Parkinsonism Is Associated with Altered SMA-Basal Ganglia Structural and Functional Connectivity in Frontotemporal Degeneration
Abstract
:1. Introduction
2. Materials and Methods
2.1. Participants
2.2. Clinical and Neuropsychological Assessment
2.3. MRI Data Acquisition
- -
- High-resolution three-dimensional (3D) T1-weighted (T1-3D) MPRAGE sequence (repetition time (TR) = 2400 ms, echo time (TE) = 2.12 ms, inversion time (TI) = 1000 ms, flip angle = 8°, field of view (FOV) = 256 mm, matrix = 256 × 256, 176 sagittal slices 1-mm thick, no gap);
- -
- Diffusion tensor imaging (DTI) single-shot, echo-planar, spin-echo sequence with 10 interspersed volumes of b = 0 (b0) and 64 gradient directions, TR = 4600 ms, TE = 78 ms, multiband acceleration factor = 2, monopolar diffusion scheme, FOV = 192 mm, matrix = 96 × 96, b = 1000 s/mm2, 72 contiguous axial 2-mm thick slices;
- -
- Blood oxygen level-dependent (BOLD) single-shot echo-planar imaging (TR = 3000 ms, TE = 30 ms, flip angle = 89°, FOV = 192 mm, 64 × 64 matrix, 50 contiguous axial 3-mm thick slices, 140 volumes, voxel size = 3 mm3), with all patients instructed to close their eyes and remain awake during the resting-state functional MRI acquisitions;
- -
- Dual turbo spin-echo, proton density (PD) and T2-weighted images (TR = 3320 ms, TE1 = 10 ms, TE2 = 103 ms, FOV = 220 mm, matrix = 384 × 384, 25 axial slices 4-mm thick, 30% gap);
- -
- High-resolution 3D fluid-attenuated inversion recovery (FLAIR) sequence (TR = 6000 ms, TE = 395 ms, TI = 2100 ms, FOV = 256 mm, matrix = 256 × 256, 176 sagittal slices 1-mm thick, no gap).
- -
- Two expert radiologists (PP and CG, with more than 20 and 10 years of experience, respectively) examined all MRIs to assess the presence of T2 and T2 FLAIR white matter hyperintensities (WMH). The amount of WMH was quantified using the four-stage Fazekas visual rating scale (Fazekas 0–1 = no to mild WMH, Fazekas 2 = moderate WMH, Fazekas 3 = severe WMH) [32].
2.4. MRI Analysis
2.4.1. Data Preprocessing
2.4.2. Cortical Thickness
2.4.3. Basal Ganglia and Thalamus Volumetry
2.4.4. Selection of Regions of Interest (ROIs)
2.4.5. Structural Connectivity—Tractography
2.4.6. Functional Connectivity—ROI-to-ROI Correlation Analyses
2.5. Statistical Analyses
3. Results
3.1. Cortical Thickness and Basal Ganglia/Thalamic Volumetry
3.2. Structural Connectivity
3.3. Functional Connectivity
3.4. Correlation Analyses
4. Discussion
4.1. Cortical Thickness in FTD
4.2. Striatal Degeneration in FTD with Parkinsonism
4.3. Reduced SMA-Basal Ganglia Structural and Functional Connectivity in FTD with Parkinsonism
4.4. Study Strengths and Limitations
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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HC (N = 30) | FTD (N = 30) | p * | Park− (N = 18) | Park+ (N = 12) | p * | |
---|---|---|---|---|---|---|
Demographic/clinical features | ||||||
Age | 68.2 ± 6.4 | 70.1 ± 7.4 | ns | 68.1 ± 7.8 | 73.3 ± 5.8 | ns |
Female/male, n | 9/21 | 9/21 | ns | 7/11 | 2/10 | ns |
Disease duration, y | - | 3.8 ± 1.9 | - | 3.7 ± 1.9 | 4.1 ± 1.8 | ns |
FTD-subtype (nfv-PPA/bv-FTD), n | - | 19/11 | - | 10/8 | 9/3 | ns |
Neuropsychological scores | ||||||
CDR-FTD | - | 6.4 ± 3.4 | - | 6.5 ± 3.3 | 6.3 ± 3.7 | ns |
MMSE | - | 20.6 ± 7.1 | - | 21.2 ± 7.3 | 19.7 ± 7.1 | ns |
FAB | - | 10.8 ± 4.3 | - | 11.7 ± 4.1 | 9.2 ± 4.2 | ns |
TMT A, sec | - | 142.3 ± 99.1 | - | 135.5 ± 104.8 | 155.5 ± 91.7 | ns |
TMT B, sec | - | 224.5 ± 90.5 | - | 196.7 ± 96.9 | 276.9 ± 46.0 | ns |
VSF | - | 20.4 ± 11.4 | - | 21.3 ± 11.8 | 18.8 ± 10.9 | ns |
VPF | - | 14.0 ± 12.1 | - | 14.9 ± 13.0 | 12.1 ± 10.6 | ns |
MDS-UPDRS-III § | - | 17.8 ± 10.4 § | - | - | 17.8 ± 10.4 | - |
HC | Park− | Park+ | p * | H | Post hoc | |
---|---|---|---|---|---|---|
L global cortical thickness (mm) | 2.361 ± 0.08 | 2.217 ± 0.12 | 2.204 ± 0.12 | <0.001 | 21.02 | HC-Park− p < 0.001 |
HC-Park+ p = 0.001 | ||||||
Park−Park+ ns | ||||||
R global cortical thickness (mm) | 2.356 ± 0.08 | 2.279 ± 0.11 | 2.252 ± 0.09 | 0.003 | 10.95 | HC-Park− p = 0.038 |
HC-Park+ p = 0.007 | ||||||
Park−Park+ ns | ||||||
L global cortical volume | 0.1344 ± 0.0093 | 0.1195 ± 0.0146 | 0.1197 ± 0.0167 | <0.001 | 17.07 | HC-Park− p = 0.001 |
HC-Park+ p = 0.009 | ||||||
Park−Park+ ns | ||||||
R global cortical volume | 0.1377 ± 0.0079 | 0.1278 ± 0.0123 | 0.1261 ± 0.0140 | <0.001 | 13.01 | HC-Park− p = 0.006 |
HC-Park+ p = 0.016 | ||||||
Park− Park+ ns | ||||||
L putamen, fraction | 0.0028 ± 0.0003 | 0.0025 ± 0.0006 | 0.0023 ± 0.0005 | 0.010 | 9.22 | HC-Park− ns |
HC-Park+ p = 0.016 | ||||||
Park− Park+ ns | ||||||
R putamen, fraction | 0.0029 ± 0.0002 | 0.0027 ± 0.0004 | 0.0025 ± 0.0004 | 0.004 | 10.86 | HC-Park− ns |
HC-Park+ p = 0.004 | ||||||
Park− Park+ ns | ||||||
L globus pallidus, fraction | 0.0012 ± 0.0001 | 0.0011 ± 0.0002 | 0.0010 ± 0.0002 | ns | - | - |
R globus pallidus, fraction | 0.0012 ± 0.0002 | 0.0011 ± 0.0001 | 0.0011 ± 0.0002 | ns | - | - |
L thalamic fraction, fraction | 0.0046 ± 0.0005 | 0.0041 ± 0.0005 | 0.0041 ± 0.0005 | <0.001 | 17.10 | HC-Park− p = 0.002 |
HC-Park+ p = 0.003 | ||||||
Park−Park+ ns | ||||||
R thalamic fraction, fraction | 0.0045 ± 0.0003 | 0.0043 ± 0.0005 | 0.0041 ± 0.0004 | 0.009 | 9.33 | HC-Park− ns |
HC-Park+ p = 0.007 | ||||||
Park− Park+ ns |
HC | Park− | Park+ | p * | H | Post Hoc | |
---|---|---|---|---|---|---|
WM Tracts–FA | ||||||
SMA-putamen | 0.478 ± 0.04 | 0.454 ± 0.05 | 0.433 ± 0.03 | 0.003 | 11.31 | HC-Park− ns |
HC-Park+ p = 0.003 | ||||||
Park–Park+ ns | ||||||
SMA-pallidus | 0.500 ± 0.04 | 0.481 ± 0.05 | 0.455 ± 0.02 | 0.006 | 10.36 | HC-Park− ns |
HC-Park+ p = 0.004 | ||||||
Park–Park+ ns | ||||||
SMA-thalamus | 0.504 ± 0.04 | 0.487 ± 0.05 | 0.462 ± 0.03 | 0.012 | 8.93 | HC-Park− ns |
HC-Park+ p = 0.008 | ||||||
Park–Park+ ns | ||||||
M1-putamen | 0.496 ± 0.05 | 0.472 ± 0.05 | 0.452 ± 0.03 | ns | - | - |
M1-pallidus | 0.518 ± 0.05 | 0.497 ± 0.05 | 0.478 ± 0.03 | ns | - | - |
M1-thalamus | 0.519 ± 0.05 | 0.510 ± 0.05 | 0.492 ± 0.04 | ns | - | - |
ROI pairs RSFC–r (Z-transformed) | ||||||
SMA-putamen | 0.689 ± 0.25 | 0.714 ± 0.21 | 0.465 ± 0.19 | 0.012 | 8.76 | HC-Park− ns |
HC-Park+ p = 0.017 | ||||||
Park—Park+ p = 0.027 | ||||||
SMA-pallidus | 0.492 ± 0.19 | 0.485 ± 0.17 | 0.346 ± 0.19 | ns | - | - |
SMA-thalamus | 0.665 ± 0.24 | 0.793 ± 0.29 | 0.604 ± 0.36 | ns | - | - |
M1-putamen | 0.638 ± 0.29 | 0.698 ± 0.22 | 0.510 ± 0.33 | ns | - | - |
M1-pallidus | 0.465 ± 0.23 | 0.487 ± 0.16 | 0.348 ± 0.21 | ns | - | - |
M1-thalamus | 0.717 ± 0.31 | 0.828 ± 0.31 | 0.626 ± 0.36 | ns | - | - |
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Piervincenzi, C.; Suppa, A.; Petsas, N.; Fabbrini, A.; Trebbastoni, A.; Asci, F.; Giannì, C.; Berardelli, A.; Pantano, P. Parkinsonism Is Associated with Altered SMA-Basal Ganglia Structural and Functional Connectivity in Frontotemporal Degeneration. Biomedicines 2023, 11, 522. https://doi.org/10.3390/biomedicines11020522
Piervincenzi C, Suppa A, Petsas N, Fabbrini A, Trebbastoni A, Asci F, Giannì C, Berardelli A, Pantano P. Parkinsonism Is Associated with Altered SMA-Basal Ganglia Structural and Functional Connectivity in Frontotemporal Degeneration. Biomedicines. 2023; 11(2):522. https://doi.org/10.3390/biomedicines11020522
Chicago/Turabian StylePiervincenzi, Claudia, Antonio Suppa, Nikolaos Petsas, Andrea Fabbrini, Alessandro Trebbastoni, Francesco Asci, Costanza Giannì, Alfredo Berardelli, and Patrizia Pantano. 2023. "Parkinsonism Is Associated with Altered SMA-Basal Ganglia Structural and Functional Connectivity in Frontotemporal Degeneration" Biomedicines 11, no. 2: 522. https://doi.org/10.3390/biomedicines11020522
APA StylePiervincenzi, C., Suppa, A., Petsas, N., Fabbrini, A., Trebbastoni, A., Asci, F., Giannì, C., Berardelli, A., & Pantano, P. (2023). Parkinsonism Is Associated with Altered SMA-Basal Ganglia Structural and Functional Connectivity in Frontotemporal Degeneration. Biomedicines, 11(2), 522. https://doi.org/10.3390/biomedicines11020522