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Research ArticleResearch Article: New Research, Cognition and Behavior

Resting State BOLD Variability of the Posterior Medial Temporal Lobe Correlates with Cognitive Performance in Older Adults with and without Risk for Cognitive Decline

Tyler J. Good, Joshua Villafuerte, Jennifer D. Ryan, Cheryl L. Grady and Morgan D. Barense
eNeuro 19 March 2020, 7 (3) ENEURO.0290-19.2020; DOI: https://doi.org/10.1523/ENEURO.0290-19.2020
Tyler J. Good
1Rotman Research Institute, Baycrest Health Sciences, Toronto M6A 2E1, Ontario
2Department of Psychology, University of Toronto, Toronto M5S 3G3, Ontario
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Joshua Villafuerte
1Rotman Research Institute, Baycrest Health Sciences, Toronto M6A 2E1, Ontario
2Department of Psychology, University of Toronto, Toronto M5S 3G3, Ontario
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Jennifer D. Ryan
1Rotman Research Institute, Baycrest Health Sciences, Toronto M6A 2E1, Ontario
2Department of Psychology, University of Toronto, Toronto M5S 3G3, Ontario
3Department of Psychiatry, University of Toronto, Toronto M5T 1R8, Ontario
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Cheryl L. Grady
1Rotman Research Institute, Baycrest Health Sciences, Toronto M6A 2E1, Ontario
2Department of Psychology, University of Toronto, Toronto M5S 3G3, Ontario
3Department of Psychiatry, University of Toronto, Toronto M5T 1R8, Ontario
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Morgan D. Barense
1Rotman Research Institute, Baycrest Health Sciences, Toronto M6A 2E1, Ontario
2Department of Psychology, University of Toronto, Toronto M5S 3G3, Ontario
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Figures

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  • Figure 1.
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    Figure 1.

    The at-risk group scored lower than controls on three neuropsychological factors (cognitive control/speed, memory, and intelligence), though the group difference did not quite reach significance. A, Violin plots showing the distribution of factor scores for each group. B, Results from a group comparison PLS that found a marginal effect such that the at-risk group scored lower than controls on the cognitive control, memory and intelligence factors (p = 0.053). Bootstrap ratios (BSRs) are plotted and represent a linear combination of the factors weighted by how strongly they contribute to the latent variable. Negative BSRs indicate the at-risk group had lower scores than controls on these factors. BSRs may be interpreted similar to z score (>|2.5| akin to p < 0.05), suggesting again that the at-risk group’s lower scores on the control/speed, memory, and intelligence factors was approaching significance. Error bars represent 1 SE = standard error. C, Distribution of MoCA scores in the present sample. The black dashed line indicates the recommended MoCA cutoff score (26 points out of 30).

  • Figure 2.
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    Figure 2.

    A behavioral PLS (p = 0.01, 87% covariance) found age was negatively correlated with scores on the VOSP silhouette, VOSP progressive silhouette, and WASI matrix reasoning tests in the at-risk group, but not controls. The left bar graph shows the correlation between age and the pattern of neuropsychological tests shown on the right. The error bars represent 95% confidence intervals. Bootstrap ratios are pictured on the right, representing a linear combination of the neuropsychological tests weighted by how much they contribute to the latent variable. Bootstrap ratios may be interpreted like z scores, such that bootstrap ratios >|2.5| are considered to be reliably correlated with age in the group(s) that are significantly contributing to the latent variable. Immediate (imm), delayed (del), sillhoutte (sil), version (Ver).

  • Figure 3.
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    Figure 3.

    Multivariate PLS analysis of the relationship between SDBOLD and 8 variables (age, MoCA score, global FA and MD, and score on 4 neuropsychological factors). In controls, SDBOLD (particularly in the MTL) was associated with higher cognitive control/speed and intelligence scores, but lower visuospatial and memory scores. These relationships were weaker in the at-risk group. A, The first latent variable (p < 0.001, 41.1% covariance) from the omnibus, between groups behavioral PLS assessing correlations between the 8 variables and SDBOLD. The bars represent the correlation between each variable with the pattern of SDBOLD shown in the corresponding brain plot (B). The error bars represent 95% confidence intervals, so the error bars of variables significantly contributing to the latent variable will not cross zero. B Brain plots showing the bootstrap ratios for the latent variable, which may be interpreted like z scores. That is, the highlighted voxels are reliably associated with the related variables in A that significantly contribute to the latent variable. To clearly show the spatial pattern of the respective latent variable, only voxels with bootstrap ratios >|4| are pictured.

  • Figure 4.
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    Figure 4.

    Multivariate PLS analysis of the relationship between SDBOLD and gray matter volume in the HC and MTL. In the at-risk group, reduced volumetry in the CA1, CA3/DG, PHC, and alERC was associated with higher SDBOLD in the MTL. The effect was less widespread in controls. A, B, The first latent variable (p < 0.0001, 72.0% covariance) from the omnibus between groups behavioral PLS assessing correlations between volumetry of 7 MTL regions (3 hippocampal subfields and 4 MTL subregions) and MTL SDBOLD. A, The bars represent the correlation between each MTL subregion with the pattern of SDBOLD shown in the corresponding brain plot (B). The error bars represent 95% confidence intervals, so the error bars of variables significantly contributing to the latent variable will not cross zero. B, Brain plots showing the bootstrap ratios for the latent variable, which may be interpreted like z scores. Voxels with bootstrap ratios >|2.5| are pictured and considered to be reliably correlated with the brain volumes that are significantly contributing to the latent variable. C, Scatter plot shows the correlation between brain scores from the PLS comparing whole-brain SDBOLD and several predictor variables (Fig. 3) and the brain scores from the PLS comparing MTL variability and volumes. The strong correlation (at-risk: r = 0.89, p < 0.0001; controls: r = 0.91, p < 0.0001) indicates that the pattern of SDBOLD that is associated with behavior is highly similar to the pattern of SDBOLD associated with MTL volumes. Brain volumes: HC subfields (CA1, dentate gyrus/CA2 and 3, and subiculum) and MTL cortices (alERC, pmERC, PRC, and PHC).

Tables

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    Table 1

    Demographic characteristics

    At-risk (SD)Controls (SD)
    n2020
    MoCA23.4 (1.9), all <2627.9 (1.7), all >26
    Age71.5 (6.5)70.3 (4.5)
    Education15.5 (2.9)16.5 (2.8)
    Sex17 female13 female
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    Table 2

    Factor loadings for neuropsychological tests

    Neuropsychological TestSubtest1. Visuospatial2. Cognitive control/speed3. Memory4. Intelligence
    RCFTImmediate recall 0.87 -0.030.060.13
    Delayed recall 0.84 -0.010.080.24
    VOSPSilhouettes 0.58 0.1300.23
    Progressive silhouettes 0.69 0.23-0.090.2
    WASIBlock design 0.53 0.160.37 0.53
    Trail making test (TMT)Alternating (version A) 0.46 0.54 0.11−0.14
    Sequential (version B) 0.41 0.69 0.30.18
    WAISDigit span forward−0.31 0.72 −0.130.18
    Digit span backward0.08 0.79 0.210.08
    WMSImmediate recall−0.080.2 0.85 0.28
    Delayed recall0.090.05 0.88 −0.02
    WASIMatrix reasoning0.360.60.06 0.42
    Vocabulary0.240.190.15 0.83
    Similarity0.240.080.05 0.8
    Proportion of variance accounted for by each factor0.240.180.150.13
    • *Loadings >|0.40| are bold to assist with factor interpretation.

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    Table 3.

    Significant clusters representing relationship between SDBOLD and eight variables (Fig. 3)

    ROI nameMNI coordinates, mm; x, y, zCluster size, voxelsBSR
    Left parahippocampal gyrus27, 22, 137898.13
    Right thalamus17, 26, 163697.31
    Left lateral occipital cortex31, 12, 26327.02
    Right caudate, subcallosal cortex21, 36, 17307.28
    Left temporal fusiform cortex31, 30, 8295.72
    Right superior parietal lobule15, 21, 34285.89
    Right superior temporal gyrus, posterior division6, 23, 18287.09
    Left superior parietal lobule29, 19, 34256.53
    Left occipital pole25, 8, 20255.57
    Left middle frontal gyrus33, 36, 25195.7
    Left superior temporal gyrus38, 23, 18175.84
    Left middle temporal gyrus38, 28, 15165.08
    Right insular cortex12, 29, 17134.69
    Right frontal pole14, 42, 24125.72
    Left postcentral gyrus33, 24, 30115.25
    Right precuneus cortex21, 11, 28115.65
    Right paracingulate gyrus20, 44, 16105.56
    Right superior paracingulate gyrus20, 37, 27104.59
    Left caudate25, 36, 2085.23
    Right frontal operculum cortex13, 38, 1884.95
    Right angular gyrus6, 19, 2174.87
    Right insular cortex14, 32, 2075.2
    Right parietal operculum cortex11, 25, 2274.51
    Left postcentral gyrus38, 27, 2475.42
    Left juxstapositional lobule cortex (formerly supplementary morter cortex)22, 28, 3174.75
    Left precuneus cortex23, 18, 3475.13
    Left precuneus cortex27, 16, 2064.82
    Right frontal pole22, 46, 2565.11
    Right frontal pole10, 33, 855.06
    Right lateral occipital cortex, superior division14, 15, 2855.38
    Right precuneus cortex20, 18, 3155.13
    • Only clusters of five voxels or larger with bootstrap ratio (BSR) >|4| are included.

Extended Data

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    Supplementary Table 2-2. Download Table 2-2, DOCX file.

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Resting State BOLD Variability of the Posterior Medial Temporal Lobe Correlates with Cognitive Performance in Older Adults with and without Risk for Cognitive Decline
Tyler J. Good, Joshua Villafuerte, Jennifer D. Ryan, Cheryl L. Grady, Morgan D. Barense
eNeuro 19 March 2020, 7 (3) ENEURO.0290-19.2020; DOI: 10.1523/ENEURO.0290-19.2020

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Resting State BOLD Variability of the Posterior Medial Temporal Lobe Correlates with Cognitive Performance in Older Adults with and without Risk for Cognitive Decline
Tyler J. Good, Joshua Villafuerte, Jennifer D. Ryan, Cheryl L. Grady, Morgan D. Barense
eNeuro 19 March 2020, 7 (3) ENEURO.0290-19.2020; DOI: 10.1523/ENEURO.0290-19.2020
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Keywords

  • aging
  • BOLD fMRI
  • BOLD variability
  • MCI

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