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Articles, Systems/Circuits

Local Activity Determines Functional Connectivity in the Resting Human Brain: A Simultaneous FDG-PET/fMRI Study

Valentin Riedl, Katarzyna Bienkowska, Carola Strobel, Masoud Tahmasian, Timo Grimmer, Stefan Förster, Karl J. Friston, Christian Sorg and Alexander Drzezga
Journal of Neuroscience 30 April 2014, 34 (18) 6260-6266; DOI: https://doi.org/10.1523/JNEUROSCI.0492-14.2014
Valentin Riedl
1Departments of Neuroradiology,
2Nuclear Medicine, and
4Technische Universität München-Neuroimaging Center, Klinikum Rechts der Isar der Technischen Universität München, 81675 München, Germany,
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Katarzyna Bienkowska
1Departments of Neuroradiology,
4Technische Universität München-Neuroimaging Center, Klinikum Rechts der Isar der Technischen Universität München, 81675 München, Germany,
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Carola Strobel
1Departments of Neuroradiology,
4Technische Universität München-Neuroimaging Center, Klinikum Rechts der Isar der Technischen Universität München, 81675 München, Germany,
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Masoud Tahmasian
1Departments of Neuroradiology,
2Nuclear Medicine, and
4Technische Universität München-Neuroimaging Center, Klinikum Rechts der Isar der Technischen Universität München, 81675 München, Germany,
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Timo Grimmer
3Psychiatry, and
4Technische Universität München-Neuroimaging Center, Klinikum Rechts der Isar der Technischen Universität München, 81675 München, Germany,
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Stefan Förster
2Nuclear Medicine, and
4Technische Universität München-Neuroimaging Center, Klinikum Rechts der Isar der Technischen Universität München, 81675 München, Germany,
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Karl J. Friston
5The Wellcome Trust Centre for Neuroimaging, University College London, London WC1N 3BG, United Kingdom, and
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Christian Sorg
1Departments of Neuroradiology,
3Psychiatry, and
4Technische Universität München-Neuroimaging Center, Klinikum Rechts der Isar der Technischen Universität München, 81675 München, Germany,
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Alexander Drzezga
6Department of Nuclear Medicine, Uniklinik Köln, 50937 Köln, Germany
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  • Figure 1.
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    Figure 1.

    LA and FC during resting-state CLOSED (left) and OPEN (right) conditions. A, SPMs of whole-brain voxelwise one sample t tests for FDG uptake controlling for each subject's grand mean signal. B, SPMs of whole-brain voxelwise one-sample t tests on individual FC maps revealing rs-FC for seed ROI V1 (V1-FC). Regions (red) with V1-FC during the CLOSED condition include primary and secondary visual cortex, and inferior parietal and temporoparietal areas. Additional regions with V1-FC during the OPEN condition include cingulate, insular, and prefrontal cortices; brainstem; thalamus; and cerebellum. C, SPMs of whole-brain voxelwise one sample t tests on individual FC maps revealing rs-FC for averaged seed ROI of the SAL network (SAL-FC). Regions (red) with SAL-FC during the CLOSED condition include cingulate, insular, superior parietal, and prefrontal cortices; brainstem; thalamus; and cerebellum. Additional regions with SAL-FC during the OPEN condition included primary and secondary visual, and anterior cingulate cortices. All SPMs are thresholded at an FWE-corrected p value of <0.05 and are superimposed on a high-resolution T1-weighted anatomical image. x, z, Coordinates of brain slices in MNI space; R, right side of the brain.

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    Figure 2.

    Quantitative relationship between LA and FC in the resting human brain. A, SPMs of whole-brain voxelwise ANCOVA for LA changes controlling for each subject's grand mean signal. Regions (cyan) with increased LA during the OPEN condition included V1, aI, aCC, and mCC. FWE corrected, p < 0.05. R, Right. B, SPMs of whole-brain voxelwise independent-samples t tests on individual FC maps for seed ROIs (cyan) V1 (V1-FC; top row) and SAL hubs (SAL-FC; bottom row) revealing FC changes. Regions (yellow) with increased V1-FC during the OPEN condition include SAL hubs, thalamus, brainstem, and cerebellum; the main region with increased SAL-FC during the OPEN condition was V1 and parts of aCC. p < 0.05, FWE corrected. C, Voxelwise conjunction showing regions (violet) with increased LA and FC. An exemplary distribution of voxel values of LA (y-axis) and V1-FC (x-axis) of aI taken from the first subject is shown on the right side. To quantify the relationship between LA and FA, we calculated the SpaSi[LA, FC] ROI coefficient for each subject and each ROI as the voxelwise spatial correlation between normalized LA and between-network FC values, and subsequently analyzed them in a two-way ANOVA. D, Post hoc independent-samples t tests revealed significantly increased SpaSiOPEN for ROIs V1, aCC, and aI. **p < 0.005, ***p < 0.0005. Error bars denote 5th and 95th percentiles. No difference occurred in V1 for within-network connectivity (V1[V1-FC]) and in mCC for between-network FC. E, Mean square of SpaSiCLOSED and SpaSiOPEN, indicating the voxelwise variability of FC explained by LA. *p < 0.05, ***p < 0.0005, one-sample t tests performed separately for SpaSiCLOSED and SpaSiOPEN. Cluster coordinates for all SPMs and cluster sizes for conjunction regions can be found in Table 1.

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    Table 1.

    Brain regions with increased LA, increased FC, and overlapping increases in LA and FC

    RegionCenter of mass (x, y, z coordinates in MNI space)PET statisticsfMRI statisticsCluster size overlap (voxels)
    V1 seedSAL seed
    Occipital cortex: calcarine, lingual, fusiform gyrus15, −74, 714.75181
    −15, −99, 94.57
    9, −81, 94.82
    Extrastriate cortex−41, −81, 1910.19
    Cuneus18, −79, 318.58
    mCC0, −31, 3711.81212
    −3, −21, 365.44
    Left insula−39, −13, 1311.13
    Left aI−51, 11, 78.85211
    −42, 15, −37.03
    Left inferior frontal gyrus−48, 29, −28.84
    Left superior frontal gyrus−30, 66, 65.89
    Right superior frontal gyrus24, 63, −66.81
    Middle superior frontal gyrus−6, 50, 3710.6
    aCC−6, 20, 378.78212
    0, 21, 308.55
    0, 27, 215.27
    Medial subgenual frontal gyrus−6, 20, −208.68
    Right aI36, 14, 48.64284
    51, 21, −66.22
    Fusiform/inferior temporal gyrus36, −10, −387.94
    Thalamus−3, −24, 65.71
    Cerebellum36, −54, −278.55
    Brainstem−3, −21, −186.42
    • Data are t statistics, unless otherwise indicated. Bold indicates overlapping increases in LA and FC. See also Figure 1 and main text.

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The Journal of Neuroscience: 34 (18)
Journal of Neuroscience
Vol. 34, Issue 18
30 Apr 2014
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Local Activity Determines Functional Connectivity in the Resting Human Brain: A Simultaneous FDG-PET/fMRI Study
Valentin Riedl, Katarzyna Bienkowska, Carola Strobel, Masoud Tahmasian, Timo Grimmer, Stefan Förster, Karl J. Friston, Christian Sorg, Alexander Drzezga
Journal of Neuroscience 30 April 2014, 34 (18) 6260-6266; DOI: 10.1523/JNEUROSCI.0492-14.2014

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Local Activity Determines Functional Connectivity in the Resting Human Brain: A Simultaneous FDG-PET/fMRI Study
Valentin Riedl, Katarzyna Bienkowska, Carola Strobel, Masoud Tahmasian, Timo Grimmer, Stefan Förster, Karl J. Friston, Christian Sorg, Alexander Drzezga
Journal of Neuroscience 30 April 2014, 34 (18) 6260-6266; DOI: 10.1523/JNEUROSCI.0492-14.2014
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Keywords

  • energy metabolism
  • functional connectivity
  • PET/MR imaging

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