Detecting Static and Dynamic Differences between Eyes-Closed and Eyes-Open Resting States Using ASL and BOLD fMRI

Zou, Qihong; Yuan, Binke; Gu, Hong; Liu, Dongqiang; Wang, Danny J.J.; Gao, Jia‐Hong; Yang, Yihong; Zang, Yu‐Feng

doi:10.1371/journal.pone.0121757

Cited by 51 publications

(58 citation statements)

References 53 publications

(47 reference statements)

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“…3), a key region which has been well-documented in previous dopaminergic positron emission tomography (PET) 27 and meta-analysis of RS-fMRI 11 . The results of EOEC data were very consistent with those of previous RS-fMRI studies 28,29 , e.g., higher ALFF in the sensorimotor cortex and lower ALFF in the lateral occipital cortex in EC than in EO (Fig. 3).…”

Section: Discussionsupporting

confidence: 90%

Small effect size leads to reproducibility failure in resting-state fMRI studies

Jia

Zhao

Barton

et al. 2018

Preprint

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Thousands of papers using resting-state functional magnetic resonance imaging (RS-fMRI) have been published on brain disorders. Results in each paper may have survived correction for multiple comparison. However, since there have been no robust results from large scale meta-analysis, we do not know how many of published results are truly positives. The present meta-analytic work included 60 original studies, with 57 studies (4 datasets, 2266 participants) that used a between-group design and 3 studies (1 dataset, 107 participants) that employed a within-group design. To evaluate the effect size of brain disorders, a very large neuroimaging dataset ranging from neurological to psychiatric disorders together with healthy individuals have been analyzed. Parkinson's disease off levodopa (PD-off) included 687 participants from 15 studies. PD on levodopa (PD-on) included 261 participants from 9 studies. Autism spectrum disorder (ASD) included 958 participants from 27 studies. The meta-analyses of a metric named amplitude of low frequency fluctuation (ALFF) showed that the effect size (Hedges' g) was 0.19 -0.39 for the 4 datasets using between-group design and 0.46 for the dataset using within-group design. The effect size of PD-off, PD-on and ASD were 0.23, 0.39, and 0.19, respectively. Using the meta-analysis results as the robust results, the between-group design results of each study showed high false negative rates (median 99%), high false discovery rates (median 86%), and low accuracy (median 1%), regardless of whether stringent or liberal multiple comparison correction was used. The findings were similar for 4 RS-fMRI metrics including ALFF, regional homogeneity, and degree centrality, as well as for another widely used RS-fMRI metric namely seed-based functional connectivity. These observations suggest that multiple comparison correction does not control for false discoveries across multiple studies when the effect sizes are relatively small. Meta-analysis on un-thresholded t-maps is critical for the recovery of ground truth. We recommend that to achieve high reproducibility through meta-analysis, the neuroimaging research field should share raw data or, at minimum, provide un-thresholded statistical images.

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Section: Discussionsupporting

confidence: 90%

Small effect size leads to reproducibility failure in resting-state fMRI studies

Jia

Zhao

Barton

et al. 2018

Preprint

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“…The test–retest analysis results and the inhomogeneous nMSSD/VSD ratio shown in this paper suggest nMSSD and VSD as two different but reliable indices for characterizing resting-state brain activity. Using rsfMRI data acquired with eyes closed and eyes open, nMSSD and VSD revealed brain difference patterns similar to those reported in previous studies [28, 46], suggesting that nMSSD and VSD are sensitive to regional activity alterations during brain state change.…”

Section: Discussionsupporting

confidence: 82%

Assessing the mean strength and variations of the time-to-time fluctuations of resting-state brain activity

Zang

Ding

et al. 2016

Med Biol Eng Comput

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The time-to-time fluctuations (TTFs) of resting-state brain activity as captured by resting-state fMRI (rsfMRI) have been repeatedly shown to be informative of functional brain structures and disease-related alterations. TTFs can be characterized by the mean and the range of successive difference. The former can be measured with the mean squared successive difference (MSSD), which is mathematically similar to standard deviation; the latter can be calculated by the variability of the successive difference (VSD). The purpose of this study was to evaluate both the resting state-MSSD and VSD of rsfMRI regarding their test–retest stability, sensitivity to brain state change, as well as their biological meanings. We hypothesized that MSSD and VSD are reliable in resting brain; both measures are sensitive to brain state changes such as eyes-open compared to eyes-closed condition; both are predictive of age. These hypotheses were tested with three rsfMRI datasets and proven true, suggesting both MSSD and VSD as reliable and useful tools for resting-state studies.

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“…Taglizucchi and colleagues showed that instructing subjects to keep their eyes open with/without fixation during the experiment resulted in a decreased amount of sleep than eyes closed (Tagliazucchi and Laufs, 2014 It would be relatively difficult to ask patients to maintain their gaze on a fixation for quite a few minutes. As did in some previous studies (Liu et al, 2013;Yang et al, 2007;Yuan et al, 2014;Zou et al, 2009;Zou et al, 2015), the current study also only focused on the comparisons of the eyes closed state and eyes open without fixation state and hopefully this study would be more helpful to clinical studies. Future comprehensive test-retest reliability studies including EC and EO with/without fixation are warranted.…”

Section: Test-retest Reliability Of Eyes-open and Eyes-closed Statesmentioning

confidence: 99%

“…It was observed almost one century ago by Berger (Berger, 1929(Berger, , 1930) that the EEG alpha rhythm disappeared when the eyes were open, as compared to the case when the eyes were closed. BOLD fMRI studies have shown brain activity differences between the EO and EC states in the visual cortex (Jao et al, 2013;Liu et al, 2013;Yang et al, 2007;Zou et al, 2009;Zou et al, 2015), motor and auditory cortices (Jao et al, 2013;Liu et al, 2013;Yuan et al, 2014;Zou et al, 2015), and the default mode network (Jao et al, 2013;Liu et al, 2013;Yan et al, 2009). Using the ASL technique, significant CBF increases in the primary and secondary visual areas (Brodmann area (BA) 17, 18) for EO compared with EC state (Hermes et al, 2007;Zou et al, 2015) have been reported.…”

Section: Introductionmentioning

confidence: 99%

Reliability comparison of spontaneous brain activities between BOLD and CBF contrasts in eyes-open and eyes-closed resting states

et al. 2015

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Blood oxygenation level dependent (BOLD) and arterial spin labeling (ASL) are two predominant resting-state fMRI techniques in mapping spontaneous brain activities. At single voxel level, cerebral blood flow (CBF) measured by ASL and amplitude of low frequency fluctuations (ALFF) of BOLD have been recognized as useful indices to characterize brain function in health and disease. However, no study has directly compared the test-retest reliability between BOLD and CBF contrasts on the same group of subjects at single voxel level. Moreover, both eyes-open and eyes-closed conditions have been employed as resting states, but it is still not clear which state is more reliable. Here we collected BOLD and ASL data during eyes-open and eyes-closed states across three scanning visits on twenty-two healthy young subjects. CBF-mean, BOLD-and CBF-ALFF were computed to characterize corresponding brain activities at single voxel level. Seed-based functional connectivity (FC) with the posterior cingulate cortex (PCC) was further calculated for both BOLD and CBF data. Intra-class correlation was used as the index of long-term reliability between visits 1 and 2 (two months apart) and short-term reliability between visits 2 and 3 (on the same day). Both short-and long-term reliabilities for CBF-mean and BOLD-ALFF were high, but were lower for CBF-ALFF, BOLD-and CBF-FC in both eyes-open and eyes-closed states. Direct comparisons showed that brain regions with the highest reliability of CBF-mean were mainly in the gray matter. The reliability of CBF-ALFF and BOLD-FC was lower than that of BOLD-ALFF, and the reliability of CBF-FC was lower than those of both CBF-ALFF and BOLD-FC. Furthermore, we observed that reliabilities of the eyes-open state were higher than those of the eyes-closed state for both imaging contrasts, though the effect size was small. Voxel-wise comparisons demonstrated that the long-term reliability of BOLD-ALFF was significantly higher with eyes open in the visual system, and both the short-and long-term reliability of BOLD-FC was slightly higher with eyes open in the default mode network. Moreover, we showed that denoising decreased the reliability of both ALFF and FC of both BOLD and ASL contrasts. In conclusion, our results indicated that CBF-mean and BOLD-ALFF could both be used as reliable indices for characterizing resting-state brain activities at single voxel level and recommended the eyesopen state for resting-state studies, especially for those targeting the visual system and default mode network.

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Detecting Static and Dynamic Differences between Eyes-Closed and Eyes-Open Resting States Using ASL and BOLD fMRI

Cited by 51 publications

References 53 publications

Small effect size leads to reproducibility failure in resting-state fMRI studies

Small effect size leads to reproducibility failure in resting-state fMRI studies

Assessing the mean strength and variations of the time-to-time fluctuations of resting-state brain activity

Reliability comparison of spontaneous brain activities between BOLD and CBF contrasts in eyes-open and eyes-closed resting states

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