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      Cortical and Subcortical Coordination of Visual Spatial Attention Revealed by Simultaneous EEG–fMRI Recording

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          Abstract

          Visual spatial attention has been studied in humans with both electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) individually. However, due to the intrinsic limitations of each of these methods used alone, our understanding of the systems-level mechanisms underlying attentional control remains limited. Here, we examined trial-to-trial covariations of concurrently recorded EEG and fMRI in a cued visual spatial attention task in humans, which allowed delineation of both the generators and modulators of the cue-triggered event-related oscillatory brain activity underlying attentional control function. The fMRI activity in visual cortical regions contralateral to the cued direction of attention covaried positively with occipital gamma-band EEG, consistent with activation of cortical regions representing attended locations in space. In contrast, fMRI activity in ipsilateral visual cortical regions covaried inversely with occipital alpha-band oscillations, consistent with attention-related suppression of the irrelevant hemispace. Moreover, the pulvinar nucleus of the thalamus covaried with both of these spatially specific, attention-related, oscillatory EEG modulations. Because the pulvinar's neuroanatomical geometry makes it unlikely to be a direct generator of the scalp-recorded EEG, these covariational patterns appear to reflect the pulvinar's role as a regulatory control structure, sending spatially specific signals to modulate visual cortex excitability proactively. Together, these combined EEG/fMRI results illuminate the dynamically interacting cortical and subcortical processes underlying spatial attention, providing important insight not realizable using either method alone.

          SIGNIFICANCE STATEMENT Noninvasive recordings of changes in the brain's blood flow using functional magnetic resonance imaging and electrical activity using electroencephalography in humans have individually shown that shifting attention to a location in space produces spatially specific changes in visual cortex activity in anticipation of a stimulus. The mechanisms controlling these attention-related modulations of sensory cortex, however, are poorly understood. Here, we recorded these two complementary measures of brain activity simultaneously and examined their trial-to-trial covariations to gain insight into these attentional control mechanisms. This multi-methodological approach revealed the attention-related coordination of visual cortex modulation by the subcortical pulvinar nucleus of the thalamus while also disentangling the mechanisms underlying the attentional enhancement of relevant stimulus input and those underlying the concurrent suppression of irrelevant input.

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          Author and article information

          Journal
          J Neurosci
          J. Neurosci
          jneuro
          jneurosci
          J. Neurosci
          The Journal of Neuroscience
          Society for Neuroscience
          0270-6474
          1529-2401
          16 August 2017
          16 February 2018
          : 37
          : 33
          : 7803-7810
          Affiliations
          [1] 1Center for Cognitive Neuroscience, Duke University, Durham, North Carolina 27708,
          [2] 2Department of Psychology, Institute for Mind and Brain, and McCausland Center for Brain Imaging, University of South Carolina, Columbia, South Carolina 29201,
          [3] 3Department of Experimental Psychology, Ghent University, Henri Dunantlaan 2, 9000 Ghent, Belgium,
          [4] 4Brain Imaging and Analysis Center, Duke University School of Medicine, Durham, North Carolina 27710,
          [5] 5Neuropsychology Laboratory, Department of Psychology, European Medical School, University of Oldenburg, Lower Saxony, Oldenburg 26129, Germany, and
          [6] 6Department of Psychiatry, Duke University, Durham, North Carolina 27708
          Author notes
          Correspondence should be addressed to Jessica Green, Institute for Mind and Brain, University of South Carolina, 1800 Gervais St., Columbia, SC 29201. jessica.green@ 123456sc.edu , or to Marty Woldorff, Center for Cognitive Neuroscience, Duke University, Box 90999, Durham, NC 27708, woldorff@ 123456duke.edu

          Author contributions: C.N.B. and M.G.W. designed research; J.J.G., C.N.B., K.C.R., L.-C.C., and R.M.K. performed research; A.W.S. contributed unpublished reagents/analytic tools; J.J.G. analyzed data; J.J.G., C.N.B., K.C.R., L.-C.C., R.M.K., A.W.S., and M.G.W. wrote the paper.

          Author information
          http://orcid.org/0000-0003-3570-529X
          http://orcid.org/0000-0001-5963-2780
          http://orcid.org/0000-0002-0676-7611
          http://orcid.org/0000-0002-2683-4551
          Article
          PMC5559758 PMC5559758 5559758 0326-17
          10.1523/JNEUROSCI.0326-17.2017
          5559758
          28698387
          07d48589-43a0-4fc8-9f4e-6983b332d20c
          Copyright © 2017 the authors 0270-6474/17/377803-08$15.00/0
          History
          : 30 January 2017
          : 7 June 2017
          : 5 July 2017
          Categories
          Research Articles
          Behavioral/Cognitive

          fMRI,attentional control,EEG,pulvinar,visual cortex
          fMRI, attentional control, EEG, pulvinar, visual cortex

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