Magnetic resonance imaging techniques for visualization of the subthalamic nucleus

A review

View More View Less
  • 1 Department of Biomedical Engineering, Eindhoven University of Technology, Eindhoven;
  • 3 Departments of Radiology,
  • 4 Biomedical Engineering, and
  • 5 Neurosurgery, and
  • 6 Maastricht Institute for Neuromodulative Development, Maastricht University Medical Center, Maastricht, The Netherlands; and
  • 2 Fraunhofer MEVIS, Bremen, Germany
Restricted access

Purchase Now

USD  $45.00

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

USD  $505.00

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

USD  $600.00
Print or Print + Online

The authors reviewed 70 publications on MR imaging–based targeting techniques for identifying the subthalamic nucleus (STN) for deep brain stimulation in patients with Parkinson disease. Of these 70 publications, 33 presented quantitatively validated results.

There is still no consensus on which targeting technique to use for surgery planning; methods vary greatly between centers. Some groups apply indirect methods involving anatomical landmarks, or atlases incorporating anatomical or functional data. Others perform direct visualization on MR imaging, using T2-weighted spin echo or inversion recovery protocols.

The combined studies do not offer a straightforward conclusion on the best targeting protocol. Indirect methods are not patient specific, leading to varying results between cases. On the other hand, direct targeting on MR imaging suffers from lack of contrast within the subthalamic region, resulting in a poor delineation of the STN. These deficiencies result in a need for intraoperative adaptation of the original target based on test stimulation with or without microelectrode recording.

It is expected that future advances in MR imaging technology will lead to improvements in direct targeting. The use of new MR imaging modalities such as diffusion MR imaging might even lead to the specific identification of the different functional parts of the STN, such as the dorsolateral sensorimotor part, the target for deep brain stimulation.

Abbreviations used in this paper: AC = anterior commissure; DBS = deep brain stimulation; FSE = fast spin echo; IR = inversion recovery; MCP = midcommissural point; MER = microelectrode recording; MPRAGE = magnetization prepared rapid acquisition gradient echo; PC = posterior commissure; STIR = short tau inversion recovery; STN = subthalamic nucleus; TSE = turbo spin echo.

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

USD  $505.00

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

USD  $600.00

Contributor Notes

Address correspondence to: Ellen J. L. Brunenberg, Eindhoven University of Technology, Department of Biomedical Engineering, WH 2.106, PO Box 513, 5600 MB Eindhoven, The Netherlands. email: ellenbrunenberg@gmail.com.

Please include this information when citing this paper: published online July 29, 2011; DOI: 10.3171/2011.6.JNS101571.

  • 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

    • Search Google Scholar
    • Export Citation
  • 2

    Acar F, , Miller JP, , Berk MC, , Anderson G, & Burchiel KJ: Safety of anterior commissure-posterior commissure-based target calculation of the subthalamic nucleus in functional stereotactic procedures. Stereotact Funct Neurosurg 85:287291, 2007

    • Search Google Scholar
    • Export Citation
  • 3

    Andrade-Souza YM, , Schwalb JM, , Hamani C, , Eltahawy H, , Hoque T, & Saint-Cyr J, : Comparison of three methods of targeting the subthalamic nucleus for chronic stimulation in Parkinson's disease. Neurosurgery 56:2 Suppl 360368, 2005

    • Search Google Scholar
    • Export Citation
  • 4

    Andrade-Souza YM, , Schwalb JM, , Hamani C, , Hoque T, , Saint-Cyr J, & Lozano AM: Comparison of 2-dimensional magnetic resonance imaging and 3-planar reconstruction methods for targeting the subthalamic nucleus in Parkinson disease. Surg Neurol 63:357363, 2005

    • Search Google Scholar
    • Export Citation
  • 5

    Ardekani BA, & Bachman AH: Model-based automatic detection of the anterior and posterior commissures on MRI scans. Neuroimage 46:677682, 2009

    • Search Google Scholar
    • Export Citation
  • 6

    Ashkan K, , Blomstedt P, , Zrinzo L, , Tisch S, , Yousry T, & Limousin-Dowsey P, : Variability of the subthalamic nucleus: the case for direct MRI guided targeting. Br J Neurosurg 21:197200, 2007

    • Search Google Scholar
    • Export Citation
  • 7

    Aziz TZ, , Nandi D, , Parkin S, , Liu X, , Giladi N, & Bain P, : Targeting the subthalamic nucleus. Stereotact Funct Neurosurg 77:8790, 2001

  • 8

    Bardinet E, , Bhattacharjee M, , Dormont D, , Pidoux B, , Malandain G, & Schüpbach M, : A three-dimensional histological atlas of the human basal ganglia. II. Atlas deformation strategy and evaluation in deep brain stimulation for Parkinson disease Clinical article. J Neurosurg 110:208219, 2009

    • Search Google Scholar
    • Export Citation
  • 9

    Bardinet E, , Dormont D, , Malandain G, , Bhattacharjee M, , Pidoux B, & Saleh C, : Retrospective cross-evaluation of a histological and deformable 3D atlas of the basal ganglia on series of Parkinsonian patients treated by deep brain stimulation. Med Image Comput Comput Assist Interv 8:Pt 2 385393, 2005

    • Search Google Scholar
    • Export Citation
  • 10

    Bejjani BP, , Dormont D, , Pidoux B, , Yelnik J, , Damier P, & Arnulf I, : Bilateral subthalamic stimulation for Parkinson's disease by using three-dimensional stereotactic magnetic resonance imaging and electrophysiological guidance. J Neurosurg 92:615625, 2000

    • Search Google Scholar
    • Export Citation
  • 11

    Benabid AL, , Koudsie A, , Benazzouz A, , Le Bas JF, & Pollak P: Imaging of subthalamic nucleus and ventralis intermedius of the thalamus. Mov Disord 17:3 Suppl 3 S123S129, 2002

    • Search Google Scholar
    • Export Citation
  • 12

    Bonny J, , Durif F, , Bazin JE, , Touraille E, , Yelnik J, & Renou JP: Contrast optimization of Macaca mulatta basal ganglia in magnetic resonance images at 4.7 Tesla. J Neurosci Methods 107:2530, 2001

    • Search Google Scholar
    • Export Citation
  • 13

    Breit S, , LeBas JF, , Koudsie A, , Schulz J, , Benazzouz A, & Pollak P, : Pretargeting for the implantation of stimulation electrodes into the subthalamic nucleus: a comparative study of magnetic resonance imaging and ventriculography. Neurosurgery 58:1 Suppl ONS83ONS95, 2006

    • Search Google Scholar
    • Export Citation
  • 14

    Brunenberg E, , Pelgrim E, , ter Haar Romeny B, & Platel B: kmeans and graph cuts clustering of diffusion MRI in rat STN. Proc Intl Soc Mag Reson Med 18:4045, 2010. (Abstract)

    • Search Google Scholar
    • Export Citation
  • 15

    Brunenberg EJL, , Vilanova A, , Visser-Vandewalle V, , Temel Y, , Ackermans L, & Platel B, : Automatic trajectory planning for deep brain stimulation: a feasibility study. Med Image Comput Comput Assist Interv 10:Pt 1 584592, 2007

    • Search Google Scholar
    • Export Citation
  • 16

    Brunenberg EJL, , Prckovska V, , Platel B, , Strijkers GJ, & ter Haar Romeny BM: Untangling a fiber bundle knot: preliminary results on STN connectivity using DTI and HARDI on rat brains. Proc Intl Soc Mag Reson Med 17:741, 2009. (Abstract)

    • Search Google Scholar
    • Export Citation
  • 17

    Caire F, , Ouchchane L, , Coste J, , Gabrillargues J, , Derost P, & Ulla M, : Subthalamic nucleus location: relationships between stereotactic AC-PC-based diagrams and MRI anatomy-based contours. Stereotact Funct Neurosurg 87:337347, 2009

    • Search Google Scholar
    • Export Citation
  • 18

    Castro FJ, , Pollo C, , Meuli R, , Maeder P, , Cuisenaire O, & Cuadra MB, : A cross validation study of deep brain stimulation targeting: from experts to atlas-based, segmentation-based and automatic registration algorithms. IEEE Trans Med Imaging 25:14401450, 2006

    • Search Google Scholar
    • Export Citation
  • 19

    Cho ZH, , Min HK, , Oh SH, , Han JY, , Park CW, & Chi JG, : Direct visualization of deep brain stimulation targets in Parkinson disease with the use of 7-tesla magnetic resonance imaging. Clinical article. J Neurosurg 113:639647, 2010

    • Search Google Scholar
    • Export Citation
  • 20

    Cho ZH, , Oh SH, , Kim JM, , Park SY, , Kwon DH, & Jeong HJ, : Direct visualization of Parkinson's disease by in vivo human brain imaging using 7.0T magnetic resonance imaging. Mov Disord 26:713718, 2011

    • Search Google Scholar
    • Export Citation
  • 21

    Coenen VA, , Mädler B, , Schiffbauer H, , Urbach H, & Allert N: Individual fiber anatomy of the subthalamic region revealed with DTI—a concept to identify the DBS target for tremor suppression: erratum. Neurosurgery 68:17801781, 2011

    • Search Google Scholar
    • Export Citation
  • 22

    Collins DL, , Zijdenbos AP, , Kollokian V, , Sled JG, , Kabani NJ, & Holmes CJ, : Design and construction of a realistic digital brain phantom. IEEE Trans Med Imaging 17:463468, 1998

    • Search Google Scholar
    • Export Citation
  • 23

    Cuny E, , Guehl D, , Burbaud P, , Gross C, , Dousset V, & Rougier A: Lack of agreement between direct magnetic resonance imaging and statistical determination of a subthalamic target: the role of electrophysiological guidance. J Neurosurg 97:591597, 2002

    • Search Google Scholar
    • Export Citation
  • 24

    D'Haese PF, , Cetinkaya E, , Konrad PE, , Kao C, & Dawant BM: Computer-aided placement of deep brain stimulators: from planning to intraoperative guidance. IEEE Trans Med Imaging 24:14691478, 2005

    • Search Google Scholar
    • Export Citation
  • 25

    Daniluk S, & Davies K: Optimal stimulation site. J Neurosurg 108:425429, 2008. (Letter)

  • 26

    Daniluk S, , Davies KG, , Ellias SA, , Novak P, & Nazzaro JM: Assessment of the variability in the anatomical position and size of the subthalamic nucleus among patients with advanced Parkinson's disease using magnetic resonance imaging. Acta Neurochir (Wien) 152:201210, 2010

    • Search Google Scholar
    • Export Citation
  • 27

    Danish SF, , Jaggi JL, , Moyer JT, , Finkel L, & Baltuch GH: Conventional MRI is inadequate to delineate the relationship between the red nucleus and subthalamic nucleus in Parkinson's disease. Stereotact Funct Neurosurg 84:1218, 2006

    • Search Google Scholar
    • Export Citation
  • 28

    Davies KG, & Daniluk S: Stereotactic targeting of the subthalamic nucleus: relevance of magnetic resonance-based evaluation of interindividual variation in diencephalic anatomy. Stereotact Funct Neurosurg 86:330331, 2008

    • Search Google Scholar
    • Export Citation
  • 29

    Dormont D, , Ricciardi KG, , Tandé D, , Parain K, , Menuel C, & Galanaud D, : Is the subthalamic nucleus hypointense on T2-weighted images? A correlation study using MR imaging and stereotactic atlas data. AJNR Am J Neuroradiol 25:15161523, 2004

    • Search Google Scholar
    • Export Citation
  • 30

    Dormont D, , Seidenwurm D, , Galanaud D, , Cornu P, , Yelnik J, & Bardinet E: Neuroimaging and deep brain stimulation. AJNR Am J Neuroradiol 31:1523, 2010

    • Search Google Scholar
    • Export Citation
  • 31

    Duay V, , Bresson X, , Castro JS, , Pollo C, , Cuadra MB, & Thiran JP: An active contour-based atlas registration model applied to automatic subthalamic nucleus targeting on MRI: method and validation. Med Image Comput Comput Assist Interv 11:Pt 2 980988, 2008

    • Search Google Scholar
    • Export Citation
  • 32

    Egidi M, , Rampini P, , Locatelli M, , Farabola M, , Priori A, & Pesenti A, : Visualisation of the subthalamic nucleus: a multiple sequential image fusion (MuSIF) technique for direct stereotaxic localisation and postoperative control. Neurol Sci 23:2 Suppl 2 S71S72, 2002

    • Search Google Scholar
    • Export Citation
  • 33

    Elolf E, , Bockermann V, , Gringel T, , Knauth M, , Dechent P, & Helms G: Improved visibility of the subthalamic nucleus on high-resolution stereotactic MR imaging by added susceptibility (T2*) contrast using multiple gradient echoes. AJNR Am J Neuroradiol 28:10931094, 2007

    • Search Google Scholar
    • Export Citation
  • 34

    Giller CA, , Babcock EE, & Mendelsohn DB: Use of sagittal images for localization of the subthalamic nucleus. Technical note. J Neurosurg 102:571575, 2005

    • Search Google Scholar
    • Export Citation
  • 35

    Guehl D, , Edwards R, , Cuny E, , Burbaud P, , Rougier A, & Modolo J, : Statistical determination of the optimal subthalamic nucleus stimulation site in patients with Parkinson disease. J Neurosurg 106:101110, 2007

    • Search Google Scholar
    • Export Citation
  • 36

    Guo T, , Deoni SCL, , Finnis KW, , Parrent AG, & Peters TM: Application of T1 and T2 maps for stereotactic deep-brain neurosurgery planning. Conf Proc IEEE Eng Med Biol Soc 5:54165419, 2005

    • Search Google Scholar
    • Export Citation
  • 37

    Guo T, , Finnis KW, , Deoni SC, , Parrent AG, & Peters TM: Comparison of different targeting methods for subthalamic nucleus deep brain stimulation. Med Image Comput Comput Assist Interv 9:Pt 1 768775, 2006

    • Search Google Scholar
    • Export Citation
  • 38

    Guo T, , Parrent AG, & Peters TM: Automatic target and trajectory identification for deep brain stimulation (DBS) procedures. Med Image Comput Comput Assist Interv 10:Pt 1 483490, 2007

    • Search Google Scholar
    • Export Citation
  • 39

    Guo T, , Parrent AG, & Peters TM: Surgical targeting accuracy analysis of six methods for subthalamic nucleus deep brain stimulation. Comput Aided Surg 12:325334, 2007

    • Search Google Scholar
    • Export Citation
  • 40

    Hamani C, , Richter EO, , Andrade-Souza Y, , Hutchison W, , Saint-Cyr JA, & Lozano AM: Correspondence of microelectrode mapping with magnetic resonance imaging for subthalamic nucleus procedures. Surg Neurol 63:249253, 2005

    • Search Google Scholar
    • Export Citation
  • 41

    Hamani C, , Saint-Cyr JA, , Fraser J, , Kaplitt M, & Lozano AM: The subthalamic nucleus in the context of movement disorders. Brain 127:420, 2004

    • Search Google Scholar
    • Export Citation
  • 42

    Hamel W, , Fietzek U, , Morsnowski A, , Schrader B, , Herzog J, & Weinert D, : Deep brain stimulation of the subthalamic nucleus in Parkinson's disease: evaluation of active electrode contacts. J Neurol Neurosurg Psychiatry 74:10361046, 2003

    • Search Google Scholar
    • Export Citation
  • 43

    Hamid NA, , Mitchell RD, , Mocroft P, , Westby GWM, , Milner J, & Pall H: Targeting the subthalamic nucleus for deep brain stimulation: technical approach and fusion of pre- and postoperative MR images to define accuracy of lead placement. J Neurol Neurosurg Psychiatry 76:409414, 2005

    • Search Google Scholar
    • Export Citation
  • 44

    Hariz MI, , Krack P, , Melvill R, , Jorgensen JV, , Hamel W, & Hirabayashi H, : A quick and universal method for stereotactic visualization of the subthalamic nucleus before and after implantation of deep brain stimulation electrodes. Stereotact Funct Neurosurg 80:96101, 2003

    • Search Google Scholar
    • Export Citation
  • 45

    Helms G, , Gringel T, , Knauth M, , Dechent P, & Elolf E: Delineation of the subthalamic nucleus (STN) on high-resolution maps of R2*. Proc Intl Soc Mag Reson Med 16:880, 2008. (Abstract)

    • Search Google Scholar
    • Export Citation
  • 46

    Hunsche S, , Sauner D, , Maarouf M, , Poggenborg J, , Lackner K, & Sturm V, : Intraoperative X-ray detection and MRI-based quantification of brain shift effects subsequent to implantation of the first electrode in bilateral implantation of deep brain stimulation electrodes. Stereotact Funct Neurosurg 87:322329, 2009

    • Search Google Scholar
    • Export Citation
  • 47

    Ishimori T, , Nakano S, , Mori Y, , Seo R, , Togami T, & Masada T, : Preoperative identification of subthalamic nucleus for deep brain stimulation using three-dimensional phase sensitive inversion recovery technique. Magn Reson Med Sci 6:225229, 2007

    • Search Google Scholar
    • Export Citation
  • 48

    Kitajima M, , Kakeda S, , Moriya J, , Ohnari N, , Sato T, & Hayashida Y, : Direct visualization of normal subthalamic nucleus with high resolution MR imaging at 3.0 T: comparison between FSE T2-WI and fast STIR image. Proc Intl Soc Mag Reson Med 15:780, 2007. (Abstract)

    • Search Google Scholar
    • Export Citation
  • 49

    Koike Y, , Shima F, , Nakamizo A, & Miyagi Y: Direct localization of subthalamic nucleus supplemented by single-track electrophysiological guidance in deep brain stimulation lead implantation: techniques and clinical results. Stereotact Funct Neurosurg 86:173178, 2008

    • Search Google Scholar
    • Export Citation
  • 50

    Lanotte MM, , Rizzone M, , Bergamasco B, , Faccani G, , Melcarne A, & Lopiano L: Deep brain stimulation of the subthalamic nucleus: anatomical, neurophysiological, and outcome correlations with the effects of stimulation. J Neurol Neurosurg Psychiatry 72:5358, 2002

    • Search Google Scholar
    • Export Citation
  • 51

    Lebel RM, , Eissa A, , Gee M, , Wieler M, , Martin WR, & Wilman AH: MRI methods at 4.7 T for imaging Parkinson's disease. Proc Intl Soc Mag Reson Med 16:2283, 2008. (Abstract)

    • Search Google Scholar
    • Export Citation
  • 52

    Lee C, , Young B, & Sanders MF: The role of the supramammillary commissure in MR localization of the subthalamic nucleus. Stereotact Funct Neurosurg 84:193204, 2006

    • Search Google Scholar
    • Export Citation
  • 53

    Lemaire JJ, , Coste J, , Ouchchane L, , Caire F, , Nuti C, & Derost P, : Brain mapping in stereotactic surgery: a brief overview from the probabilistic targeting to the patient-based anatomic mapping. Neuroimage 37:1 Suppl 1 S109S115, 2007

    • Search Google Scholar
    • Export Citation
  • 54

    Lemaire JJ, , Coste J, , Ouchchane L, , Hemm S, , Derost P, & Ulla M, : MRI anatomical mapping and direct stereotactic targeting in the subthalamic region: functional and anatomical correspondence in Parkinson's disease. Int J CARS 2:7585, 2007

    • Search Google Scholar
    • Export Citation
  • 55

    Littlechild P, , Varma TRK, , Eldridge PR, , Fox S, , Forster A, & Fletcher N, : Variability in position of the subthalamic nucleus targeted by magnetic resonance imaging and microelectrode recordings as compared to atlas co-ordinates. Stereotact Funct Neurosurg 80:8287, 2003

    • Search Google Scholar
    • Export Citation
  • 56

    Liu X, , Rowe J, , Nandi D, , Hayward G, , Parkin S, & Stein J, : Localisation of the subthalamic nucleus using Radionics Image Fusion and Stereoplan combined with field potential recording. A technical note. Stereotact Funct Neurosurg 76:6373, 2001

    • Search Google Scholar
    • Export Citation
  • 57

    Menuel C, , Garnero L, , Bardinet E, , Poupon F, , Phalippou D, & Dormont D: Characterization and correction of distortions in stereotactic magnetic resonance imaging for bilateral subthalamic stimulation in Parkinson disease. J Neurosurg 103:256266, 2005

    • Search Google Scholar
    • Export Citation
  • 58

    Mori S, & Zhang J: Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51:527539, 2006

  • 59

    Nowinski WL, , Belov D, , Pollak P, & Benabid AL: A probabilistic functional atlas of the human subthalamic nucleus. Neuroinformatics 2:381398, 2004

    • Search Google Scholar
    • Export Citation
  • 60

    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 84:4655, 2006

    • Search Google Scholar
    • Export Citation
  • 61

    Nowinski WL, , Thirunavuukarasuu A, , Liu J, & Benabid AL: Correlation between the anatomical and functional human subthalamic nucleus. Stereotact Funct Neurosurg 85:8893, 2007

    • Search Google Scholar
    • Export Citation
  • 62

    Ortega M, , Juan MC, , Alcañiz M, , Gil JA, & Monserrat C: Deformable brain atlas validation of the location of subthalamic nucleus using T1-weighted MR images of patients operated on for Parkinson's. Comput Med Imaging Graph 32:367378, 2008

    • Search Google Scholar
    • Export Citation
  • 63

    Pallavaram S, , D'Haese PF, , Kao C, , Yu H, , Remple M, & Neimat J, : A new method for creating electrophysiological maps for DBS surgery and their application to surgical guidance. Med Image Comput Comput Assist Inter 11:Pt 1 670677, 2008

    • Search Google Scholar
    • Export Citation
  • 64

    Pallavaram S, , Dawant BM, , Koyama T, , Yu H, , Neimat J, & Konrad PE, : Validation of a fully automatic method for the routine selection of the anterior and posterior commissures in magnetic resonance images. Stereotact Funct Neurosurg 87:148154, 2009

    • Search Google Scholar
    • Export Citation
  • 65

    Pallavaram S, , Yu H, , Spooner J, , D'Haese PF, , Bodenheimer B, & Konrad PE, : Intersurgeon variability in the selection of anterior and posterior commissures and its potential effects on target localization. Stereotact Funct Neurosurg 86:113119, 2008

    • Search Google Scholar
    • Export Citation
  • 66

    Patel NK, , Heywood P, , O'Sullivan K, , Love S, & Gill SS: MRI-directed subthalamic nucleus surgery for Parkinson's disease. Stereotact Funct Neurosurg 78:132145, 2002

    • Search Google Scholar
    • Export Citation
  • 67

    Patel NK, , Khan S, & Gill SS: Comparison of atlas- and magnetic-resonance-imaging-based stereotactic targeting of the subthalamic nucleus in the surgical treatment of Parkinson's disease. Stereotact Funct Neurosurg 86:153161, 2008

    • Search Google Scholar
    • Export Citation
  • 68

    Patel NK, , Plaha P, , O'Sullivan K, , McCarter R, , Heywood P, & Gill SS: MRI directed bilateral stimulation of the subthalamic nucleus in patients with Parkinson's disease. J Neurol Neurosurg Psychiatry 74:16311637, 2003

    • Search Google Scholar
    • Export Citation
  • 69

    Pollak P, , Benabid AL, , Gross C, , Gao DM, , Laurent A, & Benazzouz A, : [Effects of the stimulation of the subthalamic nucleus in Parkinson disease.]. Rev Neurol (Paris) 149:175176, 1993. (Fr)

    • Search Google Scholar
    • Export Citation
  • 70

    Pollo C, , Meuli R, , Maeder P, , Vingerhoets F, , Ghika J, & Villemure JG: Subthalamic nucleus deep brain stimulation for Parkinson's disease: magnetic resonance imaging targeting using visible anatomical landmarks. Stereotact Funct Neurosurg 80:7681, 2003

    • Search Google Scholar
    • Export Citation
  • 71

    Rauscher A, , Witoszynskyj S, , Kolind S, , Coenen V, & Li D: Visualization of the subthalamic nuclei at high spatial resolution and high contrast with susceptibility weighted phase imaging. Proc Intl Soc Mag Reson Med 16:879, 2008. (Abstract)

    • Search Google Scholar
    • Export Citation
  • 72

    Richter EO, , Hoque T, , Halliday W, , Lozano AM, & Saint-Cyr JA: Determining the position and size of the subthalamic nucleus based on magnetic resonance imaging results in patients with advanced Parkinson disease. J Neurosurg 100:541546, 2004

    • Search Google Scholar
    • Export Citation
  • 73

    Rijkers K, , Temel Y, , Visser-Vandewalle V, , Vanormelingen L, , Vandersteen M, & Adriaensen P, : The microanatomical environment of the subthalamic nucleus. Technical note. J Neurosurg 107:198201, 2007

    • Search Google Scholar
    • Export Citation
  • 74

    Rodriguez-Oroz MC, , Zamarbide I, , Guridi J, , Palmero MR, & Obeso JA: Efficacy of deep brain stimulation of the subthalamic nucleus in Parkinson's disease 4 years after surgery: double blind and open label evaluation. J Neurol Neurosurg Psychiatry 75:13821385, 2004

    • Search Google Scholar
    • Export Citation
  • 75

    Saint-Cyr JA, , Hoque T, , Pereira LCM, , Dostrovsky JO, , Hutchison WD, & Mikulis DJ, : Localization of clinically effective stimulating electrodes in the human subthalamic nucleus on magnetic resonance imaging. J Neurosurg 97:11521166, 2002

    • Search Google Scholar
    • Export Citation
  • 76

    Sánchez Castro FJ, , Pollo C, , Villemure JG, & Thiran JP: Automatic subthalamic nucleus targeting for deep brain stimulation. A validation study. International Congress Series (CARS 2005: Computer Assisted Radiology and Surgery) Amsterdam, Elsevier, 2005. 1281:804809

    • Search Google Scholar
    • Export Citation
  • 77

    Schaltenbrand G, & Wahren W: Atlas for Stereotaxy of the Human Brain ed 2 Stuttgart, Thieme, 1977

  • 78

    Schlaier J, , Schoedel P, , Lange M, , Winkler J, , Warnat J, & Dorenbeck U, : Reliability of atlas-derived coordinates in deep brain stimulation. Acta Neurochir (Wien) 147:11751180, 2005

    • Search Google Scholar
    • Export Citation
  • 79

    Schuurman PR, , de Bie RM, , Majoie CB, , Speelman JD, & Bosch DA: A prospective comparison between three-dimensional magnetic resonance imaging and ventriculography for target-coordinate determination in frame-based functional stereotactic neurosurgery. J Neurosurg 91:911914, 1999

    • Search Google Scholar
    • Export Citation
  • 80

    Slavin KV, , Thulborn KR, , Wess C, & Nersesyan H: Direct visualization of the human subthalamic nucleus with 3T MR imaging. AJNR Am J Neuroradiol 27:8084, 2006

    • Search Google Scholar
    • Export Citation
  • 81

    Starr PA: Placement of deep brain stimulators into the subthalamic nucleus or globus pallidus internus: technical approach. Stereotact Funct Neurosurg 79:118145, 2002

    • Search Google Scholar
    • Export Citation
  • 82

    Starr PA, , Christine CW, , Theodosopoulos PV, , Lindsey N, , Byrd D, & Mosley A, : Implantation of deep brain stimulators into the subthalamic nucleus: technical approach and magnetic resonance imaging-verified lead locations. J Neurosurg 97:370387, 2002

    • Search Google Scholar
    • Export Citation
  • 83

    Starr PA, , Vitek JL, , DeLong M, & Bakay RA: Magnetic resonance imaging-based stereotactic localization of the globus pallidus and subthalamic nucleus. Neurosurgery 44:303314, 1999

    • Search Google Scholar
    • Export Citation
  • 84

    Sun DA, , Yu H, , Spooner J, , Tatsas AD, , Davis T, & Abel TW, : Postmortem analysis following 71 months of deep brain stimulation of the subthalamic nucleus for Parkinson disease. Case report. J Neurosurg 109:325329, 2008

    • Search Google Scholar
    • Export Citation
  • 85

    Talairach J, & Tournoux P: Co-planar Stereotaxic Atlas of the Human Brain New York, Thieme, 1988

  • 86

    Taoka T, , Hirabayashi H, , Nakagawa H, , Sakamoto M, , Kitano S, & Takahama J, : “Sukeroku sign” and “dent internal-capsule sign”—identification guide for targeting the subthalamic nucleus for placement of deep brain stimulation electrodes. Neuroradiology 51:1116, 2009

    • Search Google Scholar
    • Export Citation
  • 87

    Taoka T, , Kubota Y, , Hirabayashi H, , Nakagawa H, , Sakamoto M, & Iwasaki S, : Signal and shape of subthalamic nucleus on susceptibility-weighted image (SWI): comparison with STIR image. Proc Intl Soc Mag Reson Med 15:2175, 2007. (Abstract)

    • Search Google Scholar
    • Export Citation
  • 88

    Temel Y, , Blokland A, , Steinbusch HWM, & Visser-Vandewalle V: The functional role of the subthalamic nucleus in cognitive and limbic circuits. Prog Neurobiol 76:393413, 2005

    • Search Google Scholar
    • Export Citation
  • 89

    Temel Y, , Kessels A, , Tan S, , Topdag A, , Boon P, & Visser-Vandewalle V: Behavioural changes after bilateral subthalamic stimulation in advanced Parkinson disease: a systematic review. Parkinsonism Relat Disord 12:265272, 2006

    • Search Google Scholar
    • Export Citation
  • 90

    Temel Y, , Prinsenberg T, & Visser-Vandewalle V: Imaging of the subthalamic nucleus for deep brain stimulation: a systematic review. Neuromodulation 11:812, 2008

    • Search Google Scholar
    • Export Citation
  • 91

    Toda H, , Sawamoto N, , Hanakawa T, , Saiki H, , Matsumoto S, & Okumura R, : A novel composite targeting method using high-field magnetic resonance imaging for subthalamic nucleus deep brain stimulation. Clinical article. J Neurosurg 111:737745, 2009

    • Search Google Scholar
    • Export Citation
  • 92

    Tsai ST, , Lin SH, , Lin SZ, , Chen JY, , Lee CW, & Chen SY: Neuropsychological effects after chronic subthalamic stimulation and the topography of the nucleus in Parkinson's disease. Neurosurgery 61:E1024E1030, 2007

    • Search Google Scholar
    • Export Citation
  • 93

    Tuch DS, , Reese TG, , Wiegell MR, , Makris N, , Belliveau JW, & Wedeen VJ: High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity. Magn Reson Med 48:577582, 2002

    • Search Google Scholar
    • Export Citation
  • 94

    Vertinsky AT, , Coenen VA, , Lang DJ, , Kolind S, , Honey CR, & Li D, : Localization of the subthalamic nucleus: optimization with susceptibility-weighted phase MR imaging. AJNR Am J Neuroradiol 30:17171724, 2009

    • Search Google Scholar
    • Export Citation
  • 95

    Visser-Vandewalle V, , van der Linden C, , Temel Y, , Celik H, , Ackermans L, & Spincemaille G, : Long-term effects of bilateral subthalamic nucleus stimulation in advanced Parkinson disease: a four year follow-up study. Parkinsonism Relat Disord 11:157165, 2005

    • Search Google Scholar
    • Export Citation
  • 96

    Volkmann J, , Allert N, , Voges J, , Weiss PH, , Freund HJ, & Sturm V: Safety and efficacy of pallidal or subthalamic nucleus stimulation in advanced PD. Neurology 56:548551, 2001

    • Search Google Scholar
    • Export Citation
  • 97

    Volz S, , Hattingen E, , Preibisch C, , Gasser T, & Deichmann R: Reduction of susceptibility-induced signal losses in multi-gradient-echo images: application to improved visualization of the subthalamic nucleus. Neuroimage 45:11351143, 2009

    • Search Google Scholar
    • Export Citation
  • 98

    Voon V, , Kubu C, , Krack P, , Houeto JL, & Tröster AI: Deep brain stimulation: neuropsychological and neuropsychiatric issues. Mov Disord 21:Suppl 14 S305S327, 2006

    • Search Google Scholar
    • Export Citation
  • 99

    Wu ML, , Young GS, & Chen NK: Midbrain nuclei visualization improved by susceptibility-enhanced 3D multi-echo SSFP for deep brain stimulation guidance. Proc Intl Soc Mag Reson Med 18:701, 2010. (Abstract)

    • Search Google Scholar
    • Export Citation
  • 100

    Yelnik J, , Bardinet E, , Dormont D, , Malandain G, , Ourselin S, & Tandé D, : A three-dimensional, histological and deformable atlas of the human basal ganglia. I Atlas construction based on immunohistochemical and MRI data. Neuroimage 34:618638, 2007

    • Search Google Scholar
    • Export Citation
  • 101

    Young GS, & Chen NK: High contrast susceptibility weighted imaging: Reliable Unwrapping Susceptibility Technique (RUST SWI) improved visualization of midbrain nuclei for deep brain stimulation. Proc Intl Soc Mag Reson Med 15:937, 2007. (Abstract)

    • Search Google Scholar
    • Export Citation
  • 102

    Zhu XL, , Hamel W, , Schrader B, , Weinert D, , Hedderich J, & Herzog J, : Magnetic resonance imaging-based morphometry and landmark correlation of basal ganglia nuclei. Acta Neurochir (Wien) 144:959969, 2002

    • Search Google Scholar
    • Export Citation
  • 103

    Zonenshayn M, , Rezai AR, , Mogilner AY, , Beric A, , Sterio D, & Kelly PJ: Comparison of anatomic and neurophysiological methods for subthalamic nucleus targeting. Neurosurgery 47:282294, 2000

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 570 233 26
Full Text Views 238 10 1
PDF Downloads 156 9 1
EPUB Downloads 0 0 0