture elicited by salient distracting stimuli and its history-contingent modulation. Results indicated that stimulation of neither site produced measurable effects in the overall ability to filter-out salient distractors, unlike what we found by stimulating rFEF in our prior study (Lega et al., 2019). However, robust effects were found when

Open Practices

The study in this article earned Open Materials and Open Data badges for transparent practices. The analyses codes have not been archived in a public repository yet, but they are available for the reader upon request to the Corresponding Author. The analysis code, together with the datasets and the digital study materials are available online at https://osf.io/nry9v/, stored on the Open Science Framework data sharing platform.

Declaration of competing interest

The authors declare no competing interests.

Acknowledgements

This research was supported by funding from the Italian Government (Ministero dell’Istruzione, dell’Università e della Ricerca; Bando PRIN 2015) to L.C. The funding agency had no role in the research.

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