Occipital alpha activity during stimulus processing gates the information flow to object-selective cortex.

Given the limited processing capabilities of the sensory system, it is essential that attended information is gated to downstream areas, whereas unattended information is blocked. While it has been proposed that alpha band (8-13 Hz) activity serves to route information to downstream regions by inhib...

Full description

Bibliographic Details
Main Authors: Johanna M Zumer, René Scheeringa, Jan-Mathijs Schoffelen, David G Norris, Ole Jensen
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-10-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.1001965
id doaj-fb8957e70ad04de19a4b8d188372e4f5
record_format Article
spelling doaj-fb8957e70ad04de19a4b8d188372e4f52021-07-02T19:59:11ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852014-10-011210e100196510.1371/journal.pbio.1001965Occipital alpha activity during stimulus processing gates the information flow to object-selective cortex.Johanna M ZumerRené ScheeringaJan-Mathijs SchoffelenDavid G NorrisOle JensenGiven the limited processing capabilities of the sensory system, it is essential that attended information is gated to downstream areas, whereas unattended information is blocked. While it has been proposed that alpha band (8-13 Hz) activity serves to route information to downstream regions by inhibiting neuronal processing in task-irrelevant regions, this hypothesis remains untested. Here we investigate how neuronal oscillations detected by electroencephalography in visual areas during working memory encoding serve to gate information reflected in the simultaneously recorded blood-oxygenation-level-dependent (BOLD) signals recorded by functional magnetic resonance imaging in downstream ventral regions. We used a paradigm in which 16 participants were presented with faces and landscapes in the right and left hemifields; one hemifield was attended and the other unattended. We observed that decreased alpha power contralateral to the attended object predicted the BOLD signal representing the attended object in ventral object-selective regions. Furthermore, increased alpha power ipsilateral to the attended object predicted a decrease in the BOLD signal representing the unattended object. We also found that the BOLD signal in the dorsal attention network inversely correlated with visual alpha power. This is the first demonstration, to our knowledge, that oscillations in the alpha band are implicated in the gating of information from the visual cortex to the ventral stream, as reflected in the representationally specific BOLD signal. This link of sensory alpha to downstream activity provides a neurophysiological substrate for the mechanism of selective attention during stimulus processing, which not only boosts the attended information but also suppresses distraction. Although previous studies have shown a relation between the BOLD signal from the dorsal attention network and the alpha band at rest, we demonstrate such a relation during a visuospatial task, indicating that the dorsal attention network exercises top-down control of visual alpha activity.https://doi.org/10.1371/journal.pbio.1001965
collection DOAJ
language English
format Article
sources DOAJ
author Johanna M Zumer
René Scheeringa
Jan-Mathijs Schoffelen
David G Norris
Ole Jensen
spellingShingle Johanna M Zumer
René Scheeringa
Jan-Mathijs Schoffelen
David G Norris
Ole Jensen
Occipital alpha activity during stimulus processing gates the information flow to object-selective cortex.
PLoS Biology
author_facet Johanna M Zumer
René Scheeringa
Jan-Mathijs Schoffelen
David G Norris
Ole Jensen
author_sort Johanna M Zumer
title Occipital alpha activity during stimulus processing gates the information flow to object-selective cortex.
title_short Occipital alpha activity during stimulus processing gates the information flow to object-selective cortex.
title_full Occipital alpha activity during stimulus processing gates the information flow to object-selective cortex.
title_fullStr Occipital alpha activity during stimulus processing gates the information flow to object-selective cortex.
title_full_unstemmed Occipital alpha activity during stimulus processing gates the information flow to object-selective cortex.
title_sort occipital alpha activity during stimulus processing gates the information flow to object-selective cortex.
publisher Public Library of Science (PLoS)
series PLoS Biology
issn 1544-9173
1545-7885
publishDate 2014-10-01
description Given the limited processing capabilities of the sensory system, it is essential that attended information is gated to downstream areas, whereas unattended information is blocked. While it has been proposed that alpha band (8-13 Hz) activity serves to route information to downstream regions by inhibiting neuronal processing in task-irrelevant regions, this hypothesis remains untested. Here we investigate how neuronal oscillations detected by electroencephalography in visual areas during working memory encoding serve to gate information reflected in the simultaneously recorded blood-oxygenation-level-dependent (BOLD) signals recorded by functional magnetic resonance imaging in downstream ventral regions. We used a paradigm in which 16 participants were presented with faces and landscapes in the right and left hemifields; one hemifield was attended and the other unattended. We observed that decreased alpha power contralateral to the attended object predicted the BOLD signal representing the attended object in ventral object-selective regions. Furthermore, increased alpha power ipsilateral to the attended object predicted a decrease in the BOLD signal representing the unattended object. We also found that the BOLD signal in the dorsal attention network inversely correlated with visual alpha power. This is the first demonstration, to our knowledge, that oscillations in the alpha band are implicated in the gating of information from the visual cortex to the ventral stream, as reflected in the representationally specific BOLD signal. This link of sensory alpha to downstream activity provides a neurophysiological substrate for the mechanism of selective attention during stimulus processing, which not only boosts the attended information but also suppresses distraction. Although previous studies have shown a relation between the BOLD signal from the dorsal attention network and the alpha band at rest, we demonstrate such a relation during a visuospatial task, indicating that the dorsal attention network exercises top-down control of visual alpha activity.
url https://doi.org/10.1371/journal.pbio.1001965
work_keys_str_mv AT johannamzumer occipitalalphaactivityduringstimulusprocessinggatestheinformationflowtoobjectselectivecortex
AT renescheeringa occipitalalphaactivityduringstimulusprocessinggatestheinformationflowtoobjectselectivecortex
AT janmathijsschoffelen occipitalalphaactivityduringstimulusprocessinggatestheinformationflowtoobjectselectivecortex
AT davidgnorris occipitalalphaactivityduringstimulusprocessinggatestheinformationflowtoobjectselectivecortex
AT olejensen occipitalalphaactivityduringstimulusprocessinggatestheinformationflowtoobjectselectivecortex
_version_ 1721323221637136384