Dynamics and Concordance Abnormalities Among Indices of Intrinsic Brain Activity in Individuals With Subjective Cognitive Decline: A Temporal Dynamics Resting-State Functional Magnetic Resonance Imaging Analysis

Abstract

Individuals with subjective cognitive decline (SCD) are more likely to develop into Alzheimer disease (AD) in the future. Resting-state functional magnetic resonance imaging (rs-fMRI) studies have shown alterations of intrinsic brain activity (IBA) in SCD individuals. However, rs-fMRI studies to date have mainly focused on static characteristics of IBA, with few studies reporting dynamics- and concordance-related changes in IBA indices in SCD individuals. To investigate these aberrant changes, a temporal dynamic analysis of rs-fMRI data was conducted on 94 SCD individuals (71.07 ± 6.18 years, 60 female), 75 (74.36 ± 8.42 years, 35 female) mild cognitive impairment (MCI) patients, and 82 age-, gender-, and education-matched controls (NCs; 73.88 ± 7.40 years, 49 female) from the Alzheimer's Disease Neuroimaging Initiative database. The dynamics and concordance of the rs-fMRI indices were calculated. The results showed that SCD individuals had a lower amplitude of low-frequency fluctuations dynamics in bilateral hippocampus (HP)/parahippocampal gyrus (PHG)/fusiform gyrus (FG) and bilateral cerebellum, a lower fractional amplitude of low-frequency fluctuation dynamics in bilateral precuneus (PreCu) and paracentral lobule, and a lower regional homogeneity dynamics in bilateral cerebellum, vermis, and left FG compared with the other two groups, whereas those in MCI patients were higher (Gaussian random field-corrected, voxel-level P < 0.001, cluster-level P < 0.05). Furthermore, SCD individuals had higher concordance in bilateral HP/PHG/FG, temporal lobe, and left midcingulate cortex than NCs, but those in MCI were lower than those in NCs. No correlation between concordance values and neuropsychological scale scores was found. SCD individuals showed both dynamics and concordance-related alterations in IBA, which indicates a compensatory mechanism in SCD individuals. Temporal dynamics analysis offers a novel approach to capturing brain alterations in individuals with SCD.

Keywords: Alzheimer's disease; intrinsic brain activity; resting-state functional MRI; subjective cognitive decline; temporal dynamics analysis.

Figure 1

Brief information about dynamic and concordance indices calculation.

Figure 2

Regions with differences in dALFF between the SCD, MCI, and NC groups and post-hoc analysis brain maps (GRF-corrected, voxel-level P < 0.001, cluster-level P < 0.05). (A) Differences in dALFF were shown in bilateral HP/PHG/FG, which extended to the left STG/MTG/TP and bilateral cerebellum among groups (red). (B) dALFF values in the MCI group were higher than those in the NC group (red), whereas those in the SCD group were lower than those in the other two groups (blue). dALFF, dynamics of amplitude of low-frequency fluctuations; FG, fusiform gyrus; GRF, Gaussian random field; HP, hippocampus; MCI, mild cognitive impairment; MTG, middle temporal gyrus; NC, normal control; PHG, parahippocampal gyrus; SCD, subjective cognitive decline; STG, superior temporal gyrus; TP, temporal pole.

Figure 3

Regions with differences in dfALFF between the SCD, MCI, and NC groups and post-hoc analysis brain maps (GRF-corrected, voxel-level P < 0.001, cluster-level P < 0.05). (A) Differences in dfALFF were shown in bilateral PreCu and paracentral lobule (red). (B) dfALFF values in the MCI group were higher than those in the NC group (red), whereas those in the SCD group were lower than those in the other two groups (blue). dfALFF, dynamics of fractional amplitude of low-frequency fluctuations; GRF, Gaussian random field; MCI, mild cognitive impairment; NC, normal control; PreCu, precuneus; SCD, subjective cognitive decline.

Figure 4

Regions with differences in dReHo between the SCD, MCI, and NC groups and post-hoc analysis brain maps (GRF-corrected, voxel-level P < 0.001, cluster-level P < 0.05). (A) Differences in dReHo were shown in left cerebellum posterior lobe, which extended to the left FG, vermis, and right cerebellum anterior lobe (red). (B) dReHo values in the MCI group were higher than those in the NC group (red), whereas those in the SCD group were lower than those in the other two groups (blue). dReHo, dynamics of regional homogeneity; FG, fusiform gyrus; GRF, Gaussian random field; MCI, mild cognitive impairment; NC, normal control; SCD, subjective cognitive decline.

Figure 5

Comparison of volume-wise concordance indices among the SCD, MCI, and NC groups. (A) Volume-wise concordance time series of typical SCD, MCI, and NC subjects. (B) Comparison of mean volume-wise concordance indices. (C) Comparison of the SD of volume-wise concordance indices. MCI, mild cognitive impairment; NC, normal control; SCD, subjective cognitive decline; SD, Standard deviation. *P < 0.05; **P < 0.01; ns, no significance.

Figure 6

Regions with differences in voxel-wise concordance between the SCD, MCI, and NC groups and post-hoc analysis brain maps (GRF-corrected, voxel-level P < 0.001, cluster-level P < 0.05). (A) Concordance differences were found in left HP/PHG, left insula/TP, left MCC, right TP/FG, right Rolandic operculum (RO)/insula (red). (B) The concordance of these regions in the MCI patients was lower than that in the NCs (blue), whereas the concordance in SCD patients was higher than that in the other two groups (red). FG, fusiform gyrus; GRF, Gaussian random field; HP, hippocampus; MCC, midcingulate cortex; MCI, mild cognitive impairment; NC, normal control; PHG, parahippocampal gyrus; RO, Rolandic operculum; SCD, subjective cognitive decline; TP, temporal pole.