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Journal of Neurology

, Volume 263, Issue 10, pp 2120–2126 | Cite as

Thalamic interictal epileptiform discharges in deep brain stimulated epilepsy patients

  • Catherine M. Sweeney-ReedEmail author
  • Harim Lee
  • Stefan Rampp
  • Tino Zaehle
  • Lars Buentjen
  • Juergen Voges
  • Martin Holtkamp
  • Hermann Hinrichs
  • Hans-Jochen Heinze
  • Friedhelm C. SchmittEmail author
Original Communication

Abstract

The relationships between interictal epileptiform discharges (IEDs) in the anterior (ANT) and dorsomedial nuclei (DMNT) of the thalamus and electro-clinical parameters in pharmacoresistant focal epilepsy patients receiving intrathalamic electrodes for deep brain stimulation (DBS) were investigated. Thalamus-localized IEDs (LIEDs) and surface EEG (sEEG)-IEDs were evaluated in eight patients who underwent ANT-DBS. Occurrence and frequency of ANT- and DMNT-LIEDs and pre-operative sEEG-IEDs were examined with respect to seizure onset location and seizure outcome following ANT-DBS. LIEDs were identified in all eight patients, in the ANT, DMNT, or both. ANT-LIEDs were observed in all patients with an unequivocal temporal seizure onset zone. The ANT-LIED frequency correlated with pre-surgical sEEG-IED frequency (ρ = 0.76, p = 0.033) and predicted ANT-DBS responsiveness (T = −2.6; p = 0.0428). Of the five patients with bilateral sEEG-IEDs, all had ANT-LIEDs, but only one patient had DMNT-LIEDs. All patients with no or unilateral sEEG-IEDs had DMNT-LIEDs. Observation of LIEDS in the ANT and DMNT supports the hypothesis that these nuclei are involved in propagation of focal epileptic activity. Their correspondence with differing electro-clinical features suggests that these nuclei are functionally distinguishable nodes within the epileptic networks of individual patients.

Keywords

Anterior nucleus of the thalamus Dorsomedial nucleus of the thalamus Refractory epilepsy Deep brain stimulation Interictal epileptiform discharges 

Notes

Acknowledgments

H.-B. Straub, K. Bohlmann (Epilepsy-Center Berlin-Brandenburg, Germany), A. Kowski (Department of Neurology, Charité-Universitätsmedizin Berlin, Germany), and T. Mayer (Saxon Epilepsy-Center, Germany) supported patient recruitment.

Compliance with ethical standards

Conflicts of interest

The study was funded by departmental funding from the University Clinic for Neurology, Magdeburg. Prof. Voges served as consultant for Medtronic and Sapiens Inc.; Prof. Holtkamp holds the “Friedrich-von-Bodelschwingh endowed Professorship for Clinical and Experimental Epileptology” at the ChariteUniversitaetsmedizin Berlin funded by von Bodelschwingh Foundation, Dr. Schmitt and Prof. Voges have received reimbursement for traveling expenses and/or speaker honoraria from Medtronic Inc. The remaining authors have no conflicts of interest.

Ethical standard

Data collection was approved by the Local Ethics Committee of the Otto von Guericke University, Magdeburg and has therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. All patients provided prior informed written consent.

Supplementary material

415_2016_8246_MOESM1_ESM.pdf (67 kb)
Online Resource 1 Additional clinical information. Pt = patient; M = male; F = female; HS = hippocampal sclerosis; * after temporal lobectomy; LTG = lamotrigine; LCM = lacosamide; RTG = retigabine; STP = stiripentol; OXC = oxcarbazepine; CLB = clobazepam; CBZ = carbamazepine; PHT = phenytoin; ZNS = zonisamid; LEV = levetiracetam (PDF 67 kb)
415_2016_8246_MOESM2_ESM.pdf (67 kb)
Online Resource 2 Electrode coordinates depicted for Patient 5 in Fig. 1. To determine the z-axis coordinates of the locations indicated by the crosshairs, a distortion factor (d-z = 1.1) was calculated between the thalamus height in the individual brain and that in the Morel atlas [19]. Uncorrected data are provided in parentheses. The same procedure was performed for the y-axis values by comparing the intercommisural line lengths (d-ACPC = 1.16). All values were rounded in 0.5 mm steps, and the coordinates were projected onto the closest slice provided by the Morel atlas. AC–PC = anterior and posterior commissural points, referring to the shortest intraventricular distance between the commissures, used as a reference system for stereotactic coordinates [18]. MC = mid-commissural level (PDF 67 kb)

References

  1. 1.
    Picot MC, Baldy-Moulinier M, Daurès JP et al (2008) The prevalence of epilepsy and pharmacoresistant epilepsy in adults: a population-based study in a Western European country. Epilepsia 49:1230–1238. doi: 10.1111/j.1528-1167.2008.01579.x CrossRefPubMedGoogle Scholar
  2. 2.
    Bien C, Raabe A, Schramm J et al (2013) Trends in presurgical evaluation and surgical treatment of epilepsy at one centre from 1988–2009. J Neurol Neurosurg Psychiatry 84:54–61. doi: 10.1136/jnnp-2011-301763 CrossRefPubMedGoogle Scholar
  3. 3.
    Lee KJ, Jang KS, Shon YM (2006) Chronic deep brain stimulation of subthalamic and anterior thalamic nuclei for controlling refractory partial epilepsy. Acta Neurochir Suppl. doi: 10.1007/978-3-211-35205-2-17 Google Scholar
  4. 4.
    Fisher R, Salanova V, Witt T et al (2010) Electrical stimulation of the anterior nucleus of thalamus for treatment of refractory epilepsy. Epilepsia 51:899–908. doi: 10.1111/j.1528-1167.2010.02536.x CrossRefPubMedGoogle Scholar
  5. 5.
    Kerrigan JF, Litt B, Fisher RS et al (2004) Electrical stimulation of the anterior nucleus of the thalamus for the treatment of intractable epilepsy. Epilepsia 45:346–354. doi: 10.1111/j.0013-9580.2004.01304.x CrossRefPubMedGoogle Scholar
  6. 6.
    Lim S-N, Lee S-T, Tsai Y-T et al (2007) Electrical stimulation of the anterior nucleus of the thalamus for intractable epilepsy: a long-term follow-up study. Epilepsia 48:342–347. doi: 10.1111/j.1528-1167.2006.00898.x CrossRefPubMedGoogle Scholar
  7. 7.
    Andrade D, Zumsteg D, Hamani C et al (2006) Long-term follow-up of patients with thalamic deep brain stimulation for epilepsy. Neurology 66:1571–1573CrossRefPubMedGoogle Scholar
  8. 8.
    Salanova V, Witt T, Worth R et al (2015) Long-term efficacy and safety of thalamic stimulation for drug-resistant partial epilepsy. Neurology 84:1017–1025. doi: 10.1212/WNL.0000000000001334 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Mirski MA, Rossell LA, Terry JB, Fisher RS (1997) Anticonvulsant effect of anterior thalamic high frequency electrical stimulation in the rat. Epilepsy Res 28:89–100. doi: 10.1016/S0920-1211(97)00034-X CrossRefPubMedGoogle Scholar
  10. 10.
    Lee KJ, Shon YM, Cho CB (2012) Long-term outcome of anterior thalamic nucleus stimulation for intractable epilepsy. Stereotact Funct Neurosurg 90:379–385. doi: 10.1159/000339991 CrossRefPubMedGoogle Scholar
  11. 11.
    Zhang DX, Bertram EH (2015) Suppressing limbic seizures by stimulating medial dorsal thalamic nucleus: factors for efficacy. Epilepsia 56:479–488. doi: 10.1111/epi.12916 CrossRefPubMedGoogle Scholar
  12. 12.
    Bertram EH, Mangan PS, Zhang D et al (2001) The midline thalamus: alterations and a potential role in limbic epilepsy. Epilepsia 42:967–978. doi: 10.1046/j.1528-1157.2001.042008967.x CrossRefPubMedGoogle Scholar
  13. 13.
    Cassidy RM, Gale K (1998) Mediodorsal thalamus plays a critical role in the development of limbic motor seizures. J Neurosci 18:9002–9009PubMedGoogle Scholar
  14. 14.
    Zumsteg D, Lozano AM, Wennberg RA (2006) Rhythmic cortical EEG synchronization with low frequency stimulation of the anterior and medial thalamus for epilepsy. Clin Neurophysiol 117:2272–2278. doi: 10.1016/j.clinph.2006.06.707 CrossRefPubMedGoogle Scholar
  15. 15.
    Osorio I, Frei MG, Lozano AM, Wennberg R (2015) Subcortical (thalamic) automated seizure detection: a new option for contingent therapy delivery. Epilepsia 56:e156–e160. doi: 10.1111/epi.13124 CrossRefPubMedGoogle Scholar
  16. 16.
    Buentjen L, Kopitzki K, Schmitt FC et al (2014) Direct targeting of the thalamic anteroventral nucleus for deep brain stimulation by T1-weighted magnetic resonance imaging at 3 T. Stereotact Funct Neurosurg 92:25–30. doi: 10.1159/000351525 CrossRefPubMedGoogle Scholar
  17. 17.
    Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19:1233–1239. doi: 10.1016/S1053-8119(03)00169-1 CrossRefPubMedGoogle Scholar
  18. 18.
    Schaltenbrand G, Wahren W (1977) Atlas for stereotaxy of the human brain. Thieme Medical Publishers, New YorkGoogle Scholar
  19. 19.
    Morel A (2007) Stereotactic atlas of the human thalamus and basal ganglia. CRC Press, New YorkCrossRefGoogle Scholar
  20. 20.
    Sweeney-Reed CM, Zaehle T, Voges J et al (2014) Corticothalamic phase synchrony and cross-frequency coupling predict human memory formation. Elife. doi: 10.7554/eLife.05352 PubMedPubMedCentralGoogle Scholar
  21. 21.
    Sweeney-Reed CM, Zaehle T, Voges J et al (2016) Pre-stimulus thalamic theta power predicts human memory formation. Neuroimage 138:100–108. doi: 10.1016/j.neuroimage.2016.05.042 CrossRefPubMedGoogle Scholar
  22. 22.
    Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Earlbaum Associates, HillsdaleGoogle Scholar
  23. 23.
    Krendl R, Lurger S, Baumgartner C (2008) Absolute spike frequency predicts surgical outcome in TLE with unilateral hippocampal atrophy. Neurology 71:413–418. doi: 10.1212/01.wnl.0000310775.87331.90 CrossRefPubMedGoogle Scholar
  24. 24.
    Vertes RP, Albo Z, Viana di Prisco G (2001) Theta-rhythmically firing neurons in the anterior thalamus: implications for mnemonic functions of Papez’s circuit. Neuroscience 104:619–625. doi: 10.1016/S0306-4522(01)00131-2 CrossRefPubMedGoogle Scholar
  25. 25.
    Papez JW (1937) A proposed mechanism of emotions. Arch Neurol Psychiatry 38:725–743. doi: 10.1001/archneurpsyc.1937.02260220069003 CrossRefGoogle Scholar
  26. 26.
    Stillova K, Jurak P, Chladek J et al (2015) The role of anterior nuclei of the thalamus: a subcortical gate in memory processing: an intracerebral recording study. PLoS One 10:1–13. doi: 10.1371/journal.pone.0140778 CrossRefGoogle Scholar
  27. 27.
    Zumsteg D, Lozano AM, Wieser HG, Wennberg RA (2006) Cortical activation with deep brain stimulation of the anterior thalamus for epilepsy. Clin Neurophysiol 117:192–207. doi: 10.1016/j.clinph.2005.09.015 CrossRefPubMedGoogle Scholar
  28. 28.
    Lega BC, Halpern CH, Jaggi JL, Baltuch GH (2010) Deep brain stimulation in the treatment of refractory epilepsy: update on current data and future directions. Neurobiol Dis 38:354–360. doi: 10.1016/j.nbd.2009.07.007 CrossRefPubMedGoogle Scholar
  29. 29.
    Zumsteg D, Lozano AM, Wennberg RA (2006) Mesial temporal inhibition in a patient with deep brain stimulation of the anterior thalamus for epilepsy. Epilepsia 47:1958–1962. doi: 10.1111/j.1528-1167.2006.00824.x CrossRefPubMedGoogle Scholar
  30. 30.
    Hodaie M, Wennberg RA, Dostrovsky JO, Lozano AM (2002) Chronic anterior thalamus stimulation for intractable epilepsy. Epilepsia 43:603–608. doi: 10.1046/j.1528-1157.2002.26001.x CrossRefPubMedGoogle Scholar
  31. 31.
    Rektor I, Doležalová I, Chrastina J et al (2016) High-frequency oscillations in the human anterior nucleus of the thalamus. Brain Stimul. doi: 10.1016/j.brs.2016.04.010 PubMedGoogle Scholar
  32. 32.
    Aggleton JP (2012) Multiple anatomical systems embedded within the primate medial temporal lobe: implications for hippocampal function. Neurosci Biobehav Rev 36:1579–1596. doi: 10.1016/j.neubiorev.2011.09.005 CrossRefPubMedGoogle Scholar
  33. 33.
    Guye M, Régis J, Tamura M et al (2006) The role of corticothalamic coupling in human temporal lobe epilepsy. Brain 129:1917–1928. doi: 10.1093/brain/awl151 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Catherine M. Sweeney-Reed
    • 1
    Email author
  • Harim Lee
    • 1
  • Stefan Rampp
    • 2
  • Tino Zaehle
    • 1
  • Lars Buentjen
    • 3
  • Juergen Voges
    • 3
    • 4
  • Martin Holtkamp
    • 5
  • Hermann Hinrichs
    • 1
    • 4
    • 6
  • Hans-Jochen Heinze
    • 1
    • 4
    • 6
  • Friedhelm C. Schmitt
    • 1
    Email author
  1. 1.Department of NeurologyOtto-von-Guericke UniversityMagdeburgGermany
  2. 2.Department of NeurosurgeryUniversity Hospital ErlangenErlangenGermany
  3. 3.Department of Stereotactic NeurosurgeryOtto-von-Guericke UniversityMagdeburgGermany
  4. 4.Leibniz Institute for NeurobiologyMagdeburgGermany
  5. 5.Department of Neurology, Epilepsy-Center Berlin-BrandenburgCharité-Universitätsmedizin BerlinBerlinGermany
  6. 6.German Center for Neurodegenerative Diseases (DZNE)MagdeburgGermany

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