Functional connectivity between prefrontal and parietal cortex drives visuo-spatial attention shifts.

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Abstract

It is well established that the frontal eye-fields (FEF) in the dorsal attention network (DAN) guide top-down selective attention. In addition, converging evidence implies a causal role for the FEF in attention shifting, which is also known to recruit the ventral attention network (VAN) and fronto-striatal regions. To investigate the causal influence of the FEF as (part of) a central hub between these networks, we applied thetaburst transcranial magnetic stimulation (TBS) off-line, combined with functional magnetic resonance (fMRI) during a cued visuo-spatial attention shifting paradigm. We found that TBS over the right FEF impaired performance on a visual discrimination task in both hemifields following attention shifts, while only left hemifield performance was affected when participants were cued to maintain the focus of attention. These effects recovered ca. 20min post stimulation. Furthermore, particularly following attention shifts, TBS suppressed the neural signal in bilateral FEF, right inferior and superior parietal lobule (IPL/SPL) and bilateral supramarginal gyri (SMG). Immediately post stimulation, functional connectivity was impaired between right FEF and right SMG as well as right putamen. Importantly, the extent of decreased connectivity between right FEF and right SMG correlated with behavioural impairment following attention shifts. The main finding of this study demonstrates that influences from right FEF on SMG in the ventral attention network causally underly attention shifts, presumably by enabling disengagement from the current focus of attention.

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Most cited references 38

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Human ability to attend to visual stimuli based on their spatial locations requires the parietal cortex. One hypothesis maintains that parietal cortex controls the voluntary orienting of attention toward a location of interest. Another hypothesis emphasizes its role in reorienting attention toward visual targets appearing at unattended locations. Here, using event-related functional magnetic resonance (ER-fMRI), we show that distinct parietal regions mediated these different attentional processes. Cortical activation occurred primarily in the intraparietal sulcus when a location was attended before visual-target presentation, but in the right temporoparietal junction when the target was detected, particularly at an unattended location.

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Detection of a visual signal requires information to reach a system capable of eliciting arbitrary responses required by the experimenter. Detection latencies are reduced when subjects receive a cue that indicates where in the visual field the signal will occur. This shift in efficiency appears to be due to an alignment (orienting) of the central attentional system with the pathways to be activated by the visual input. It would also be possible to describe these results as being due to a reduced criterion at the expected target position. However, this description ignores important constraints about the way in which expectancy improves performance. First, when subjects are cued on each trial, they show stronger expectancy effects than when a probable position is held constant for a block, indicating the active nature of the expectancy. Second, while information on spatial position improves performance, information on the form of the stimulus does not. Third, expectancy may lead to improvements in latency without a reduction in accuracy. Fourth, there appears to be little ability to lower the criterion at two positions that are not spatially contiguous. A framework involving the employment of a limited-capacity attentional mechanism seems to capture these constraints better than the more general language of criterion setting. Using this framework, we find that attention shifts are not closely related to the saccadic eye movement system. For luminance detection the retina appears to be equipotential with respect to attention shifts, since costs to unexpected stimuli are similar whether foveal or peripheral. These results appear to provide an important model system for the study of the relationship between attention and the structure of the visual system.

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Author and article information

Journal

Journal ID (iso-abbrev): Neuropsychologia

Title: Neuropsychologia

Publisher: Elsevier BV

ISSN (Electronic): 1873-3514

ISSN (Print): 0028-3932

Publication date (Electronic): May 2017

Volume: 99

Affiliations

[1 ] Institute of Cognitive Neuroscience, University College London, London WC1N 3AR, UK; Wellcome Trust Centre for Neuroimaging, University College London, London WC1N 3BG, UK. Electronic address: TH.Heinen@donders.ru.nl.

[2 ] Institute of Cognitive Neuroscience, University College London, London WC1N 3AR, UK; Wellcome Trust Centre for Neuroimaging, University College London, London WC1N 3BG, UK.

[3 ] Wellcome Trust Centre for Neuroimaging, University College London, London WC1N 3BG, UK.