Top

Published in:

08-03-2024 | Somatosensory Evoked Potential | Neurology and Preclinical Neurological Studies - Original Article

Somatosensory evoked potentials recorded from DBS electrodes: the origin of subcortical N18

Authors: Arif Abdulbaki, Johannes C. Wöhrle, Christian Blahak, Ralf Weigel, Katja Kollewe, H. Holger Capelle, Hansjörg Bäzner, Joachim K. Krauss

Published in: Journal of Neural Transmission | Issue 4/2024

Abstract

The different peaks of somatosensory-evoked potentials (SEP) originate from a variety of anatomical sites in the central nervous system. The origin of the median nerve subcortical N18 SEP has been studied under various conditions, but the exact site of its generation is still unclear. While it has been claimed to be located in the thalamic region, other studies indicated its possible origin below the pontomedullary junction. Here, we scrutinized and compared SEP recordings from median nerve stimulation through deep brain stimulation (DBS) electrodes implanted in various subcortical targets. We studied 24 patients with dystonia, Parkinson’s disease, and chronic pain who underwent quadripolar electrode implantation for chronic DBS and recorded median nerve SEPs from globus pallidus internus (GPi), subthalamic nucleus (STN), thalamic ventral intermediate nucleus (Vim), and ventral posterolateral nucleus (VPL) and the centromedian–parafascicular complex (CM-Pf). The largest amplitude of the triphasic potential of the N18 complex was recorded in Vim. Bipolar recordings confirmed the origin to be close to Vim electrodes (and VPL/CM-Pf) and less close to STN electrodes. GPi recorded only far-field potentials in unipolar derivation. Recordings from DBS electrodes located in different subcortical areas allow determining the origin of certain subcortical SEP waves more precisely. The subcortical N18 of the median nerve SEP—to its largest extent—is generated ventral to the Vim in the region of the prelemniscal radiation/ zona incerta.

Abdallat M, Saryyeva A, Blahak C, Wolf ME, Weigel R, Loher TJ, Runge J, Heissler HE, Kinfe TM, Krauss JK (2021) Centromedian-parafascicular and somatosensory thalamic deep brain stimulation for treatment of chronic neuropathic pain: a contemporary series of 40 patients. Biomedicines 9(7):731. https://doi.org/10.3390/biomedicines9070731CrossRefPubMedPubMedCentral

Albe-Fessard D, Tasker R, Yamashiro K, Chodakiewitz J, Dostrovsky J (1986) Comparison in man of short latency averaged evoked potentials recorded in thalamic and scalp hand zones of representation. Electroencephalogr Clin Neurophysiol 65(6):405–415. https://doi.org/10.1016/0168-5597(86)90020-1CrossRefPubMed

Beck AK, Lütjens G, Schwabe K, Dengler R, Krauss JK, Sandmann P (2018) Thalamic and basal ganglia regions are involved in attentional processing of behaviorally significant events: evidence from simultaneous depth and scalp EEG. Brain Struct Funct 223(1):461–474. https://doi.org/10.1007/s00429-017-1506-zCrossRefPubMed

Beck AK, Sandmann P, Dürschmid S, Schwabe K, Saryyeva A, Krauss JK (2020) Neuronal activation in the human centromedian-parafascicular complex predicts cortical responses to behaviorally significant auditory events. Neuroimage 1(211):116583. https://doi.org/10.1016/j.neuroimage.2020.116583CrossRef

Birk P, Struppler A (1989) Functional neuroanatomy of the target area for the treatment of pathological tremor: an electrophysiological approach. Stereotact Funct Neurosurg 52(2–4):164–170. https://doi.org/10.1159/000099497CrossRefPubMed

Celesia GG (1979) Somatosensory evoked potentials recorded directly from human thalamus and Sm I cortical area. Arch Neurol 36(7):399–405. https://doi.org/10.1001/archneur.1979.00500430029003CrossRefPubMed

Deuschl G, Antonini A, Costa J, Śmiłowska K, Berg D, Corvol JC, Fabbrini G, Ferreira J, Foltynie T, Mir P, Schrag A, Seppi K, Taba P, Ruzicka E, Selikhova M, Henschke N, Villanueva G, Moro E (2022) European academy of neurology/movement disorder society-European section guideline on the treatment of Parkinson’s disease: I. Invasive therapies. Mov Disord 37(7):1360–1374. https://doi.org/10.1002/mds.29066CrossRefPubMed

Hanajima R, Dostrovsky JO, Lozano AM, Hutchison WD, Davis KD, Chen R, Ashby P (2004) Somatosensory evoked potentials (SEPs) recorded from deep brain stimulation (DBS) electrodes in the thalamus and subthalamic nucleus (STN). Clin Neurophysiol 115(2):424–434. https://doi.org/10.1016/j.clinph.2003.09.027CrossRefPubMed

Hashimoto I (1984) Somatosensory evoked potentials from the human brain-stem: origins of short latency potentials. Electroencephalogr Clin Neurophysiol 57(3):221–227. https://doi.org/10.1016/0013-4694(84)90123-8CrossRefPubMed

Insola A, Rossi S, Mazzone P, Pasqualetti P (1999) Parallel processing of sensory inputs: an evoked potentials study in Parkinsonian patients implanted with thalamic stimulators. Clin Neurophysiol 110(1):146–151. https://doi.org/10.1016/s0168-5597(98)00055-0CrossRefPubMed

Katayama Y, Tsubokawa T (1987) Somatosensory evoked potentials from the thalamic sensory relay nucleus (VPL) in humans: correlations with short latency somatosensory evoked potentials recorded at the scalp. Electroencephalogr Clin Neurophysiol 68(3):187–201. https://doi.org/10.1016/0168-5597(87)90026-8CrossRefPubMed

Kitagawa M, Murata J, Uesugi H, Hanajima R, Ugawa Y, Saito H (2007) Characteristics and distribution of somatosensory evoked potentials in the subthalamic region. J Neurosurg 107(3):548–554. https://doi.org/10.3171/JNS-07/09/0548CrossRefPubMed

Klostermann F, Vesper J, Curio G (2003) Identification of target areas for deep brain stimulation in human basal ganglia substructures based on median nerve sensory evoked potential criteria. J Neurol Neurosurg Psychiatry 74(8):1031–1035. https://doi.org/10.1136/jnnp.74.8.1031CrossRefPubMedPubMedCentral

Krauss JK, Lipsman N, Aziz T, Boutet A, Brown P, Chang JW, Davidson B, Grill WM, Hariz MI, Horn A, Schulder M, Mammis A, Tass PA, Volkmann J, Lozano AM (2021) Technology of deep brain stimulation: current status and future directions. Nat Rev Neurol 17(2):75–87. https://doi.org/10.1038/s41582-020-00426-zCrossRefPubMed

Lozano AM, Lipsman N, Bergman H, Brown P, Chabardes S, Chang JW, Matthews K, McIntyre CC, Schlaepfer TE, Schulder M, Temel Y, Volkmann J, Krauss JK (2019) Deep brain stimulation: current challenges and future directions. Nat Rev Neurol 15(3):148–160. https://doi.org/10.1038/s41582-018-0128-2CrossRefPubMedPubMedCentral

Morioka T, Shima F, Kato M, Fukui M (1989) Origin and distribution of thalamic somatosensory evoked potentials in humans. Electroencephalogr Clin Neurophysiol 74(3):186–193. https://doi.org/10.1016/0013-4694(89)90004-7CrossRefPubMed

Moro E, LeReun C, Krauss JK, Albanese A, Lin JP, Walleser Autiero S, Brionne TC, Vidailhet M (2017) Efficacy of pallidal stimulation in isolated dystonia: a systematic review and meta-analysis. Eur J Neurol 24(4):552–560. https://doi.org/10.1111/ene.13255CrossRefPubMedPubMedCentral

Passmore SR, Murphy B, Lee TD (2014) The origin, and application of somatosensory evoked potentials as a neurophysiological technique to investigate neuroplasticity. J Can Chiropr Assoc 58(2):170–183PubMedPubMedCentral

Pesenti A, Priori A, Locatelli M, Egidi M, Rampini P, Tamma F, Caputo E, Chiesa V, Barbieri S (2003) Subthalamic somatosensory evoked potentials in Parkinson’s disease. Mov Disord 18(11):1341–1345. https://doi.org/10.1002/mds.10519CrossRefPubMed

Rezaei A, Lahtinen J, Neugebauer F, Antonakakis M, Piastra MC, Koulouri A, Wolters CH, Pursiainen S (2021) Reconstructing subcortical and cortical somatosensory activity via the RAMUS inverse source analysis technique using median nerve SEP data. Neuroimage 15(245):118726. https://doi.org/10.1016/j.neuroimage.2021.118726CrossRef

Runge J, Cassini Ascencao L, Blahak C, Kinfe TM, Schrader C, Wolf ME, Saryyeva A, Krauss JK (2021) Deep brain stimulation in patients on chronic antiplatelet or anticoagulation treatment. Acta Neurochir (wien) 163(10):2825–2831. https://doi.org/10.1007/s00701-021-04931-yCrossRefPubMed

Runge J, Nagel JM, Cassini Ascencao L, Blahak C, Kinfe TM, Schrader C, Wolf ME, Saryyeva A, Krauss JK (2022) Are transventricular approaches associated with increased hemorrhage? A comparative study in a series of 624 deep brain stimulation surgeries. Oper Neurosurg (hagerstown) 23(2):e108–e113. https://doi.org/10.1227/ons.0000000000000275CrossRefPubMed

Schuepbach WM, Rau J, Knudsen K, Volkmann J, Krack P, Timmermann L, Hälbig TD, Hesekamp H, Navarro SM, Meier N, Falk D, Mehdorn M, Paschen S, Maarouf M, Barbe MT, Fink GR, Kupsch A, Gruber D, Schneider GH, Seigneuret E, Kistner A, Chaynes P, Ory-Magne F, Brefel Courbon C, Vesper J, Schnitzler A, Wojtecki L, Houeto JL, Bataille B, Maltête D, Damier P, Raoul S, Sixel-Doering F, Hellwig D, Gharabaghi A, Krüger R, Pinsker MO, Amtage F, Régis JM, Witjas T, Thobois S, Mertens P, Kloss M, Hartmann A, Oertel WH, Post B, Speelman H, Agid Y, Schade-Brittinger C, Deuschl G, EARLYSTIM Study Group (2013) Neurostimulation for Parkinson’s disease with early motor complications. N Engl J Med 368(7):610–622. https://doi.org/10.1056/NEJMoa1205158CrossRefPubMed

Sheth SA, Mayberg HS (2023) Deep brain stimulation for obsessive-compulsive disorder and depression. Annu Rev Neurosci 10(46):341–358. https://doi.org/10.1146/annurev-neuro-110122-110434CrossRef

Sonoo M, Genba K, Zai W, Iwata M, Mannen T, Kanazawa I (1992) Origin of the widespread N18 in median nerve SEP. Electroencephalogr Clin Neurophysiol 84(5):418–425. https://doi.org/10.1016/0168-5597(92)90028-aCrossRefPubMed

Suzuki I, Mayanagi Y (1984) Intracranial recording of short latency somatosensory evoked potentials in man: identification of origin of each component. Electroencephalogr Clin Neurophysiol 59(4):286–296. https://doi.org/10.1016/0168-5597(84)90046-7CrossRefPubMed

Taira T, Amano K, Kawamura H, Tanikawa T, Kawabatake H, Notani M, Iseki H, Shiwaku T, Nagao T, Iwata Y et al (1987) Short latency somatosensory-evoked potentials–direct recording from the human midbrain and thalamus. Acta Neurochir Suppl (wien) 39:170–173. https://doi.org/10.1007/978-3-7091-8909-2_45CrossRefPubMed

Tomberg C, Desmedt JE, Ozaki I, Noël P (1991) Nasopharyngeal recordings of somatosensory evoked potentials document the medullary origin of the N18 far-field. Electroencephalogr Clin Neurophysiol 80(6):496–503. https://doi.org/10.1016/0168-5597(91)90131-gCrossRefPubMed

Trenado C, Elben S, Friggemann L, Gruhn S, Groiss SJ, Vesper J, Schnitzler A, Wojtecki L (2017) Long-latency somatosensory evoked potentials of the subthalamic nucleus in patients with Parkinson’s disease. PLoS ONE 12(1):e0168151. https://doi.org/10.1371/journal.pone.0168151CrossRefPubMedPubMedCentral

Trenado C, Elben S, Friggemann L, Groiss SJ, Vesper J, Schnitzler A, Wojtecki L (2018) Intraoperative localization of the subthalamic nucleus using long-latency somatosensory evoked potentials. Neuromodulation 21(6):582–587. https://doi.org/10.1111/ner.12727CrossRefPubMed

Tsuji S, Shibasaki H, Kato M, Kuroiwa Y, Shima F (1984) Subcortical, thalamic and cortical somatosensory evoked potentials to median nerve stimulation. Electroencephalogr Clin Neurophysiol 59(6):465–476. https://doi.org/10.1016/0168-5597(84)90005-4CrossRefPubMed

Valls-Solé J, Compta Y, Costa J, Valldeoriola F, Rumià J (2008) Human central nervous system circuits examined through the electrodes implanted for deep brain stimulation. Clin Neurophysiol 119(6):1219–1231. https://doi.org/10.1016/j.clinph.2007.12.020CrossRefPubMed

Woehrle JC, Blahak C, Kekelia K, Capelle HH, Baezner H, Grips E, Weigel R, Krauss JK (2009) Chronic deep brain stimulation for segmental dystonia. Stereotact Funct Neurosurg 87(6):379–384. https://doi.org/10.1159/000249819CrossRefPubMed

Title: Somatosensory evoked potentials recorded from DBS electrodes: the origin of subcortical N18
Authors: Arif Abdulbaki
Johannes C. Wöhrle
Christian Blahak
Ralf Weigel
Katja Kollewe
H. Holger Capelle
Hansjörg Bäzner
Joachim K. Krauss
Publication date: 08-03-2024
Publisher: Springer Vienna
Keywords: Somatosensory Evoked Potential
Somatosensory Evoked Potential
Deep Brain Stimulation
Dystonia
Parkinson's Disease
Published in: Journal of Neural Transmission / Issue 4/2024
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI: https://doi.org/10.1007/s00702-024-02752-8

At a glance: The STEP trials

Springer Medicine

Somatosensory evoked potentials recorded from DBS electrodes: the origin of subcortical N18

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2024

High-dose glucocorticoids in COVID-19 patients with acute encephalopathy: clinical and imaging findings in a retrospective cohort study

Correlation between the MNCD classification-based staging of Parkinson’s disease and quality of life: a cross-sectional study

Association between autonomic dysfunction with motor and non-motor symptoms in patients with Parkinson's disease

More than fear? Brain activation patterns of dental phobic patients before and after an exposure-based treatment

Prof. DDr. Gregor K. Wenning (1964–2024)

Mild cognitive impairment in Huntington’s disease: challenges and outlooks