Elsevier

Cortex

Volume 133, December 2020, Pages 247-265
Cortex

Special Issue “Attention & Motor Processes”: Research Report
Large-scale brain networks underlying non-spatial attention updating: Towards understanding the function of the temporoparietal junction

https://doi.org/10.1016/j.cortex.2020.09.023Get rights and content

Abstract

The temporoparietal junction (TPJ) and related areas are activated when a target stimulus appears at unexpected locations in Posner's spatial-cueing paradigm, and also when deviant stimuli are presented within a series of standard events in oddball paradigms. This type of activation corresponds to the ventral attention network (VAN), for regions defined on the basis of the spatial task. However, involvement of the VAN in object-based updating of attention has rarely been examined. In the present study, we used functional magnetic resonance imaging to investigate brain responses to (i) invalid targets after category-cueing and (ii) neutrally cued targets deviating in category from the background series of pictures. Bilateral TPJ activation was observed in response to invalidly cued targets, as compared to neutrally cued targets. Reference to the main large-scale brain networks showed that peaks of this activation located in the angular gyrus and inferior parietal lobule belonged to the default mode (DMN) and fronto-parietal networks (FPN), respectively. We found that VAN regions were involved only for simple detection activity. We conclude that spatial and non-spatial reorienting of attention rely on different network underpinnings. Our data suggest that DMN and FPN activity may support the ability to disengage from contextually irrelevant information.

Introduction

Studies of visual attention commonly refer to two large-scale brain networks involved in attentional control: the dorsal attention network (DAN) for directing and maintaining focus of attention, and the ventral attention network (VAN) for attentional updating. Activity in the DAN has been shown to increase after cues that convey task-relevant information about place, direction, colour, category, or other attributes of the upcoming, sought-after target (e.g., Corbetta, Kincade, Ollinger, McAvoy, & Shulman, 2000; Dombert, Kuhns, Mengotti, Fink, & Vossel, 2016; Egner et al., 2008; Kanwisher & Wojciulik, 2000; Kincade, Abrams, Astafiev, Shulman, & Corbetta, 2005; Shulman et al., 1999). Engagement of the VAN was demonstrated at target appearance after infrequent invalid spatial cues in the Posner paradigm (Corbetta & Shulman, 2002), a condition that required reorienting of attention to the behaviourally-relevant target in the contralateral hemifield. Results of other tasks suggest that the VAN is also involved in non-spatial reorienting of attention, i.e., updating the attributes and/or identity of objects in the focus of attention (Corbetta & Shulman, 2002; Geng & Vossel, 2013; Macaluso & Doricchi, 2013). However, evidence for VAN engagement in the reorienting of both spatial and feature- and/or object-based attention remains much less consistent than in the case of the DAN.

The involvement of the VAN is most often inferred from increased blood-oxygen-level dependent (BOLD) activity in the temporoparietal junction (TPJ) when an incoming stimulus violates expectations (Asplund, Todd, Snyder, & Marois, 2010; Beck & Kastner, 2014; Doricchi, Macci, Silvetti, & Macaluso, 2010). The TPJ refers to the area at the junction of the inferior parietal lobule and superior temporal sulcus. The notion that the TPJ is a critical part of the VAN came from the seminal works of Corbetta and colleagues (Corbetta, Patel, & Shulman, 2008; Corbetta & Shulman, 2002; Fox, Corbetta, Snyder, Vincent, & Raichle, 2006). Their review presented meta-analyses of both spatial and non-spatial attention tasks, which showed heterogeneous but overlapping activations in the vicinity of the TPJ to unattended and/or infrequent targets (Corbetta & Shulman, 2002). These activations occurred predominantly in the right hemisphere. A link between task activations and brain functional networks was established by means of resting-state seed-voxel correlations, which determined the resting-state connectivity for each active site (Fox et al., 2006). Importantly, seeds used to verify the networks underlying the orienting and reorienting of attention were obtained in the meta-analysis of the Posner tasks only. Meta-analytic work for non-spatial reorienting was based on tasks requiring the detection of low-frequency events, i.e., “oddballs”. The similarity between the spatial and non-spatial reorienting process was based on the fact that invalid targets in the Posner task and oddball stimuli were less frequent than valid targets or standard stimuli. Supposedly, when subjects detected such infrequent and/or unexpected events, they had to break the current attentional set and adopt a new one on the basis of the incoming stimulus (Corbetta & Shulman, 2002, p. 211). However, likely due to the high variability of both protocols and results, there was no attempt to provide seed-voxel verification of the networks involved in the reorienting of attention in these oddball tasks. Similarly, later studies on non-spatial attention largely assumed that their tasks engaged the same network as involved in the Posner task on the basis of similarity of activations (i.e., activity observed in the area of the TPJ) and broad similarity of cognitive requirements (i.e., reacting to unexpected and/or infrequent stimuli; Serences et al. 2005; Asplund et al., 2010; Ortiz-Tudela, Martín-Arévalo, Chica, & Lupiáñez, 2018). Although considerable inconsistencies were identified, for e.g., with respect to the laterality of effects (i.e., according to the original account, the VAN should be strongly right-lateralised but many studies showed symmetrical or even left-lateralised TPJ activation at target appearance; see Geng & Vossel, 2013, for discussion), the results were discussed with reference to the VAN (Beck & Kastner, 2014; Dugué, Merriam, Heeger, & Carrasco, 2018; Geng & Vossel, 2013; Macaluso & Doricchi, 2013).

In our opinion, however, involvement of the VAN in non-spatial updating of attention has yet to be verified. First, it may be questioned if the oddball detection represents a good model for non-spatial attention updating. In some cases, top-down attention may be focused on the infrequent target throughout the whole task, thus not requiring additional updating at its reappearance (Kubit & Jack, 2013). To-date, little is known about the functional correlates of non-spatial reorienting in tasks with different requirements, for e.g., in tasks wherein attention is directly oriented to incorrect targets by means of invalid cueing. For example, a cueing task designed specifically to compare spatial and feature-based attention within a single experiment failed to show increased TPJ activity at the appearance of an invalid target when the cue was related to its colour (Dombert et al., 2016, but see also; Galashan & Siemann, 2017). Second, a recent study that tested activity in classic versions of both the Posner and oddball tasks by means of a local independent components analysis (ICA) restricted to the posterior parietal and temporal areas showed different neural hubs responsible for updating in these two tasks (Igelström, Webb, Kelly, & Graziano, 2016). On the other hand, the most recent meta-analysis of oddball tasks (Kim, 2014) showed that oddball-related effects belonged to the VAN by referring to the 7-network brain parcellation by Yeo's group (Yeo et al., 2011).

Variable definitions of the VAN might itself form an important source of confusion. It is not clear how the VAN that is based on the Posner paradigm matches the resting-state network defined independently from tasks results (i.e., with data-driven methods of parcellation), and the functional ventral frontoparietal network that is invoked by many studies (e.g., Dombert et al., 2016; Han & Marois, 2014; Indovina & Macaluso, 2007; Serences et al., 2005; Vossel et al., 2014; Weidner, Krummenacher, Reimann, Müller, & Fink, 2009). These discrepancies call for a direct evaluation of the networks underlying task results, with an explicit description of which networks were considered (i.e., how they were delineated).

Taken together, the functional mechanisms of reorienting of attention are well-characterised for spatial attention but remain unclear for other forms of attentional control. In particular, it has not yet been determined if, by activating the TPJ, target-related updating of attention in the non-spatial domain (1) engages hubs of the same network as better-verified spatial tasks, and (2) whether this process is well reflected by oddball detection. To answer these questions, we analysed activity in the TPJ region using a task that employed a modified Posner-type cueing scheme and engaged object-based attention rather than spatial attention. Participants were asked to detect pictures of faces and houses within a series of pictures from another category (objects). Cues presented in each trial named one of the target categories or none of the categories, leading to valid, invalid, and neutral cue-target associations. On the basis of invalid cueing we probed the reorienting of attention between house and face stimuli. Comparing the response to neutrally cued targets and the search period baseline allowed us to probe the simple detection of infrequent target, which resembles oddball-related effects. As predicted, both the invalid cueing and simple target detection produced the most pronounced signal modulation in the lateral-parietal cortex, in the vicinity of the TPJ. However, non-spatial updating in the face of invalid target stimuli depended on hubs outside of the VAN.

Section snippets

Materials and methods

We report how we determined our sample size, all data exclusions, all inclusion and exclusion criteria, and whether they had been established prior to data analysis, all manipulations, and all measures in this study. No part of this study has been pre-registered prior to the research being conducted.

Behavioural results

We compared RTs and accuracy when the information about the category of a target picture provided by the cue was valid, neutral, or invalid. The effects of cueing were evaluated using 3×2 mixed model ANOVAs, with cue type (valid, neutral, invalid) as the within-subject factor, and validity ratio (80/20, 67/33) as the between-subject factor (to control for the two task versions).

The analysis of RTs (Fig. 2A) revealed a significant main effect of cue type [F (2,46) = 29.70, p < .001], reflecting

Discussion

The current study focused on various modes of non-spatial updating and their reliance on activation of the TPJ. By combining Posner-like cueing and a serial presentation of picture stimuli, we aimed to elicit a reorienting of attention between expected and unexpected target categories, and a simple reaction to low-frequency target category, which are both thought to involve the VAN. The comparison of responses to invalid targets and to targets appearing after the neutral cue revealed increased

Conclusions

In the current study, we demonstrated that activity in the vicinity of the TPJ region, involved in updating object-based attention after an invalid cue, cannot be sufficiently described by the sole reference to the VAN. By referring to independently defined resting-state networks, we demonstrated that this activity should be also attributed to the DMN and FPN. Operations within these networks are presumably related to the necessity of evaluating the contextual meaning of incoming stimuli and

Data availability

The conditions of our ethics approval do not permit public archiving of raw individual data. Readers seeking access to the data should contact the lead author Katarzyna Jurewicz. Access will be granted to named individuals in accordance with ethical requirements governed in collaboration agreement. All data that are necessary and sufficient to replicate all the processing steps and analyses will be permitted as part of a collaboration to requestors who meet these requirements. Individual and

CRediT authorship contribution statement

Katarzyna Jurewicz: Conceptualization, Methodology, Investigation, Formal Analysis, Visualization, Data curation, Writing-Original Draft, Funding acquisition.

Katarzyna Paluch: Conceptualization, Investigation, Writing-Review & Editing.

Tomasz Wolak: Supervision, Software.

Andrzej Wróbel: Supervision, Resources, Writing-Review & Editing.

Open practices

The study in this article earned and Open Materials badge for transparent practices. Materials and data for the study are available at https://osf.io/vj9p8/.

Acknowledgements

This work was supported by National Science Centre, Poland (grant numbers 2015/19/N/HS6/02364, 2016/20/W/NZ4/00354).

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