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Temporal dynamics and response modulation across the human visual system in a spatial attention task: an ECoG study

Martin, Anne B. and Yang, Xiaofang and Saalmann, Yuri B. and Wang, Liang and Shestyuk, Avgusta and Lin, Jack J. and Parvizi, Josef and Knight, Robert T. and Kastner, Sabine (2019) Temporal dynamics and response modulation across the human visual system in a spatial attention task: an ECoG study. Journal of Neuroscience, 39 (2). pp. 333-352. ISSN 0270-6474. PMCID PMC6325255. http://resolver.caltech.edu/CaltechAUTHORS:20181129-132500988

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1523/jneurosci.1889-18.2018DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6325255/PubMed CentralArticle
ORCID:
AuthorORCID
Martin, Anne B.0000-0001-5454-4597
Yang, Xiaofang0000-0003-0598-6860
Saalmann, Yuri B.0000-0001-8880-6698
Shestyuk, Avgusta0000-0003-1734-8153
Parvizi, Josef0000-0001-8520-7948
Additional Information:© 2019 the authors. Beginning six months after publication the Work will be made freely available to the public on SfN’s website to copy, distribute, or display under a Creative Commons Attribution 4.0 International (CC BY 4.0) license (https://creativecommons.org/licenses/by/4.0/). Received July 23, 2018; revised Oct. 15, 2018; accepted Nov. 6, 2018. This work was supported by the National Institute of Mental Health Conte Center Grant 1P50MH109429 (S.K., R.T.K., and J.P.), the National Institute of Mental Health Grants R01MH064043 (S.K. and R.T.K.), R01MH109954 (J.P.), and R01MH110311 (Y.B.S.), the National Institute of Neurological Disorders and Stroke Grant R01R37NS21135 (R.T.K.), and the James S. McDonnell Foundation 21st Century Science Initiative, Understanding Human Cognition, collaborative Grant (S.K. and R.T.K.). We thank Michael Arcaro for help with implementing the probabilistic atlas. 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. The authors declare no competing financial interests.
Funders:
Funding AgencyGrant Number
NIH1P50MH109429
NIHR01MH064043
NIHR01MH109954
NIHR01MH110311
NIHR01R37NS21135
James S. McDonnell FoundationUNSPECIFIED
Subject Keywords:attention latencies; onset latencies; spatial response fields; topographic atlas
PubMed Central ID:PMC6325255
Record Number:CaltechAUTHORS:20181129-132500988
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20181129-132500988
Official Citation:Temporal Dynamics and Response Modulation across the Human Visual System in a Spatial Attention Task: An ECoG Study. Anne B. Martin, Xiaofang Yang, Yuri B. Saalmann, Liang Wang, Avgusta Shestyuk, Jack J. Lin, Josef Parvizi, Robert T. Knight, Sabine Kastner. Journal of Neuroscience 9 January 2019, 39 (2) 333-352; DOI: 10.1523/JNEUROSCI.1889-18.2018
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:91334
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:29 Nov 2018 21:40
Last Modified:27 Feb 2019 20:29

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