Characterization of focal cortical dysplasia with balloon cells by layer-specific markers: Evidence for differential vulnerability of interneurons

Epilepsia. 2017 Apr;58(4):635-645. doi: 10.1111/epi.13690. Epub 2017 Feb 16.

Abstract

Objective: Focal cortical dysplasia (FCD) is a major cause of pharmacoresistant focal epilepsy. Little is known about the pathomechanisms underlying the characteristic cytoarchitectural abnormalities associated with FCD. In the present study, a broad panel of markers identifying layer-specific neuron subpopulations was applied to characterize dyslamination and structural alterations in FCD with balloon cells (FCD 2b).

Methods: Pan-neuronal neuronal nuclei (NeuN) and layer-specific protein expression (Reelin, Calbindin, Calretinin, SMI32 (nonphosphorylated neurofilament H), Parvalbumin, transducin-like enhancer protein 4 (TLE4), and Vimentin) was studied by immunohistochemistry on paraffin sections of FCD2b cases (n = 22) and was compared to two control groups with (n = 7) or without epilepsy (n = 4 postmortem cases). Total and layer-specific neuron densities were systematically quantified by cell counting considering age at surgery and brain region.

Results: We show that in FCD2b total neuron densities across all six cortical layers were not significantly different from controls. In addition, we present evidence that a basic laminar arrangement of layer-specific neuron subtypes was preserved despite the severe disturbance of cortical structure. SMI32-positive pyramidal neurons showed no significant difference in total numbers, but a reduction in layers III and V. The densities of supragranular Calbindin- and Calretinin-positive interneurons in layers II and III were not different from controls, whereas Parvalbumin-expressing interneurons, primarily located in layer IV, were significantly reduced in numbers when compared to control cases without epilepsy. In layer VI, the density of TLE4-positive projection neurons was significantly increased. Altogether, these data show that changes in cellular composition mainly affect deep cortical layers in FCD2b.

Significance: The application of a broad panel of markers defining layer-specific neuronal subpopulations revealed that in FCD2b neuronal diversity and a basic laminar arrangement are maintained despite the severe disturbance of cytoarchitecture. Moreover, it showed that Parvalbumin-positive, inhibitory interneurons are highly vulnerable in contrast to other interneuron subtypes, possibly related to the epileptic condition.

Keywords: Epilepsy; Lamination; Malformation; Neocortical brain development; Parvalbumin.

MeSH terms

  • Adolescent
  • Adult
  • Calbindin 2 / metabolism
  • Cell Adhesion Molecules, Neuronal / metabolism
  • Cell Count
  • Child
  • Child, Preschool
  • Epilepsy / pathology*
  • Extracellular Matrix Proteins / metabolism
  • Female
  • Humans
  • Infant
  • Interneurons / classification*
  • Interneurons / metabolism*
  • Male
  • Malformations of Cortical Development, Group I / pathology*
  • Middle Aged
  • Nerve Tissue Proteins / metabolism
  • Neurofilament Proteins / metabolism
  • Parvalbumins / metabolism
  • Phosphopyruvate Hydratase / metabolism
  • Reelin Protein
  • Serine Endopeptidases / metabolism
  • Statistics, Nonparametric
  • Young Adult

Substances

  • Calbindin 2
  • Cell Adhesion Molecules, Neuronal
  • Extracellular Matrix Proteins
  • Nerve Tissue Proteins
  • Neurofilament Proteins
  • Parvalbumins
  • Reelin Protein
  • neurofilament protein H
  • RELN protein, human
  • Serine Endopeptidases
  • Phosphopyruvate Hydratase

Supplementary concepts

  • Focal cortical dysplasia of Taylor