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Perceptual integration rapidly activates dorsal visual pathway to guide local processing in early visual areas

Rapidly grouping local elements into an organized object (i.e., perceptual integration) is a fundamental yet challenging task, especially in noisy contexts. Previous studies demonstrate that ventral visual pathway, which is widely known to mediate object recognition, engages in the process by convey...

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Detalles Bibliográficos
Autores principales: Liu, Ling, Wang, Fan, Zhou, Ke, Ding, Nai, Luo, Huan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5726727/
https://www.ncbi.nlm.nih.gov/pubmed/29190640
http://dx.doi.org/10.1371/journal.pbio.2003646
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author Liu, Ling
Wang, Fan
Zhou, Ke
Ding, Nai
Luo, Huan
author_facet Liu, Ling
Wang, Fan
Zhou, Ke
Ding, Nai
Luo, Huan
author_sort Liu, Ling
collection PubMed
description Rapidly grouping local elements into an organized object (i.e., perceptual integration) is a fundamental yet challenging task, especially in noisy contexts. Previous studies demonstrate that ventral visual pathway, which is widely known to mediate object recognition, engages in the process by conveying object-level information processed in high-level areas to modulate low-level sensory areas. Meanwhile, recent evidence suggests that the dorsal visual pathway, which is not typically attributable to object recognition, is also involved in the process. However, the underlying whole-brain fine spatiotemporal neuronal dynamics remains unknown. Here we used magnetoencephalography (MEG) recordings in combination with a temporal response function (TRF) approach to dissociate the time-resolved neuronal response that specifically tracks the perceptual grouping course. We demonstrate that perceptual integration initiates robust and rapid responses along the dorsal visual pathway in a reversed hierarchical manner, faster than the ventral pathway. Specifically, the anterior intraparietal sulcus (IPS) responds first (i.e., within 100 ms), followed by activities backpropagating along the dorsal pathway to early visual areas (EVAs). The IPS activity causally modulates the EVA response, even when the global form information is task-irrelevant. The IPS-to-EVA response profile fails to appear when the global form could not be perceived. Our results support the crucial function of the dorsal visual pathway in perceptual integration, by quickly extracting a coarse global template (i.e., an initial object representation) within first 100 ms to guide subsequent local sensory processing so that the ambiguities in the visual inputs can be efficiently resolved.
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spelling pubmed-57267272017-12-27 Perceptual integration rapidly activates dorsal visual pathway to guide local processing in early visual areas Liu, Ling Wang, Fan Zhou, Ke Ding, Nai Luo, Huan PLoS Biol Research Article Rapidly grouping local elements into an organized object (i.e., perceptual integration) is a fundamental yet challenging task, especially in noisy contexts. Previous studies demonstrate that ventral visual pathway, which is widely known to mediate object recognition, engages in the process by conveying object-level information processed in high-level areas to modulate low-level sensory areas. Meanwhile, recent evidence suggests that the dorsal visual pathway, which is not typically attributable to object recognition, is also involved in the process. However, the underlying whole-brain fine spatiotemporal neuronal dynamics remains unknown. Here we used magnetoencephalography (MEG) recordings in combination with a temporal response function (TRF) approach to dissociate the time-resolved neuronal response that specifically tracks the perceptual grouping course. We demonstrate that perceptual integration initiates robust and rapid responses along the dorsal visual pathway in a reversed hierarchical manner, faster than the ventral pathway. Specifically, the anterior intraparietal sulcus (IPS) responds first (i.e., within 100 ms), followed by activities backpropagating along the dorsal pathway to early visual areas (EVAs). The IPS activity causally modulates the EVA response, even when the global form information is task-irrelevant. The IPS-to-EVA response profile fails to appear when the global form could not be perceived. Our results support the crucial function of the dorsal visual pathway in perceptual integration, by quickly extracting a coarse global template (i.e., an initial object representation) within first 100 ms to guide subsequent local sensory processing so that the ambiguities in the visual inputs can be efficiently resolved. Public Library of Science 2017-11-30 /pmc/articles/PMC5726727/ /pubmed/29190640 http://dx.doi.org/10.1371/journal.pbio.2003646 Text en © 2017 Liu et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Liu, Ling
Wang, Fan
Zhou, Ke
Ding, Nai
Luo, Huan
Perceptual integration rapidly activates dorsal visual pathway to guide local processing in early visual areas
title Perceptual integration rapidly activates dorsal visual pathway to guide local processing in early visual areas
title_full Perceptual integration rapidly activates dorsal visual pathway to guide local processing in early visual areas
title_fullStr Perceptual integration rapidly activates dorsal visual pathway to guide local processing in early visual areas
title_full_unstemmed Perceptual integration rapidly activates dorsal visual pathway to guide local processing in early visual areas
title_short Perceptual integration rapidly activates dorsal visual pathway to guide local processing in early visual areas
title_sort perceptual integration rapidly activates dorsal visual pathway to guide local processing in early visual areas
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5726727/
https://www.ncbi.nlm.nih.gov/pubmed/29190640
http://dx.doi.org/10.1371/journal.pbio.2003646
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