Whole-brain analytic measures of network communication reveal increased structure-function correlation in right temporal lobe epilepsy

The in vivo structure-function relationship is key to understanding brain network reorganization due to pathologies. This relationship is likely to be particularly complex in brain network diseases such as temporal lobe epilepsy, in which disturbed large-scale systems are involved in both transient electrical events and long-lasting functional and structural impairments. Herein, we estimated this relationship by analyzing the correlation between structural connectivity and functional connectivity in terms of analytical network communication parameters. As such, we targeted the gradual topological structure-function reorganization caused by the pathology not only at the whole brain scale but also both in core and peripheral regions of the brain. We acquired diffusion (dMRI) and resting-state fMRI (rsfMRI) data in seven right-lateralized TLE (rTLE) patients and fourteen healthy controls and analyzed the structure-function relationship by using analytical network communication metrics derived from the structural connectome. In rTLE patients, we found a widespread hypercorrelated functional network. Network communication analysis revealed greater unspecific branching of the shortest path (search information) in the structural connectome and a higher global correlation between the structural and functional connectivity for the patient group. We also found evidence for a preserved structural rich-club in the patient group. In sum, global augmentation of structure-function correlation might be linked to a smaller functional repertoire in rTLE patients, while sparing the central core of the brain which may represent a pathway that facilitates the spread of seizures.

[1]  Linda Douw,et al.  Altered structural connectome in temporal lobe epilepsy. , 2014, Radiology.

[2]  Philippe Kahane,et al.  Temporal lobe epilepsy and hippocampal sclerosis: Lessons from depth EEG recordings , 2010, Epilepsia.

[3]  N. Voets,et al.  Structural substrates for resting network disruption in temporal lobe epilepsy. , 2012, Brain : a journal of neurology.

[4]  P. Chauvel,et al.  Decreased basal fMRI functional connectivity in epileptogenic networks and contralateral compensatory mechanisms , 2009, Human brain mapping.

[5]  Alan Connelly,et al.  MRtrix: Diffusion tractography in crossing fiber regions , 2012, Int. J. Imaging Syst. Technol..

[6]  O. Sporns,et al.  Rich-Club Organization of the Human Connectome , 2011, The Journal of Neuroscience.

[7]  Alexander Leemans,et al.  The B‐matrix must be rotated when correcting for subject motion in DTI data , 2009, Magnetic resonance in medicine.

[8]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[9]  O. Sporns,et al.  Key role of coupling, delay, and noise in resting brain fluctuations , 2009, Proceedings of the National Academy of Sciences.

[10]  M. Symms,et al.  Structural changes in the temporal lobe and piriform cortex in frontal lobe epilepsy , 2014, Epilepsy Research.

[11]  J. Régis,et al.  The role of corticothalamic coupling in human temporal lobe epilepsy. , 2006, Brain : a journal of neurology.

[12]  Clifford R Jack,et al.  Rich club analysis in the Alzheimer's disease connectome reveals a relatively undisturbed structural core network , 2015, Human brain mapping.

[13]  P A Robinson,et al.  Determination of effective brain connectivity from functional connectivity with application to resting state connectivities. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[14]  Josemir W Sander,et al.  Microdysgenesis with abnormal cortical myelinated fibres in temporal lobe epilepsy: a histopathological study with calbindin D‐28‐K immunohistochemistry , 2000, Neuropathology and applied neurobiology.

[15]  F. Bartolomei,et al.  Imaging structural and functional connectivity: towards a unified definition of human brain organization? , 2008, Current opinion in neurology.

[16]  Alan C. Evans,et al.  A nonparametric method for automatic correction of intensity nonuniformity in MRI data , 1998, IEEE Transactions on Medical Imaging.

[17]  M. de Curtis,et al.  Do seizures and epileptic activity worsen epilepsy and deteriorate cognitive function? , 2013, Epilepsia.

[18]  Joaquín Goñi,et al.  Abnormal rich club organization and functional brain dynamics in schizophrenia. , 2013, JAMA psychiatry.

[19]  Henry Kennedy,et al.  A Predictive Network Model of Cerebral Cortical Connectivity Based on a Distance Rule , 2013, Neuron.

[20]  G. V. Goddard,et al.  A permanent change in brain function resulting from daily electrical stimulation. , 1969, Experimental neurology.

[21]  N. Canessa,et al.  Social cognition dysfunctions in patients with epilepsy: Evidence from patients with temporal lobe and idiopathic generalized epilepsies , 2015, Epilepsy & Behavior.

[22]  D. Hu,et al.  Influence of Resting-State Network on Lateralization of Functional Connectivity in Mesial Temporal Lobe Epilepsy , 2015, American Journal of Neuroradiology.

[23]  Neda Bernasconi,et al.  Graph-theoretical analysis reveals disrupted small-world organization of cortical thickness correlation networks in temporal lobe epilepsy. , 2011, Cerebral cortex.

[24]  Chun-Hung Yeh,et al.  Resolving crossing fibres using constrained spherical deconvolution: Validation using diffusion-weighted imaging phantom data , 2008, NeuroImage.

[25]  Fabrice Wendling,et al.  Impaired consciousness during temporal lobe seizures is related to increased long-distance cortical-subcortical synchronization. , 2009, Brain : a journal of neurology.

[26]  O. Sporns Structure and function of complex brain networks , 2013, Dialogues in clinical neuroscience.

[27]  G. Deco,et al.  Emerging concepts for the dynamical organization of resting-state activity in the brain , 2010, Nature Reviews Neuroscience.

[28]  Yang Wang,et al.  Characteristics and variability of structural networks derived from diffusion tensor imaging , 2012, NeuroImage.

[29]  J. Bellanger,et al.  Neural networks involving the medial temporal structures in temporal lobe epilepsy , 2001, Clinical Neurophysiology.

[30]  W Harkness,et al.  Microdysgenesis in temporal lobe epilepsy. A quantitative and immunohistochemical study of white matter neurones. , 2001, Brain : a journal of neurology.

[31]  Agatha Lenartowicz,et al.  Effect of lateralized temporal lobe epilepsy on the default mode network , 2012, Epilepsy & Behavior.

[32]  Richard F. Betzel,et al.  Resting-brain functional connectivity predicted by analytic measures of network communication , 2013, Proceedings of the National Academy of Sciences.

[33]  E. Bullmore,et al.  A Resilient, Low-Frequency, Small-World Human Brain Functional Network with Highly Connected Association Cortical Hubs , 2006, The Journal of Neuroscience.

[34]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[35]  Olaf Sporns,et al.  Network structure of cerebral cortex shapes functional connectivity on multiple time scales , 2007, Proceedings of the National Academy of Sciences.

[36]  Maria Thom,et al.  Investigation of widespread neocortical pathology associated with hippocampal sclerosis in epilepsy: A postmortem study , 2011, Epilepsia.

[37]  Fabrice Bartolomei,et al.  Graph theoretical analysis of structural and functional connectivity MRI in normal and pathological brain networks , 2010, Magnetic Resonance Materials in Physics, Biology and Medicine.

[38]  Gustavo Deco,et al.  Functional connectivity dynamics: Modeling the switching behavior of the resting state , 2015, NeuroImage.

[39]  M. Breakspear,et al.  The connectomics of brain disorders , 2015, Nature Reviews Neuroscience.

[40]  Sharon Chiang,et al.  Clinical correlates of graph theory findings in temporal lobe epilepsy , 2014, Seizure.

[41]  Linda Douw,et al.  Dissociated multimodal hubs and seizures in temporal lobe epilepsy , 2015, Annals of clinical and translational neurology.

[42]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[43]  Enzo Tagliazucchi,et al.  Multimodal Imaging of Dynamic Functional Connectivity , 2015, Front. Neurol..

[44]  J. Gotman,et al.  Generalized epileptic discharges show thalamocortical activation and suspension of the default state of the brain. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[45]  M. Raichle,et al.  Lag threads organize the brain’s intrinsic activity , 2015, Proceedings of the National Academy of Sciences.

[46]  Sophie Achard,et al.  Nodal approach reveals differential impact of lateralized focal epilepsies on hub reorganization , 2015, NeuroImage.

[47]  C. Yasuda,et al.  Distinct functional and structural MRI abnormalities in mesial temporal lobe epilepsy with and without hippocampal sclerosis , 2014, Epilepsia.

[48]  M. Greicius,et al.  Greater than the sum of its parts: a review of studies combining structural connectivity and resting-state functional connectivity , 2009, Brain Structure and Function.

[49]  J. Gotman,et al.  Patterns of altered functional connectivity in mesial temporal lobe epilepsy , 2012, Epilepsia.

[50]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[51]  O Sporns,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009, Proceedings of the National Academy of Sciences.

[52]  Biyu J. He,et al.  Impaired and facilitated functional networks in temporal lobe epilepsy☆ , 2013, NeuroImage: Clinical.

[53]  B. Bernhardt,et al.  Mapping thalamocortical network pathology in temporal lobe epilepsy , 2012, Neurology.

[54]  S. Spencer Neural Networks in Human Epilepsy: Evidence of and Implications for Treatment , 2002, Epilepsia.

[55]  Leonardo L. Gollo,et al.  Dwelling quietly in the rich club: brain network determinants of slow cortical fluctuations , 2015, Philosophical Transactions of the Royal Society B: Biological Sciences.

[56]  Olivier Colliot,et al.  Structural connectivity differences in left and right temporal lobe epilepsy , 2014, NeuroImage.

[57]  Eswar Damaraju,et al.  Tracking whole-brain connectivity dynamics in the resting state. , 2014, Cerebral cortex.

[58]  E. Bullmore,et al.  The hubs of the human connectome are generally implicated in the anatomy of brain disorders , 2014, Brain : a journal of neurology.

[59]  Catherine R. Traynor,et al.  Thalamotemporal impairment in temporal lobe epilepsy: A combined MRI analysis of structure, integrity, and connectivity , 2014, Epilepsia.

[60]  Christian Beaulieu,et al.  White matter abnormalities associate with type and localization of focal epileptogenic lesions , 2015, Epilepsia.

[61]  Sharon Chiang,et al.  Structural–functional coupling changes in temporal lobe epilepsy , 2015, Brain Research.

[62]  Bernd Weber,et al.  Voxel‐Based Statistical Analysis of Fractional Anisotropy and Mean Diffusivity in Patients with Unilateral Temporal Lobe Epilepsy of Unknown Cause , 2013, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[63]  Alan Connelly,et al.  Quantification of voxel-wise total fibre density: Investigating the problems associated with track-count mapping , 2015, NeuroImage.

[64]  A. Connelly,et al.  Improved probabilistic streamlines tractography by 2 nd order integration over fibre orientation distributions , 2009 .

[65]  Seokjun Hong,et al.  Imaging structural and functional brain networks in temporal lobe epilepsy , 2013, Front. Hum. Neurosci..

[66]  Stephen E. Rose,et al.  HOMOR: Higher Order Model Outlier Rejection for high b-value MR diffusion data , 2012, NeuroImage.

[67]  Walter H Backes,et al.  White matter network abnormalities are associated with cognitive decline in chronic epilepsy. , 2012, Cerebral cortex.

[68]  Helmut Laufs,et al.  Functional imaging of seizures and epilepsy: evolution from zones to networks. , 2012, Current opinion in neurology.

[69]  Huafu Chen,et al.  Altered Functional Connectivity and Small-World in Mesial Temporal Lobe Epilepsy , 2010, PloS one.

[70]  Anbupalam Thalamuthu,et al.  The organisation of the elderly connectome , 2015, NeuroImage.

[71]  Gustavo Deco,et al.  Resting brains never rest: computational insights into potential cognitive architectures , 2013, Trends in Neurosciences.

[72]  Leonardo L. Gollo,et al.  Time-resolved resting-state brain networks , 2014, Proceedings of the National Academy of Sciences.

[73]  Olaf Sporns,et al.  The Human Connectome: A Structural Description of the Human Brain , 2005, PLoS Comput. Biol..

[74]  Edward T. Bullmore,et al.  Whole-brain anatomical networks: Does the choice of nodes matter? , 2010, NeuroImage.

[75]  Leonardo Bonilha,et al.  Medial temporal lobe epilepsy is associated with neuronal fibre loss and paradoxical increase in structural connectivity of limbic structures , 2012, Journal of Neurology, Neurosurgery & Psychiatry.

[76]  Stuart Crozier,et al.  Apparent Fibre Density: A novel measure for the analysis of diffusion-weighted magnetic resonance images , 2012, NeuroImage.

[77]  Dustin Scheinost,et al.  Potential Use and Challenges of Functional Connectivity Mapping in Intractable Epilepsy , 2013, Front. Neurol..

[78]  Edward T. Bullmore,et al.  Network-based statistic: Identifying differences in brain networks , 2010, NeuroImage.

[79]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[80]  Jacobus F. A. Jansen,et al.  Functional and Structural Network Impairment in Childhood Frontal Lobe Epilepsy , 2014, PloS one.

[81]  Tore Opsahl,et al.  Prominence and control: the weighted rich-club effect. , 2008, Physical review letters.

[82]  Huafu Chen,et al.  Altered functional-structural coupling of large-scale brain networks in idiopathic generalized epilepsy. , 2011, Brain : a journal of neurology.