Microelectrode recording findings within the tractography-defined ventral intermediate nucleus

Nicolas Kon Kam King Division of Neurosurgery, Department of Surgery, University of Toronto;
Department of Neurosurgery, National Neuroscience Institute, Singapore; and

Search for other papers by Nicolas Kon Kam King in
Current site
Google Scholar
PubMed
Close
 FRCSEd(SN), PhD
,
Vibhor Krishna Division of Neurosurgery, Department of Surgery, University of Toronto;
Center for Neuromodulation, Department of Neurosurgery, The Ohio State University, Columbus, Ohio

Search for other papers by Vibhor Krishna in
Current site
Google Scholar
PubMed
Close
 MD
,
Diellor Basha Department of Physiology, Toronto Western Hospital, University of Toronto, Ontario, Canada;

Search for other papers by Diellor Basha in
Current site
Google Scholar
PubMed
Close
 BS
,
Gavin Elias Division of Neurosurgery, Department of Surgery, University of Toronto;

Search for other papers by Gavin Elias in
Current site
Google Scholar
PubMed
Close
 BA
,
Francesco Sammartino Division of Neurosurgery, Department of Surgery, University of Toronto;

Search for other papers by Francesco Sammartino in
Current site
Google Scholar
PubMed
Close
 MD
,
Mojgan Hodaie Division of Neurosurgery, Department of Surgery, University of Toronto;
Division of Brain Imaging, Behaviour Systems Neuroscience, Toronto Western Research Institute;

Search for other papers by Mojgan Hodaie in
Current site
Google Scholar
PubMed
Close
 MD
,
Andres M. Lozano Division of Neurosurgery, Department of Surgery, University of Toronto;

Search for other papers by Andres M. Lozano in
Current site
Google Scholar
PubMed
Close
 MD, PhD
, and
William D. Hutchison Department of Physiology, Toronto Western Hospital, University of Toronto, Ontario, Canada;

Search for other papers by William D. Hutchison in
Current site
Google Scholar
PubMed
Close
 PhD
Restricted access

Purchase Now

USD  $45.00

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

USD  $536.00

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

USD  $636.00
USD  $45.00
USD  $536.00
USD  $636.00
Print or Print + Online Sign in

OBJECTIVE

The ventral intermediate nucleus (VIM) of the thalamus is not visible on structural MRI. Therefore, direct VIM targeting methods for stereotactic tremor surgery are desirable. The authors previously described a direct targeting method for visualizing the VIM and its structural connectivity using deterministic tractography. In this combined electrophysiology and imaging study, the authors investigated the electrophysiology within this tractography-defined VIM (T-VIM).

METHODS

Thalamic neurons were classified based on their relative location to the T-VIM: dorsal, within, and ventral to the T-VIM. The authors identified the movement-responsive cells (kinesthetic and tremor cells), performed spike analysis (firing rate and burst index), and local field potential analysis (area under the curve for 13–30 Hz). Tremor efficacy in response to microstimulation along the electrode trajectory was also assessed in relation to the T-VIM.

RESULTS

Seventy-three cells from a total of 9 microelectrode tracks were included for this analysis. Movement-responsive cells (20 kinesthetic cells and 26 tremor cells) were identified throughout the electrode trajectories. The mean firing rate and burst index of cells (n = 27) within the T-VIM are 18.8 ± 9.8 Hz and 4.5 ± 5.4, respectively. Significant local field potential beta power was identified within the T-VIM (area under the curve for 13–30 Hz = 6.6 ± 7.7) with a trend toward higher beta power in the dorsal T-VIM. The most significant reduction in tremor was also observed in the dorsal T-VIM.

CONCLUSIONS

The electrophysiological findings within the VIM thalamus defined by tractography, or T-VIM, correspond with the known microelectrode recording characteristics of the VIM in patients with tremor.

ABBREVIATIONS

CRST = Clinical Rating Scale for Tremor; DBS = deep brain stimulation; DRT = dentatorubrothalamic tract; DTI = diffusion tensor imaging; ISI = interspike interval; LFP = local field potential; MER = microelectrode recording; ML = medial lemniscus; PT = pyramidal tract; ROI = region of interest; T-VIM = tractography-based VIM; VIM = ventral intermediate nucleus.
  • Collapse
  • Expand
  • 1

    Abosch A, Yacoub E, Ugurbil K, Harel N: An assessment of current brain targets for deep brain stimulation surgery with susceptibility-weighted imaging at 7 tesla. Neurosurgery 67:17451756, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Alavi M, Dostrovsky JO, Hodaie M, Lozano AM, Hutchison WD: Spatial extent of β oscillatory activity in and between the subthalamic nucleus and substantia nigra pars reticulata of Parkinson's disease patients. Exp Neurol 245:6071, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Anthofer J, Steib K, Fellner C, Lange M, Brawanski A, Schlaier J: The variability of atlas-based targets in relation to surrounding major fibre tracts in thalamic deep brain stimulation. Acta Neurochir (Wien) 156:14971504, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Asanuma C, Thach WT, Jones EG: Distribution of cerebellar terminations and their relation to other afferent terminations in the ventral lateral thalamic region of the monkey. Brain Res 286:237265, 1983

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Barbe MT, Liebhart L, Runge M, Pauls KA, Wojtecki L, Schnitzler A, et al.: Deep brain stimulation in the nucleus ventralis intermedius in patients with essential tremor: habituation of tremor suppression. J Neurol 258:434439, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Basha D, Dostrovsky JO, Lopez Rios AL, Hodaie M, Lozano AM, Hutchison WD: Beta oscillatory neurons in the motor thalamus of movement disorder and pain patients. Exp Neurol 261:782790, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Bastian AJ, Thach WT: Cerebellar outflow lesions: a comparison of movement deficits resulting from lesions at the levels of the cerebellum and thalamus. Ann Neurol 38:881892, 1995

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Behrens TEJ, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CAM, Boulby PA, et al.: Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6:750757, 2003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Benabid AL, Pollak P, Gervason C, Hoffmann D, Gao DM, Hommel M, et al.: Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet 337:403406, 1991

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Brierley JB, Beck E: The significance in human stereotactic brain surgery of individual variation in the diencephalon and globus pallidus. J Neurol Neurosurg Psychiatry 22:287298, 1959

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Byne W, Buchsbaum MS, Kemether E, Hazlett EA, Shinwari A, Mitropoulou V, et al.: Magnetic resonance imaging of the thalamic mediodorsal nucleus and pulvinar in schizophrenia and schizotypal personality disorder. Arch Gen Psychiatry 58:133140, 2001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Coenen VA, Allert N, Paus S, Kronenbürger M, Urbach H, Mädler B: Modulation of the cerebello-thalamo-cortical network in thalamic deep brain stimulation for tremor: a diffusion tensor imaging study. Neurosurgery 75:657670, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Colebatch JG, Findley LJ, Frackowiak RS, Marsden CD, Brooks DJ: Preliminary report: activation of the cerebellum in essential tremor. Lancet 336:10281030, 1990

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Deuschl G, Raethjen J, Lindemann M, Krack P: The pathophysiology of tremor. Muscle Nerve 24:716735, 2001

  • 15

    Elias WJ, Huss D, Voss T, Loomba J, Khaled M, Zadicario E, et al.: A pilot study of focused ultrasound thalamotomy for essential tremor. N Engl J Med 369:640648, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Favilla CG, Ullman D, Wagle Shukla A, Foote KD, Jacobson CE IV, Okun MS: Worsening essential tremor following deep brain stimulation: disease progression versus tolerance. Brain 135:14551462, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Gringel T, Schulz-Schaeffer W, Elolf E, Frölich A, Dechent P, Helms G: Optimized high-resolution mapping of magnetization transfer (MT) at 3 Tesla for direct visualization of substructures of the human thalamus in clinically feasible measurement time. J Magn Reson Imaging 29:12851292, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Hamani C, Dostrovsky JO, Lozano AM: The motor thalamus in neurosurgery. Neurosurgery 58:146158, 2006

  • 19

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

  • 20

    Hirai T, Ohye C, Nagaseki Y, Matsumura M: Cytometric analysis of the thalamic ventralis intermedius nucleus in humans. J Neurophysiol 61:478487, 1989

  • 21

    Hua SE, Lenz FA, Zirh TA, Reich SG, Dougherty PM: Thalamic neuronal activity correlated with essential tremor. J Neurol Neurosurg Psychiatry 64:273276, 1998

  • 22

    Hyam JA, Owen SL, Kringelbach ML, Jenkinson N, Stein JF, Green AL, et al.: Contrasting connectivity of the ventralis intermedius and ventralis oralis posterior nuclei of the motor thalamus demonstrated by probabilistic tractography. Neurosurgery 70:162169, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Johansen-Berg H, Behrens TE, Sillery E, Ciccarelli O, Thompson AJ, Smith SM, et al.: Functional-anatomical validation and individual variation of diffusion tractography-based segmentation of the human thalamus. Cereb Cortex 15:3139, 2005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Kaneoke Y, Vitek JL: Burst and oscillation as disparate neuronal properties. J Neurosci Methods 68:211223, 1996

  • 25

    Kincses ZT, Szabó N, Valálik I, Kopniczky Z, Dézsi L, Klivényi P, et al.: Target identification for stereotactic thalamotomy using diffusion tractography. PLoS One 7:e29969, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Klein JC, Barbe MT, Seifried C, Baudrexel S, Runge M, Maarouf M, et al.: The tremor network targeted by successful VIM deep brain stimulation in humans. Neurology 78:787795, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Kumar R, Lozano AM, Sime E, Lang AE: Long-term followup of thalamic deep brain stimulation for essential and parkinsonian tremor. Neurology 61:16011604, 2003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Kwon HG, Hong JH, Hong CP, Lee DH, Ahn SH, Jang SH: Dentatorubrothalamic tract in human brain: diffusion tensor tractography study. Neuroradiology 53:787791, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Lee BH, Lee KH, Chung SS, Chang JW: Neurophysiological identification and characterization of thalamic neurons with single unit recording in essential tremor patients. Acta Neurochir Suppl 87:133136, 2003

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Lenz FA, Dostrovsky JO, Tasker RR, Yamashiro K, Kwan HC, Murphy JT: Single-unit analysis of the human ventral thalamic nuclear group: somatosensory responses. J Neurophysiol 59:299316, 1988

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Lenz FA, Jaeger CJ, Seike MS, Lin YC, Reich SG: Single-neuron analysis of human thalamus in patients with intention tremor and other clinical signs of cerebellar disease. J Neurophysiol 87:20842094, 2002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Lenz FA, Kwan HC, Dostrovsky JO, Tasker RR, Murphy JT, Lenz YE: Single unit analysis of the human ventral thalamic nuclear group. Activity correlated with movement Brain 113:17951821, 1990

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Lenz FA, Kwan HC, Martin RL, Tasker RR, Dostrovsky JO, Lenz YE: Single unit analysis of the human ventral thalamic nuclear group. Tremor-related activity in functionally identified cells. Brain 117:531543, 1994

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Lipsman N, Schwartz ML, Huang Y, Lee L, Sankar T, Chapman M, et al.: MR-guided focused ultrasound thalamotomy for essential tremor: a proof-of-concept study. Lancet Neurol 12:462468, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Nicoletti G, Manners D, Novellino F, Condino F, Malucelli E, Barbiroli B, et al.: Diffusion tensor MRI changes in cerebellar structures of patients with familial essential tremor. Neurology 74:988994, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Papavassiliou E, Rau G, Heath S, Abosch A, Barbaro NM, Larson PS, et al.: Thalamic deep brain stimulation for essential tremor: relation of lead location to outcome. Neurosurgery 54:11201130, 2004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Sammartino F, Krishna V, King NKK, Lozano AM, Schwartz ML, Huang Y, et al.: Tractography-based ventral intermediate nucleus targeting: novel methodology and intraoperative validation. Mov Disord [epub ahead of print] 2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Schlaier J, Anthofer J, Steib K, Fellner C, Rothenfusser E, Brawanski A, et al.: Deep brain stimulation for essential tremor: targeting the dentato-rubro-thalamic tract?. Neuromodulation 18:105112, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Schuurman PR, Bosch DA, Bossuyt PM, Bonsel GJ, van Someren EJ, de Bie RM, et al.: A comparison of continuous thalamic stimulation and thalamotomy for suppression of severe tremor. N Engl J Med 342:461468, 2000

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Sedrak M, Gorgulho A, Frew A, Behnke E, DeSalles A, Pouratian N: Diffusion tensor imaging and colored fractional anisotropy mapping of the ventralis intermedius nucleus of the thalamus. Neurosurgery 69:11241130, 2011

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Shih LC, LaFaver K, Lim C, Papavassiliou E, Tarsy D: Loss of benefit in VIM thalamic deep brain stimulation (DBS) for essential tremor (ET): how prevalent is it?. Parkinsonism Relat Disord 19:676679, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Shin DH, Han BS, Kim HS, Lee PH: Diffusion tensor imaging in patients with essential tremor. AJNR Am J Neuroradiol 29:151153, 2008

  • 43

    Thomas C, Ye FQ, Irfanoglu MO, Modi P, Saleem KS, Leopold DA, et al.: Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited. Proc Natl Acad Sci U S A 111:1657416579, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Timmermann L, Gross J, Dirks M, Volkmann J, Freund HJ, Schnitzler A: The cerebral oscillatory network of parkinsonian resting tremor. Brain 126:199212, 2003

  • 45

    Traynor C, Heckemann RA, Hammers A, O'Muircheartaigh J, Crum WR, Barker GJ, et al.: Reproducibility of thalamic segmentation based on probabilistic tractography. Neuroimage 52:6985, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46

    Traynor CR, Barker GJ, Crum WR, Williams SC, Richardson MP: Segmentation of the thalamus in MRI based on T1 and T2. Neuroimage 56:939950, 2011

  • 47

    Unrath A, Klose U, Grodd W, Ludolph AC, Kassubek J: Directional colour encoding of the human thalamus by diffusion tensor imaging. Neurosci Lett 434:322327, 2008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48

    Velasco F, Velasco M, Romo R, Maldonado H: Production and suppression of tremor by mesencephalic tegmental lesions in monkeys. Exp Neurol 64:516527, 1979

  • 49

    Wiegell MR, Tuch DS, Larsson HB, Wedeen VJ: Automatic segmentation of thalamic nuclei from diffusion tensor magnetic resonance imaging. Neuroimage 19:391401, 2003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50

    Wintermark M, Huss DS, Shah BB, Tustison N, Druzgal TJ, Kassell N, et al.: Thalamic connectivity in patients with essential tremor treated with MR imaging-guided focused ultrasound: in vivo fiber tracking by using diffusion-tensor MR imaging. Radiology 272:202209, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51

    Wu YR, Levy R, Ashby P, Tasker RR, Dostrovsky JO: Does stimulation of the GPi control dyskinesia by activating inhibitory axons?. Mov Disord 16:208216, 2001

  • 52

    Yamada K, Akazawa K, Yuen S, Goto M, Matsushima S, Takahata A, et al.: MR imaging of ventral thalamic nuclei. AJNR Am J Neuroradiol 31:732735, 2010

  • 53

    Yamada K, Nagakane Y, Yoshikawa K, Kizu O, Ito H, Kubota T, et al.: Somatotopic organization of thalamocortical projection fibers as assessed with MR tractography. Radiology 242:840845, 2007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 54

    Young GS, Feng F, Shen H, Chen NK: Susceptibility-enhanced 3-Tesla T1-weighted spoiled gradient echo of the midbrain nuclei for guidance of deep brain stimulation implantation. Neurosurgery 65:809815, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 55

    Yovel Y, Assaf Y: Virtual definition of neuronal tissue by cluster analysis of multi-parametric imaging (virtual-dot-com imaging). Neuroimage 35:5869, 2007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 56

    Zesiewicz TA, Elble R, Louis ED, Hauser RA, Sullivan KL, Dewey RB Jr, et al.: Practice parameter: therapies for essential tremor: report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 64:20082020, 2005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 57

    Ziyan U, Tuch D, Westin CF: Segmentation of thalamic nuclei from DTI using spectral clustering. Med Image Comput Comput Assist Interv 9:807814, 2006

Metrics

All Time Past Year Past 30 Days
Abstract Views 123 123 49
Full Text Views 2580 251 5
PDF Downloads 1488 262 9
EPUB Downloads 0 0 0