Cited by 2,101Functional Brain Connectivity StudiesNeural and Behavioral Psychology StudiesVisual Attention and Saliency Detection

The DOI matches its Crossref record; 60 of the 60 references it cites were found in a registry or an index; none of the 78 sources its claims cite is checked for support yet.

Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems

Open access
Fox, Michael D., Corbetta, Maurizio, Snyder, Abraham Z., Vincent, Justin L., Raichle, Marcus E.·2006·Proceedings of the National Academy of Sciences

Abstract

On the basis of task-related imaging studies in normal human subjects, it has been suggested that two attention systems exist in the human brain: a bilateral dorsal attention system involved in top-down orienting of attention and a right-lateralized ventral attention system involved in reorienting attention in response to salient sensory stimuli. An important question is whether this functional organization emerges only in response to external attentional demands or is represented more fundamentally in the internal dynamics of brain activity. To address this question, we examine correlations in spontaneous fluctuations of the functional MRI blood oxygen level-dependent signal in the absence of task, stimuli, or explicit attentional demands. We identify a bilateral dorsal attention system and a right-lateralized ventral attention system solely on the basis of spontaneous activity. Further, we observe regions in the prefrontal cortex correlated with both systems, a potential mechanism for mediating the functional interaction between systems. These findings demonstrate that the neuroanatomical substrates of human attention persist in the absence of external events, reflected in the correlation structure of spontaneous activity.

Overview

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TL;DR

Spontaneous BOLD fluctuations in resting-state fMRI are sufficient to recover the dorsal and ventral human attention systems, with the dorsal system bilateral and the ventral system right-lateralized. The two systems are largely segregated, with prefrontal overlap suggesting a possible interaction site.

Key findings

  • Four attention seed regions—IPS and FEF (dorsal), TPJ and VFC (ventral)—partition into two systems on the basis of spontaneous activity: IPS/FEF and TPJ/VFC correlations were significantly stronger than any other region pair (all region pairs not equally correlated, F(5,45)=23.70, P<0.0001; pairwise P<0.005).
  • Correlation-map similarity and overlap also separated the systems: spatial correlation across maps differed significantly (F(5,45)=15.54, P<0.0001), as did fractional overlap (F(5,45)=17.04, P<0.0001), with IPS/FEF and TPJ/VFC pairs most similar/overlapping.
  • Dorsal maps were bilateral, whereas ventral maps were right-lateralized: laterality differed by spatial correlation (F(3,27)=28.28, P<0.0001) and fractional overlap (F(3,27)=39.79, P<0.0001); IPS/FEF maps were significantly more bilateral than VFC/TPJ maps (spatial correlation P<0.05; overlap P<0.006).
  • Intrinsically defined dorsal and ventral systems were largely segregated; overlap regions were found in right middle frontal gyrus, inferior frontal gyrus, and inferior parietal cortex, with the prefrontal regions suggested as possible interaction sites after controlling for nonneuronal factors.

Methods

  • Functional MRI data were acquired in 10 normal subjects during three resting conditions: visual fixation on a crosshair, eyes open during low-level illumination, and eyes closed; these data had been used previously in a study of anticorrelated functional networks.
  • Seed regions for IPS, FEF, TPJ, and VFC were defined from a meta-analysis of previous task-based attention studies, and seed-based correlation analyses were performed on preprocessed resting-state data.
  • Main analyses used temporal correlation, spatial correlation, and fractional overlap, with random-effects analysis across the population and a significance threshold of P<0.01; systems were defined by conjunction across all three resting-state conditions.

Limitations

  • Stated: the exact nature of spontaneous BOLD fluctuations is unknown, and unconstrained behavior/cognition during rest cannot be ruled out as a source of some spontaneous BOLD activity, although the paper argues it is unlikely to be the predominant source.
  • Stated: the inferior parietal overlap region may be attributable to nonneuronal factors such as averaging, spatial resolution, or locally coherent noise, unlike the prefrontal overlap regions.
  • Evident: the sample is small (10 subjects), the seed regions are derived from prior task-based studies, and the resting-state correlation design cannot establish directionality or causality between systems or link spontaneous fluctuations directly to attentional performance.

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Integrity signals

Registry

Crossref · 10.1073/pnas.0604187103

Cites

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Claims the paper makes

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    Coherent spontaneous fluctuations are present continuously across all brain regions.

    “Finally, coherent spontaneous fluctuations are present continuously across all brain regions.”
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Citations

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  1. D. Cordes, V. M. Haughton, K. Arfanakis, G. J. Wendt, P. A. Turski, C. H. Moritz, M. A. Quigley, M. E. Meyerand Am. J. Neuroradiol. 21, 1636–1644 (2000).

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Metadata

Authors
Fox, M. D., Corbetta, M., Snyder, A. Z., Vincent, J. L., & Raichle, M. E.
Affiliations
Washington University in St. Louis (US)
Venue
Proceedings of the National Academy of Sciences
Published
2006-06-27
Volume
103
Issue
26
Pages
10046-10051
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
OpenAlex
W2045758998
Cited by
2,101
References
60
Citations by year
2026: 54 · 2025: 93 · 2024: 111 · 2023: 93 · 2022: 122 · 2021: 127 · 2020: 190 · 2019: 132 · 2018: 132 · 2017: 116 · 2016: 118 · 2015: 118 · 2014: 129 · 2013: 122 · 2012: 116
FWCI
24.43
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed (publishedVersion)
  • Padua Research Archive (University of Padova) (submittedVersion, other-oa)
Funders
  • National Institutes of Health (5f30ns054398-02, NS06833)
  • National Institute of Mental Health (MH 7192-06, R01MH071920)
  • National Institute of Neurological Disorders and Stroke (F30 NS 054398-01, F30 NS-054398, NS 048013, R01NS048013, P50NS006833, NS 06833)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Physical Sciences › Computer Science › Computer Vision and Pattern Recognition › Visual Attention and Saliency Detection
Keywords
spontaneous neuronal activity, resting-state brain activity, top-down attention, prefrontal cortex, functional connectivity, hemispheric lateralization, attentional control
MeSH terms
Attention, Brain Mapping, Humans, Magnetic Resonance Imaging, Neurons, Oxygen, Prefrontal Cortex

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