Divergent network connectivity changes in behavioural variant frontotemporal dementia and Alzheimer's disease

被引:760
作者
Zhou, Juan [1 ]
Greicius, Michael D. [2 ]
Gennatas, Efstathios D. [1 ]
Growdon, Matthew E. [1 ]
Jang, Jung Y. [1 ]
Rabinovici, Gil D. [1 ]
Kramer, Joel H. [1 ]
Weiner, Michael [3 ]
Miller, Bruce L. [1 ]
Seeley, William W. [1 ]
机构
[1] Univ Calif San Francisco, Dept Neurol, Memory & Aging Ctr, San Francisco, CA 94117 USA
[2] Stanford Univ, Sch Med, Dept Neurol & Neurol Sci, Funct Imaging Neuropsychiat Disorders Lab, Stanford, CA 94305 USA
[3] Dept Vet Affairs Med Ctr, Ctr Imaging Neurodegenerat Dis, San Francisco, CA 94121 USA
关键词
functional magnetic resonance imaging; frontotemporal dementia; Alzheimer's disease; functional connectivity; biomarker; RESTING-STATE NETWORKS; INDEPENDENT COMPONENT ANALYSIS; DEFAULT-MODE; FUNCTIONAL CONNECTIVITY; LOBAR DEGENERATION; BRAIN ACTIVITY; COGNITIVE IMPAIRMENT; FMRI; DEFICITS; CORTEX;
D O I
10.1093/brain/awq075
中图分类号
R74 [神经病学与精神病学];
学科分类号
摘要
Resting-state or intrinsic connectivity network functional magnetic resonance imaging provides a new tool for mapping large-scale neural network function and dysfunction. Recently, we showed that behavioural variant frontotemporal dementia and Alzheimer's disease cause atrophy within two major networks, an anterior 'Salience Network' (atrophied in behavioural variant frontotemporal dementia) and a posterior 'Default Mode Network' (atrophied in Alzheimer's disease). These networks exhibit an anti-correlated relationship with each other in the healthy brain. The two diseases also feature divergent symptom-deficit profiles, with behavioural variant frontotemporal dementia undermining social-emotional function and preserving or enhancing visuospatial skills, and Alzheimer's disease showing the inverse pattern. We hypothesized that these disorders would exert opposing connectivity effects within the Salience Network (disrupted in behavioural variant frontotemporal dementia but enhanced in Alzheimer's disease) and the Default Mode Network (disrupted in Alzheimer's disease but enhanced in behavioural variant frontotemporal dementia). With task-free functional magnetic resonance imaging, we tested these ideas in behavioural variant frontotemporal dementia, Alzheimer's disease and healthy age-matched controls (n = 12 per group), using independent component analyses to generate group-level network contrasts. As predicted, behavioural variant frontotemporal dementia attenuated Salience Network connectivity, most notably in frontoinsular, cingulate, striatal, thalamic and brainstem nodes, but enhanced connectivity within the Default Mode Network. Alzheimer's disease, in contrast, reduced Default Mode Network connectivity to posterior hippocampus, medial cingulo-parieto-occipital regions and the dorsal raphe nucleus, but intensified Salience Network connectivity. Specific regions of connectivity disruption within each targeted network predicted intrinsic connectivity enhancement within the reciprocal network. In behavioural variant frontotemporal dementia, clinical severity correlated with loss of right frontoinsular Salience Network connectivity and with biparietal Default Mode Network connectivity enhancement. Based on these results, we explored whether a combined index of Salience Network and Default Mode Network connectivity might discriminate between the three groups. Linear discriminant analysis achieved 92% clinical classification accuracy, including 100% separation of behavioural variant frontotemporal dementia and Alzheimer's disease. Patients whose clinical diagnoses were supported by molecular imaging, genetics, or pathology showed 100% separation using this method, including four diagnostically equivocal 'test' patients not used to train the algorithm. Overall, the findings suggest that behavioural variant frontotemporal dementia and Alzheimer's disease lead to divergent network connectivity patterns, consistent with known reciprocal network interactions and the strength and deficit profiles of the two disorders. Further developed, intrinsic connectivity network signatures may provide simple, inexpensive, and non-invasive biomarkers for dementia differential diagnosis and disease monitoring.
引用
收藏
页码:1352 / 1367
页数:16
相关论文
共 102 条
[31]   A voxel-based morphometric study of ageing in 465 normal adult human brains [J].
Good, CD ;
Johnsrude, IS ;
Ashburner, J ;
Henson, RNA ;
Friston, KJ ;
Frackowiak, RSJ .
NEUROIMAGE, 2001, 14 (01) :21-36
[32]   Default-mode activity during a passive sensory task: Uncoupled from deactivation but impacting activation [J].
Greicius, MD ;
Menon, V .
JOURNAL OF COGNITIVE NEUROSCIENCE, 2004, 16 (09) :1484-1492
[33]   Default-mode network activity distinguishes Alzheimer's disease from healthy aging: Evidence from functional MRI [J].
Greicius, MD ;
Srivastava, G ;
Reiss, AL ;
Menon, V .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2004, 101 (13) :4637-4642
[34]   Functional connectivity in the resting brain: A network analysis of the default mode hypothesis [J].
Greicius, MD ;
Krasnow, B ;
Reiss, AL ;
Menon, V .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2003, 100 (01) :253-258
[35]  
Grinberg LT, 2009, NEUROPATH APPL NEURO, V35, P406, DOI [10.1111/j.1365-2990.2008.00997.x, 10.1111/j.1365-2990.2009.00997.x]
[36]   Distinct Cerebellar Contributions to Intrinsic Connectivity Networks [J].
Habas, Christophe ;
Kamdar, Nirav ;
Nguyen, Daniel ;
Prater, Katherine ;
Beckmann, Christian F. ;
Menon, Vinod ;
Greicius, Michael D. .
JOURNAL OF NEUROSCIENCE, 2009, 29 (26) :8586-8594
[37]   Brain connectivity related to working memory performance [J].
Hampson, Michelle ;
Driesen, Naomi R. ;
Skudlarski, Pawel ;
Gore, John C. ;
Constable, R. Todd .
JOURNAL OF NEUROSCIENCE, 2006, 26 (51) :13338-13343
[38]   Regional coherence changes in the early stages of Alzheimer's disease: A combined structural and resting-state functional MRI study [J].
He, Yong ;
Wang, Liang ;
Zang, Yufeng ;
Tian, Lixia ;
Zhang, Xinqing ;
Li, Kuncheng ;
Jiang, Tianzi .
NEUROIMAGE, 2007, 35 (02) :488-500
[39]   The limbic lobe and its output channels: Implications for emotional functions and adaptive behavior [J].
Heimer, L ;
Van Hoesen, GW .
NEUROSCIENCE AND BIOBEHAVIORAL REVIEWS, 2006, 30 (02) :126-147
[40]   Spatial Remapping of Cortico-striatal Connectivity in Parkinson's Disease [J].
Helmich, Rick C. ;
Derikx, Loes C. ;
Bakker, Maaike ;
Scheeringa, Rene ;
Bloem, Bastiaan R. ;
Toni, Ivan .
CEREBRAL CORTEX, 2010, 20 (05) :1175-1186