Damage to the right temporoparietal junction, but not lateral prefrontal or insular cortex, amplifies the role of goal-directed attention

Elena Pedrazzini,Radek Ptak

doi:10.1038/s41598-018-36537-3

Elena Pedrazzini, Radek Ptak

Open Access

https://doi.org/10.1038/s41598-018-36537-3

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Abstract

Whether an object captures attention depends on the interplay between its saliency and current behavioral predispositions of the observer. Neuroimaging work has implied a ventral attention network, comprising the temporoparietal junction (TPJ), lateral prefrontal cortex (lPFC) and the insula, in attentional orienting toward salient events. Activity of the TPJ is driven by novel and unexpected objects, while the lateral prefrontal cortex is involved in stimulus-driven as well as goal-directed processing. The insula in turn, is part of a saliency network, which has been implicated in detecting biologically salient signals. These roles predict that damage to the TPJ, lPFC, or insula should affect performance in tasks measuring the capture of attention by salient and behaviorally relevant events. Here, we show that patients with lesions to the right TPJ have a characteristic increase of attentional capture by relevant distracters. In contrast, damage to the lPFC or insular cortex only increases reaction times, irrespective of the task-relevant properties of distracters. These findings show that acquired damage to the TPJ pathologically amplifies the capture of attention by task-relevant information, and thus indicate that the TPJ has a decisive role in goal-directed orienting.

Highlights

Objects in our environment may capture attention because of their physical characteristics, or because of our behavioral predispositions[1,2]
Single-unit studies show that neurons in the lateral intraparietal cortex and the frontal eye fields are activated already 45–60 ms following the sudden onset of a stimulus[19,20,21], which is substantially earlier than inferior parietal cortex (~90 ms)[22]
We asked patients with acquired damage to the temporoparietal junction (TPJ), the lateral prefrontal cortex (lPFC)/Insula, or subcortical white matter (SUBCORT group) and healthy control subjects (CONT group) to react to a colored shape, which was preceded by a brief peripheral cue (Fig. 1)

Summary

Introduction

Objects in our environment may capture attention because of their physical characteristics, or because of our behavioral predispositions[1,2]. A functional connectivity study found that the right lPFC is coupled to the dorsal and ventral attention networks, suggesting a possible role as integrator of goal-directed and stimulus-driven attention[31] This interpretation is supported by the finding that during visual search the lPFC shows activity consistent with goal-oriented processing, and reacts upon the appearance of salient surprise stimuli[32]. This proposal is motivated by the involvement of the insula in a ‘saliency network’[34], which is activated upon the appearance of biologically significant stimuli, in particular when these affect bodily functions[35] Such partly overlapping conceptions of the role of lPFC and insula are even more complicated by the fact, that the right TPJ has been conceived as a switch that interrupts processing and terminates the current task set when an unexpected event requires attention[36]. Contrary to this prediction we found that damage to the TPJ, but not the lPFC/insula, pathologically increases reflexive attentional capture by task-relevant distracter stimuli

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