Download PDF
Journal of Pediatric Epilepsy 2018; 07(01): 014-020
DOI: 10.1055/s-0038-1637731
Original Article
Georg Thieme Verlag KG Stuttgart · New York

Thalamocortical Tracts, but not the Putamen, Present Microstructural Abnormalities in Juvenile Myoclonic Epilepsy: A Diffusion Tractography Study

Eman H. Esmail
1   Department of Neurology, Cairo University, Giza, Egypt
,
Hadeel M. Seif El Dein
2   Department of Radiology, Pediatric University Hospital, Cairo University, Giza, Egypt
,
Inas A. Yassine
3   Department of Systems and Biomedical Engineering, Cairo University, Giza, Egypt
4   Center for Informatics Science, Nile University, Giza, Egypt
,
Rania Zakaria
2   Department of Radiology, Pediatric University Hospital, Cairo University, Giza, Egypt
› Author Affiliations Funding This is an academic research study performed using the facilities of the institution. Grants or funding were not received for this work.
Further Information

Publication History

20 July 2017

13 February 2018

Publication Date:
31 March 2018 (online)

    Permissions and Reprints

Abstract

Background and Purpose The pathology of juvenile myoclonic epilepsy (JME) is related to thalamocortical dysfunction, and the putamen is closely related to the thalamocortical circuit. The purpose of this study is to evaluate the microstructure of the thalamo-cortico-striatal circuit in JME patients using diffusion tensor imaging (DTI).

Materials and Methods This case–control study was conducted on 13 patients with JME (10 females and 3 males with a mean age of 23.38 ± 4.75 years) and 9 age- and sex-matched volunteers as control subjects. All subjects underwent DTI and conventional magnetic resonance imaging. The data were then processed via denoising, registration, and segmentation of the internal capsule and right and left putamen using the FMRIB Software Library (FSL). The FSL was also used to calculate the different anisotropy measures: the fractional anisotropy (FA), mean diffusivity (MD), longitudinal diffusivity (LD), and radial diffusivity (RD).

Results The patients with JME had lower FA and higher LD in the thalamocortical tracts and lower MD in the frontal corticospinal tracts than the control subjects (p = 0.014, 0.001, and 0.04, respectively). No other significant differences were detected between the patients with JME and control subjects. The values measured in the right putamen were not significantly different from those measured in the left putamen in either the patients or controls.

Conclusion This study demonstrates that microstructural abnormalities occur in the thalamocortical tracts but not the putamen of patients with JME. Nevertheless, microstructural asymmetry was not observed in the patients with JME.

Keywords

epilepsy - diffusion - fractional anisotropy - putamen - thalamocortical - white matter - asymmetry

Authors' Contribution

 1. Eman H. Esmail supervised the clinical data collection, revised the statistical analysis of the results, and participated in writing and revising the results and writing the manuscript.


 2. Hadeel M. Seif El Dien performed all radiological investigations, participated in writing and revising the manuscript, and performed correspondence for publication.


 3. Inas A. Yassine performed image processing and participated in writing and revising the manuscript.


 4. Rania Zakaria supervised the work and revised the manuscript.


 

  • References

  • 1 Zifkin B, Andermann E, Andermann F. Mechanisms, genetics, and pathogenesis of juvenile myoclonic epilepsy. Curr Opin Neurol 2005; 18 (02) 147-153
    CrossrefPubMedGoogle Scholar
  • 2 Berg AT, Berkovic SF, Brodie MJ. , et al. Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005-2009. Epilepsia 2010; 51 (04) 676-685
    CrossrefPubMedGoogle Scholar
  • 3 Panayiotopoulos CP, Obeid T, Tahan AR. Juvenile myoclonic epilepsy: a 5-year prospective study. Epilepsia 1994; 35 (02) 285-296
    CrossrefPubMedGoogle Scholar
  • 4 Montalenti E, Imperiale D, Rovera A, Bergamasco B, Benna P. Clinical features, EEG findings and diagnostic pitfalls in juvenile myoclonic epilepsy: a series of 63 patients. J Neurol Sci 2001; 184 (01) 65-70
    CrossrefPubMedGoogle Scholar
  • 5 Delgado-Escueta AV, Enrile-Bacsal F. Juvenile myoclonic epilepsy of Janz. Neurology 1984; 34 (03) 285-294
    CrossrefPubMedGoogle Scholar
  • 6 Pedersen SB, Petersen KA. Juvenile myoclonic epilepsy: clinical and EEG features. Acta Neurol Scand 1998; 97 (03) 160-163
    PubMedGoogle Scholar
  • 7 Gotman J, Grova C, Bagshaw A, Kobayashi E, Aghakhani Y, Dubeau F. Generalized epileptic discharges show thalamocortical activation and suspension of the default state of the brain. Proc Natl Acad Sci U S A 2005; 102 (42) 15236-15240
    CrossrefPubMedGoogle Scholar
  • 8 Roger J, Dreifuss F, Martinez-Lage M. ; Commission on Classification and Terminology of the International League Against Epilepsy. Proposal for revised classification of epilepsies and epileptic syndromes. Epilepsia 1989; 30 (04) 389-399
    CrossrefPubMedGoogle Scholar
  • 9 Devinsky O, Gershengorn J, Brown E, Perrine K, Vazquez B, Luciano D. Frontal functions in juvenile myoclonic epilepsy. Neuropsychiatry Neuropsychol Behav Neurol 1997; 10 (04) 243-246
    PubMedGoogle Scholar
  • 10 Piazzini A, Turner K, Vignoli A, Canger R, Canevini MP. Frontal cognitive dysfunction in juvenile myoclonic epilepsy. Epilepsia 2008; 49 (04) 657-662
    CrossrefPubMedGoogle Scholar
  • 11 Pulsipher DT, Seidenberg M, Guidotti L. , et al. Thalamofrontal circuitry and executive dysfunction in recent-onset juvenile myoclonic epilepsy. Epilepsia 2009; 50 (05) 1210-1219
    CrossrefPubMedGoogle Scholar
  • 12 Landvogt C, Buchholz HG, Bernedo V, Schreckenberger M, Werhahn KJ. Alteration of dopamine D2/D3 receptor binding in patients with juvenile myoclonic epilepsy. Epilepsia 2010; 51 (09) 1699-1706
    CrossrefPubMedGoogle Scholar
  • 13 Leh SE, Ptito A, Chakravarty MM, Strafella AP. Fronto-striatal connections in the human brain: a probabilistic diffusion tractography study. Neurosci Lett 2007; 419 (02) 113-118
    CrossrefPubMedGoogle Scholar
  • 14 Deppe M, Kellinghaus C, Duning T. , et al. Nerve fiber impairment of anterior thalamocortical circuitry in juvenile myoclonic epilepsy. Neurology 2008; 71 (24) 1981-1985
    CrossrefPubMedGoogle Scholar
  • 15 Woermann FG, Free SL, Koepp MJ, Sisodiya SM, Duncan JS. Abnormal cerebral structure in juvenile myoclonic epilepsy demonstrated with voxel-based analysis of MRI. Brain 1999; 122 (Pt 11): 2101-2108
    CrossrefPubMedGoogle Scholar
  • 16 Woermann FG, Free SL, Koepp MJ, Ashburner J, Duncan JS. Voxel-by-voxel comparison of automatically segmented cerebral gray matter--A rater-independent comparison of structural MRI in patients with epilepsy. Neuroimage 1999; 10 (04) 373-384
    CrossrefPubMedGoogle Scholar
  • 17 Kim JH, Lee JK, Koh SB. , et al. Regional grey matter abnormalities in juvenile myoclonic epilepsy: a voxel-based morphometry study. Neuroimage 2007; 37 (04) 1132-1137
    CrossrefPubMedGoogle Scholar
  • 18 Tae WS, Hong SB, Joo EY. , et al. Structural brain abnormalities in juvenile myoclonic epilepsy patients: volumetry and voxel-based morphometry. Korean J Radiol 2006; 7 (03) 162-172
    CrossrefPubMedGoogle Scholar
  • 19 Betting LE, Li LM, Lopes-Cendes I, Guerreiro MM, Guerreiro CA, Cendes F. Correlation between quantitative EEG and MRI in idiopathic generalized epilepsy. Hum Brain Mapp 2010; 31 (09) 1327-1338
    CrossrefPubMedGoogle Scholar
  • 20 Simonyan K, Tovar-Moll F, Ostuni J. , et al. Focal white matter changes in spasmodic dysphonia: a combined diffusion tensor imaging and neuropathological study. Brain 2008; 131 (Pt 2): 447-459
    CrossrefPubMedGoogle Scholar
  • 21 Gattellaro G, Minati L, Grisoli M. , et al. White matter involvement in idiopathic Parkinson disease: a diffusion tensor imaging study. Am J Neuroradiol 2009; 30 (06) 1222-1226
    CrossrefPubMedGoogle Scholar
  • 22 Basser PJ, Mattiello J, LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophys J 1994; 66 (01) 259-267
    CrossrefPubMedGoogle Scholar
  • 23 Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed 2002; 15 (7–8): 435-455
    CrossrefPubMedGoogle Scholar
  • 24 Concha L, Livy DJ, Beaulieu C, Wheatley BM, Gross DW. In vivo diffusion tensor imaging and histopathology of the fimbria-fornix in temporal lobe epilepsy. J Neurosci 2010; 30 (03) 996-1002
    CrossrefPubMedGoogle Scholar
  • 25 Kasteleijn-Nolst Trenité DG, Schmitz B, Janz D. , et al. Consensus on diagnosis and management of JME: from founder's observations to current trends. Epilepsy Behav 2013; 28 (1, Suppl 1): S87-S90
    CrossrefPubMedGoogle Scholar
  • 26 Smith SM, Jenkinson M, Woolrich MW. , et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004; 23 (Suppl. 01) S208-S219
    CrossrefPubMedGoogle Scholar
  • 27 Holmes MD, Quiring J, Tucker DM. Evidence that juvenile myoclonic epilepsy is a disorder of frontotemporal corticothalamic networks. Neuroimage 2010; 49 (01) 80-93
    CrossrefPubMedGoogle Scholar
  • 28 Savic I, Lekvall A, Greitz D, Helms G. MR spectroscopy shows reduced frontal lobe concentrations of N-acetyl aspartate in patients with juvenile myoclonic epilepsy. Epilepsia 2000; 41 (03) 290-296
    CrossrefPubMedGoogle Scholar
  • 29 Lin K, Carrete Jr H, Lin J. , et al. Magnetic resonance spectroscopy reveals an epileptic network in juvenile myoclonic epilepsy. Epilepsia 2009; 50 (05) 1191-1200
    CrossrefPubMedGoogle Scholar
  • 30 Liu M, Concha L, Beaulieu C, Gross DW. Distinct white matter abnormalities in different idiopathic generalized epilepsy syndromes. Epilepsia 2011; 52 (12) 2267-2275
    CrossrefPubMedGoogle Scholar
  • 31 Keller SS, Ahrens T, Mohammadi S. , et al. Microstructural and volumetric abnormalities of the putamen in juvenile myoclonic epilepsy. Epilepsia 2011; 52 (09) 1715-1724
    CrossrefPubMedGoogle Scholar
  • 32 Kim JH, Suh SI, Park SY. , et al. Microstructural white matter abnormality and frontal cognitive dysfunctions in juvenile myoclonic epilepsy. Epilepsia 2012; 53 (08) 1371-1378
    CrossrefPubMedGoogle Scholar
  • 33 Alexander AL, Lee JE, Lazar M, Field AS. Diffusion tensor imaging of the brain. Neurotherapeutics 2007; 4 (03) 316-329
    CrossrefPubMedGoogle Scholar
  • 34 Hagen T, Ahlhelm F, Reiche W. Apparent diffusion coefficient in vasogenic edema and reactive astrogliosis. Neuroradiology 2007; 49 (11) 921-926
    CrossrefPubMedGoogle Scholar
  • 35 O'Muircheartaigh J, Vollmar C, Barker GJ. , et al. Abnormal thalamocortical structural and functional connectivity in juvenile myoclonic epilepsy. Brain 2012; 135 (Pt 12): 3635-3644
    CrossrefPubMedGoogle Scholar
  • 36 Schmierer K, Wheeler-Kingshott CA, Boulby PA. , et al. Diffusion tensor imaging of post mortem multiple sclerosis brain. Neuroimage 2007; 35 (02) 467-477
    CrossrefPubMedGoogle Scholar
  • 37 Diehl B, Najm I, Ruggieri P. , et al. Postictal diffusion-weighted imaging for the localization of focal epileptic areas in temporal lobe epilepsy. Epilepsia 2001; 42 (01) 21-28
    CrossrefPubMedGoogle Scholar
  • 38 Dreifuss S, Vingerhoets FJ, Lazeyras F. , et al. Volumetric measurements of subcortical nuclei in patients with temporal lobe epilepsy. Neurology 2001; 57 (09) 1636-1641
    CrossrefPubMedGoogle Scholar
  • 39 Keller SS, Roberts N. Voxel-based morphometry of temporal lobe epilepsy: an introduction and review of the literature. Epilepsia 2008; 49 (05) 741-757
    CrossrefPubMedGoogle Scholar
  • 40 Seeck M, Dreifuss S, Lantz G. , et al. Subcortical nuclei volumetry in idiopathic generalized epilepsy. Epilepsia 2005; 46 (10) 1642-1645
    CrossrefPubMedGoogle Scholar
  • 41 Ikeda M. Iron overload without the C282Y mutation in patients with epilepsy. J Neurol Neurosurg Psychiatry 2001; 70 (04) 551-553
    CrossrefPubMedGoogle Scholar
  • 42 Syvertsen MR, Thuve S, Stordrange BS, Brodtkorb E. Clinical heterogeneity of juvenile myoclonic epilepsy: follow-up after an interval of more than 20 years. Seizure 2014; 23 (05) 344-348
    CrossrefPubMedGoogle Scholar
  • 43 Murthy JM, Rao CM, Meena AK. Clinical observations of juvenile myoclonic epilepsy in 131 patients: a study in South India. Seizure 1998; 7 (01) 43-47
    CrossrefPubMedGoogle Scholar
  • 44 Cvetkovska E, Panov S, Kuzmanovski I. Clinical genetic study in juvenile myoclonic epilepsy. Seizure 2014; 23 (10) 903-905
    CrossrefPubMedGoogle Scholar
  • 45 Smith Y, Raju DV, Pare JF, Sidibe M. The thalamostriatal system: a highly specific network of the basal ganglia circuitry. Trends Neurosci 2004; 27 (09) 520-527
    CrossrefPubMedGoogle Scholar
  • 46 Brown P, Marsden CD. What do the basal ganglia do?. Lancet 1998; 351 (9118): 1801-1804
    CrossrefPubMedGoogle Scholar
  • 47 O'Muircheartaigh J, Vollmar C, Barker GJ. , et al. Focal structural changes and cognitive dysfunction in juvenile myoclonic epilepsy. Neurology 2011; 76 (01) 34-40
    CrossrefPubMedGoogle Scholar
  • 48 Richardson MP, Grosse P, Allen PJ, Turner R, Brown P. BOLD correlates of EMG spectral density in cortical myoclonus: description of method and case report. Neuroimage 2006; 32 (02) 558-565
    CrossrefPubMedGoogle Scholar
  • 49 Peng SJ, Harnod T, Tsai JZ. , et al. Evaluation of subcortical grey matter abnormalities in patients with MRI-negative cortical epilepsy determined through structural and tensor magnetic resonance imaging. BMC Neurol 2014; 14: 104
    CrossrefPubMedGoogle Scholar