Resting state functional connectivity demonstrates increased segregation in bilateral temporal lobe epilepsy

Abstract

Objective Temporal lobe epilepsy (TLE) is the most common type of focal epilepsy. An increasingly identified subset of patients with TLE consists of those who show bilaterally independent temporal lobe seizures. The purpose of this study was to leverage network neuroscience to better understand the interictal whole brain network of bilateral TLE (BiTLE). Methods In this study, using a multicenter resting state functional magnetic resonance imaging (rs‐fMRI) data set, we constructed whole‐brain functional networks of 19 patients with BiTLE, and compared them to those of 75 patients with unilateral TLE (UTLE). We quantified resting‐state, whole‐brain topological properties using metrics derived from network theory, including clustering coefficient, global efficiency, participation coefficient, and modularity. For each metric, we computed an average across all brain regions, and iterated this process across network densities. Curves of network density vs each network metric were compared between groups. Finally, we derived a combined metric, which we term the “integration‐segregation axis,” by combining whole‐brain average clustering coefficient and global efficiency curves, and applying principal component analysis (PCA)–based dimensionality reduction. Results Compared to UTLE, BiTLE had decreased global efficiency (p = .031), and decreased whole brain average participation coefficient across a range of network densities (p = .019). Modularity maximization yielded a larger number of smaller communities in BiTLE than in UTLE (p = .020). Differences in network properties separate BiTLE and UTLE along the integration‐segregation axis, with regions within the axis having a specificity of up to 0.87 for BiTLE. Along the integration‐segregation axis, UTLE patients with poor surgical outcomes were distributed in the same regions as BiTLE, and network metrics confirmed similar patterns of increased segregation in both BiTLE and poor outcome UTLE. Significance Increased interictal whole‐brain network segregation, as measured by rs‐fMRI, is specific to BiTLE, as well as poor surgical outcome UTLE, and may assist in non‐invasively identifying this patient population prior to intracranial electroencephalography or device implantation.

Atypical connectome topography and signal flow in temporal lobe epilepsy

“…This could indicate an imbalance of functional segregation and integration. [92][93][94] By supporting hierarchical information transmission, sensory-to-transmodal segregation may facilitate specialized processing, and contribute to integrative function. 95 Our findings were prominent in temporal and ventromedial prefrontal cortices, transmodal regions known to be vulnerable to TLErelated compromise.…”

Closed-loop electrical stimulation to prevent focal epilepsy progression and long-term memory impairment

“…In patients, a similar tradeoff revealed decreased IED-spindling coupling modulation associated with increased incidence of independent IEDs. Our cellular level observations suggest a pathological adaptation in epilepsy( 45 ), and could underpin the interictal network segregation identified by resting state functional MRI in patients with progressive focal epilepsy( 46 ).…”

iEEG‐recon: A fast and scalable pipeline for accurate reconstruction of intracranial electrodes and implantable devices

“…Multimodal studies that combine iEEG with neuroimaging, such as diffusion tensor imaging, are also of interest across disciplines, including epilepsy. 11,34,35 Functional neuroimaging, such as resting-state functional MRI, has also demonstrated widespread abnormalities in focal epilepsy, [36][37][38] yet direct intracranial electrophysiological correlates of these abnormalities are lacking. iEEG-recon provides a natural framework for bridging intracranial electrophysiology and neuroimaging by allowing different structural and functional neuroimaging-based atlases to be used in the electrode reconstruction process.…”