Disruption of cerebral networks and cognitive impairment in Alzheimer disease

Journal article


Reijmer, Yael D., Leemans, Alexander, Caeyenberghs, Karen, Heringa, Sophie M. and Biessels, Geert J.. (2013). Disruption of cerebral networks and cognitive impairment in Alzheimer disease. Neurology. 80(15), pp. 1370 - 1377. https://doi.org/10.1212/WNL.0b013e31828c2ee5
AuthorsReijmer, Yael D., Leemans, Alexander, Caeyenberghs, Karen, Heringa, Sophie M. and Biessels, Geert J.
Abstract

Objective: To examine the relation between measures of whole-brain white matter connectivity and cognitive performance in patients with early Alzheimer disease ( AD ) using a network-based approach and to assess whether network parameters provide information that is complementary to conventional MRI markers of AD. Methods: Fifty patients ( mean age 78.8 ± 7.1 years ) with early AD were recruited via a memory clinic. In addition, 15 age-, sex-, and education-matched control participants were used as a reference group. All participants underwent a 3-T MRI scan and cognitive assessment. Diffusion tensor imaging–based tractography was used to reconstruct the brain network of each individual, followed by graph theoretical analyses. Overall network efficiency was assessed by measures of local ( clustering coefficient, local efficiency ) and global ( path length, global efficiency ) connectivity. Age-, sex-, and education-adjusted cognitive scores were related to network measures and to conventional MRI parameters ( i.e., degree of cerebral atrophy and small-vessel disease ). Results: The structural brain network of patients showed reduced local efficiency compared to controls. Within the patient group, worse performance in memory and executive functioning was related to decreased local efficiency ( r = 0.434; p = 0.002 ), increased path length ( r = -0.538; p < 0.001 ), and decreased global efficiency ( r = 0.431; p = 0.005 ). Measures of network efficiency explained up to 27% of the variance in cognitive functioning on top of conventional MRI markers ( p < 0.01 ). Conclusion: This study shows that network-based analysis of brain white matter connections provides a novel way to reveal the structural basis of cognitive dysfunction in AD.

Year2013
JournalNeurology
Journal citation80 (15), pp. 1370 - 1377
PublisherLippincott Williams & Wilkins
ISSN0028-3878
Digital Object Identifier (DOI)https://doi.org/10.1212/WNL.0b013e31828c2ee5
Scopus EID2-s2.0-84876235134
Page range1370 - 1377
Publisher's version
File Access Level
Controlled
Place of publicationUnited States of America
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Serbruyns, Leen, Leunissen, Inge, van Ruitenbeek, Peter, Pauwels, Lisa, Caeyenberghs, Karen, Solesio-Jofre, Elena, Geurts, Monique, Cuypers, Koen, Meesen, Raf L., Sunaert, Stefan, Leemans, Alexander and Swinnen, Stephen P.. (2016). Alterations in brain white matter contributing to age-related slowing of task switching performance: The role of radial diffusivity and magnetization transfer ratio. Human Brain Mapping. 37(11), pp. 4084 - 4098. https://doi.org/10.1002/hbm.23297
Neural signature of developmental coordination disorder in the structural connectome independent of autism comorbidity
Caeyenberghs, Karen, Taymans, Tom, Wilson, Peter Henry, Vanderstraeten, Guy, Hosseini, Hadi and Van Waelvelde, Hilde. (2016). Neural signature of developmental coordination disorder in the structural connectome independent of autism comorbidity. Developmental Science. 19(4), pp. 599 - 612. https://doi.org/10.1111/desc.12424
Task complexity and location specific changes of cortical thickness in executive and salience networks after working memory training
Metzler-Baddeley, Claudia, Caeyenberghs, Karen, Foley, Sonya and Jones, Derek Kenton. (2016). Task complexity and location specific changes of cortical thickness in executive and salience networks after working memory training. NeuroImage. 130, pp. 48 - 62. https://doi.org/10.1016/j.neuroimage.2016.01.007
Revealing hot cognition in children with motor coordination problems: What's the go?
Rahimi-Golkhandan, S., Steenbergen, B., Piek, J. P., Caeyenberghs, K. and Wilson, Peter Henry. (2016). Revealing hot cognition in children with motor coordination problems: What's the go? Research in Developmental Disabilities. 106, pp. 55 - 64. https://doi.org/10.1016/j.bandc.2016.04.010
Longitudinal data on cortical thickness before and after working memory training
Metzler-Baddeley, Claudia, Caeyenberghs, Karen, Foley, Sonya and Jones, Derek Kenton. (2016). Longitudinal data on cortical thickness before and after working memory training. Data in Brief. 7, pp. 1143 - 1147. https://doi.org/10.1016/j.dib.2016.03.090
Structural brain connectivity and the sit-to-stand-to-sit performance in individuals with nonspecific low back pain: A diffusion magnetic resonance imaging-based network analysis
Pijnenburg, Madelon, Hadi Hosseini, S. M., Brumagne, Simon, Janssens, Lotte, Goossens, Nina and Caeyenberghs, Karen. (2016). Structural brain connectivity and the sit-to-stand-to-sit performance in individuals with nonspecific low back pain: A diffusion magnetic resonance imaging-based network analysis. Brain Connectivity. 6(10), pp. 795 - 803. https://doi.org/10.1089/brain.2015.0401
Coupling of online control and inhibitory systems in children with atypical motor development: A growth curve modelling study
Ruddock, Scott, Caeyenberghs, Karen, Piek, Jan, Sugden, David, Hyde, Christian, Morris, Sue, Rigoli, Daniela, Steenbergen, Bert and Wilson, Peter. (2016). Coupling of online control and inhibitory systems in children with atypical motor development: A growth curve modelling study. Brain and Cognition. 109, pp. 84 - 95. https://doi.org/10.1016/j.bandc.2016.08.001
Bimanual motor deficits in older adults predicted by diffusion tensor imaging metrics of corpus callosum subregions
Serbruyns, Leen, Gooijers, J, Caeyenberghs, Karen, Meesen, R, Cuypers, K, Sisti, Helene, Leemans, A and Swinnen, Stephan. (2015). Bimanual motor deficits in older adults predicted by diffusion tensor imaging metrics of corpus callosum subregions. Brain Structure and Function. 220(1), pp. 273 - 290. https://doi.org/10.1007/s00429-013-0654-z
Regional volumes in brain stem and cerebellum are associated with postural impairments in young brain-injured patients
Drijkoningen, David, Leunissen, Inge, Caeyenberghs, Karen, Hoogkamer, Wouter, Sunaert, Stefan, Duysens, Jacques and Swinnen, Stephen P.. (2015). Regional volumes in brain stem and cerebellum are associated with postural impairments in young brain-injured patients. Human Brain Mapping. 36(12), pp. 4897 - 4909. https://doi.org/10.1002/hbm.22958
Training-induced improvements in postural control are accompanied by alterations in cerebellar white matter in brain injured patients
Drijkoningen, David, Caeyenberghs, Karen, Leunissen, Inge, Vander Linden, Catharine, Leemans, Alexander, Sunaert, Stefan, Duysens, Jacques and Swinnen, Stephen. (2015). Training-induced improvements in postural control are accompanied by alterations in cerebellar white matter in brain injured patients. NeuroImage: Clinical. 7, pp. 240 - 251. https://doi.org/10.1016/j.nicl.2014.12.006
Resonance: An interactive tabletop artwork for co-located group rehabilitation and play
Duckworth, Jonathan, Mumford, Nick, Caeyenberghs, Karen, Eldridge, Ross Michael, Mayson, Scott, Thomas, Patrick R., Shum, David, Williams, Gavin and Wilson, Peter Henry. (2015). Resonance: An interactive tabletop artwork for co-located group rehabilitation and play. Universal Access in Human-Computer Interaction. Germany: Springer-Verlag. pp. 420 - 431 https://doi.org/10.1007/978-3-319-20684-4_41
Neural correlates of motor deficits in young patients with traumatic brain injury
Caeyenberghs, Karen and Swinnen, Stephen P.. (2015). Neural correlates of motor deficits in young patients with traumatic brain injury. In In A. W. Toga, K. Zilles, K. Amunts, M. Mesulam and S. Kastner (Ed.). Brain mapping : An encyclopedic reference ; volume 2 pp. 461-468 Academic Press. https://doi.org/10.1016/B978-0-12-397025-1.00025-7
Coupling online control and inhibitory systems in children with Developmental Coordination Disorder : Goal-directed reaching
Ruddock, Scott, Piek, Jan, Sugden, David, Morris, Sue, Hyde, Christian, Caeyenberghs, Karen and Wilson, Peter. (2015). Coupling online control and inhibitory systems in children with Developmental Coordination Disorder : Goal-directed reaching. Research in Developmental Disabilities. 36, pp. 244 - 255. https://doi.org/10.1016/j.ridd.2014.10.013
Schizophrenia-like topological changes in the structural connectome of individuals with subclinical psychotic experiences
Drakesmith, Mark, Caeyenberghs, Karen, Dutt, Anirban, Zammit, Stanley, Evans, C John, Reichenberg, Abraham, Lewis, Glyn, David, Anthony and Jones, Derek. (2015). Schizophrenia-like topological changes in the structural connectome of individuals with subclinical psychotic experiences. Human Brain Mapping. 36(7), pp. 2629 - 2643. https://doi.org/10.1002/hbm.22796
Associations between muscle strength asymmetry and impairments in gait and posture in young brain-injured patients
Drijkoningen, David, Caeyenberghs, Karen, Vander Linden, Catharine, Van Herpe, Katrin, Duysens, Jacques and Swinnen, Stephan P.. (2015). Associations between muscle strength asymmetry and impairments in gait and posture in young brain-injured patients. Journal of Neurotrauma. 32(17), pp. 1324 - 1332. https://doi.org/10.1089/neu.2014.3787
Dynamics of the connectome in Huntington's disease: A longitudinal diffusion MRI study
Odish, Omar F. F., Caeyenberghs, Karen, Hosseini, Hadi, van den Bogaard, Simon J.A., Roos, Raymund A.C. and Leemans, Alexander. (2015). Dynamics of the connectome in Huntington's disease: A longitudinal diffusion MRI study. NeuroImage: Clinical. 9, pp. 32 - 43. https://doi.org/10.1016/j.nicl.2015.07.003
Second generation system development and multi-centre studies of the Elements VR-rehab system
Mumford, Nick, Shum, David, Thomas, Patrick, Steenbergen, Bert, Duckworth, Jonathan, Eldridge, Ross, Williams, Gavin, Green, Dido, Rogers, Jeff, Caeyenberghs, Karen and Wilson, Peter H.. (2015). Second generation system development and multi-centre studies of the Elements VR-rehab system. 2015 International Conference on Virtual Rehabilitation. Spain: IEEE Computer Society. pp. 164 - 165 https://doi.org/10.1109/ICVR.2015.7358601
Resting-state functional connectivity of the sensorimotor network in individuals with nonspecific low back pain and the association with the sit-to-stand-to-sit task
Pijnenburg, Madelon, Brumagne, Simon, Caeyenberghs, Karen, Janssens, Lotte, Goossens, Nina, Marinazzo, Daniele, Swinnen, Stephen P., Claeys, Kurt and Siugzdaite, Roma. (2015). Resting-state functional connectivity of the sensorimotor network in individuals with nonspecific low back pain and the association with the sit-to-stand-to-sit task. Brain Connectivity. 5(5), pp. 303 - 311. https://doi.org/10.1089/brain.2014.0309
Abnormal wiring of the connectome in adults with high-functioning autism spectrum disorder
Roine, Ulrika, Roine, Timo, Salmi, Juha, Nieminen-von Wendt, Taina, Tani, Pekka, Leppämäki, Sami, Rintahaka, Pertti, Caeyenberghs, Karen, Leemans, Alexander and Sams, Mikko. (2015). Abnormal wiring of the connectome in adults with high-functioning autism spectrum disorder. Molecular Autism. 6(1), pp. 1 - 11. https://doi.org/10.1186/s13229-015-0058-4
The vulnerability to suicidal behavior is associated with reduced connectivity strength
Bijttebier, Stijn, Caeyenberghs, Karen, van den Ameele, Hans, Achten, Eric, Rujescu, Dan, Titeca, Koen and van Heeringen, Kees. (2015). The vulnerability to suicidal behavior is associated with reduced connectivity strength. Frontiers in Human Neuroscience (online). 9, pp. 1 - 11. https://doi.org/10.3389/fnhum.2015.00632
Overcoming the effects of false positives and threshold bias in graph theoretical analyses of neuroimaging data
Drakesmith, M., Caeyenberghs, Karen, Dutt, A., Lewis, G., David, A. and Jones, D.. (2015). Overcoming the effects of false positives and threshold bias in graph theoretical analyses of neuroimaging data. NeuroImage. 118, pp. 313 - 333. https://doi.org/10.1016/j.neuroimage.2015.05.011
Functional connectivity density and balance in young patients with traumatic axonal injury
Caeyenberghs, Karen, Siugzdaite, Roma, Drijkoningen, David, Marinazzo, Daniele and Swinnen, Stephen P.. (2015). Functional connectivity density and balance in young patients with traumatic axonal injury. Brain Connectivity. 5(7), pp. 423 - 432. https://doi.org/10.1089/brain.2014.0293
Hyperconnectivity in juvenile myoclonic epilepsy: A network analysis
Caeyenberghs, Karen, Powell, H., Thomas, Rhys, Brindley, Lisa, Church, Carla, Evans, John, Muthukumaraswamy, Suresh, Jones, Derek and Hamandi, Khalid. (2015). Hyperconnectivity in juvenile myoclonic epilepsy: A network analysis. NeuroImage: Clinical. 7, pp. 98 - 104. https://doi.org/10.1016/j.nicl.2014.11.018
Subcortical volume analysis in traumatic brain injury: The importance of the fronto-striato-thalamic circuit in task switching
Leunissen, Inge, Coxon, James P., Caeyenberghs, Karen, Michiels, Karla, Sunaert, Stefan and Swinnen, Stephan P.. (2014). Subcortical volume analysis in traumatic brain injury: The importance of the fronto-striato-thalamic circuit in task switching. Cortex. 51(1), pp. 67 - 81. https://doi.org/10.1016/j.cortex.2013.10.009
Microstructural integrity of the superior cerebellar peduncle is associated with an impaired proprioceptive weighting capacity in individuals with non-specific low back pain
Pijnenburg, Madelon, Caeyenberghs, Karen, Janssens, Lotte, Goossens, Nina, Swinnen, Stephen P., Sunaert, Stefan and Brumagne, Simon. (2014). Microstructural integrity of the superior cerebellar peduncle is associated with an impaired proprioceptive weighting capacity in individuals with non-specific low back pain. PLoS ONE. 9(6), pp. 1 - 7. https://doi.org/10.1371/journal.pone.0100666
Hemispheric lateralization of topological organization in structural brain networks
Caeyenberghs, Karen and Leemans, Alexander. (2014). Hemispheric lateralization of topological organization in structural brain networks. Human Brain Mapping. 35(9), pp. 4944 - 4957. https://doi.org/10.1002/hbm.22524
Deficient motor timing in children with neurofibromatosis type 1
Debrabant, Julie, Plasschaert, Ellen, Caeyenberghs, Karen, Vingerhoets, Guy, Legius, Eric, Janssens, Sandra and Van Waelvelde, Hilde. (2014). Deficient motor timing in children with neurofibromatosis type 1. Research in Developmental Disabilities. 35(11), pp. 3131 - 3138. https://doi.org/10.1016/j.ridd.2014.07.059
White matter organization in relation to upper limb motor control in healthy subjects: exploring the added value of diffusion kurtosis imaging
Gooijers, J., Leemans, A., Van Cauter, S., Sunaert, S., Swinnen, S. P. and Caeyenberghs, K.. (2014). White matter organization in relation to upper limb motor control in healthy subjects: exploring the added value of diffusion kurtosis imaging. Brain Structure and Function. 219(5), pp. 1627 - 1638. https://doi.org/10.1007/s00429-013-0590-y
Altered structural networks and executive deficits in traumatic brain injury patients
Caeyenberghs, K., Leemans, A., Leunissen, I., Gooijers, J., Michiels, K., Sunaert, S. and Swinnen, S. P.. (2014). Altered structural networks and executive deficits in traumatic brain injury patients. Brain Structure and Function. 219(1), pp. 193 - 209. https://doi.org/10.1007/s00429-012-0494-2
Task switching in traumatic brain injury relates to cortico-subcortical integrity
Leunissen, Inge, Coxon, James P., Caeyenberghs, Karen, Michiels, Karla, Sunaert, Stefan and Swinnen, Stephen P.. (2014). Task switching in traumatic brain injury relates to cortico-subcortical integrity. Human Brain Mapping. 35(5), pp. 2459 - 2469. https://doi.org/10.1002/hbm.22341
Neural underpinnings of impaired predictive motor timing in children with Developmental Coordination Disorder
Debrabant, Julie, Gheysen, Freja, Caeyenberghs, Karen, Waelvelde, Hilde Van and Vingerhoets, Guy. (2013). Neural underpinnings of impaired predictive motor timing in children with Developmental Coordination Disorder. Research in Developmental Disabilities. 34(5), pp. 1478 - 1487. https://doi.org/10.1016/j.ridd.2013.02.008
Bimanual motor coordination in older adults is associated with increased functional brain connectivity: A graphceoretical analysis
Heitger, Marcus H., Goble, Daniel J., Dhollander, Thijs, Dupont, Patrick, Caeyenberghs, Karen, Leemans, Alexander, Sunaert, Stefan and Swinnen, Stephen P.. (2013). Bimanual motor coordination in older adults is associated with increased functional brain connectivity: A graphceoretical analysis. PLoS ONE. 8(4), pp. 1 - 17. https://doi.org/10.1371/journal.pone.0062133
Diffusion tensor imaging metrics of the corpus callosum in relation to bimanual coordination: Effect of task complexity and sensory feedback
Gooijers, Jolien, Caeyenberghs, Karen, Sisti, Helene M., Geurts, Monique, Heitger, Marcus H., Leemans, Alexander and Swinnen, Stephen P.. (2013). Diffusion tensor imaging metrics of the corpus callosum in relation to bimanual coordination: Effect of task complexity and sensory feedback. Human Brain Mapping. 34(1), pp. 241 - 252. https://doi.org/10.1002/hbm.21429
Topological correlations of structural and functional networks in patients with traumatic brain injury
Caeyenberghs, Karen, Leemans, Alexander, Leunissen, Inge, Michiels, Karla and Swinnen, Stephen P.. (2013). Topological correlations of structural and functional networks in patients with traumatic brain injury. Frontiers in Human Neuroscience. 7, pp. 1 - 11. https://doi.org/10.3389/fnhum.2013.00726
Disturbed cortico-subcortical interactions during motor task switching in traumatic brain injury
Leunissen, Inge, Coxon, James P., Geurts, Monique, Caeyenberghs, Karen, Michiels, Karla, Sunaert, Stefan and Swinnen, Stephen P.. (2013). Disturbed cortico-subcortical interactions during motor task switching in traumatic brain injury. Human Brain Mapping. 34(6), pp. 1254 - 1271. https://doi.org/10.1002/hbm.21508
Graph analysis of functional brain networks for cognitive control of action in traumatic brain injury
Caeyenberghs, Karen, Leemans, Alexander, Heitger, Marcus H., Leunissen, Inge, Dhollander, Thijs, Sunaert, Stefan, Dupont, Patrick and Swinnen, Stephen P.. (2012). Graph analysis of functional brain networks for cognitive control of action in traumatic brain injury. Brain. 135(4), pp. 1293 - 1307. https://doi.org/10.1093/brain/aws048
Microstructural organization of corpus callosum projections to prefrontal cortex predicts bimanual motor learning
Sisti, Helene M., Geurts, Monique, Gooijers, Jolien, Heitger, Marcus H., Caeyenberghs, Karen, Beets, Iseult A. M., Serbruyns, Leen, Leemans, Alexander and Swinnen, Stephen P.. (2012). Microstructural organization of corpus callosum projections to prefrontal cortex predicts bimanual motor learning. Learning and Memory. 19(8), pp. 351 - 357. https://doi.org/10.1101/lm.026534.112
Brain connectivity and postural control in young traumatic brain injury patients: A diffusion MRI based network analysis
Caeyenberghs, Karen, Leemans, A., De Decker, C., Heitger, Marcus H., Drijkoningen, David, Linden, C. Vander, Sunaert, S. and Swinnen, Stephen P.. (2012). Brain connectivity and postural control in young traumatic brain injury patients: A diffusion MRI based network analysis. NeuroImage. 1(1), pp. 106 - 115. https://doi.org/10.1016/j.nicl.2012.09.011
Motor learning-induced changes in functional brain connectivity as revealed by means of graphceoretical network analysis
Heitger, Marcus H., Ronsse, R., Dhollander, Thijs, Dupont, Patrick, Caeyenberghs, Karen and Swinnen, Stephen P.. (2012). Motor learning-induced changes in functional brain connectivity as revealed by means of graphceoretical network analysis. NeuroImage. 61(3), pp. 633 - 650. https://doi.org/10.1016/j.neuroimage.2012.03.067
Testing multiple coordination constraints with a novel bimanual visuomotor task
Sisti, Helene M., Geurts, Monique, Clerckx, Rene´, Gooijers, Jolien, Coxon, James P., Heitger, Marcus H., Caeyenberghs, Karen, Beets, Iseult A., Serbruyns, Leen and Swinnen, Stephen P.. (2011). Testing multiple coordination constraints with a novel bimanual visuomotor task. PLoS ONE. 6(8), pp. 1 - 11. https://doi.org/10.1371/journal.pone.0023619
Keeping an eye on imagery: The role of eye movements during motor imagery training
Heremans, E., Smits-Engelsman, Bouwien, Caeyenberghs, Karen, Vercruysse, S., Nieuwboer, A., Feys, P. and Helsen, W. F.. (2011). Keeping an eye on imagery: The role of eye movements during motor imagery training. Neuroscience. 195, pp. 37 - 44. https://doi.org/10.1016/j.neuroscience.2011.07.030
Correlations between white matter integrity and motor function in traumatic brain injury patients
Caeyenberghs, Karen, Leemans, Alexander, Geurts, Monique, Vander Linden, Catharine, Smits-Engelsman, Bouwien C. M., Sunaert, Stefan and Swinnen, Stephen P.. (2011). Correlations between white matter integrity and motor function in traumatic brain injury patients. Neurorehabilitation and Neural Repair. 25(6), pp. 492 - 502. https://doi.org/10.1177/1545968310394870
Bimanual coordination and corpus callosum microstructure in young adults with traumatic brain injury: A diffusion tensor imaging study
Caeyenberghs, Karen, Leemans, Alexander, Coxon, James P., Leunissen, Inge, Drijkoningen, David, Geurts, Monique, Gooijers, Jolien, Michiels, Karla, Sunaert, Stefan and Swinnen, Stephen P.. (2011). Bimanual coordination and corpus callosum microstructure in young adults with traumatic brain injury: A diffusion tensor imaging study. Journal of Neurotrauma. 28(6), pp. 897 - 913. https://doi.org/10.1089/neu.2010.1721
Motor imagery development in primary school children
Caeyenberghs, Karen, Tsoupas, Jenny, Wilson, Peter and Smits-Engelsman, Bouwein C. M.. (2009). Motor imagery development in primary school children. Developmental Neuropsychology. 34(1), pp. 103 - 121. https://doi.org/10.1080/87565640802499183
Increasing convergence between imagined and executed movement across development: Evidence for the emergence of movement representations
Caeyenberghs, Karen, Wilson, Peter, Van Roon, Dominique, Swinnen, Stephen and Smits-Engelsman, Bouwein C. M.. (2009). Increasing convergence between imagined and executed movement across development: Evidence for the emergence of movement representations. Developmental Science. 12(3), pp. 474 - 483. https://doi.org/10.1111/j.1467-7687.2008.00803.x