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Research ArticleResearch Article: New Research, Sensory and Motor Systems

Correlated and Anticorrelated Binocular Disparity Modulate GABA+ and Glutamate/Glutamine Concentrations in the Human Visual Cortex

Jacek Matuszewski, Ivan Alvarez, William T. Clarke, Andrew J. Parker, Holly Bridge and I. Betina Ip
eNeuro 25 February 2025, 12 (3) ENEURO.0355-24.2025; https://doi.org/10.1523/ENEURO.0355-24.2025
Jacek Matuszewski
1Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, United Kingdom
2Laboratory of Brain Imaging, Nencki Institute of Experimental Biology, Polish Academy of Sciences, Warsaw 02-093, Poland
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Ivan Alvarez
1Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, United Kingdom
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  • ORCID record for Ivan Alvarez
William T. Clarke
1Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, United Kingdom
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Andrew J. Parker
3Institut für Biologie, Otto-von-Guericke Universität, Magdeburg 39120, Germany
4Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3PT, United Kingdom
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Holly Bridge
1Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, United Kingdom
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I. Betina Ip
1Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, United Kingdom
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    Visual Abstract

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    Figure 1.

    Diagram of random dot stereograms displayed inside the MRI scanner. Two stimulus types were used which were consistent within participants: a, stimuli were composed of dynamic random dot stereograms (RDS) appearing like depth-defined squares for participants (Pts) 001–006, or spatial sinusoids, moving closer and farther in depth to the fixation plane over time, for participants (Pts) 007–018. Disparity type did not affect GABA+ concentrations, and data were pooled together. b, Example maximum absolute disparity in degrees over time. Participants were instructed to monitor the luminance of the RDS stimuli and press a button on a button box when the luminance increased. The main conditions were (c) correlated disparity, which presented matching contrast of dots presented to the left and right eye, and anticorrelated disparity, which switched the contrast of the dots. White dots were matched with a black dot and black dots with a white dot. Anticorrelated disparity did not evoke any depth percept. d, Example images of sinusoid RDS in anaglyph, with large disparity amplitude (top, left) and small disparity amplitude (bottom, left). Example anticorrelated images are to the right (top right and bottom right).

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    Figure 2.

    MRS voxel in early and ventral visual cortex and group spectra for each condition. a, Proton magnetic resonance spectroscopy (MRS) voxel locations for all 18 participants positioned in the early visual cortex (EVC; blue) and (b) right lateral occipital cortex (LO; blue) displayed on the MNI152 2 mm standard brain. c, Boxplots show %BOLD change to objects inside the LO voxel and proportion overlap between statistical activation maps to objects and the LO voxel. d, Group MRS spectra for each condition and voxel, including only data that was used for the main GABA+ analysis. The black line represents the mean across participants, the gray area shows ±1 standard deviation across participants, and the red line shows the model fit. Spectral amplitude is scaled to arbitrary units. x-axis shows chemical shift in parts per million. Slice positions are indicated in MNI coordinates. The boxplot shows the central 50% range of the data, the whiskers span 1.5 the interquartile range from the upper and lower quartile. R, right hemisphere.

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    Figure 3.

    MRS quality measures in early visual cortex (EVC) and lateral occipital cortex (LO). Boxplots show spectral quality measure NAA linewidth by voxel and condition (a) and goodness of model fit measure absolute Cramér–Rao lower bounds (CRLB) for GABA+ by voxel and condition (b). EVC, black boxplot, blue dots; LO, orange boxplot, orange dots. The boxplot shows the central 50% range of the data, the whiskers span 1.5 of the interquartile range from the upper and lower quartile. Corr, correlated condition; Anti, Anticorrelated condition; FWHM, full-width at half-maximum.

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    Figure 4.

    Bar plots show concentrations of metabolites for visual conditions for the early visual cortex. GABA+ (a), Glx (b), and Glx/GABA+ (excitation/inhibition) ratio (c). Dots show individual participants. Error bars are ±1 SD. Bonferroni–Holm adjusted p values, *<0.05, **<0.01; marginal significance ♢<0.1. Voxels show overlap across 18 participants. R, right hemisphere; EVC, early visual cortex; GABA+, γ-aminobutyric acid + macromolecules; Glx, glutamate + glutamine; Corr, correlated condition; Anti, anticorrelated condition. Slice positionis indicated in MNI coordinates.

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    Figure 5.

    Bar plots show concentrations of metabolites for visual condition for the lateral occipital cortex. GABA+ (a), Glx (b), and Glx/GABA+ (excitation/inhibition) ratio (c). Dots show individual participants. Error bars are ±1 SD. Bonferroni–Holm adjusted p values, *<0.05, **<0.01; marginal significance ♢ < 0.1. Voxels show overlap across 18 participants. R, right hemisphere; LO, lateral occipital cortex; GABA+, γ-aminobutyric acid + macromolecules; Glx, glutamate + glutamine; Corr, correlated condition; Anti, anticorrelated condition. Slice positions are indicated in MNI coordinates.

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    Figure 6.

    Glx and GABA+ were correlated within conditions for EVC and LO. Correlations between Glx and GABA+ for EVC (a) and for LO (b). Pooled across conditions for EVC (c) and LO (d). Model fit is plotted where p < 0.05 uncorrected. Colors indicate condition; red, correlated (Corr); blue, rest; green, anticorrelated (Anti); black, pooled across conditions. GABA+, γ-aminobutyric acid + macromolecules; Glx, glutamate + glutamine.

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    Figure 7.

    Correlation between %BOLD change to objects with Glx and GABA+ in the lateral occipital voxel. Plots show correlation between %BOLD change to objects with Glx during (a) rest, (b) correlated (Corr), and (c) anticorrelated (Anti) disparity in LO. Below, plots show the correlation between %BOLD change to objects with GABA+ during (d) rest, (e) correlated, and (f) anticorrelated disparity in LO. Model fit is plotted where p < 0.05, Bonferroni corrected. LO, lateral occipital cortex; GABA+, γ-aminobutyric acid + macromolecules; Glx, glutamate + glutamine + glutathione; BF10, Bayes factor in favor of the alternative hypothesis. * p < 0.05, Bonferroni corrected.

Tables

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    Table 1.

    Partial correlation while controlling for confounding factors for the early visual cortex (EVC) and lateral occipital cortex (LO)

    Controlling forEVCLO
    rCorrected p valuerCorrected p value
    Spectral quality0.530.0005***0.540.0005***
    Age0.510.0015**0.63<0.0001****
    Sex0.480.003**0.65<0.0001****
    GABA+ fit error0.390.034*0.450.00195**
    Glx fit error0.300.209 NS0.60<0.0001****
    Spectral quality, Age, Sex, GABA+ fit error and Glx fit error0.2140.169 NS0.3920.0124*
    • p values were Bonferroni corrected for five multiple comparisons except for the full model. GABA+, γ-aminobutyric acid + macromolecules; Glx, glutamate + glutamine + glutathione. *p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001, NS, not significant.

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March 2025
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Correlated and Anticorrelated Binocular Disparity Modulate GABA+ and Glutamate/Glutamine Concentrations in the Human Visual Cortex
Jacek Matuszewski, Ivan Alvarez, William T. Clarke, Andrew J. Parker, Holly Bridge, I. Betina Ip
eNeuro 25 February 2025, 12 (3) ENEURO.0355-24.2025; DOI: 10.1523/ENEURO.0355-24.2025

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Correlated and Anticorrelated Binocular Disparity Modulate GABA+ and Glutamate/Glutamine Concentrations in the Human Visual Cortex
Jacek Matuszewski, Ivan Alvarez, William T. Clarke, Andrew J. Parker, Holly Bridge, I. Betina Ip
eNeuro 25 February 2025, 12 (3) ENEURO.0355-24.2025; DOI: 10.1523/ENEURO.0355-24.2025
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Keywords

  • anticorrelation
  • binocular disparity
  • fMRS
  • GABAergic inhibition
  • lateral occipital cortex
  • ventral visual cortex

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