Special Issue “The Brain’s Brake”: Research ReportModulating the influence of recent trial history on attentional capture via transcranial magnetic stimulation (TMS) of right TPJ
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.
References (92)
- et al.
Mixed-effects modeling with crossed random effects for subjects and items
Journal of Memory and Language
(2008) - et al.
Random effects structure for confirmatory hypothesis testing: Keep it maximal
Journal of Memory and Language
(2013) - et al.
Cortical control of inhibition of return: Causal evidence for task-dependent modulations by dorsal and ventral parietal regions
Cortex; a Journal Devoted To the Study of the Nervous System and Behavior
(2013) - et al.
Cortical control of Inhibition of Return: Exploring the causal contributions of the left parietal cortex
Cortex; a Journal Devoted To the Study of the Nervous System and Behavior
(2013) - et al.
Accuracy of an individualized MR-based head model for navigated brain stimulation
Psychiatry Research - Neuroimaging
(2012) - et al.
ScienceDirect getting rid of visual distractors : The why , when , how , and where
Current Opinion in Psychology
(2019) - et al.
The reorienting system of the human brain: From environment to theory of mind
Neuron
(2008) - et al.
Transient reduction of visual distraction following electrical stimulation of the prefrontal cortex
Cognition
(2015) - et al.
Challenges to attention: A continuous arterial spin labeling (ASL) study of the effects of distraction on sustained attention
Neuroimage
(2011) - et al.
Altering spatial priority maps via statistical learning of target selection and distractor filtering
Cortex; a Journal Devoted To the Study of the Nervous System and Behavior
(2018)
Role of frontal cortex in attentional capture by singleton distractors
Brain and Cognition
Right temporoparietal junction activation by a salient contextual cue facilitates target discrimination
Neuroimage
Re-evaluating the role of TPJ in attentional control: Contextual updating?
Neuroscience and Biobehavioral Reviews
Expectancies modulate attentional capture by salient color singletons
Vision Research
Breakdown of functional connectivity in frontoparietal networks underlies behavioral deficits in spatial neglect
Neuron
Interactions between task difficulty and hemispheric distribution of attended locations: Implications for the splitting attention debate
Cognitive Brain Research
Attentional capture in visual search: Capture and post-capture dynamics revealed by EEG
Neuroimage
Sham TMS: Intracerebral measurement of the induced electrical field and the induction of motor-evoked potentials
Biological Psychiatry
Dimension-based attention modulates feed-forward visual processing
Acta Psychologica
Right temporal-parietal junction engagement during spatial reorienting does not depend on strategic attention control
Neuropsychologia
Distinct roles of the intraparietal sulcus and temporoparietal junction in attentional capture from distractor features: An individual differences approach
Neuropsychologia
Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research
Clinical Neurophysiology
Discrimination within and between hemifields: A new constraint on theories of attention
Neuropsychologia
Attentional control: Temporal relationships within the fronto-parietal network
Neuropsychologia
Expectation (and attention) in visual cognition
Trends in Cognitive Sciences
Cue validity modulates the neural correlates of covert endogenous orienting of attention in parietal and frontal cortex
Neuroimage
Raincloud plots: A multi-platform tool for robust data visualization
Wellcome Open Research
Independent resources for attentional tracking in the left and right visual hemifields
Psychological Science
Neural mechanisms of visual attention: Object-based selection of a region in space
Journal of Cognitive Neuroscience
lme4: Linear mixed-effect models using Eigen and S4. (R package version 1.1-7)
Neural coding of prior expectations in hierarchical intention inference
Scientific Reports
Right temporoparietal junction and attentional reorienting
Human Brain Mapping
Neural basis of visual selective attention
Wiley Interdisciplinary Reviews: Cognitive Science
Dorsal and ventral parietal contributions to spatial orienting in the human brain
Journal of Neuroscience
Voluntary orienting is dissociated from target detection in human posterior parietal cortex
Nature Neuroscience
Control of goal-directed and stimulus-driven attention in the brain
Nature Reviews Neuroscience
Neural mechanisms of selective visual attention. Annual review of neuroscience
Suppression history of distractor location biases attentional and oculomotor control
Visual Cognition
Contextual knowledge configures attentional control networks
Journal of Neuroscience
Effective connectivity during feature-based attentional capture: Evidence against the attentional reorienting hypothesis of TPJ
Cerebral Cortex
Neural correlates of the spatial and expectancy components of endogenous and stimulus-driven orienting of attention in the posner task
Cerebral Cortex
A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities
Journal of Neurophysiology
Specific visual subregions of TPJ mediate reorienting of spatial attention
Cerebral Cortex
Neural correlates of attentional capture in visual search
Journal of Cognitive Neuroscience
Failures to ignore entirely irrelevant distractors: The role of load
Journal of Experimental Psychology. Applied
Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems
Proceedings of the National Academy of Sciences
Cited by (0)
- 1
These authors contributed equally to this work.