Preferential susceptibility of limbic cortices to microstructural damage in temporal lobe epilepsy: A quantitative T1 mapping study

Neuroimage. 2018 Nov 15:182:294-303. doi: 10.1016/j.neuroimage.2017.06.002. Epub 2017 Jun 3.

Abstract

The majority of MRI studies in temporal lobe epilepsy (TLE) have utilized morphometry to map widespread cortical alterations. Morphological markers, such as cortical thickness or grey matter density, reflect combinations of biological events largely driven by overall cortical geometry rather than intracortical tissue properties. Because of its sensitivity to intracortical myelin, quantitative measurement of longitudinal relaxation time (qT1) provides and an in vivo proxy for cortical microstructure. Here, we mapped the regional distribution of qT1 in a consecutive cohort of 24 TLE patients and 20 healthy controls. Compared to controls, patients presented with a strictly ipsilateral distribution of qT1 increases in temporopolar, parahippocampal and orbitofrontal cortices. Supervised statistical learning applied to qT1 maps could lateralize the seizure focus in 92% of patients. Intracortical profiling of qT1 along streamlines perpendicular to the cortical mantle revealed marked effects in upper levels that tapered off at the white matter interface. Findings remained robust after correction for cortical thickness and interface blurring, suggesting independence from previously reported morphological anomalies in this disorder. Mapping of qT1 along hippocampal subfield surfaces revealed marked increases in anterior portions of the ipsilateral CA1-3 and DG that were also robust against correction for atrophy. Notably, in operated patients, qualitative histopathological analysis of myelin stains in resected hippocampal specimens confirmed disrupted internal architecture and fiber organization. Both hippocampal and neocortical qT1 anomalies were more severe in patients with early disease onset. Finally, analysis of resting-state connectivity from regions of qT1 increases revealed altered intrinsic functional network embedding in patients, particularly to prefrontal networks. Analysis of qT1 suggests a preferential susceptibility of ipsilateral limbic cortices to microstructural damage, possibly related to disrupted myeloarchitecture. These alterations may reflect atypical neurodevelopment and affect the integrity of fronto-limbic functional networks.

Keywords: Epilepsy; Function; MRI; Microstructure; Multimodal.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Brain Mapping / methods*
  • Cerebral Cortex* / diagnostic imaging
  • Cerebral Cortex* / pathology
  • Cerebral Cortex* / physiopathology
  • Epilepsy, Temporal Lobe* / diagnostic imaging
  • Epilepsy, Temporal Lobe* / pathology
  • Epilepsy, Temporal Lobe* / physiopathology
  • Female
  • Hippocampus / diagnostic imaging
  • Hippocampus / pathology
  • Hippocampus / physiopathology
  • Humans
  • Limbic Lobe / diagnostic imaging
  • Limbic Lobe / pathology
  • Limbic Lobe / physiopathology
  • Magnetic Resonance Imaging / methods*
  • Male
  • Middle Aged
  • Young Adult