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

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          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. 20 min 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.

          Highlights

          • •

            Thetaburst stimulation to the right FEF temporarily impairs bilateral attention shifts.

          • •

            Lateralised behavioural deficits in the contralateral hemifield are observed when cued to maintain attention.

          • •

            These effects recover ca. 20 min post stimulation.

          • •

            During shifts, neural activity is suppressed following right FEF TBS in the dorsal attention network and supramarginal gyri.

          • •

            Influences from right FEF to SMG causally underlie attention shifts, presumably by enabling disengagement from current focus.

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          Most cited references38

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          Voluntary orienting is dissociated from target detection in human posterior parietal cortex.

          Maurizio Corbetta, J Michelle Kincade, John M. Ollinger … (2000)
          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.
          Article 0 comments Cited 295 times – based on 0 reviews     Review now
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            Neuronal oscillations and multisensory interaction in primary auditory cortex.

            Peter Lakatos, Chi-Ming Chen, Monica N O'Connell … (2007)
            Recent anatomical, physiological, and neuroimaging findings indicate multisensory convergence at early, putatively unisensory stages of cortical processing. The objective of this study was to confirm somatosensory-auditory interaction in A1 and to define both its physiological mechanisms and its consequences for auditory information processing. Laminar current source density and multiunit activity sampled during multielectrode penetrations of primary auditory area A1 in awake macaques revealed clear somatosensory-auditory interactions, with a novel mechanism: somatosensory inputs appear to reset the phase of ongoing neuronal oscillations, so that accompanying auditory inputs arrive during an ideal, high-excitability phase, and produce amplified neuronal responses. In contrast, responses to auditory inputs arriving during the opposing low-excitability phase tend to be suppressed. Our findings underscore the instrumental role of neuronal oscillations in cortical operations. The timing and laminar profile of the multisensory interactions in A1 indicate that nonspecific thalamic systems may play a key role in the effect.
            Article 0 comments Cited 252 times – based on 0 reviews     Review now
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              Attention and the detection of signals.

              Lisa B. Davidson, Joshua C. Snyder, M Posner (1980)
              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

                Contributors
                Klaartje Heinen
                Journal
                Journal ID (nlm-ta): Neuropsychologia
                Journal ID (iso-abbrev): Neuropsychologia
                Title: Neuropsychologia
                Publisher: Pergamon Press
                ISSN (Print): 0028-3932
                ISSN (Electronic): 1873-3514
                Publication date PMC-release: 1 May 2017
                Publication date (Print): May 2017
                Volume: 99
                Pages: 81-91
                Affiliations
                [a ]Institute of Cognitive Neuroscience, University College London, London WC1N 3AR, UK
                [b ]Wellcome Trust Centre for Neuroimaging, University College London, London WC1N 3BG, UK
                Author notes
                [* ]Corresponding author at: Institute of Cognitive Neuroscience, University College London, London WC1N 3AR, UK. TH.Heinen@ 123456donders.ru.nl kheinen@ 123456gmail.com
                [1]

                Present address: Donders Centre for Cognitive Neuroimaging, Radboud University, 6525 EN Nijmegen, The Netherlands.

                [2]

                Present address: School of Psychology & Clinical Language Sciences, University of Reading, Reading RG6 7BE, UK.

                [3]

                Present address: Laboratory for Social and Neural System Research (SNS-Lab), University of Zurich, Zurich CH-8006, Switzerland.

                Article
                Publisher ID: S0028-3932(17)30069-6
                DOI: 10.1016/j.neuropsychologia.2017.02.024
                PMC ID: 5415819
                PubMed ID: 28254653
                SO-VID: 87312901-5616-498d-8afb-89b4a9cda4e1
                Copyright © © 2017 The Authors
                License:

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                Date received : 12 July 2016
                Date revision received : 13 December 2016
                Date accepted : 26 February 2017
                Categories
                Subject: Article

                ScienceOpen disciplines: Neurology
                Keywords: attention shifts,frontal eye-fields,thetaburst tms,fmri
                Data availability:
                ScienceOpen disciplines: Neurology
                Keywords: attention shifts, frontal eye-fields, thetaburst tms, fmri

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