Share：
Share this content in WeChat
X
[Chinese][PDF]3775
• Clinical Article •
Interhemispheric structural connectivity abnormalities in Alzheimer's disease and mild cognitive impairment: A DTI-based study
LIU Fan  NING Ruipeng  YU Qiurong  YIN Dazhi  LI Qianwen  LIU Ling  LI Renren  ZHANG Wei  LI Yunxia  FAN Mingxia 

Cite this article as: LIU F, NING R P, YU Q R, et al. Interhemispheric structural connectivity abnormalities in Alzheimer's disease and mild cognitive impairment: A DTI-based study[J]. Chin J Magn Reson Imaging, 2023, 14(6): 9-17. DOI:10.12015/issn.1674-8034.2023.06.002.


[Abstract] Objective To explore the structural connectivity changes through the corpus callosum in the interhemispheric homologous brain regions of Alzheimer's disease (AD) and mild cognitive impairment (MCI) and the relation with clinical cognitive function and activities of daily living.Materials and Methods MR diffusion tensor imaging data of 23 AD patients (AD group), 47 MCI patients (MCI group) and 37 healthy controls (HC group) were collected. Using the high-resolution transcallosal tract template, the fractional anisotropy (FA) and mean diffusivity (MD) of 32 transcallosal tracts connecting the interhemispheric homologous brain areas (including prefrontal lobe, sensory motor area, parietal lobe, temporal lobe and occipital lobe) among the three groups were calculated and compared. In the AD and MCI groups, water diffusion index values (FA and MD) of transcallosal tracts to the different homologous brain regions were further correlated with the basic scale of Montreal Cognitive Assessment (MoCA_B) and the scale of Activities of Daily Living Scale (ADL).Results Compared with HC, the mean MD values of all transcallosal nerve fiber bundles in the AD group had significantly increased (P＜0.05, FDR correction), and most transcallosal nerve fiber tracts of AD group (excluding the tracts to the orbital frontal, inferior frontal orbital, and ventral premotor areas) had significantly lower FA values (P＜0.05, FDR correction); The mean FA values and MD values of all transcallosal nerve fiber tracts to the interhemispheric homologous brain areas in the MCI group were not significantly different from the HC group. The mean FA values and MD values of some transcallosal tracts (excluding the tracts to the prefrontal and sensorimotor areas) in the AD group were significant different from the MCI group (P＜0.05, FDR correction). The mean FA values and MD values of all transcallosal nerve fiber bundles were not significantly correlated with the MoCA_B scores, but the mean FA values and MD values of multiple fiber bundles (including tracts to the dorsolateral prefrontal lobe, sensorimotor area, parietal lobe, occipital lobe and temporal lobe) were significantly correlated with the ADL scores (P＜0.05, FDR correction).Conclusions This study suggests that AD had more severe and extensive damage in the interhemispheric structural connectivity than MCI, and in AD, the degeneration of interhemispheric structural connectivity in the callosal fibers is more associated with a decline in activities of daily living. The severity of the transcallosal nerve fiber bundles damage may be used as an important reference index to assess the ability of live activities in AD.
[Keywords] neurodegenerative disease；Alzheimer's disease；mild cognitive impairment；diffusion tensor imaging；transcallosal fiber tracts；magnetic resonance imaging

LIU Fan1   NING Ruipeng1   YU Qiurong1   YIN Dazhi2, 3   LI Qianwen1   LIU Ling1   LI Renren4   ZHANG Wei4   LI Yunxia4*   FAN Mingxia1*  

1 Shanghai Key Laboratory of Magnetic Resonance, School of Physics and Electronic Science, East China Normal University, Shanghai 200062, China

2 School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, China

3 Shanghai Changning District Mental Health Center, Shanghai 200335, China

4 Department of Neurology, Tongji Hospital, School of Medicine, Tongji University, Shanghai 200092, China

Corresponding author: Li YX, E-mail: Doctorliyunxia@163.com Fan MX, E-mail: mxfan@phy.ecnu.edu.cn

Conflicts of interest   None.

ACKNOWLEDGMENTS National Natural Science Foundation of China (No. 32271096); Shanghai Shenkang Hospital Development Center Clinical Technology Innovation Emerging Frontier Project (No. SHDC12021110); Project Supported by the Shanghai Committee of Science and Technology (No. 22Y11903500); Project funding from Shanghai Municipal Health Commission (No. 2022JC018).
Received  2023-03-27
Accepted  2023-05-17
DOI: 10.12015/issn.1674-8034.2023.06.002
Cite this article as: LIU F, NING R P, YU Q R, et al. Interhemispheric structural connectivity abnormalities in Alzheimer's disease and mild cognitive impairment: A DTI-based study[J]. Chin J Magn Reson Imaging, 2023, 14(6): 9-17. DOI:10.12015/issn.1674-8034.2023.06.002.

[1]
WANG X D, REN M, ZHU M W, et al. Corpus callosum atrophy associated with the degree of cognitive decline in patients with Alzheimer's dementia or mild cognitive impairment: a meta-analysis of the region of interest structural imaging studies[J]. J Psychiatr Res, 2015, 63: 10-19. DOI: 10.1016/j.jpsychires.2015.02.005.
[2]
ARAQUE CABALLERO M Á, SUÁREZ-CALVET M, DUERING M, et al. White matter diffusion alterations precede symptom onset in autosomal dominant Alzheimer's disease[J]. Brain, 2018, 141(10): 3065-3080. DOI: 10.1093/brain/awy229.
[3]
TALWAR P, KUSHWAHA S, CHATURVEDI M, et al. Systematic review of different neuroimaging correlates in mild cognitive impairment and alzheimer's disease[J]. Clin Neuroradiol, 2021, 31(4): 953-967. DOI: 10.1007/s00062-021-01057-7.
[4]
SPOTORNO N, STRANDBERG O, VIS G, et al. Measures of cortical microstructure are linked to amyloid pathology in Alzheimer's disease[J]. Brain, 2023, 146(4): 1602-1614. DOI: 10.1093/brain/awac343.
[5]
XIAO D Q, WANG K S, THERIAULT L, et al. White matter integrity and key structures affected in Alzheimer's disease characterized by diffusion tensor imaging[J]. Eur J Neurosci, 2022, 56(8): 5319-5331. DOI: 10.1111/ejn.15815.
[6]
BRUEGGEN K, DYRBA M, CARDENAS-BLANCO A, et al. Structural integrity in subjective cognitive decline, mild cognitive impairment and Alzheimer's disease based on multicenter diffusion tensor imaging[J]. J Neurol, 2019, 266(10): 2465-2474. DOI: 10.1007/s00415-019-09429-3.
[7]
BERGAMINO M, KEELING E G, WALSH R R, et al. Systematic assessment of the impact of DTI methodology on fractional anisotropy measures in alzheimer's disease[J]. Tomography, 2021, 7(1): 20-38. DOI: 10.3390/tomography7010003.
[8]
WANG P N, CHOU K H, CHANG N J, et al. Callosal degeneration topographically correlated with cognitive function in amnestic mild cognitive impairment and Alzheimer's disease dementia[J]. Hum Brain Mapp, 2014, 35(4): 1529-1543. DOI: 10.1002/hbm.22271.
[9]
PRETI M G, BAGLIO F, LAGANÀ M M, et al. Assessing corpus callosum changes in Alzheimer's disease: comparison between tract-based spatial statistics and atlas-based tractography[J/OL]. PLoS One, 2012, 7(4): e35856 [2023-03-26]. https://www.ncbi.nlm.nih.gov/pubmed/22545143. DOI: 10.1371/journal.pone.0035856.
[10]
TU M C, HUANG W H, HSU Y H, et al. Comparison of neuropsychiatric symptoms and diffusion tensor imaging correlates among patients with subcortical ischemic vascular disease and Alzheimer's disease[J/OL]. BMC Neurol, 2017, 17(1): 144 [2023-03-26]. https://www.ncbi.nlm.nih.gov/pubmed/28754095. DOI: 10.1186/s12883-017-0911-5.
[11]
HOY A R, LY M, CARLSSON C M, et al. Microstructural white matter alterations in preclinical Alzheimer's disease detected using free water elimination diffusion tensor imaging[J/OL]. PLoS One, 2017, 12(3): e0173982 [2023-03-26]. https://www.ncbi.nlm.nih.gov/pubmed/28291839. DOI: 10.1371/journal.pone.0173982.
[12]
BAGLIO F, SARESELLA M, PRETI M G, et al. Neuroinflammation and brain functional disconnection in Alzheimer's disease[J/OL]. Front Aging Neurosci, 2013, 5: 81 [2023-03-26]. https://www.ncbi.nlm.nih.gov/pubmed/24324435. DOI: 10.3389/fnagi.2013.00081.
[13]
ARCHER D B, COOMBES S A, MCFARLAND N R, et al. Development of a transcallosal tractography template and its application to dementia[J]. Neuroimage, 2019, 200: 302-312. DOI: 10.1016/j.neuroimage.2019.06.065.
[14]
JACK C R, BENNETT D A, BLENNOW K, et al. NIA-AA Research Framework: toward a biological definition of Alzheimer's disease[J]. Alzheimers Dement, 2018, 14(4): 535-562. DOI: 10.1016/j.jalz.2018.02.018.
[15]
ALBERT M S, DEKOSKY S T, DICKSON D, et al. The diagnosis of mild cognitive impairment due to Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease[J]. Alzheimers Dement, 2011, 7(3): 270-279. DOI: 10.1016/j.jalz.2011.03.008.
[16]
KELEMAN A A, BOLLINGER R M, WISCH J K, et al. Assessment of instrumental activities of daily living in preclinical alzheimer disease[J]. OTJR (Thorofare N J), 2022, 42(4): 277-285. DOI: 10.1177/15394492221100701.
[17]
O'DWYER L, LAMBERTON F, BOKDE A L, et al. Using diffusion tensor imaging and mixed-effects models to investigate primary and secondary white matter degeneration in Alzheimer's disease and mild cognitive impairment[J]. J Alzheimers Dis, 2011, 26(4): 667-682. DOI: 10.3233/JAD-2011-110137.
[18]
ZHANG X, SUN Y, LI W P, et al. Characterization of white matter changes along fibers by automated fiber quantification in the early stages of Alzheimer's disease[J/OL]. Neuroimage Clin, 2019, 22: 101723 [2023-03-26]. https://www.ncbi.nlm.nih.gov/pubmed/30798166. DOI: 10.1016/j.nicl.2019.101723.
[19]
COLLIJ L E, INGALA S, TOP H, et al. White matter microstructure disruption in early stage amyloid pathology[J/OL]. Alzheimers Dement (Amst), 2021, 13(1): e12124 [2023-03-26]. https://www.ncbi.nlm.nih.gov/pubmed/33816751. DOI: 10.1002/dad2.12124.
[20]
BONDI M W, EDMONDS E C, JAK A J, et al. Neuropsychological criteria for mild cognitive impairment improves diagnostic precision, biomarker associations, and progression rates[J]. J Alzheimers Dis, 2014, 42(1): 275-289. DOI: 10.3233/JAD-140276.
[21]
RAJAN S, BRETTSCHNEIDER J, COLLINGWOOD J F, et al. Regional segmentation strategy for DTI analysis of human corpus callosum indicates motor function deficit in mild cognitive impairment[J/OL]. J Neurosci Methods, 2020, 345: 108870 [2023-03-26]. https://www.ncbi.nlm.nih.gov/pubmed/32687851. DOI: 10.1016/j.jneumeth.2020.108870.
[22]
DAI Z J, HE Y. Disrupted structural and functional brain connectomes in mild cognitive impairment and Alzheimer's disease[J]. Neurosci Bull, 2014, 30(2): 217-232. DOI: 10.1007/s12264-013-1421-0.
[23]
RAGHAVAN S, PRZYBELSKI S A, REID R I, et al. Reduced fractional anisotropy of the genu of the corpus callosum as a cerebrovascular disease marker and predictor of longitudinal cognition in MCI[J]. Neurobiol Aging, 2020, 96: 176-183. DOI: 10.1016/j.neurobiolaging.2020.09.005.
[24]
ZHOU Y, SI X P, CHEN Y Y, et al. Hippocampus- and thalamus-related fiber-specific white matter reductions in mild cognitive impairment[J]. Cereb Cortex, 2022, 32(15): 3159-3174. DOI: 10.1093/cercor/bhab407.
[25]
ARCHER D B, MOORE E E, SHASHIKUMAR N, et al. Free-water metrics in medial temporal lobe white matter tract projections relate to longitudinal cognitive decline[J]. Neurobiol Aging, 2020, 94: 15-23. DOI: 10.1016/j.neurobiolaging.2020.05.001.
[26]
QIN L Z, GUO Z W, MCCLURE M A, et al. White matter changes from mild cognitive impairment to Alzheimer's disease: a meta-analysis[J]. Acta Neurol Belg, 2021, 121(6): 1435-1447. DOI: 10.1007/s13760-020-01322-5.
[27]
ZHOU S W, CHEN S T, LIU X L, et al. Physical activity improves cognition and activities of daily living in adults with alzheimer's disease: a systematic review and meta-analysis of randomized controlled trials[J/OL]. Int J Environ Res Public Health, 2022, 19(3): 1216 [2023-03-26]. https://www.ncbi.nlm.nih.gov/pubmed/35162238. DOI: 10.3390/ijerph19031216.
[28]
SAINI F, DELL'ACQUA F, STRYDOM A. Structural connectivity in down syndrome and alzheimer's disease[J/OL]. Front Neurosci, 2022, 16: 908413 [2023-03-26]. https://www.ncbi.nlm.nih.gov/pubmed/35937882. DOI: 10.3389/fnins.2022.908413.
[29]
ARCHER D B, MOORE E E, PAMIDIMUKKALA U, et al. The relationship between white matter microstructure and self-perceived cognitive decline[J/OL]. Neuroimage Clin, 2021, 32: 102794 [2023-03-26]. https://www.ncbi.nlm.nih.gov/pubmed/34479171. DOI: 10.1016/j.nicl.2021.102794.
[30]
JIA J J, XU J, LIU J, et al. Comprehensive management of daily living activities, behavioral and psychological symptoms, and cognitive function in patients with alzheimer's disease: a Chinese consensus on the comprehensive management of alzheimer's disease[J]. Neurosci Bull, 2021, 37(7): 1025-1038. DOI: 10.1007/s12264-021-00701-z.
[31]
GU L, XU H, QIAN F. Effects of non-invasive brain stimulation on alzheimer's disease[J]. J Prev Alzheimers Dis, 2022, 9(3): 410-424. DOI: 10.14283/jpad.2022.40.
[32]
GUSTAVSON D E, ARCHER D B, ELMAN J A, et al. Associations among executive function Abilities, free Water, and white matter microstructure in early old age[J/OL]. Neuroimage Clin, 2023, 37: 103279 [2023-03-26]. https://www.ncbi.nlm.nih.gov/pubmed/36493704. DOI: 10.1016/j.nicl.2022.103279.
[33]
KUMAR S, DE LUCA A, LEEMANS A, et al. Topology of diffusion changes in corpus callosum in Alzheimer's disease: an exploratory case-control study[J/OL]. Front Neurol, 2022, 13: 1005406 [2023-03-26]. https://www.ncbi.nlm.nih.gov/pubmed/36530616. DOI: 10.3389/fneur.2022.1005406.
[34]
LI W H, ZHAO Z L, LIU M, et al. Multimodal classification of alzheimer's disease and amnestic mild cognitive impairment: integrated 18F-FDG PET and DTI study[J]. J Alzheimer's Dis, 2022, 85(3): 1063-1075. DOI: 10.3233/jad-215338.
[35]
RIECKMANN A, VAN DIJK K R, SPERLING R A, et al. Accelerated decline in white matter integrity in clinically normal individuals at risk for Alzheimer's disease[J]. Neurobiol Aging, 2016, 42: 177-188. DOI: 10.1016/j.neurobiolaging.2016.03.016.
[36]
LIN Y, JIANG W J, SHAN P Y, et al. The role of repetitive transcranial magnetic stimulation (rTMS) in the treatment of cognitive impairment in patients with Alzheimer's disease: a systematic review and meta-analysis[J]. J Neurol Sci, 2019, 398: 184-191. DOI: 10.1016/j.jns.2019.01.038.
[37]
JAFARI Z, KOLB B E, MOHAJERANI M H. Neural oscillations and brain stimulation in Alzheimer's disease[J]. Prog Neurobiol, 2020, 194: 101878 [2023-03-26]. https://www.ncbi.nlm.nih.gov/pubmed/32615147. DOI: 10.1016/j.pneurobio.2020.101878.
[38]
BASHIR S, UZAIR M, ABUALAIT T, et al. Effects of transcranial magnetic stimulation on neurobiological changes in Alzheimer's disease (Review)[J/OL]. Mol Med Rep, 2022, 25(4): 109 [2023-03-26]. https://www.ncbi.nlm.nih.gov/pubmed/35119081. DOI: 10.3892/mmr.2022.12625.

PREV Expert consensus on the clinical application of large bore MRI in fetal disease
NEXT MVPA method study for distinguishing the cognitive level of healthy elderly people based on resting-state fMRI
  


LINK


Tel & Fax: +8610-67113815    E-mail: editor@cjmri.cn