Defining the optimal target for anterior thalamic deep brain stimulation in patients with drug-refractory epilepsy

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  • 1 Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, Massachusetts;
  • 2 Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea;
  • 3 Department of Radiology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts;
  • 4 Department of Neurology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul;
  • 5 Department of Neurosurgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul; and
  • 6 Department of Health Sciences and Technology, SAIHST, Sungkyunkwan University, Seoul, Republic of Korea
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OBJECTIVE

The anterior thalamic nucleus (ATN) is a common target for deep brain stimulation (DBS) for the treatment of drug-refractory epilepsy. However, no atlas-based optimal DBS (active contacts) target within the ATN has been definitively identified. The object of this retrospective study was to analyze the relationship between the active contact location and seizure reduction to establish an atlas-based optimal target for ATN DBS.

METHODS

From among 25 patients who had undergone ATN DBS surgery for drug-resistant epilepsy between 2016 and 2018, those who had follow-up evaluations for more than 1 year were eligible for study inclusion. After an initial stimulation period of 6 months, patients were classified as responsive (≥ 50% median decrease in seizure frequency) or nonresponsive (< 50% median decrease in seizure frequency) to treatment. Stimulation parameters and/or active contact positions were adjusted in nonresponsive patients, and their responsiveness was monitored for at least 1 year. Postoperative CT scans were coregistered nonlinearly with preoperative MR images to determine the center coordinate and atlas-based anatomical localizations of all active contacts in the Montreal Neurological Institute (MNI) 152 space.

RESULTS

Nineteen patients with drug-resistant epilepsy were followed up for at least a year following bilateral DBS electrode implantation targeting the ATN. Active contacts located more adjacent to the center of gravity of the anterior half of the ATN volume, defined as the anterior center (AC), were associated with greater seizure reduction than those not in this location. Intriguingly, the initially nonresponsive patients could end up with much improved seizure reduction by adjusting the active contacts closer to the AC at the final postoperative follow-up.

CONCLUSIONS

Patients with stimulation targeting the AC may have a favorable seizure reduction. Moreover, the authors were able to obtain additional good outcomes after electrode repositioning in the initially nonresponsive patients. Purposeful and strategic trajectory planning to target this optimal region may predict favorable outcomes of ATN DBS.

ABBREVIATIONS AC = anterior center, i.e., the center of gravity of the anterior half of the ATN; AED = antiepileptic drug; ATN = anterior thalamic nucleus; DBS = deep brain stimulation; DISTAL = DBS Intrinsic Template AtLas; EVA = extraventricular approach; IPG = internal pulse generator; MNI = Montreal Neurological Institute; MTT = mammillothalamic tract; R28 = region 28; SyN = symmetric image normalization; TVA = transventricular approach.

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Contributor Notes

Correspondence Young-Min Shon: Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea. youngmin.shon@samsung.com.

INCLUDE WHEN CITING Published online May 8, 2020; DOI: 10.3171/2020.2.JNS193226.

W.G. and B.B.K. contributed equally to this work and share first authorship.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

  • 1

    Devinsky O, Vezzani A, O’Brien TJ, Epilepsy. Nat Rev Dis Primers. 2018;4:18024.

  • 2

    Kerrigan JF, Litt B, Fisher RS, Electrical stimulation of the anterior nucleus of the thalamus for the treatment of intractable epilepsy. Epilepsia. 2004;45(4):346354.

    • Search Google Scholar
    • Export Citation
  • 3

    Krishna V, King NK, Sammartino F, Anterior nucleus deep brain stimulation for refractory epilepsy: insights into patterns of seizure control and efficacious target. Neurosurgery. 2016;78(6):802811.

    • Search Google Scholar
    • Export Citation
  • 4

    Lee KJ, Shon YM, Cho CB. Long-term outcome of anterior thalamic nucleus stimulation for intractable epilepsy. Stereotact Funct Neurosurg. 2012;90(6):379385.

    • Search Google Scholar
    • Export Citation
  • 5

    Osorio I, Overman J, Giftakis J, Wilkinson SB. High frequency thalamic stimulation for inoperable mesial temporal epilepsy. Epilepsia. 2007;48(8):15611571.

    • Search Google Scholar
    • Export Citation
  • 6

    Kim SH, Lim SC, Kim J, Long-term follow-up of anterior thalamic deep brain stimulation in epilepsy: a 11-year, single center experience. Seizure. 2017;52:154161.

    • Search Google Scholar
    • Export Citation
  • 7

    Oh YS, Kim HJ, Lee KJ, Cognitive improvement after long-term electrical stimulation of bilateral anterior thalamic nucleus in refractory epilepsy patients. Seizure. 2012;21(3):183187.

    • Search Google Scholar
    • Export Citation
  • 8

    Möttönen T, Katisko J, Haapasalo J, Defining the anterior nucleus of the thalamus (ANT) as a deep brain stimulation target in refractory epilepsy: delineation using 3 T MRI and intraoperative microelectrode recording. Neuroimage Clin. 2015;7:823829.

    • Search Google Scholar
    • Export Citation
  • 9

    Lehtimäki K, Möttönen T, Järventausta K, Outcome based definition of the anterior thalamic deep brain stimulation target in refractory epilepsy. Brain Stimul. 2016;9(2):268275.

    • Search Google Scholar
    • Export Citation
  • 10

    Cukiert A, Lehtimäki K. Deep brain stimulation targeting in refractory epilepsy. Epilepsia. 2017;58(suppl 1):8084.

  • 11

    Kim SH, Son BC, Lim SC, EEG driving response during low-frequency stimulation of anterior thalamic nucleus: is it a good predictor of the correct location of DBS electrode? Clin Neurophysiol. 2014;125(5):10651066.

    • Search Google Scholar
    • Export Citation
  • 12

    Fisher RS, Velasco AL. Electrical brain stimulation for epilepsy. Nat Rev Neurol. 2014;10(5):261270.

  • 13

    Horn A, Kühn AA. Lead-DBS: a toolbox for deep brain stimulation electrode localizations and visualizations. Neuroimage. 2015;107:127135.

    • Search Google Scholar
    • Export Citation
  • 14

    Avants BB, Epstein CL, Grossman M, Gee JC. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal. 2008;12(1):2641.

    • Search Google Scholar
    • Export Citation
  • 15

    Fonov V, Evans AC, Botteron K, Unbiased average age-appropriate atlases for pediatric studies. Neuroimage. 2011;54(1):313327.

  • 16

    Schönecker T, Kupsch A, Kühn AA, Automated optimization of subcortical cerebral MR imaging-atlas coregistration for improved postoperative electrode localization in deep brain stimulation. AJNR Am J Neuroradiol. 2009;30(10):19141921.

    • Search Google Scholar
    • Export Citation
  • 17

    Husch A, V Petersen M, Gemmar P, PaCER—a fully automated method for electrode trajectory and contact reconstruction in deep brain stimulation. Neuroimage Clin. 2017;17:8089.

    • Search Google Scholar
    • Export Citation
  • 18

    Ewert S, Plettig P, Li N, Toward defining deep brain stimulation targets in MNI space: a subcortical atlas based on multimodal MRI, histology and structural connectivity. Neuroimage. 2018;170:271282.

    • Search Google Scholar
    • Export Citation
  • 19

    Hassler R. Architectonic organization of the thalamic nuclei. In: Schaltenbrand G, ed. Stereotaxy of the Human Brain. Georg Thieme Verlag; 1977.

    • Search Google Scholar
    • Export Citation
  • 20

    Chakravarty MM, Bertrand G, Hodge CP, The creation of a brain atlas for image guided neurosurgery using serial histological data. Neuroimage. 2006;30(2):359376.

    • Search Google Scholar
    • Export Citation
  • 21

    Koeppen JA, Nahravani F, Kramer M, Electrical stimulation of the anterior thalamus for epilepsy: clinical outcome and analysis of efficient target. Neuromodulation. 2019;22(4):465471.

    • Search Google Scholar
    • Export Citation
  • 22

    Herrman H, Egge A, Konglund AE, Anterior thalamic deep brain stimulation in refractory epilepsy: a randomized, double-blinded study. Acta Neurol Scand. 2019;139(3):294304.

    • Search Google Scholar
    • Export Citation
  • 23

    Lehtimäki K, Coenen VA, Gonçalves Ferreira A, The surgical approach to the anterior nucleus of thalamus in patients with refractory epilepsy: experience from the International Multicenter Registry (MORE). Neurosurgery. 2019;84(1):141150.

    • Search Google Scholar
    • Export Citation
  • 24

    Van Gompel JJ, Klassen BT, Worrell GA, Anterior nuclear deep brain stimulation guided by concordant hippocampal recording. Neurosurg Focus. 2015;38(6):E9.

    • Search Google Scholar
    • Export Citation
  • 25

    Wang YC, Grewal SS, Middlebrooks EH, Targeting analysis of a novel parietal approach for deep brain stimulation of the anterior nucleus of the thalamus for epilepsy. Epilepsy Res. 2019;153:16.

    • Search Google Scholar
    • Export Citation
  • 26

    Nowinski WL, Liu J, Arumugam T. Quantification and visualization of three-dimensional inconsistency of the globus pallidus internus in the Schaltenbrand-Wahren brain atlas. Stereotact Funct Neurosurg. 2006;84(5-6):236242.

    • Search Google Scholar
    • Export Citation
  • 27

    Nowinski WL, Liu J, Thirunavuukarasuu A. Quantification and visualization of the three-dimensional inconsistency of the subthalamic nucleus in the Schaltenbrand-Wahren brain atlas. Stereotact Funct Neurosurg. 2006;84(1):4655.

    • Search Google Scholar
    • Export Citation
  • 28

    Nowinski WL, Liu J, Thirunavuukarasuu A. Quantification and visualization of three-dimensional inconsistency of the ventrointermediate nucleus of the thalamus in the Schaltenbrand-Wahren brain atlas. Acta Neurochir (Wien). 2008;150(7):647653.

    • Search Google Scholar
    • Export Citation
  • 29

    Harston GW, Minks D, Sheerin F, Optimizing image registration and infarct definition in stroke research. Ann Clin Transl Neurol. 2017;4(3):166174.

    • Search Google Scholar
    • Export Citation
  • 30

    Woods RP, Grafton ST, Watson JD, Automated image registration: II. Intersubject validation of linear and nonlinear models. J Comput Assist Tomogr. 1998;22(1):153165.

    • Search Google Scholar
    • Export Citation
  • 31

    Gloor P, Guberman AH. The temporal lobe & limbic system. CMAJ. 1997;157:15971598.

  • 32

    Hirai T, Jones EG. A new parcellation of the human thalamus on the basis of histochemical staining. Brain Res Brain Res Rev. 1989;14(1):134.

    • Search Google Scholar
    • Export Citation
  • 33

    Schaltenbrand G, Wahren W. Atlas for Stereotaxy of the Human Brain. Georg Thieme Verlag; 1977.

  • 34

    Mai JK, Majtanik M. Toward a common terminology for the thalamus. Front Neuroanat. 2019;12:114.

  • 35

    Mirski MA, Ferrendelli JA. Anterior thalamic mediation of generalized pentylenetetrazol seizures. Brain Res. 1986;399(2):212223.

  • 36

    Mirski MA, McKeon AC, Ferrendelli JA. Anterior thalamus and substantia nigra: two distinct structures mediating experimental generalized seizures. Brain Res. 1986;397(2):377380.

    • Search Google Scholar
    • Export Citation
  • 37

    Mirski MA, Rossell LA, Terry JB, Fisher RS. Anticonvulsant effect of anterior thalamic high frequency electrical stimulation in the rat. Epilepsy Res. 1997;28(2):89100.

    • Search Google Scholar
    • Export Citation
  • 38

    Le Gros Clark WE, Boggon RH. On the connections of the anterior nucleus of the thalamus. J Anat. 1933;67(Pt 2):215226.9.

  • 39

    See AAQ, King NKK. Improving surgical outcome using diffusion tensor imaging techniques in deep brain stimulation. Front Surg. 2017;4:54.

    • Search Google Scholar
    • Export Citation
  • 40

    Mueller SG, Laxer KD, Barakos J, Involvement of the thalamocortical network in TLE with and without mesiotemporal sclerosis. Epilepsia. 2010;51(8):14361445.

    • Search Google Scholar
    • Export Citation

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