Changes in local brain function in mild cognitive impairment due to semantic dementia

Abstract

Aims: Mild cognitive impairment due to semantic dementia represents the preclinical stage, involving cognitive decline dominated by semantic impairment below the semantic dementia standard. Therefore, studying mild cognitive impairment due to semantic dementia may identify changes in patients before progression to dementia. However, whether changes in local functional activity occur in preclinical stages of semantic dementia remains unknown. Here, we explored local functional changes in patients with mild cognitive impairment due to semantic dementia using resting-state functional MRI.

Methods: We administered a battery of neuropsychological tests to twenty-two patients with mild cognitive impairment due to semantic dementia (MCI-SD group) and nineteen healthy controls (HC group). We performed structural MRI to compare gray matter volumes, and resting-state functional MRI with multiple sub-bands and indicators to evaluate functional activity.

Results: Neuropsychological tests revealed a significant decline in semantic performance in the MCI-SD group, but no decline in other cognitive domains. Resting-state functional MRI revealed local functional changes in multiple brain regions in the MCI-SD group, distributed in different sub-bands and indicators. In the normal band, local functional changes were only in the gray matter atrophic area. In the other sub-bands, more regions with local functional changes outside atrophic areas were found across various indicators. Among these, the degree centrality of the left precuneus in the MCI-SD group was positively correlated with general semantic tasks (oral sound naming, word-picture verification).

Conclusion: Our study revealed local functional changes in mild cognitive impairment due to semantic dementia, some of which were located outside the atrophic gray matter. Driven by functional connectivity changes, the left precuneus might play a role in preclinical semantic dementia. The study proved the value of frequency-dependent sub-bands, especially the slow-2 and slow-3 sub-bands.

Keywords: frequency-dependent; mild cognitive impairment; resting-state functional MRI; semantic dementia.

FIGURE 1

GMV differences and local functional changes in normal band, slow‐4, slow‐5, and slow‐2 band. The MCI‐SD group was compared with the HC group. (A) VBM analysis shows gray matter regions with GMV differences across groups. (B) In the normal band, the fALFF decreased in Temporal_Pole_Sup_R, Frontal_Inf_Orb_R, Temporal_Sup_R, Rolandic_Oper_R, Heschl_R, Insula_R, Frontal_Mid_R, Frontal_Sup_R. (C) In slow‐4 band, fALFF decreased in Temporal_Sup_R, Heschl_R, Cuneus_R, Precuneus_R, Parietal_Sup_R, Supp_Motor_Area. ReHo decreased in Frontal_Inf_Tri_R, Postcentral_R, SupraMarginal_R. (D) In slow‐5 band, ReHo decreased in Parietal_Inf_L. DC decreased in Cingulum_Ant_R, Frontal_Sup_Medial_R, Cingulum_Ant_L. (E) In slow‐2 band, ALFF decreased in Parietal_Inf_L, SupraMarginal_L. FALFF decreased in Occipital_Inf_R, Occipital_Mid_R, Temporal_Mid_R, Parietal_Sup_L. Wavelet‐ALFF decreased in Temporal_Mid_L, SupraMarginal_L, Temporal_Sup_L, Parietal_Inf_L, Angular_L, Postcentral_L, Parietal_Inf_L. ReHo decreased in Temporal_Mid_L, White Matter. DC decreased in SupraMarginal_R, Parietal_Inf_R. (GRF, voxel‐wise p < 0.001, cluster‐wise p < 0.05, two‐tailed). Brain region labels are taken from the Anatomical Automatic Labeling atlas (AAL). ALFF, amplitude of low‐frequency fluctuation; fALFF, fractional amplitude of low‐frequency fluctuation; Wavelet‐ALFF, wavelet‐based amplitude of low‐frequency fluctuation; ReHo, regional homogeneity; DC, degree centrality

FIGURE 2

Local functional changes in slow‐3 band and correlation analysis. (A) The MCI‐SD group compared with the HC group in the slow‐3 band. ALFF decreased in Temporal_Mid_L, SupraMarginal_L, Angular_L, Parietal_Inf_L, Postcentral_L. FALFF decreased Insula_L, Caudate_L, Putamen_L. PerAF decreased in Frontal_Inf_Tri_R, Frontal_Inf_Oper_R, Precentral_R, Frontal_Mid_R, Cingulum_Ant_R. Wavelet‐ALFF decreased in Temporal_Mid_L, SupraMarginal_L, Parietal_Inf_L, Angular_L, and Postcentral_L. ReHo increased in the Temporal_Inf_R, Temporal_Mid_R, and Fusiform_R. DC decreased in the Precuneus_L, Precuneus_R, and Cingulum_Mid_L (GRF, voxel‐wise p < 0.001, cluster‐wise p < 0.05, two‐tailed). (B) Correlation analysis of DC in the left precuneus with WPV and SN. WPV, word‐picture verification, SN, oral sound naming. The dots in the dot graph were the values of the peak points of clusters. Brain region labels are taken from the Anatomical Automatic Labeling atlas (AAL). ALFF, amplitude of low‐frequency fluctuation; fALFF, fractional amplitude of low‐frequency fluctuation; PerAF, percent amplitude of fluctuation; Wavelet‐ALFF, wavelet‐based amplitude of low‐frequency fluctuation; ReHo, regional homogeneity; DC, degree centrality