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      Involvement of the dorsal and ventral attention networks in visual attention span

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          Abstract

          Visual attention span (VAS), which refers to the window size of multielement parallel processing in a short time, plays an important role in higher‐level cognition (e.g., reading) as required by encoding large amounts of information input. However, it is still a matter of debate about the underlying neural mechanism of VAS. In the present study, a modified visual 1‐back task was designed by using nonverbal stimuli and nonverbal responses, in which possible influences of target presence and position were considered to identify more pure VAS processing. A task‐driven functional magnetic resonance imaging (fMRI) experiment was then performed, and 30 healthy adults participated in this study. Results of confirmatory and exploratory analyses consistently revealed that both dorsal attention network (DAN) and ventral attention network (VAN) were significantly activated during this visual simultaneous processing. In particular, more significant activation in the left superior parietal lobule (LSPL), as compared to that in the bilateral inferior frontal gyrus (IFGs), suggested a greater involvement of DAN in VAS‐related processing in contrast to VAN. In addition, it was also found that the activation in temporoparietal junctions (TPJs) were suppressed during multielement processing only in the target‐absent condition. The current results suggested the recruitment of LSPL in covert attentional shifts and top‐down control of VAS resources distribution during the rapid visual simultaneous processing, as well as the involvement of bilateral IFGs (especially RIFG) in both VAS processing and inhibitory control. The present findings might bring some enlightenments for diagnosis of the atypicality of attentional disorders and reading difficulties.

          Abstract

          A prospective visual 1‐back task used during functional magnetic resonance imaging (fMRI) scanning were designed to examine the neural mechanism of visual attention span (VAS) which is a basic cognitive ability and plays an important role in higher‐level cognition (e.g., reading) as required by encoding large amounts of information input. Results of confirmatory and exploratory analyses consistently revealed greater involvement of dorsal attention network (DAN, e.g., left superior parietal lobule) as compared to ventral attention network (VAN, e.g., bilateral inferior frontal gyrus) in this visual simultaneous processing. The present findings bring some enlightenments for diagnosis of the atypicality of attentional disorders and reading difficulties.

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          Control of goal-directed and stimulus-driven attention in the brain.

          We review evidence for partially segregated networks of brain areas that carry out different attentional functions. One system, which includes parts of the intraparietal cortex and superior frontal cortex, is involved in preparing and applying goal-directed (top-down) selection for stimuli and responses. This system is also modulated by the detection of stimuli. The other system, which includes the temporoparietal cortex and inferior frontal cortex, and is largely lateralized to the right hemisphere, is not involved in top-down selection. Instead, this system is specialized for the detection of behaviourally relevant stimuli, particularly when they are salient or unexpected. This ventral frontoparietal network works as a 'circuit breaker' for the dorsal system, directing attention to salient events. Both attentional systems interact during normal vision, and both are disrupted in unilateral spatial neglect.
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            The reorienting system of the human brain: from environment to theory of mind.

            Survival can depend on the ability to change a current course of action to respond to potentially advantageous or threatening stimuli. This "reorienting" response involves the coordinated action of a right hemisphere dominant ventral frontoparietal network that interrupts and resets ongoing activity and a dorsal frontoparietal network specialized for selecting and linking stimuli and responses. At rest, each network is distinct and internally correlated, but when attention is focused, the ventral network is suppressed to prevent reorienting to distracting events. These different patterns of recruitment may reflect inputs to the ventral attention network from the locus coeruleus/norepinephrine system. While originally conceptualized as a system for redirecting attention from one object to another, recent evidence suggests a more general role in switching between networks, which may explain recent evidence of its involvement in functions such as social cognition.
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              A theory of visual attention.

              A unified theory of visual recognition and attentional selection is developed by integrating the biased-choice model for single-stimulus recognition (Luce, 1963; Shepard, 1957) with a choice model for selection from multielement displays (Bundesen, Pedersen, & Larsen, 1984) in a race model framework. Mathematically, the theory is tractable, and it specifies the computations necessary for selection. The theory is applied to extant findings from a broad range of experimental paradigms. The findings include effects of object integrality in selective report, number and spatial position of targets in divided-attention paradigms, selection criterion and number of distracters in focused-attention paradigms, delay of selection cue in partial report, and consistent practice in search. On the whole, the quantitative fits are encouraging.
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                Author and article information

                Contributors
                ppliang@cnu.edu.cn
                Journal
                Hum Brain Mapp
                Hum Brain Mapp
                10.1002/(ISSN)1097-0193
                HBM
                Human Brain Mapping
                John Wiley & Sons, Inc. (Hoboken, USA )
                1065-9471
                1097-0193
                04 January 2022
                15 April 2022
                : 43
                : 6 ( doiID: 10.1002/hbm.v43.6 )
                : 1941-1954
                Affiliations
                [ 1 ] Key Laboratory of Learning and Cognition, School of Psychology Capital Normal University Beijing China
                [ 2 ] Department of Psychology Tsinghua University Beijing China
                [ 3 ] Department of Psychology Zhejiang University Hangzhou China
                Author notes
                [*] [* ] Correspondence

                Peipeng Liang, School of Psychology, Capital Normal University (East Campus), 23A, Fuwai Baiduizi, Haidian District, Beijing, China.

                Email: ppliang@ 123456cnu.edu.cn

                Author information
                https://orcid.org/0000-0002-5392-8094
                https://orcid.org/0000-0002-8361-976X
                Article
                HBM25765
                10.1002/hbm.25765
                8933248
                34984762
                3ace11c9-76ed-4cca-b6cd-0e999392c4a7
                © 2022 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 07 November 2021
                : 08 June 2021
                : 09 December 2021
                Page count
                Figures: 5, Tables: 3, Pages: 14, Words: 11597
                Funding
                Funded by: National Natural Science Foundation of China , doi 10.13039/501100001809;
                Award ID: 31871117
                Funded by: National Key Research and Development Project of China
                Award ID: 2020YFC2007302
                Funded by: Beijing Nova Program , doi 10.13039/501100005090;
                Award ID: 2016000021223TD07
                Funded by: Key Research Project of Academy for Multidisciplinary Studies, Capital Normal University
                Award ID: JCKXYJY2019019
                Categories
                Research Article
                Research Articles
                Custom metadata
                2.0
                April 15, 2022
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.1.2 mode:remove_FC converted:18.03.2022

                Neurology
                a prospective visual 1‐back task,attention networks,neural mechanism,visual attention span

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