Magnetic resonance imaging techniques for visualization of the subthalamic nucleus

A review

Ellen J. L. Brunenberg 1 , Bram Platel 2 , Paul A. M. Hofman 3 , Bart M. ter Haar Romeny 1 , 4 and Veerle Visser-Vandewalle 5 , 6
View More View Less
1 1Department of Biomedical Engineering, Eindhoven University of Technology, Eindhoven;
2 2Fraunhofer MEVIS, Bremen, Germany
3 3Departments of Radiology,
4 4Biomedical Engineering, and
5 5Neurosurgery, and
6 6Maastricht Institute for Neuromodulative Development, Maastricht University Medical Center, Maastricht, The Netherlands; and
DOI:
https://doi.org/10.3171/2011.6.JNS101571
Restricted access

All currencies in US Dollar

PayPal Logo

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.

Volume 115 (2011): Issue 5 (Nov 2011)

in Journal of Neurosurgery
Cover Journal of Neurosurgery

Article Information

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.

Keywords:
deep brain stimulation; targeting; subthalamic nucleus; MR imaging; functional neurosurgery
Page Count:
971–984

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Diagram showing AC-PC line–based targeting in a sagittal plane. After the AC and PC are identified, the midcommissural point (MCP) is determined. From there, the STN position can be calculated using fixed distances (often 12 mm lateral, 3 mm inferior, and 3 mm posterior) based on an atlas.

  • View in gallery

    Diagram showing red nucleus–based targeting in an axial plane. The center of the STN lies on the same line as the anterior boundary of the red nucleus (RN).

  • View in gallery

    Diagram showing targeting based on the nigrocapsular angle, in a sagittal plane. The STN lies in the corner that is formed by the descending internal capsule (IC) and the substantia nigra (SN).

  • View in gallery

    Diagram illustrating the concept of indirect targeting based on atlas mapping. On the upper left, an atlas slice with anatomical information can be seen, containing labeled structures. At the bottom left, a functional atlas is represented, consisting of a cloud of target points that were used in previously performed DBS operations. On the right, the patient's MR imaging data can be seen. The gray arrows represent the transformation that is necessary to map the atlases to the patient's MR imaging data, resulting in overlaid information as shown in the center.

  • View in gallery

    Coronal T2-weighted FSE MR image showing direct visualization of the STN.

  • View in gallery

    Coronal IR MR image showing direct visualization of the STN.

  • View in gallery

    Axial susceptibility-weighted MR image showing direct visualization of the STN.

Diagram showing AC-PC line–based targeting in a sagittal plane. After the AC and PC are identified, the midcommissural point (MCP) is determined. From there, the STN position can be calculated using fixed distances (often 12 mm lateral, 3 mm inferior, and 3 mm posterior) based on an atlas.

Diagram showing red nucleus–based targeting in an axial plane. The center of the STN lies on the same line as the anterior boundary of the red nucleus (RN).

Diagram showing targeting based on the nigrocapsular angle, in a sagittal plane. The STN lies in the corner that is formed by the descending internal capsule (IC) and the substantia nigra (SN).

Diagram illustrating the concept of indirect targeting based on atlas mapping. On the upper left, an atlas slice with anatomical information can be seen, containing labeled structures. At the bottom left, a functional atlas is represented, consisting of a cloud of target points that were used in previously performed DBS operations. On the right, the patient's MR imaging data can be seen. The gray arrows represent the transformation that is necessary to map the atlases to the patient's MR imaging data, resulting in overlaid information as shown in the center.

Coronal T2-weighted FSE MR image showing direct visualization of the STN.

Coronal IR MR image showing direct visualization of the STN.

Axial susceptibility-weighted MR image showing direct visualization of the STN.

References

1

Abosch AYacoub EUgurbil KHarel N: An assessment of current brain targets for deep brain stimulation surgery with susceptibility-weighted imaging at 7 tesla. Neurosurgery 67:1745–17562010

2

Acar FMiller JPBerk MCAnderson GBurchiel KJ: Safety of anterior commissure-posterior commissure-based target calculation of the subthalamic nucleus in functional stereotactic procedures. Stereotact Funct Neurosurg 85:287–2912007

3

Andrade-Souza YMSchwalb JMHamani CEltahawy HHoque TSaint-Cyr J: Comparison of three methods of targeting the subthalamic nucleus for chronic stimulation in Parkinson's disease. Neurosurgery 56:2 Suppl360–3682005

4

Andrade-Souza YMSchwalb JMHamani CHoque TSaint-Cyr JLozano AM: Comparison of 2-dimensional magnetic resonance imaging and 3-planar reconstruction methods for targeting the subthalamic nucleus in Parkinson disease. Surg Neurol 63:357–3632005

5

Ardekani BABachman AH: Model-based automatic detection of the anterior and posterior commissures on MRI scans. Neuroimage 46:677–6822009

6

Ashkan KBlomstedt PZrinzo LTisch SYousry TLimousin-Dowsey P: Variability of the subthalamic nucleus: the case for direct MRI guided targeting. Br J Neurosurg 21:197–2002007

7

Aziz TZNandi DParkin SLiu XGiladi NBain P: Targeting the subthalamic nucleus. Stereotact Funct Neurosurg 77:87–902001

8

Bardinet EBhattacharjee MDormont DPidoux BMalandain GSchüpbach 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 110:208–2192009

9

Bardinet EDormont DMalandain GBhattacharjee MPidoux BSaleh 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 2385–3932005

10

Bejjani BPDormont DPidoux BYelnik JDamier PArnulf I: Bilateral subthalamic stimulation for Parkinson's disease by using three-dimensional stereotactic magnetic resonance imaging and electrophysiological guidance. J Neurosurg 92:615–6252000

11

Benabid ALKoudsie ABenazzouz ALe Bas JFPollak P: Imaging of subthalamic nucleus and ventralis intermedius of the thalamus. Mov Disord 17:3 Suppl 3S123–S1292002

12

Bonny JDurif FBazin JETouraille EYelnik JRenou JP: Contrast optimization of Macaca mulatta basal ganglia in magnetic resonance images at 4.7 Tesla. J Neurosci Methods 107:25–302001

13

Breit SLeBas JFKoudsie ASchulz JBenazzouz APollak P: Pretargeting for the implantation of stimulation electrodes into the subthalamic nucleus: a comparative study of magnetic resonance imaging and ventriculography. Neurosurgery 58:1 SupplONS83–ONS952006

14

Brunenberg EPelgrim Eter Haar Romeny BPlatel B: kmeans and graph cuts clustering of diffusion MRI in rat STN. Proc Intl Soc Mag Reson Med 18:40452010. (Abstract)

15

Brunenberg EJLVilanova AVisser-Vandewalle VTemel YAckermans LPlatel B: Automatic trajectory planning for deep brain stimulation: a feasibility study. Med Image Comput Comput Assist Interv 10:Pt 1584–5922007

16

Brunenberg EJLPrckovska VPlatel BStrijkers GJter 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 17:7412009. (Abstract)

17

Caire FOuchchane LCoste JGabrillargues JDerost PUlla M: Subthalamic nucleus location: relationships between stereotactic AC-PC-based diagrams and MRI anatomy-based contours. Stereotact Funct Neurosurg 87:337–3472009

18

Castro FJPollo CMeuli RMaeder PCuisenaire OCuadra 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 25:1440–14502006

19

Cho ZHMin HKOh SHHan JYPark CWChi JG: Direct visualization of deep brain stimulation targets in Parkinson disease with the use of 7-tesla magnetic resonance imaging. Clinical article. J Neurosurg 113:639–6472010

20

Cho ZHOh SHKim JMPark SYKwon DHJeong HJ: Direct visualization of Parkinson's disease by in vivo human brain imaging using 7.0T magnetic resonance imaging. Mov Disord 26:713–7182011

21

Coenen VAMädler BSchiffbauer HUrbach HAllert N: Individual fiber anatomy of the subthalamic region revealed with DTI—a concept to identify the DBS target for tremor suppression: erratum. Neurosurgery 68:1780–17812011

22

Collins DLZijdenbos APKollokian VSled JGKabani NJHolmes CJ: Design and construction of a realistic digital brain phantom. IEEE Trans Med Imaging 17:463–4681998

23

Cuny EGuehl DBurbaud PGross CDousset VRougier A: Lack of agreement between direct magnetic resonance imaging and statistical determination of a subthalamic target: the role of electrophysiological guidance. J Neurosurg 97:591–5972002

24

D'Haese PFCetinkaya EKonrad PEKao CDawant BM: Computer-aided placement of deep brain stimulators: from planning to intraoperative guidance. IEEE Trans Med Imaging 24:1469–14782005

25

Daniluk SDavies K: Optimal stimulation site. J Neurosurg 108:425–4292008. (Letter)

26

Daniluk SDavies KGEllias SANovak PNazzaro 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) 152:201–2102010

27

Danish SFJaggi JLMoyer JTFinkel LBaltuch GH: Conventional MRI is inadequate to delineate the relationship between the red nucleus and subthalamic nucleus in Parkinson's disease. Stereotact Funct Neurosurg 84:12–182006

28

Davies KGDaniluk S: Stereotactic targeting of the subthalamic nucleus: relevance of magnetic resonance-based evaluation of interindividual variation in diencephalic anatomy. Stereotact Funct Neurosurg 86:330–3312008

29

Dormont DRicciardi KGTandé DParain KMenuel CGalanaud D: Is the subthalamic nucleus hypointense on T2-weighted images? A correlation study using MR imaging and stereotactic atlas data. AJNR Am J Neuroradiol 25:1516–15232004

30

Dormont DSeidenwurm DGalanaud DCornu PYelnik JBardinet E: Neuroimaging and deep brain stimulation. AJNR Am J Neuroradiol 31:15–232010

31

Duay VBresson XCastro JSPollo CCuadra MBThiran 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 2980–9882008

32

Egidi MRampini PLocatelli MFarabola MPriori APesenti 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 2S71–S722002

33

Elolf EBockermann VGringel TKnauth MDechent PHelms 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 28:1093–10942007

34

Giller CABabcock EEMendelsohn DB: Use of sagittal images for localization of the subthalamic nucleus. Technical note. J Neurosurg 102:571–5752005

35

Guehl DEdwards RCuny EBurbaud PRougier AModolo J: Statistical determination of the optimal subthalamic nucleus stimulation site in patients with Parkinson disease. J Neurosurg 106:101–1102007

36

Guo TDeoni SCLFinnis KWParrent AGPeters TM: Application of T1 and T2 maps for stereotactic deep-brain neurosurgery planning. Conf Proc IEEE Eng Med Biol Soc 5:5416–54192005

37

Guo TFinnis KWDeoni SCParrent AGPeters TM: Comparison of different targeting methods for subthalamic nucleus deep brain stimulation. Med Image Comput Comput Assist Interv 9:Pt 1768–7752006

38

Guo TParrent AGPeters TM: Automatic target and trajectory identification for deep brain stimulation (DBS) procedures. Med Image Comput Comput Assist Interv 10:Pt 1483–4902007

39

Guo TParrent AGPeters TM: Surgical targeting accuracy analysis of six methods for subthalamic nucleus deep brain stimulation. Comput Aided Surg 12:325–3342007

40

Hamani CRichter EOAndrade-Souza YHutchison WSaint-Cyr JALozano AM: Correspondence of microelectrode mapping with magnetic resonance imaging for subthalamic nucleus procedures. Surg Neurol 63:249–2532005

41

Hamani CSaint-Cyr JAFraser JKaplitt MLozano AM: The subthalamic nucleus in the context of movement disorders. Brain 127:4–202004

42

Hamel WFietzek UMorsnowski ASchrader BHerzog JWeinert D: Deep brain stimulation of the subthalamic nucleus in Parkinson's disease: evaluation of active electrode contacts. J Neurol Neurosurg Psychiatry 74:1036–10462003

43

Hamid NAMitchell RDMocroft PWestby GWMMilner JPall 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 76:409–4142005

44

Hariz MIKrack PMelvill RJorgensen JVHamel WHirabayashi 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 80:96–1012003

45

Helms GGringel TKnauth MDechent PElolf E: Delineation of the subthalamic nucleus (STN) on high-resolution maps of R2*. Proc Intl Soc Mag Reson Med 16:8802008. (Abstract)

46

Hunsche SSauner DMaarouf MPoggenborg JLackner KSturm 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 87:322–3292009

47

Ishimori TNakano SMori YSeo RTogami TMasada T: Preoperative identification of subthalamic nucleus for deep brain stimulation using three-dimensional phase sensitive inversion recovery technique. Magn Reson Med Sci 6:225–2292007

48

Kitajima MKakeda SMoriya JOhnari NSato THayashida 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 15:7802007. (Abstract)

49

Koike YShima FNakamizo AMiyagi 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 86:173–1782008

50

Lanotte MMRizzone MBergamasco BFaccani GMelcarne ALopiano L: Deep brain stimulation of the subthalamic nucleus: anatomical, neurophysiological, and outcome correlations with the effects of stimulation. J Neurol Neurosurg Psychiatry 72:53–582002

51

Lebel RMEissa AGee MWieler MMartin WRWilman AH: MRI methods at 4.7 T for imaging Parkinson's disease. Proc Intl Soc Mag Reson Med 16:22832008. (Abstract)

52

Lee CYoung BSanders MF: The role of the supramammillary commissure in MR localization of the subthalamic nucleus. Stereotact Funct Neurosurg 84:193–2042006

53

Lemaire JJCoste JOuchchane LCaire FNuti CDerost P: Brain mapping in stereotactic surgery: a brief overview from the probabilistic targeting to the patient-based anatomic mapping. Neuroimage 37:1 Suppl 1S109–S1152007

54

Lemaire JJCoste JOuchchane LHemm SDerost PUlla M: MRI anatomical mapping and direct stereotactic targeting in the subthalamic region: functional and anatomical correspondence in Parkinson's disease. Int J CARS 2:75–852007

55

Littlechild PVarma TRKEldridge PRFox SForster AFletcher 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 80:82–872003

56

Liu XRowe JNandi DHayward GParkin SStein J: Localisation of the subthalamic nucleus using Radionics Image Fusion and Stereoplan combined with field potential recording. A technical note. Stereotact Funct Neurosurg 76:63–732001

57

Menuel CGarnero LBardinet EPoupon FPhalippou DDormont D: Characterization and correction of distortions in stereotactic magnetic resonance imaging for bilateral subthalamic stimulation in Parkinson disease. J Neurosurg 103:256–2662005

58

Mori SZhang J: Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51:527–5392006

59

Nowinski WLBelov DPollak PBenabid AL: A probabilistic functional atlas of the human subthalamic nucleus. Neuroinformatics 2:381–3982004

60

Nowinski WLLiu JThirunavuukarasuu A: Quantification and visualization of the three-dimensional inconsistency of the subthalamic nucleus in the Schaltenbrand-Wahren brain atlas. Stereotact Funct Neurosurg 84:46–552006

61

Nowinski WLThirunavuukarasuu ALiu JBenabid AL: Correlation between the anatomical and functional human subthalamic nucleus. Stereotact Funct Neurosurg 85:88–932007

62

Ortega MJuan MCAlcañiz MGil JAMonserrat 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 32:367–3782008

63

Pallavaram SD'Haese PFKao CYu HRemple MNeimat 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 1670–6772008

64

Pallavaram SDawant BMKoyama TYu HNeimat JKonrad PE: Validation of a fully automatic method for the routine selection of the anterior and posterior commissures in magnetic resonance images. Stereotact Funct Neurosurg 87:148–1542009

65

Pallavaram SYu HSpooner JD'Haese PFBodenheimer BKonrad PE: Intersurgeon variability in the selection of anterior and posterior commissures and its potential effects on target localization. Stereotact Funct Neurosurg 86:113–1192008

66

Patel NKHeywood PO'Sullivan KLove SGill SS: MRI-directed subthalamic nucleus surgery for Parkinson's disease. Stereotact Funct Neurosurg 78:132–1452002

67

Patel NKKhan SGill 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 86:153–1612008

68

Patel NKPlaha PO'Sullivan KMcCarter RHeywood PGill SS: MRI directed bilateral stimulation of the subthalamic nucleus in patients with Parkinson's disease. J Neurol Neurosurg Psychiatry 74:1631–16372003

69

Pollak PBenabid ALGross CGao DMLaurent ABenazzouz A: [Effects of the stimulation of the subthalamic nucleus in Parkinson disease.]. Rev Neurol (Paris) 149:175–1761993. (Fr)

70

Pollo CMeuli RMaeder PVingerhoets FGhika JVillemure JG: Subthalamic nucleus deep brain stimulation for Parkinson's disease: magnetic resonance imaging targeting using visible anatomical landmarks. Stereotact Funct Neurosurg 80:76–812003

71

Rauscher AWitoszynskyj SKolind SCoenen VLi D: Visualization of the subthalamic nuclei at high spatial resolution and high contrast with susceptibility weighted phase imaging. Proc Intl Soc Mag Reson Med 16:8792008. (Abstract)

72

Richter EOHoque THalliday WLozano AMSaint-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 100:541–5462004

73

Rijkers KTemel YVisser-Vandewalle VVanormelingen LVandersteen MAdriaensen P: The microanatomical environment of the subthalamic nucleus. Technical note. J Neurosurg 107:198–2012007

74

Rodriguez-Oroz MCZamarbide IGuridi JPalmero MRObeso 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 75:1382–13852004

75

Saint-Cyr JAHoque TPereira LCMDostrovsky JOHutchison WDMikulis DJ: Localization of clinically effective stimulating electrodes in the human subthalamic nucleus on magnetic resonance imaging. J Neurosurg 97:1152–11662002

76

Sánchez Castro FJPollo CVillemure JGThiran JP: Automatic subthalamic nucleus targeting for deep brain stimulation. A validation study. International Congress Series (CARS 2005: Computer Assisted Radiology and Surgery) AmsterdamElsevier2005. 1281:804–809

77

Schaltenbrand GWahren W: Atlas for Stereotaxy of the Human Brain ed 2StuttgartThieme1977

78

Schlaier JSchoedel PLange MWinkler JWarnat JDorenbeck U: Reliability of atlas-derived coordinates in deep brain stimulation. Acta Neurochir (Wien) 147:1175–11802005

79

Schuurman PRde Bie RMMajoie CBSpeelman JDBosch DA: A prospective comparison between three-dimensional magnetic resonance imaging and ventriculography for target-coordinate determination in frame-based functional stereotactic neurosurgery. J Neurosurg 91:911–9141999

80

Slavin KVThulborn KRWess CNersesyan H: Direct visualization of the human subthalamic nucleus with 3T MR imaging. AJNR Am J Neuroradiol 27:80–842006

81

Starr PA: Placement of deep brain stimulators into the subthalamic nucleus or globus pallidus internus: technical approach. Stereotact Funct Neurosurg 79:118–1452002

82

Starr PAChristine CWTheodosopoulos PVLindsey NByrd DMosley A: Implantation of deep brain stimulators into the subthalamic nucleus: technical approach and magnetic resonance imaging-verified lead locations. J Neurosurg 97:370–3872002

83

Starr PAVitek JLDeLong MBakay RA: Magnetic resonance imaging-based stereotactic localization of the globus pallidus and subthalamic nucleus. Neurosurgery 44:303–3141999

84

Sun DAYu HSpooner JTatsas ADDavis TAbel TW: Postmortem analysis following 71 months of deep brain stimulation of the subthalamic nucleus for Parkinson disease. Case report. J Neurosurg 109:325–3292008

85

Talairach JTournoux P: Co-planar Stereotaxic Atlas of the Human Brain New YorkThieme1988

86

Taoka THirabayashi HNakagawa HSakamoto MKitano STakahama J: “Sukeroku sign” and “dent internal-capsule sign”—identification guide for targeting the subthalamic nucleus for placement of deep brain stimulation electrodes. Neuroradiology 51:11–162009

87

Taoka TKubota YHirabayashi HNakagawa HSakamoto MIwasaki S: Signal and shape of subthalamic nucleus on susceptibility-weighted image (SWI): comparison with STIR image. Proc Intl Soc Mag Reson Med 15:21752007. (Abstract)

88

Temel YBlokland ASteinbusch HWMVisser-Vandewalle V: The functional role of the subthalamic nucleus in cognitive and limbic circuits. Prog Neurobiol 76:393–4132005

89

Temel YKessels ATan STopdag ABoon PVisser-Vandewalle V: Behavioural changes after bilateral subthalamic stimulation in advanced Parkinson disease: a systematic review. Parkinsonism Relat Disord 12:265–2722006

90

Temel YPrinsenberg TVisser-Vandewalle V: Imaging of the subthalamic nucleus for deep brain stimulation: a systematic review. Neuromodulation 11:8–122008

91

Toda HSawamoto NHanakawa TSaiki HMatsumoto SOkumura R: A novel composite targeting method using high-field magnetic resonance imaging for subthalamic nucleus deep brain stimulation. Clinical article. J Neurosurg 111:737–7452009

92

Tsai STLin SHLin SZChen JYLee CWChen SY: Neuropsychological effects after chronic subthalamic stimulation and the topography of the nucleus in Parkinson's disease. Neurosurgery 61:E1024–E10302007

93

Tuch DSReese TGWiegell MRMakris NBelliveau JWWedeen VJ: High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity. Magn Reson Med 48:577–5822002

94

Vertinsky ATCoenen VALang DJKolind SHoney CRLi D: Localization of the subthalamic nucleus: optimization with susceptibility-weighted phase MR imaging. AJNR Am J Neuroradiol 30:1717–17242009

95

Visser-Vandewalle Vvan der Linden CTemel YCelik HAckermans LSpincemaille G: Long-term effects of bilateral subthalamic nucleus stimulation in advanced Parkinson disease: a four year follow-up study. Parkinsonism Relat Disord 11:157–1652005

96

Volkmann JAllert NVoges JWeiss PHFreund HJSturm V: Safety and efficacy of pallidal or subthalamic nucleus stimulation in advanced PD. Neurology 56:548–5512001

97

Volz SHattingen EPreibisch CGasser TDeichmann R: Reduction of susceptibility-induced signal losses in multi-gradient-echo images: application to improved visualization of the subthalamic nucleus. Neuroimage 45:1135–11432009

98

Voon VKubu CKrack PHoueto JLTröster AI: Deep brain stimulation: neuropsychological and neuropsychiatric issues. Mov Disord 21:Suppl 14S305–S3272006

99

Wu MLYoung GSChen NK: Midbrain nuclei visualization improved by susceptibility-enhanced 3D multi-echo SSFP for deep brain stimulation guidance. Proc Intl Soc Mag Reson Med 18:7012010. (Abstract)

100

Yelnik JBardinet EDormont DMalandain GOurselin STandé D: A three-dimensional, histological and deformable atlas of the human basal ganglia. I Atlas construction based on immunohistochemical and MRI data. Neuroimage 34:618–6382007

101

Young GSChen 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 15:9372007. (Abstract)

102

Zhu XLHamel WSchrader BWeinert DHedderich JHerzog J: Magnetic resonance imaging-based morphometry and landmark correlation of basal ganglia nuclei. Acta Neurochir (Wien) 144:959–9692002

103

Zonenshayn MRezai ARMogilner AYBeric ASterio DKelly PJ: Comparison of anatomic and neurophysiological methods for subthalamic nucleus targeting. Neurosurgery 47:282–2942000

TrendMD

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 66 66 31
Full Text Views 172 172 12
PDF Downloads 104 104 8
EPUB Downloads 0 0 0

PubMed

Google Scholar