Anatomic consistencies across epilepsies: a stereotactic-EEG informed high-resolution structural connectivity study

Besson, Pierre; Bandt, S. Kathleen; Proix, Timothcrée; Lagarde, Stanislas; Jirsa, Viktor K.; Ranjeva, Jean Philippe; Bartolomei, Fabricē; Guye, Maxime

doi:10.1093/brain/awx181

Cited by 76 publications

(94 citation statements)

References 94 publications

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“…A recent study of coregistered of intracranial EEG information with diffusion MRI–derived structural connectome data across a cohort of patients with temporal and extratemporal foci. The study suggested a divergence of connectivity patterns in epileptogenic compared to nonepileptogenic areas, with epileptogenic networks displaying more intact local connectivity while whole brain connectivity strength seemed to be reduced . The biologic implications of these data are not yet clear.…”

Section: Clinical Connectomicsmentioning

confidence: 91%

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Neuroimaging and connectomics of drug‐resistant epilepsy at multiple scales: From focal lesions to macroscale networks

et al. 2019

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Summary Epilepsy is among the most common chronic neurologic disorders, with 30%‐40% of patients having seizures despite antiepileptic drug treatment. The advent of brain imaging and network analyses has greatly improved the understanding of this condition. In particular, developments in magnetic resonance imaging (MRI) have provided measures for the noninvasive characterization and detection of lesions causing epilepsy. MRI techniques can probe structural and functional connectivity, and network analyses have shaped our understanding of whole‐brain anomalies associated with focal epilepsies. This review considers the progress made by neuroimaging and connectomics in the study of drug‐resistant epilepsies due to focal substrates, particularly temporal lobe epilepsy related to mesiotemporal sclerosis and extratemporal lobe epilepsies associated with malformations of cortical development. In these disorders, there is evidence of widespread disturbances of structural and functional connectivity that may contribute to the clinical and cognitive prognosis of individual patients. It is hoped that studying the interplay between macroscale network anomalies and lesional profiles will improve our understanding of focal epilepsies and assist treatment choices.

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Section: Clinical Connectomicsmentioning

confidence: 91%

“…The study suggested a divergence of connectivity patterns in epileptogenic compared to nonepileptogenic areas, with epileptogenic networks displaying more intact local connectivity while whole brain connectivity strength seemed to be reduced. 73 The biologic implications of these data are not yet clear.…”

Section: Clinical Connectomicsmentioning

confidence: 99%

Neuroimaging and connectomics of drug‐resistant epilepsy at multiple scales: From focal lesions to macroscale networks

et al. 2019

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“…46 Additional intracranial connectivity measures have also revealed increased connectivity in epileptogenic networks when compared to regions outside of the epileptogenic zone. 47 To further explore computational mechanisms of seizure dynamics, it has been speculated that local clusters of neurons may isolate themselves from the rest of the network, likely through an imbalance between local and distant connections, a mechanism described as "network tightening". 48 Under this account, however, functional isolation of the seizure-onset zone was speculated to play a role in annihilating epileptogenic activity and, as such, may represent a potential compensatory mechanism through which locally confined, seizure-related activity is prevented from spreading.…”

Section: Discussionmentioning

confidence: 99%

Functional connectome contractions in temporal lobe epilepsy: microstructural underpinnings and associations to surgical outcome

Larivière

Wang

Wael

et al. 2019

Preprint

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Larivière et al.Connectome contractions in TLE | 2 ABSTRACT OBJECTIVE. Temporal lobe epilepsy (TLE) is classically associated with hippocampal pathology, and increasingly with structural changes beyond the mesiotemporal lobe. Functional anomalies, their link to cortical morphology and microstructure, and their utility in surgical prognosis, however, remain less well understood. METHODS.We studied 30 drug-resistant TLE patients and 57 healthy controls using multimodal 3T MRI. All patients had histologically-verified hippocampal sclerosis and underwent postoperative imaging to establish the extent of surgical resection. Our analysis leveraged a novel resting-state fMRI framework that parameterizes functional connectivity distance, consolidating functional and geometric properties of macroscale brain networks. Functional findings were integrated with morphological and microstructural metrics, and associations to post-surgical seizure outcome were examined using machine learning techniques. RESULTS.Compared to controls, TLE showed connectivity distance reductions in temporo-insular and dorsomedial prefrontal networks, with the former being more marked ipsilateral to the focus.Findings were driven by contractions in long-distance connections together with an excess in shortrange connections, suggesting topological segregation of functional networks. Parallel structural profiling indicated that functional connectivity distance reductions in TLE were independent of atrophy but mediated by microstructural changes in the underlying white matter. Patients with persistent seizures showed anomalies a distinct network signature which predicted seizure outcome with 75±4% accuracy (using 5-fold cross-validation). CONCLUSIONS.Our findings suggest connectivity distance contractions as a pathoconnectomic substrate of TLE. Functional topological isolation may represent a microstructurally mediated network mechanism that tilts the balance towards epileptogenesis in affected networks.

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“…On the other hand, whilst minimizing false positives, the stringent-but necessary-statistical approach incorporated into VBM could obscure subtle common structural alterations (Keller & Roberts, 2008). Furthermore, a recently published study has shown that pathological structural connectivity causes disturbances to common large-scale functional brain networks regardless of the localization of the epileptogenic zone in patients with refractory focal epilepsy (Besson et al, 2017). One issue to therefore consider is that patients with NDfE have heterogeneous neurobiological mechanisms and different epileptogenic foci, which would not be identified using a technique such as VBM that is used to detect abnormalities common to a patient group.…”

Section: Biological and Clinical Implicationsmentioning

confidence: 99%

“…Particular anatomical circuits act as critical modulators of seizure generation and propagation, and seizure activity does not spread diffusely throughout the brain but propagates along specific anatomical pathways, regardless of the localization of the brain insult (Loscher & Ebert, 1996;Piredda & Gale, 1985). Furthermore, a recently published study has shown that pathological structural connectivity causes disturbances to common large-scale functional brain networks regardless of the localization of the epileptogenic zone in patients with refractory focal epilepsy (Besson et al, 2017). Moreover, particular deep brain regions-such as the thalamus and thalamocortical pathways-play a crucial role in the clinical expression of seizures in the epilepsies (Dreifuss et al, 2001), and anatomically support widespread distributed cortico-subcortical networks (Nieuwenhuys, Voogd, & Huijzen, 1988)-are structurally and physiologically abnormal in both hemispheres in patients with long-standing focal and generalized epilepsy disorders (Bonilha et al, 2013;He, Doucet, Sperling, Sharan, & Tracy, 2015;Kay & Szaflarski, 2014;Keller et al, 2014Keller et al, , 2015Kim et al, 2014;O'Muircheartaigh et al, 2012).…”

Section: Biological and Clinical Implicationsmentioning

confidence: 99%

Resting‐state functional brain networks in adults with a new diagnosis of focal epilepsy

et al. 2018

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ObjectivesNewly diagnosed focal epilepsy (NDfE) is rarely studied, particularly using advanced neuroimaging techniques. Many patients with NDfE experience cognitive impairments, particularly with respect to memory, sustained attention, mental flexibility, and executive functioning. Cognitive impairments have been related to alterations in resting‐state functional brain networks in patients with neurological disorders. In the present study, we investigated whether patients with NDfE had altered connectivity in large‐scale functional networks using resting‐state functional MRI.MethodsWe recruited 27 adults with NDfE and 36 age‐ and sex‐matched healthy controls. Resting‐state functional MRI was analyzed using the Functional Connectivity Toolbox (CONN). We investigate reproducibly determined large‐scale functional networks, including the default mode, salience, fronto‐parietal attention, sensorimotor, and language networks using a seed‐based approach. Network comparisons between patients and controls were thresholded using a FDR cluster‐level correction approach.ResultsWe found no significant differences in functional connectivity between seeds within the default mode, salience, sensorimotor, and language networks and other regions of the brain between patients and controls. However, patients with NDfE had significantly reduced connectivity between intraparietal seeds within the fronto‐parietal attention network and predominantly frontal and temporal cortical regions relative to controls; this finding was demonstrated including and excluding the patients with brain lesions. No common alteration in brain structure was observed in patients using voxel‐based morphometry. Findings were not influenced by treatment outcome at 1 year.ConclusionsPatients with focal epilepsy have brain functional connectivity alterations at diagnosis. Functional brain abnormalities are not necessarily a consequence of the chronicity of epilepsy and are present when seizures first emerge.

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Anatomic consistencies across epilepsies: a stereotactic-EEG informed high-resolution structural connectivity study

Cited by 76 publications

References 94 publications

Neuroimaging and connectomics of drug‐resistant epilepsy at multiple scales: From focal lesions to macroscale networks

Neuroimaging and connectomics of drug‐resistant epilepsy at multiple scales: From focal lesions to macroscale networks

Functional connectome contractions in temporal lobe epilepsy: microstructural underpinnings and associations to surgical outcome

Resting‐state functional brain networks in adults with a new diagnosis of focal epilepsy

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