Multiple-brain systems dynamically interact during tonic and phasic states to support language integrity in temporal lobe epilepsy

Modi, Shilpi; He, Xiaosong; Chaudhary, Kapil; Hinds, Walter; Crow, Andrew J D; Beloor-Suresh, Ashithkumar; Sperling, Michael R.; Tracy, Joseph I.

doi:10.1016/j.nicl.2021.102861

Cited by 4 publications

(4 citation statements)

References 68 publications

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“…This effect, however, occurred in combination with a significant enhancement of hub and segregation findings in the contralateral hemisphere. Accordingly, although diffusion and resting state studies have shown these types of extratemporal effects, 40,43–50 our data refined our understanding of these extratemporal effects by demonstrating the bias to the contralateral hemisphere and specifying the changes in topographic organization that occurred among these structural pathways. Moreover, we were able to specify the tracts involved in this topographic reorganization in FBTCS, with insula and posterior regions prominent in this regard.…”

Section: Discussionmentioning

confidence: 59%

Edge‐wise analysis reveals white matter connectivity associated with focal to bilateral tonic–clonic seizures

Javidi,

He,

Ankeeta

et al. 2024

Epilepsia

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ObjectiveFocal to bilateral tonic–clonic seizures (FBTCS) represent a challenging subtype of focal temporal lobe epilepsy (TLE) in terms of both severity and treatment response. Most studies have focused on regional brain analysis that is agnostic to the distribution of white matter (WM) pathways associated with a node. We implemented a more selective, edge‐wise approach that allowed for identification of the individual connections unique to FBTCS.MethodsT1‐weighted and diffusion‐weighted images were obtained from 22 patients with solely focal seizures (FS), 43 FBTCS patients, and 65 age/sex‐matched healthy participants (HPs), yielding streamline (STR) connectome matrices. We used diffusion tensor‐derived STRs in an edge‐wise approach to determine specific structural connectivity changes associated with seizure generalization in FBTCS compared to matched FS and HPs. Graph theory metrics were computed on both node‐ and edge‐based connectivity matrices.ResultsEdge‐wise analyses demonstrated that all significantly abnormal cross‐hemispheric connections belonged to the FBTCS group. Abnormal connections associated with FBTCS were mostly housed in the contralateral hemisphere, with graph metric values generally decreased compared to HPs. In FBTCS, the contralateral amygdala showed selective decreases in the structural connection pathways to the contralateral frontal lobe. Abnormal connections in TLE involved the amygdala, with the ipsilateral side showing increases and the contralateral decreases. All the FS findings indicated higher graph metrics for connections involving the ipsilateral amygdala. Data also showed that some FBTCS connectivity effects are moderated by aging, recent seizure frequency, and longer illness duration.SignificanceData showed that not all STR pathways are equally affected by the seizure propagation of FBTCS. We demonstrated two key biases, one indicating a large role for the amygdala in the propagation of seizures, the other pointing to the prominent role of cross‐hemispheric and contralateral hemisphere connections in FBTCS. We demonstrated topographic reorganization in FBTCS, pointing to the specific WM tracts involved.

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Section: Discussionmentioning

confidence: 59%

Edge‐wise analysis reveals white matter connectivity associated with focal to bilateral tonic–clonic seizures

Javidi,

He,

Ankeeta

et al. 2024

Epilepsia

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“…The parietal lobe, a sensory motor integration hub, encompasses numerous positive connections. Numerous studies corroborate that the human brain’s frontal-parietal cortex network [17], also known as the dorsal attention network, is involved in visual attention function. Previous studies have reported an association between the parietal lobe and cognitive function [18].…”

Section: Discussionmentioning

confidence: 94%

Connectome-based prediction of cognitive performance in patients with temporal lobe epilepsy

Qin,

Pan,

Chen

et al. 2024

NeuroReport

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Objective Temporal lobe epilepsy (TLE) patients often exhibit varying degrees of cognitive impairments. This study aims to predict cognitive performance in TLE patients by applying a connectome-based predictive model (CPM) to whole-brain resting-state functional connectivity (RSFC) data. Methods A CPM was established and leave-one-out cross-validation was employed to decode the cognitive performance of patients with TLE based on the whole-brain RSFC. Results Our findings indicate that cognitive performance in TLE can be predicted through the internal and network connections of the parietal lobe, limbic lobe, and cerebellum systems. These systems play crucial roles in cognitive control, emotion processing, and social perception and communication, respectively. In the subgroup analysis, CPM successfully predicted TLE patients with and without focal to bilateral tonic–clonic seizures (FBCTS). Additionally, significant differences were noted between the two TLE patient groups and the normal control group. Conclusion This data-driven approach provides evidence for the potential of predicting brain features based on the inherent resting-state brain network organization. Our study offers an initial step towards an individualized prediction of cognitive performance in TLE patients, which may be beneficial for diagnosis, prognosis, and treatment planning.

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“…(He et al, 2018) Indeed, previous has demonstrated that the strengthening of intrinsic networks during the resting state can work to enhance cognition at the time of actual performance. (Modi et al, 2021) The thalamus, on the other hand, serves as an important structure in temporal lobe epilepsy networks, potentially mediating focal-to-generalized seizures (He et al, 2020). The thalamus may also be an important, direct mediator of the spread of TLE structural damage originating in the temporal lobe,(Caciagli et al, 2017; Lopez et al, 2022; Zhang et al, 2017) and thalamic abnormalities are associated with poor surgical outcome.…”

Section: Discussionmentioning

confidence: 99%

“…(Sperling, 1993;Sperling et al, 1989;Sperling et al, 1992) We included pathology beyond classic hippocampal sclerosis to broaden the applicability of the study, as loss of connectivity or reserve is not dependent upon the presence of a gross macroscopic epileptogenic lesion. (Modi et al, 2021) Patients were excluded from the study for any of the following reasons: previous brain surgery; medical illness with central nervous system impact other than epilepsy; extratemporal or multifocal epilepsy; contraindications to MRI; or hospitalization for any Axis I disorder listed in the Diagnostic and Statistical Manual of Mental Disorders, V. Depressive disorders were allowed given the high comorbidity of depression and epilepsy. (Tracy et al, 2007) Neurocognitive performance was assessed at the time of patient recruitment by a group of neuropsychological tests, as part of their standard clinical care and work up for potential surgical At the same time, a total of 92 age-, and gender-matched healthy controls (HC) were recruited from the Thomas Jefferson University community.…”

Section: Study Characteristics and Neuropsychological Measuresmentioning

confidence: 99%

Normative and individual, non-normative intrinsic networks and the transition to impaired cognition

Zhang,

Hudgins,

Struck

et al. 2024

Preprint

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Despite their temporal lobe pathology, a significant subgroup of temporal lobe epilepsy (TLE) patients are able to maintain normative cognitive functioning. Here, we identify TLE patients with intact versus impaired cognitive profiles, and interrogate for the presence of both normative and highly individual intrinsic connectivity networks(ICN) – all towards understanding the transition from impaired to intact neurocognitive status. We retrospectively investigated data from 88 TLE patients and matched 91 healthy controls with resting-state functional MRI. Functional MRI data were decomposed using independent component analysis to obtain individualized ICNs. Here, we calculated the degree of match between individualized ICNs and canonical ICNs (e.g., Yeo et.al 17 resting-state network) and divided each participant’s ICNs into normative or non-normative status based on the degree of match. We found that the individualized networks matched the canonical networks less well in the cognitively impaired compared to the cognitively intact TLE patients. The cognitively impaired patients showed significant abnormalities in the profiles of both normative and non-normative networks, whereas the intact patients showed abnormalities only in non-normative networks. At the same time, we found normative networks held a strong, positive association with the neuropsychological measures, with this association negative in non-normative networks. We were able to provide the initial data demonstrating that significant cognitive deficits are associated with the status of highly-individual ICNs, making clear that the transition from intact to impaired cognitive status is not simply the result of disruption to normative brain networks.

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Multiple-brain systems dynamically interact during tonic and phasic states to support language integrity in temporal lobe epilepsy

Cited by 4 publications

References 68 publications

Edge‐wise analysis reveals white matter connectivity associated with focal to bilateral tonic–clonic seizures

Edge‐wise analysis reveals white matter connectivity associated with focal to bilateral tonic–clonic seizures

Connectome-based prediction of cognitive performance in patients with temporal lobe epilepsy

Normative and individual, non-normative intrinsic networks and the transition to impaired cognition

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