Nodal approach reveals differential impact of lateralized focal epilepsies on hub reorganization

Ridley, Ben; Rousseau, Célia; Wirsich, Jonathan; Troter, Arnaud Le; Soulier, Elisabeth; Confort‐Gouny, S.; Bartolomei, Fabricē; Ranjeva, Jean‐Philippe; Achard, Sophie; Guye, Maxime

doi:10.1016/j.neuroimage.2015.05.096

Cited by 42 publications

(51 citation statements)

References 65 publications

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“…First, the structural asymmetry is generally in favor of the left hemisphere. The left asymmetry (possibly due to a longer network maturation period; Keller, Schoene‐Bake, Gerdes, Weber, & Deppe, cited by Besson et al ()) could, indeed, be at the origin of the facilitation of the epileptic activity propagation through the brain explaining the wider modifications in the left hemisphere (Ridley et al, ). According to the second hypothesis, the right hemisphere would rather have a protective role, by being able to prevent the spread of m‐TLE seizures to other cortices and compensate for brain dysfunctions induced by seizures (Besson et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…Thus, different macroscale network modifications may appear in m‐TLE patients depending on the hippocampal subregions affected by sclerosis. Furthermore, other factors could have an impact on the connectivity in patients: gender and age (Ridley et al, ), handedness (Bettus et al, ), age of seizure onset, or pathology duration (e.g., van Dellen et al, ), antiepileptic drugs (Haneef, Levin, & Chiang, ; Vlooswijk et al, ) or interictal epileptic discharges (Ibrahim et al, ). Although we controlled for these factors, their significance and especially the effect of their interactions on durable modulation of the FC should be assessed in future studies.…”

Section: Discussionmentioning

confidence: 99%

“…Some modulating factors such as the hemispherical side of the epilepsy (left or right) are also important to consider. Namely, TLE with left seizure foci (dysfunctional hippocampus in the left hemisphere) showed more extensive and widespread changes in connectivity than TLE with right seizure foci both in language networks and in general (i.e., whole brain studies; de Campos, Coan, Lin Yasuda, Casseb, & Cendes, ; Dinkelacker, Dupont, & Samson, ; Ridley et al, ). However, these modulating factors are not always methodologically controlled for in the studies that can have relatively large but heterogeneous samples.…”

Section: Introductionmentioning

confidence: 99%

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Hubs disruption in mesial temporal lobe epilepsy. A resting‐state fMRI study on a language‐and‐memory network

Roger

Pichat

Torlay

et al. 2019

Human Brain Mapping

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Mesial temporal lobe epilepsy (mTLE) affects the brain networks at several levels and patients suffering from mTLE experience cognitive impairment for language and memory. Considering the importance of language and memory reorganization in this condition, the present study explores changes of the embedded languageand-memory network (LMN) in terms of functional connectivity (FC) at rest, as measured with functional MRI. We also evaluate the cognitive efficiency of the reorganization, that is, whether or not the reorganizations support or allow the maintenance of optimal cognitive functioning despite the seizure-related damage.Data from 37 patients presenting unifocal mTLE were analyzed and compared to 48 healthy volunteers in terms of LMN-FC using two methods: pairwise correlations (region of interest [ROI]-to-ROI) and graph theory. The cognitive efficiency of the LMN-FC reorganization was measured using correlations between FC parameters and language and memory scores. Our findings revealed a large perturbation of the LMN hubs in patients. We observed a hyperconnectivity of limbic areas near the dysfunctional hippocampus and mainly a hypoconnectivity for several cortical regions remote from the dysfunctional hippocampus. The loss of FC was more important in left mTLE (L-mTLE) than in right (R-mTLE) patients. The LMN-FC reorganization may not be always compensatory and not always useful for patients as it may be associated with lower cognitive performance. We discuss the different connectivity patterns obtained and conclude that interpretation of FC changes in relation to neuropsychological scores is important to determine cognitive efficiency, suggesting the concept of "connectome" would gain to be associated with a "cognitome" concept. K E Y W O R D S brain plasticity, functional connectivity, graph theory, language, memory, mesial temporal lobe epilepsy, resting-state fMRI

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Hubs disruption in mesial temporal lobe epilepsy. A resting‐state fMRI study on a language‐and‐memory network

Roger

Pichat

Torlay

et al. 2019

Human Brain Mapping

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“…Further sampling issues relate to inclusion of left and right TLE patients in the same group which, although controlled in statistical analysis, does not offer the opportunity to independently explore high-risk vs. low-risk differences in each subgroup separately. Such an investigation would be of interest, given the lateralization of autonomic brain circuitry ( 20 ) and the known whole-brain network differences between left and right TLE patients ( 106 ).…”

Section: Discussionmentioning

confidence: 99%

Dysfunctional Brain Networking among Autonomic Regulatory Structures in Temporal Lobe Epilepsy Patients at High Risk of Sudden Unexpected Death in Epilepsy

et al. 2017

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BackgroundSudden unexpected death in epilepsy (SUDEP) is common among young people with epilepsy. Individuals who are at high risk of SUDEP exhibit regional brain structural and functional connectivity (FC) alterations compared with low-risk patients. However, less is known about network-based FC differences among critical cortical and subcortical autonomic regulatory brain structures in temporal lobe epilepsy (TLE) patients at high risk of SUDEP.Methods32 TLE patients were risk-stratified according to the following clinical criteria: age of epilepsy onset, duration of epilepsy, frequency of generalized tonic–clonic seizures, and presence of nocturnal seizures, resulting in 14 high-risk and 18 low-risk cases. Resting-state functional magnetic resonance imaging (rs-fMRI) signal time courses were extracted from 11 bilateral cortical and subcortical brain regions involved in autonomic and other regulatory processes. After computing all pairwise correlations, FC matrices were analyzed using the network-based statistic. FC strength among the 11 brain regions was compared between the high- and low-risk patients. Increases and decreases in FC were sought, using high-risk > low-risk and low-risk > high-risk contrasts (with covariates age, gender, lateralization of epilepsy, and presence of hippocampal sclerosis).ResultsHigh-risk TLE patients showed a subnetwork with significantly reduced FC (t = 2.5, p = 0.029) involving the thalamus, brain stem, anterior cingulate, putamen and amygdala, and a second subnetwork with significantly elevated FC (t = 2.1, p = 0.031), which extended to medial/orbital frontal cortex, insula, hippocampus, amygdala, subcallosal cortex, brain stem, thalamus, caudate, and putamen.ConclusionTLE patients at high risk of SUDEP showed widespread FC differences between key autonomic regulatory brain regions compared to those at low risk. The altered FC revealed here may help to shed light on the functional correlates of autonomic disturbances in epilepsy and mechanisms involved in SUDEP. Furthermore, these findings represent possible objective biomarkers which could help to identify high-risk patients and enhance SUDEP risk stratification via the use of non-invasive neuroimaging, which would require validation in larger cohorts, with extension to patients with other epilepsies and subjects who succumb to SUDEP.

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“…For a full description of processing and graph construction please see Ridley et al ( 2015 ). Briefly, after realignment and slice-timing (SPM8, Wellcome Trust Centre, London, UK), regional masks in subject-space (FLIRT, FMRIB Software Library 1 ) based on the AAL template (Tzourio-Mazoyer et al, 2002 ) were used to obtain functional time-series from which nuisance regressors obtained from regions of interest (ROIs) in white matter and ventricles and motion parameters (three planes) were removed.…”

Section: Methodsmentioning

confidence: 99%

Alien Hand, Restless Brain: Salience Network and Interhemispheric Connectivity Disruption Parallel Emergence and Extinction of Diagonistic Dyspraxia

Ridley

Beltramone

Wirsich

et al. 2016

Front. Hum. Neurosci.

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Diagonistic dyspraxia (DD) is by far the most spectacular manifestation reported by sufferers of acute corpus callosum (CC) injury (so-called “split-brain”). In this form of alien hand syndrome, one hand acts at cross purposes with the other “against the patient’s will”. Although recent models view DD as a disorder of motor control, there is still little information regarding its neural underpinnings, due to widespread connectivity changes produced by CC insult, and the obstacle that non-volitional movements represent for task-based functional neuroimaging studies. Here, we studied patient AM, the first report of DD in patient with complete developmental CC agenesis. This unique case also offers the opportunity to study the resting-state connectomics of DD in the absence of diffuse changes subsequent to CC injury or surgery. AM developed DD following status epilepticus (SE) which resolved over a 2-year period. Whole brain functional connectivity (FC) was compared (Crawford-Howell [CH]) to 16 controls during the period of acute DD symptoms (Time 1) and after remission (Time 2). Whole brain graph theoretical models were also constructed and topological efficiency examined. At Time 1, disrupted FC was observed in inter-hemispheric and intra-hemispheric right edges, involving frontal superior and midline structures. Graph analysis indicated disruption of the efficiency of salience and right frontoparietal (FP) networks. At Time 2, after remission of diagnostic dyspraxia symptoms, FC and salience network changes had resolved. In sum, longitudinal analysis of connectivity in AM indicates that DD behaviors could result from disruption of systems that support the experience and control of volitional movements and the ability to generate appropriate behavioral responses to salient stimuli. This also raises the possibility that changes to large-scale functional architecture revealed by resting-state functional magnetic resonance imaging (fMRI) (rs-fMRI) may provide relevant information on the evolution of behavioral syndromes in addition to that provided by structural and task-based functional imaging.

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Nodal approach reveals differential impact of lateralized focal epilepsies on hub reorganization

Cited by 42 publications

References 65 publications

Hubs disruption in mesial temporal lobe epilepsy. A resting‐state fMRI study on a language‐and‐memory network

Hubs disruption in mesial temporal lobe epilepsy. A resting‐state fMRI study on a language‐and‐memory network

Dysfunctional Brain Networking among Autonomic Regulatory Structures in Temporal Lobe Epilepsy Patients at High Risk of Sudden Unexpected Death in Epilepsy

Alien Hand, Restless Brain: Salience Network and Interhemispheric Connectivity Disruption Parallel Emergence and Extinction of Diagonistic Dyspraxia

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