More than just statics: Static and temporal dynamic changes in intrinsic brain activity in unilateral temporal lobe epilepsy

Abstract

BackgroundTemporal lobe epilepsy (TLE) is the most prevalent refractory focal epilepsy and is more likely accompanied by cognitive impairment. The fully understanding of the neuronal activity underlying TLE is of great significance.ObjectiveThis study aimed to comprehensively explore the potential brain activity abnormalities affected by TLE and detect whether the changes were associated with cognition.MethodsSix static intrinsic brain activity (IBA) indicators [amplitude of low-frequency fluctuation (ALFF), fractional ALFF (fALFF), regional homogeneity (ReHo), degree centrality (DC), global signal correlation (GSCorr), and voxel-mirrored homotopic connectivity (VMHC)] and their corresponding dynamic indicators, such as dynamic ALFF (dALFF), dynamic fALFF (dfALFF), dynamic ReHo (dReHo), dynamic DC (dDC), dynamic VMHC (dVMHC), and dynamic GSCorr (dGSCorr), in 57 patients with unilateral TLE and 42 healthy volunteers were compared. Correlation analyses were also performed between these indicators in areas displaying group differences and cognitive function, epilepsy duration, and severity.ResultsMarked overlap was present among the abnormal brain regions detected using various static and dynamic indicators, primarily including increased ALFF/dALFF/fALFF in the bilateral medial temporal lobe and thalamus, decreased ALFF/dALFF/fALFF in the frontal lobe contralateral to the epileptogenic side, decreased fALFF, ReHo, dReHo, DC, dDC, GSCorr, dGSCorr, and VMHC in the temporal neocortex ipsilateral to the epileptogenic foci, decreased dReHo, dDC, dGSCorr, and dVMHC in the occipital lobe, and increased ALFF, fALFF, dfALFF, ReHo, and DC in the supplementary motor area ipsilateral to the epileptogenic foci. Furthermore, most IBA indicators in the abnormal brain region significantly correlated with the duration of epilepsy and several cognitive scale scores (P < 0.05).ConclusionThe combined application of static and dynamic IBA indicators could comprehensively reveal more real abnormal neuronal activity and the impairment and compensatory mechanisms of cognitive function in TLE. Moreover, it might help in the lateralization of epileptogenic foci and exploration of the transmission and inhibition pathways of epileptic activity.

Advances in understanding the pathogenesis of epilepsy: Unraveling the molecular mechanisms

“…The epileptic brain is identified with its hyperexcitable nature of the neural circuity. However, recent literature is studying epilepsy in a more functional framework, shifting from investigating a strict molecular activity to highlighting the dynamical role of neural circuity between various brain regions 48,49 . Thus, explaining the comorbid cognitive and psychiatric symptoms associated with epilepsy.…”

Alterations in static and dynamic regional homogeneity in mesial temporal lobe epilepsy with and without initial precipitating injury

“…The high density of glutamate receptors in the occipital cortex may lead the neurons to be in a more excited state and have a long-term influence on the neurons as the disease advances, resulting in unstable local neuronal activity in mTLE-IPI patients. The changed sReHo and dReHo in the bilateral visual cortex support the decline in patients’ visual memory, spatial attention and ability to recognize colors and letters ( Song et al, 2022 ). We noted that there were subtle differences in the areas of spontaneous brain activity alterations in the visual cortex.…”

“…These abnormal ReHo changes could be a result of the temporal neocortex’s abnormal neuroplasticity being influenced by frequent abnormal discharges ( Jiang et al, 2021 ). The MTG ( Binder et al, 2009 ) and ITG ( Ojemann et al, 2002 ) play various roles in memory, auditory processing and emotion, while the STG houses a part of the primary and association auditory cortices ( Song et al, 2022 ). Although results varied slightly due to the methodological differences, we could infer that mTLE patients (no matter with or without IPI) may be more prone to have functional deficits in social cognition, auditory processing and emotion management.…”

“…Considering the dynamic property of brain activity ( Calhoun et al, 2014 ), recent investigations ( Jiang et al, 2021 ; Liang et al, 2021 ) had explored the collaboration of brain regions by measuring the time-varying covariance of their neural signals during resting-state, among which dynamic regional homogeneity (dReHo) is a relatively common approach. An rs-fMRI study ( Song et al, 2022 ) reported decreased variability of dReHo in the temporal lobe neocortex ipsilateral to epileptic foci in mTLE. Another study reported ( Xue et al, 2022 ) that patients with major depressive disorder had decreased variability of dReHo in some brain regions associated with emotional and cognitive regulation, including the fusiform gyri, the right temporal pole and hippocampus.…”

Dynamic reconfiguration of aperiodic brain activity supports cognitive functioning in epilepsy: a neural fingerprint identification

“…At first, these findings highlight that epilepsy is a network disorder impacting the brain dynamics at the whole-brain level. Secondly, while TLE may be considered a homogeneous clinical category, there is an array of clinical presentations according to the portion of the lobe involved in seizure generation (Bartolomei et al, 2008; Narasimhan et al, 2020; Song et al, 2022). Such heterogeneity may be mirrored in corresponding variability of brain dynamics on the large scale.…”