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Ultrastructural and functional characterization of satellitosis in the human lateral amygdala associated with Ammon’s horn sclerosis

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Abstract

The amygdala displays neuronal cell loss and gliosis in human temporal lobe epilepsy (TLE). Therefore, we investigated a certain type of gliosis, called satellitosis, in the lateral amygdala (LA) of TLE patients with Ammon’s horn sclerosis (AHS, n = 15) and non-AHS (n = 12), and in autopsy controls. Satellite cells were quantified using light and electron microscopy at the somata of Nissl-stained and glutamic acid decarboxylase-negative projection neurons, and their functional properties were studied using electrophysiology. Non-AHS cases suffered from ganglioglioma, cortical dysplasia, Sturge–Weber syndrome, astrocytoma WHO III–IV, Rasmussen’s encephalitis, cerebral infarction and perinatal brain damage. TLE cases with AHS had a more prominent satellitosis as compared to non-AHS and/or autopsy cases, which correlated with epilepsy duration but not age. At ultrastructural level, the predominant type of satellite cells occurring in both AHS and non-AHS cases displayed a dark cytoplasm and an irregularly shaped dark nucleus, whereas perineuronal glial cells with a light cytoplasm and light oval nucleus were much rarer. Satellite cells expressed time- and voltage-dependent transmembrane currents as revealed by patch-clamp recordings typical for ‘complex’ glia, although only 44% of satellite cells were immunostained for the chondroitin sulfate proteoglycan NG2. Together, the perineuronal cells described here were a heterogenous cell population regarding their NG2 expression, although they resembled NG2 cells rather than bona fide oligodendrocytes and astrocytes based on their ultrastructural and electrophysiological characteristics. Thus, perineuronal satellitosis as studied in the LA seems to be a hallmark of AHS-associated TLE pathology in patients suffering from intractable epilepsy.

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Acknowledgments

Ms. Röhl and Ms. Schneider (Institute of Anatomy, Magdeburg, Germany) and Mr. O’Leary (Department of Anatomy, Cork, Ireland) are acknowledged for expert technical assistance, Ms. Stausberg and Ms. Ullmann for their aid with the clinical data. We thank C. Mawrin and K. Dietzmann (Institute of Neuropathology, University of Magdeburg Germany), and RAI de Vos (Laboratorium voor Pathologie Enschede Netherlands) for providing autopsy material. This study was supported by the Deutsche Forschungsgemeinschaft (SFB/TR3, TP C3 to DYH and CS, TP 1 to JS).

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Authors and Affiliations

  1. Institute of Anatomy, University of Magdeburg, Magdeburg, Germany

    Heidrun Faber-Zuschratter & Deniz M. Yilmazer-Hanke

  2. Institute of Cellular Neurosciences, University of Bonn, Bonn, Germany

    Kerstin Hüttmann & Christian Steinhäuser

  3. Department of Neuropathology, University of Bonn, Bonn, Germany

    Albert Becker

  4. Department of Neurosurgery, University of Bonn, Bonn, Germany

    Johannes Schramm

  5. Department of Anatomy, Biosciences Institute, University College Cork, Windle Building, Cork, Ireland

    Uchenna Okafo, Daniel Shanley & Deniz M. Yilmazer-Hanke

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  1. Heidrun Faber-Zuschratter
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Correspondence to Deniz M. Yilmazer-Hanke.

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Faber-Zuschratter, H., Hüttmann, K., Steinhäuser, C. et al. Ultrastructural and functional characterization of satellitosis in the human lateral amygdala associated with Ammon’s horn sclerosis. Acta Neuropathol 117, 545–555 (2009). https://doi.org/10.1007/s00401-009-0504-5

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