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      Temporal Dynamics and Response Modulation across the Human Visual System in a Spatial Attention Task: An ECoG Study

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          Abstract

          The selection of behaviorally relevant information from cluttered visual scenes (often referred to as “attention”) is mediated by a cortical large-scale network consisting of areas in occipital, temporal, parietal, and frontal cortex that is organized into a functional hierarchy of feedforward and feedback pathways. In the human brain, little is known about the temporal dynamics of attentional processing from studies at the mesoscopic level of electrocorticography (ECoG), that combines millisecond temporal resolution with precise anatomical localization of recording sites. We analyzed high-frequency broadband responses (HFB) responses from 626 electrodes implanted in 8 epilepsy patients who performed a spatial attention task. Electrode locations were reconstructed using a probabilistic atlas of the human visual system. HFB responses showed high spatial selectivity and tuning, constituting ECoG response fields (RFs), within and outside the topographic visual system. In accordance with monkey physiology studies, both RF widths and onset latencies increased systematically across the visual processing hierarchy. We used the spatial specificity of HFB responses to quantitatively study spatial attention effects and their temporal dynamics to probe a hierarchical top-down model suggesting that feedback signals back propagate the visual processing hierarchy. Consistent with such a model, the strengths of attentional modulation were found to be greater and modulation latencies to be shorter in posterior parietal cortex, middle temporal cortex and ventral extrastriate cortex compared with early visual cortex. However, inconsistent with such a model, attention effects were weaker and more delayed in anterior parietal and frontal cortex.

          SIGNIFICANCE STATEMENT In the human brain, visual attention has been predominantly studied using methods with high spatial, but poor temporal resolution such as fMRI, or high temporal, but poor spatial resolution such as EEG/MEG. Here, we investigate temporal dynamics and attention effects across the human visual system at a mesoscopic level that combines precise spatial and temporal measurements by using electrocorticography in epilepsy patients performing a classical spatial attention task. Electrode locations were reconstructed using a probabilistic atlas of the human visual system, thereby relating them to topography and processing hierarchy. We demonstrate regional differences in temporal dynamics across the attention network. Our findings do not fully support a top-down model that promotes influences on visual cortex by reversing the processing hierarchy.

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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
          9 January 2019
          9 July 2019
          : 39
          : 2
          : 333-352
          Affiliations
          1Princeton Neuroscience Institute,
          2Department of Psychology, Princeton University, Princeton, New Jersey 08544,
          3Helen Wills Neuroscience Institute,
          4Department of Psychology, University of California, Berkeley, Berkeley, California 94720,
          5Center for the Neurobiology of Learning and Memory,
          6Department of Biomedical Engineering,
          7Department of Neurology, University of California, Irvine, Orange, California 92868,
          8Department of Neurology and Neurological Sciences, Stanford University, Palo Alto, California 94304,
          9Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California 91125,
          10Department of Psychology, University of Wisconsin-Madison, Madison, Wisconsin 53706, and
          11CAS Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing 100101, China
          Author notes
          Correspondence should be addressed to Dr. Sabine Kastner, Princeton Neuroscience Institute and Department of Psychology, Washington Road, Princeton, NJ 08544. skastner@ 123456princeton.edu

          Author contributions: A.B.M., X.Y., Y.B.S., L.W., A.S., J.J.L., J.P., R.T.K., and S.K. edited the paper; Y.B.S. and S.K. designed research; A.S., J.J.L., J.P., and R.T.K. performed research; A.B.M., X.Y., and L.W. analyzed data; A.B.M., X.Y., and S.K. wrote the paper.

          Article
          PMC6325255 PMC6325255 6325255 1889-18
          10.1523/JNEUROSCI.1889-18.2018
          6325255
          30459219
          ea80dc6d-f941-4912-a3a8-0e9433df68b2
          Copyright © 2019 the authors 0270-6474/19/390334-20$15.00/0
          Categories
          Research Articles
          Behavioral/Cognitive

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