Electrically evoked and spontaneous neural activity in the subthalamic nucleus under general anesthesia

View More View Less
  • 1 Bionics Institute, East Melbourne;
  • | 2 Medical Bionics Department, The University of Melbourne, East Melbourne;
  • | 3 Department of Neurology, Austin Hospital, Heidelberg;
  • | 4 Department of Neurology, The Royal Melbourne Hospital, Melbourne;
  • | 5 Department of Medicine, The University of Melbourne, Parkville;
  • | 6 Department of Neurosurgery, St. Vincent’s and Austin Hospitals, Melbourne; and
  • | 7 Department of Surgery, The University of Melbourne, Heidelberg, Victoria, Australia
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $515.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $612.00
USD  $45.00
USD  $515.00
USD  $612.00
Print or Print + Online Sign in

OBJECTIVE

Deep brain stimulation (DBS) surgery is commonly performed with the patient awake to facilitate assessments of electrode positioning. However, awake neurosurgery can be a barrier to patients receiving DBS. Electrode implantation can be performed with the patient under general anesthesia (GA) using intraoperative imaging, although such techniques are not widely available. Electrophysiological features can also aid in the identification of target neural regions and provide functional evidence of electrode placement. Here we assess the presence and positional variation under GA of spontaneous beta and high-frequency oscillation (HFO) activity, and evoked resonant neural activity (ERNA), a novel evoked response localized to the subthalamic nucleus.

METHODS

ERNA, beta, and HFO were intraoperatively recorded from DBS leads comprising four individual electrodes immediately after bilateral awake implantation into the subthalamic nucleus of 21 patients with Parkinson’s disease (42 hemispheres) and after subsequent GA induction deep enough to perform pulse generator implantation. The main anesthetic agent was either propofol (10 patients) or sevoflurane (11 patients).

RESULTS

GA reduced the amplitude of ERNA, beta, and HFO activity (p < 0.001); however, ERNA amplitudes remained large in comparison to spontaneous local field potentials. Notably, a moderately strong correlation between awake ERNA amplitude and electrode distance to an “ideal” therapeutic target within dorsal STN was preserved under GA (awake: ρ = −0.73, adjusted p value [padj] < 0.001; GA: ρ = −0.69, padj < 0.001). In contrast, correlations were diminished under GA for beta (awake: ρ = −0.45, padj < 0.001; GA: ρ = −0.13, padj = 0.12) and HFO (awake: ρ = −0.69, padj < 0.001; GA: ρ = −0.33, padj < 0.001). The largest ERNA occurred at the same electrode (awake vs GA) for 35/42 hemispheres (83.3%) and corresponded closely to the electrode selected by the clinician for chronic therapy at 12 months (awake ERNA 77.5%, GA ERNA 82.5%). The largest beta amplitude occurred at the same electrode (awake vs GA) for only 17/42 (40.5%) hemispheres and 21/42 (50%) for HFO. The electrode measuring the largest awake beta and HFO amplitudes corresponded to the electrode selected by the clinician for chronic therapy at 12 months in 60% and 70% of hemispheres, respectively. However, this correspondence diminished substantially under GA (beta 20%, HFO 35%).

CONCLUSIONS

ERNA is a robust electrophysiological signal localized to the dorsal subthalamic nucleus subregion that is largely preserved under GA, indicating it could feasibly guide electrode implantation, either alone or in complementary use with existing methods.

ABBREVIATIONS

DBS = deep brain stimulation; ERNA = evoked resonant neural activity; GA = general anesthesia; HFO = high-frequency oscillation; IPG = implantable pulse generator; LFP = local field potential; MER = microelectrode recording; RMS = root mean square; STN = subthalamic nucleus.

Supplementary Materials

    • Supplemental Materials (PDF 468 KB)

Images from Minchev et al. (pp 479–488).

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $515.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $612.00
USD  $515.00
USD  $612.00
  • 1

    Chakrabarti R, Ghazanwy M, Tewari A. Anesthetic challenges for deep brain stimulation: a systematic approach. N Am J Med Sci. 2014;6(8):359369.

  • 2

    Brodsky MA, Anderson S, Murchison C, Seier M, Wilhelm J, Vederman A, Burchiel KJ. Clinical outcomes of asleep vs awake deep brain stimulation for Parkinson disease. Neurology. 2017;89(19):19441950.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Ho AL, Ali R, Connolly ID, Henderson JM, Dhall R, Stein SC, Halpern CH. Awake versus asleep deep brain stimulation for Parkinson’s disease: a critical comparison and meta-analysis. J Neurol Neurosurg Psychiatry. 2018;89(7):687691.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Paek SH, Yun JY, Song SW, Kim IK, Hwang JH, Kim JW, et al. The clinical impact of precise electrode positioning in STN DBS on three-year outcomes. J Neurol Sci. 2013;327(1-2):2531.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Okun MS, Tagliati M, Pourfar M, Fernandez HH, Rodriguez RL, Alterman RL, Foote KD. Management of referred deep brain stimulation failures: a retrospective analysis from 2 movement disorders centers. Arch Neurol. 2005;62(8):12501255.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Kim MR, Yun JY, Jeon B, Lim YH, Kim KR, Yang HJ, Paek SH. Patients’ reluctance to undergo deep brain stimulation for Parkinson’s disease. Parkinsonism Relat Disord. 2016;23:9194.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    LaHue SC, Ostrem JL, Galifianakis NB, San Luciano M, Ziman N, Wang S, et al. Parkinson’s disease patient preference and experience with various methods of DBS lead placement. Parkinsonism Relat Disord. 2017;41:2530.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Mulroy E, Robertson N, Macdonald L, Bok A, Simpson M. Patients’ perioperative experience of awake deep-brain stimulation for Parkinson disease. World Neurosurg. 2017;105:526528.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Starr PA, Martin AJ, Ostrem JL, Talke P, Levesque N, Larson PS. Subthalamic nucleus deep brain stimulator placement using high-field interventional magnetic resonance imaging and a skull-mounted aiming device: technique and application accuracy. J Neurosurg. 2010;112(3):479490.

    • Search Google Scholar
    • Export Citation
  • 10

    Burchiel KJ, McCartney S, Lee A, Raslan AM. Accuracy of deep brain stimulation electrode placement using intraoperative computed tomography without microelectrode recording. J Neurosurg. 2013;119(2):301306.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Yin Z, Luo Y, Jin Y, Yu Y, Zheng S, Duan J, et al. Is awake physiological confirmation necessary for DBS treatment of Parkinson’s disease today? A comparison of intraoperative imaging, physiology, and physiology imaging-guided DBS in the past decade. Brain Stimul. 2019;12(4):893900.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Lee PS, Weiner GM, Corson D, Kappel J, Chang YF, Suski VR, et al. Outcomes of interventional-MRI versus microelectrode recording-guided subthalamic deep brain stimulation. Front Neurol. 2018;9:241.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Ostrem JL, Ziman N, Galifianakis NB, Starr PA, Luciano MS, Katz M, et al. Clinical outcomes using ClearPoint interventional MRI for deep brain stimulation lead placement in Parkinson’s disease. J Neurosurg. 2016;124(4):908916.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Mirzadeh Z, Chapple K, Lambert M, Dhall R, Ponce FA. Validation of CT-MRI fusion for intraoperative assessment of stereotactic accuracy in DBS surgery. Mov Disord. 2014;29(14):17881795.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Telkes I, Jimenez-Shahed J, Viswanathan A, Abosch A, Ince NF. Prediction of STN-DBS electrode implantation track in Parkinson’s disease by using local field potentials. Front Neurosci. 2016;10:198.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Soares MI, Soares-Dos-Reis R, Rosas MJ, Monteiro P, Massano J. Intraoperative microelectrode recording in Parkinson’s disease subthalamic deep brain stimulation: analysis of clinical utility. J Clin Neurosci. 2019;69:104108.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Abosch A, Timmermann L, Bartley S, Rietkerk HG, Whiting D, Connolly PJ, et al. An international survey of deep brain stimulation procedural steps. Stereotact Funct Neurosurg. 2013;91(1):111.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Bour LJ, Contarino MF, Foncke EM, de Bie RM, van den Munckhof P, Speelman JD, Schuurman PR. Long-term experience with intraoperative microrecording during DBS neurosurgery in STN and GPi. Acta Neurochir (Wien). 2010;152(12):20692077.

    • Search Google Scholar
    • Export Citation
  • 19

    Krishna V, Elias G, Sammartino F, Basha D, King NK, Fasano A, et al. The effect of dexmedetomidine on the firing properties of STN neurons in Parkinson’s disease. Eur J Neurosci. 2015;42(4):20702077.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Raz A, Eimerl D, Zaidel A, Bergman H, Israel Z. Propofol decreases neuronal population spiking activity in the subthalamic nucleus of Parkinsonian patients. Anesth Analg. 2010;111(5):12851289.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Lee WW, Ehm G, Yang HJ, Song IH, Lim YH, Kim MR, et al. Bilateral deep brain stimulation of the subthalamic nucleus under sedation with propofol and fentanyl. PLoS One. 2016;11(3):e0152619.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Lettieri C, Rinaldo S, Devigili G, Pauletto G, Verriello L, Budai R, et al. Deep brain stimulation: Subthalamic nucleus electrophysiological activity in awake and anesthetized patients. Clin Neurophysiol. 2012;123(12):24062413.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Kühn AA, Kempf F, Brücke C, Gaynor Doyle L, Martinez-Torres I, Pogosyan A, et al. High-frequency stimulation of the subthalamic nucleus suppresses oscillatory β activity in patients with Parkinson’s disease in parallel with improvement in motor performance. J Neurosci. 2008;28(24):61656173.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Horn A, Neumann WJ, Degen K, Schneider GH, Kühn AA. Toward an electrophysiological “sweet spot” for deep brain stimulation in the subthalamic nucleus. Hum Brain Mapp. 2017;38(7):33773390.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Chen CC, Pogosyan A, Zrinzo LU, Tisch S, Limousin P, Ashkan K, et al. Intra-operative recordings of local field potentials can help localize the subthalamic nucleus in Parkinson’s disease surgery. Exp Neurol. 2006;198(1):214221.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Zaidel A, Spivak A, Grieb B, Bergman H, Israel Z. Subthalamic span of β oscillations predicts deep brain stimulation efficacy for patients with Parkinson’s disease. Brain. 2010;133(Pt 7):20072021.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    van Wijk BCM, Pogosyan A, Hariz MI, Akram H, Foltynie T, Limousin P, et al. Localization of beta and high-frequency oscillations within the subthalamic nucleus region. Neuroimage Clin. 2017;16:175183.

    • Search Google Scholar
    • Export Citation
  • 28

    Foffani G, Priori A, Egidi M, Rampini P, Tamma F, Caputo E, et al. 300-Hz subthalamic oscillations in Parkinson’s disease. Brain. 2003;126(Pt 10):21532163.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    López-Azcárate J, Tainta M, Rodríguez-Oroz MC, Valencia M, González R, Guridi J, et al. Coupling between beta and high-frequency activity in the human subthalamic nucleus may be a pathophysiological mechanism in Parkinson’s disease. J Neurosci. 2010;30(19):66676677.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Velly LJ, Rey MF, Bruder NJ, Gouvitsos FA, Witjas T, Regis JM, et al. Differential dynamic of action on cortical and subcortical structures of anesthetic agents during induction of anesthesia. Anesthesiology. 2007;107(2):202212.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Tsai ST, Tseng GF, Kuo CC, Chen TY, Chen SY. Sevoflurane and Parkinson’s disease: subthalamic nucleus neuronal activity and clinical outcome of deep brain stimulation. Anesthesiology. 2020;132(5):10341044.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Sinclair NC, McDermott HJ, Bulluss KJ, Fallon JB, Perera T, Xu SS, et al. Subthalamic nucleus deep brain stimulation evokes resonant neural activity. Ann Neurol. 2018;83(5):10271031.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Sinclair NC, Fallon JB, Bulluss KJ, Thevathasan W, McDermott HJ. On the neural basis of deep brain stimulation evoked resonant activity. Biomed Phys Eng Express. 2019;5(5):057001.

    • Search Google Scholar
    • Export Citation
  • 34

    Thevathasan W, Sinclair NC, Bulluss KJ, McDermott HJ. Tailoring subthalamic nucleus deep brain stimulation for Parkinson’s disease using evoked resonant neural activity. Front Hum Neurosci. 2020;14:71.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Sinclair NC, McDermott HJ, Fallon JB, Perera T, Brown P, Bulluss KJ, Thevathasan W. Deep brain stimulation for Parkinson’s disease modulates high-frequency evoked and spontaneous neural activity. Neurobiol Dis. 2019;130:104522.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Slater KD, Sinclair NC, Nelson TS, Blamey PJ, McDermott HJ. neuroBi: a highly configurable neurostimulator for a retinal prosthesis and other applications. IEEE J Transl Eng Health Med. 2015;3:3800111.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Fedorov A, Beichel R, Kalpathy-Cramer J, Finet J, Fillion-Robin JC, Pujol S, et al. 3D Slicer as an image computing platform for the Quantitative Imaging Network. Magn Reson Imaging. 2012;30(9):13231341.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Houshmand L, Cummings KS, Chou KL, Patil PG. Evaluating indirect subthalamic nucleus targeting with validated 3-tesla magnetic resonance imaging. Stereotact Funct Neurosurg. 2014;92(6):337345.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Bot M, Schuurman PR, Odekerken VJJ, Verhagen R, Contarino FM, De Bie RMA, van den Munckhof P. Deep brain stimulation for Parkinson’s disease: defining the optimal location within the subthalamic nucleus. J Neurol Neurosurg Psychiatry. 2018;89(5):493498.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Bevan MD, Magill PJ, Terman D, Bolam JP, Wilson CJ. Move to the rhythm: oscillations in the subthalamic nucleus-external globus pallidus network. Trends Neurosci. 2002;25(10):525531.

    • Search Google Scholar
    • Export Citation
  • 41

    Marmor O, Valsky D, Joshua M, Bick AS, Arkadir D, Tamir I, et al. Local vs. volume conductance activity of field potentials in the human subthalamic nucleus. J Neurophysiol. 2017;117(6):21402151.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Sinclair N, McDermott H, Xu SS, et al. Deep brain stimulation evoked resonant neural activity varies across the subthalamic nucleus. Stereotact Funct Neurosurg. 2019;97(suppl 1):159.

    • Search Google Scholar
    • Export Citation
  • 43

    Sinclair N, McDermott H, Xu SS, et al. Directional deep brain stimulation evoked resonant neural activity. Neuromodulation. 2020;23(3):e20.

Metrics

All Time Past Year Past 30 Days
Abstract Views 2085 2080 292
Full Text Views 191 191 50
PDF Downloads 241 241 65
EPUB Downloads 0 0 0