Rapid Precision Functional Mapping of Individuals Using Multi-Echo fMRI

Charles J Lynch, Jonathan D Power, Matthew A Scult, Marc Dubin, Faith M Gunning, Conor Liston, Charles J Lynch, Jonathan D Power, Matthew A Scult, Marc Dubin, Faith M Gunning, Conor Liston

Abstract

Resting-state functional magnetic resonance imaging (fMRI) is widely used in cognitive and clinical neuroscience, but long-duration scans are currently needed to reliably characterize individual differences in functional connectivity (FC) and brain network topology. In this report, we demonstrate that multi-echo fMRI can improve the reliability of FC-based measurements. In four densely sampled individual humans, just 10 min of multi-echo data yielded better test-retest reliability than 30 min of single-echo data in independent datasets. This effect is pronounced in clinically important brain regions, including the subgenual cingulate, basal ganglia, and cerebellum, and is linked to three biophysical signal mechanisms (thermal noise, regional variability in the rate of T2∗ decay, and S0-dependent artifacts) with spatially distinct influences. Together, these findings establish the potential utility of multi-echo fMRI for rapid precision mapping using experimentally and clinically tractable scan times and will facilitate longitudinal neuroimaging of clinical populations.

Keywords: functional brain networks; multi-echo fMRI; precision functional mapping; test-retest reliability.

Conflict of interest statement

Declaration of Interests C.L. is listed as an inventor for Cornell University patent applications on neuroimaging biomarkers for depression that are pending or in preparation. The authors report no biomedical financial interests or other potential conflicts of interest.

Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.

Figures

Figure 1.. Obtaining Reliable Resting-State Functional Connectivity…
Figure 1.. Obtaining Reliable Resting-State Functional Connectivity (FC) Estimates Can Require Large Quantities of Single-Echo (SE) fMRI Data Per Subject
The reliability of resting-state FC was evaluated brain-wide in three independent SE rsfMRI datasets: (A) The Midnight Scan Club (MSC) dataset (Gordon et al., 2017c), which consists of 10 individuals that underwent 10 × 30-min scans (three representative subjects are shown: MSC01, MSC04, and MSC06). (B) The CAST dataset (Newbold et al., 2020), which consists of three individuals that underwent 10–14 × 30-min scans (one representative subject shown: CAST01), (C) The MC dataset (Poldrack et al., 2015), which consists of a single individual that underwent 84 × 10-min scans. (D) FC reliability maps index (using spatial correlation) how similar the FC of each point in the brain is when calculated using the specified amount of data from a single scan versus a large amount of independent data (all other scans available for that participant concatenated). Values approaching 1 indicate better reliability. The average reliability value within FreeSurfer defined cortical and subcortical regions of interest at each scan duration (the median value across the 14 subjects) is shown. Brain regions are ordered (in descending fashion) from most reliable to least reliable. m, minute.
Figure 2.. A Key Benefit of Multi-echo…
Figure 2.. A Key Benefit of Multi-echo (ME) fMRI Is Improved BOLD Contrast and Reduced Signal Dropout after Echoes Are Combined
(A) A ME fMRI sequence acquires multiple images at different echo times (TE) spanning dozens of milliseconds. (B) Signals decay more rapidly in brain regions with a short T2* value, such as the subgenual anterior cingulate cortex (sgACC; purple). Echoes are combined such that those near the estimated T2* at each voxel are weighted most heavily, yielding an “optimally combined” ME (OC-ME) time series with improved BOLD contrast, less signal dropout, and dampened thermal noise. (C) WTE represents the optimal weight for each echo. T2* values are calculated at each point in the brains of ME01 and ME02. Differences in the FC of seed regions with different T2* values help to convey the region-specific effect of the OC-ME procedure. FC maps were created using OC-ME and two different kinds of SE data (the second echo of the ME scan and a separate fast-TR SE sequence with a faster sampling rate) that were collected from both ME01 and ME02. PFC, prefrontal cortex; TE2, second echo of the ME scan.
Figure 3.. The Optimal Combination and ME…
Figure 3.. The Optimal Combination and ME Denoising Procedures Improve the Reliability of Resting-State FC Measurements in Two Densely Sampled Individuals
The reliability of FC estimates in ME01 and ME02 after repeated imaging using a ME fMRI sequence (6 h total; 24 × 14.5-min scans acquired over a 9-month period). (A) Reliability maps were calculated using three different denoising strategies, leveraging both (OC-ME + ME-ICA), one (OC-ME + ICA-AROMA), or no (TE2 + ICA-AROMA) benefits of ME fMRI. (B) Time × reliability curves show the average reliability obtained in gray matter, subcortical structures, and the cerebellum given different scan durations. Curves from the independent SE MC and MSC datasets are provided as comparators. Transparent curves represent individual subjects. Solid lines represent the median curve within datasets. Note that the purple lines representing the different independent SE datasets can be distinguished by their unique dash spacing patterns. m, minute.
Figure 4.. The Level of Reliability Obtained…
Figure 4.. The Level of Reliability Obtained Using a ME Sequence Is Greater Than a SE Sequence with a Fast Sampling Rate
FC reliability maps derived from ME and fast-TR (800 ms) SE data acquired from the same individual (sub-ME01). (A) Insets highlight regions of cortex where differences between the two sets of reliability maps were most pronounced. (B) Reliability values in the cerebellum and in subcortex. (C) Time × reliability curves show the average reliability value (calculated separately in cortex, subcortical structures, and cerebellum) given different amounts and kinds of data acquired from sub-ME01.
Figure 5.. Functional Brain Network Topology Is…
Figure 5.. Functional Brain Network Topology Is More Reliable in Individuals Scanned Using a ME Sequence
(A) Functional brain networks identified brain-wide in ME01 using a precision mapping routine and all 6 h of OC-ME + ME-ICA data. A seed (gray sphere) placed in a patch of fronto-parietal control network (yellow) in the left lateral PFC of ME01 highlights how FC is largely constrained within-network. The effect of the OC-ME and ME-ICA procedures on the reliability of individual-specific functional brain network topology was evaluated using a mixed-effects ANOVA model. The OC-ME procedure and ME-ICA denoising algorithm additively enhanced the reliability (indexed using the adjusted Rand coefficient comparing the similarity of network partitions defined using single-scan data and all other scans concatenated) of functional topology in the four densely sampled individuals. (B and C) Comparison of adjusted Rand coefficients from OC-ME + ME-ICA data to those derived from fast-TR SE data (B) collected from the same study participant (ME01) and the three independent SE datasets (C). (D) Functional brain networks mapped using data from a single OC-ME + ME-ICA scan and all other OC-ME + ME-ICA scans (concatenated; 5.75 h total) for sub-ME01. The resting-state FC (calculated using the single-scan data) of a seed (gray sphere; highlighted using an arrow) placed in a default mode network patch is constrained within the borders of this network defined using held-out data, indicating high reliability. p denotes p value.

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