Advertisement

European Radiology

, Volume 28, Issue 9, pp 3882–3892 | Cite as

Direct localisation of the human pedunculopontine nucleus using MRI: a coordinate and fibre-tracking study

  • Fei Cong
  • Jia-Wei Wang
  • Bo Wang
  • Zhangyan Yang
  • Jing An
  • Zhentao Zuo
  • Zihao Zhang
  • Yu-Qing Zhang
  • Yan Zhuo
Magnetic Resonance
  • 433 Downloads

Abstract

Objectives

To image the pedunculopontine tegmental nucleus (PPN), a deep brain stimulation (DBS) target for Parkinson disease, using MRI with validated results.

Methods

This study used the MP2RAGE sequence with high resolution and enhanced grey-white matter contrast on a 7-T ultra-high-field MRI system to image the PPN as well as a diffusion spectrum imaging method on a 3-T MRI system to reconstruct the main fibre systems surrounding the PPN. The coordinates of the rostral and caudal PPN poles of both sides were measured in relation to the third and fourth ventricular landmarks on the 7-T image.

Results

The boundary of the PPN was delineated, and showed morphology consistent with previous histological works. The main fibres around the PPN were reconstructed. The pole coordinate results combined with the fibre spatial relationships validate the imaging results.

Conclusions

A practical protocol is provided to directly localise the PPN using MRI; the position and morphology of the PPN can be obtained and validated by locating its poles relative to two ventricular landmarks and by inspecting its spatial relationship with the surrounding fibre systems. This technique can be potentially used in clinics to define the boundary of the PPN before DBS surgery for treatment of Parkinson disease in a more precise and reliable manner.

Key points

• Combined information helps localise the PPN as a DBS target for PD patients

• Scan the PPN at 7 T and measure its coordinates against different ventricular landmarks

• Reconstruct the main fibres around the PPN using diffusion spectrum imaging

Keywords

Pedunculopontine tegmental nucleus Parkinson disease Magnetic resonance imaging Deep brain stimulation Diffusion tensor imaging 

Abbreviations and acronyms

AC

Anterior commissure

CA

Cerebral aqueduct

CTT

Central tegmental tracts

DBS

Deep brain stimulation

DIV

MP2RAGE two-echo divided image

DSCP

Decussation of the superior cerebellar peduncle

DSI

Diffusion spectrum imaging

DSI0

DSI image with b value = 0

DTI

Diffusion tensor imaging

ML

Medial lemniscus

PAG

Periaqueductal grey

PC

Posterior commissures

PD

Parkinson disease

Point B

Base point of the B-F coordinate

Point F

Fastigial point of the B-F coordinate

PPN

Pedunculopontine tegmental nucleus

QA

Mean quantitative anisotropy

REF

Second echo of the MP2RAGE image

SCP

Superior cerebellar peduncle

SNc

Substantia nigra pars compacta

STN

Subthalamic nucleus

Notes

Acknowledgements

We thank Mr. Jing Luo and Ms. Hong Xu for their assistance with the experimental conditions and Dr. Penghu Wei and Dr. Xu Yan for their technical advice.

Funding

This study has received funding from the Chinese MOST (Ministry of Science and Technology of China) “973” grant (2015CB351701), NSFC (National Natural Science Foundation of China) grants (31730039, 81601060), and Beijing Municipal Commission of Science and Technology grant (Z161100000116059).

Compliance with ethical standards

Guarantor

The scientific guarantor of this publication is Yan Zhuo.

Conflict of interest

The author Jing An is an employee of Siemens responsible for customer research support. The other authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• experimental

• performed at one institution

Supplementary material

330_2017_5299_MOESM1_ESM.docx (332 kb)
ESM 1 (DOCX 332 kb)
330_2017_5299_MOESM2_ESM.docx (137 kb)
ESM 2 (DOCX 137 kb)
330_2017_5299_MOESM3_ESM.docx (1.5 mb)
ESM 3 (DOCX 1496 kb)

References

  1. 1.
    Olszewski J, Baxter D (1982) Cytoarchitecture of the human brain stem. Karger, SwitzerlandGoogle Scholar
  2. 2.
    Paxinos G, Huang XF (1995) Atlas of the human brainstem. Academic Press, San DiegoGoogle Scholar
  3. 3.
    Strumpf H, Noesselt T, Schoenfeld MA et al (2016) Deep Brain Stimulation of the Pedunculopontine Tegmental Nucleus (PPN) Influences Visual Contrast Sensitivity in Human Observers. PLoS ONE 11:e0155206CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Okada K, Kobayashi Y (2013) Reward prediction-related increases and decreases in tonic neuronal activity of the pedunculopontine tegmental nucleus. Front Integr Neurosci 7:36CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Hong S, Hikosaka O (2014) Pedunculopontine tegmental nucleus neurons provide reward, sensorimotor, and alerting signals to midbrain dopamine neurons. Neuroscience 282:139–155CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Goetz L, Piallat B, Bhattacharjee M, Mathieu H, David O, Chabardès S (2016) The primate pedunculopontine nucleus region: towards a dual role in locomotion and waking state. J Neural Transm 123:667–678CrossRefPubMedGoogle Scholar
  7. 7.
    Pahapill PA, Lozano AM (2000) The pedunculopontine nucleus and Parkinson's disease. Brain 123:1767–1783CrossRefPubMedGoogle Scholar
  8. 8.
    Fournier-Gosselin M-P, Lipsman N, Saint-Cyr JA, Hamani C, Lozano AM (2013) Regional anatomy of the pedunculopontine nucleus: Relevance for deep brain stimulation. Mov Disord 28:1330–1336CrossRefPubMedGoogle Scholar
  9. 9.
    Karachi C, Grabli D, Bernard F et al (2010) Cholinergic mesencephalic neurons are involved in gait and postural disorders in Parkinson disease. J Clin Invest 120:2745–2754CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Kojima J, Yamaji Y, Matsumura M et al (1997) Excitotoxic lesions of the pedunculopontine tegmental nucleus produce contralateral hemiparkinsonism in the monkey. Neurosci Lett 226:111–114CrossRefPubMedGoogle Scholar
  11. 11.
    Nandi D, Aziz TZ, Giladi N, Winter J, Stein JF (2002) Reversal of akinesia in experimental parkinsonism by GABA antagonist microinjections in the pedunculopontine nucleus. Brain 125:2418–2430CrossRefPubMedGoogle Scholar
  12. 12.
    Karachi C, André A, Bertasi E, Bardinet E, Lehéricy S, Bernard FA (2012) Functional parcellation of the lateral mesencephalus. J Neurosci 32:9396–9401CrossRefPubMedGoogle Scholar
  13. 13.
    Snijders AH, Leunissen I, Bakker M et al (2011) Gait-related cerebral alterations in patients with Parkinson’s disease with freezing of gait. Brain 134:59–72CrossRefPubMedGoogle Scholar
  14. 14.
    Mazzone P, Lozano A, Stanzione P et al (2005) Implantation of human pedunculopontine nucleus: a safe and clinically relevant target in Parkinson's disease. NeuroReport 16:1877–1881CrossRefPubMedGoogle Scholar
  15. 15.
    Plaha P, Gill SS (2005) Bilateral deep brain stimulation of the pedunculopontine nucleus for Parkinson's disease. NeuroReport 16:1883–1887CrossRefPubMedGoogle Scholar
  16. 16.
    Moro E, Hamani C, Poon YY et al (2010) Unilateral pedunculopontine stimulation improves falls in Parkinson's disease. Brain 133:215–224CrossRefPubMedGoogle Scholar
  17. 17.
    Ferraye MU, Debu B, Fraix V et al (2010) Effects of pedunculopontine nucleus area stimulation on gait disorders in Parkinson's disease. Brain 133:205–214CrossRefPubMedGoogle Scholar
  18. 18.
    Schaltenbrand G, Wahren W (1977) Atlas for stereotaxy of the human brain. Thieme, Stuttgart, New YorkGoogle Scholar
  19. 19.
    Hariz MI, Krack P, Melvill R et al (2003) A quick and universal method for stereotactic visualization of the subthalamic nucleus before and after implantation of deep brain stimulation electrodes. Stereotact Funct Neurosurg 80:96–101CrossRefPubMedGoogle Scholar
  20. 20.
    Weinberger M, Hamani C, Hutchison WD, Moro E, Lozano AM, Dostrovsky JO (2008) Pedunculopontine nucleus microelectrode recordings in movement disorder patients. Exp Brain Res 188:165–174CrossRefPubMedGoogle Scholar
  21. 21.
    Shimamoto SA, Larson PS, Ostrem JL, Glass GA, Turner RS, Starr PA (2010) Physiological identification of the human pedunculopontine nucleus. J Neurol Neurosurg Psychiatry 81:80–86CrossRefPubMedGoogle Scholar
  22. 22.
    Zrinzo L, Zrinzo LV, Tisch S et al (2008) Stereotactic localization of the human pedunculopontine nucleus: atlas-based coordinates and validation of a magnetic resonance imaging protocol for direct localization. Brain 131:1588–1598CrossRefPubMedGoogle Scholar
  23. 23.
    Zrinzo L, Zrinzo L, Massey L et al (2011) Targeting of the pedunculopontine nucleus by an MRI-guided approach: a cadaver study. J Neural Transm 118:1487–1495CrossRefPubMedGoogle Scholar
  24. 24.
    Alho AT, Hamani C, Alho EJ et al (2017) Magnetic resonance diffusion tensor imaging for the pedunculopontine nucleus: proof of concept and histological correlation. Brain Struct Funct.  https://doi.org/10.1007/s00429-016-1356-0:1-12
  25. 25.
    Marques JP, Kober T, Krueger G, van der Zwaag W, Van de Moortele P-F, Gruetter R (2010) MP2RAGE, a self bias-field corrected sequence for improved segmentation and T1-mapping at high field. Neuroimage 49:1271–1281CrossRefPubMedGoogle Scholar
  26. 26.
    Wedeen VJ, Hagmann P, Tseng W-YI, Reese TG, Weisskoff RM (2005) Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn Reson Med 54:1377–1386CrossRefPubMedGoogle Scholar
  27. 27.
    Feinberg DA, Moeller S, Smith SM et al (2010) Multiplexed Echo Planar Imaging for Sub-Second Whole Brain FMRI and Fast Diffusion Imaging. PLoS ONE 5:e15710CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Setsompop K, Cohen-Adad J, Gagoski BA et al (2012) Improving diffusion MRI using simultaneous multi-slice echo planar imaging. Neuroimage 63:569–580CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Rosset A, Spadola L, Ratib O (2004) OsiriX: An Open-Source Software for Navigating in Multidimensional DICOM Images. J Digit Imaging 17:205–216CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Afshar F, Watkins ES, Yap JC (1978) Stereotaxic atlas of the human brainstem and cerebellar nuclei: a variability study. Raven Press, New YorkGoogle Scholar
  31. 31.
    Lay DC (2012) Linear Algebra and Its Applications, 4th edn. Addison Wesley, BostonGoogle Scholar
  32. 32.
    Yeh FC, Wedeen VJ, Tseng WY (2010) Generalized q-sampling imaging. IEEE Trans Med Imaging 29:1626–1635CrossRefPubMedGoogle Scholar
  33. 33.
    Fedorov A, Beichel R, Kalpathy-Cramer J et al (2012) 3D Slicer as an image computing platform for the Quantitative Imaging Network. Magn Reson Imaging 30:1323–1341CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Wedeen VJ, Wang RP, Schmahmann JD et al (2008) Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. Neuroimage 41:1267–1277CrossRefPubMedGoogle Scholar
  35. 35.
    Fernandez-Miranda JC, Pathak S, Engh J et al (2012) High-definition fiber tractography of the human brain: neuroanatomical validation and neurosurgical applications. Neurosurgery 71:430–453CrossRefPubMedGoogle Scholar
  36. 36.
    Stefani A, Lozano AM, Peppe A et al (2007) Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson's disease. Brain 130:1596–1607CrossRefPubMedGoogle Scholar
  37. 37.
    Jenkinson N, Brittain JS, Hicks SL, Kennard C, Aziz TZ (2012) On the Origin of Oscillopsia during Pedunculopontine Stimulation. Stereotact Funct Neurosurg 90:124–129CrossRefPubMedGoogle Scholar
  38. 38.
    Gut NK, Winn P (2015) Deep brain stimulation of different pedunculopontine targets in a novel rodent model of parkinsonism. J Neurosci 35:4792–4803CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Thevathasan W, Coyne TJ, Hyam JA et al (2011) Pedunculopontine nucleus stimulation improves gait freezing in Parkinson disease. Neurosurgery 69:1248–1254CrossRefPubMedGoogle Scholar
  40. 40.
    Thevathasan W, Silburn PA, Brooker H et al (2010) The impact of low-frequency stimulation of the pedunculopontine nucleus region on reaction time in parkinsonism. J Neurol Neurosurg Psychiatry 81:1099–1104CrossRefPubMedGoogle Scholar
  41. 41.
    Welter M-L, Demain A, Ewenczyk C et al (2015) PPNa-DBS for gait and balance disorders in Parkinson’s disease: a double-blind, randomised study. J Neurol 262:1515–1525CrossRefPubMedGoogle Scholar

Copyright information

© European Society of Radiology 2018

Authors and Affiliations

  • Fei Cong
    • 1
    • 2
  • Jia-Wei Wang
    • 3
  • Bo Wang
    • 1
    • 2
  • Zhangyan Yang
    • 1
    • 2
  • Jing An
    • 4
  • Zhentao Zuo
    • 1
    • 2
  • Zihao Zhang
    • 1
    • 2
  • Yu-Qing Zhang
    • 5
  • Yan Zhuo
    • 1
    • 2
  1. 1.State Key Laboratory of Brain and Cognitive Science, Beijing MR Center for Brain Research, Institute of BiophysicsChinese Academy of SciencesBeijingChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Department of Neurosurgery, Cancer HospitalChinese Academy of Medical Sciences & Peking Union Medical CollegeBeijingChina
  4. 4.Siemens Shenzhen Magnetic Resonance Ltd.Siemens MRI CenterShenzhenChina
  5. 5.Beijing Institute of Functional Neurosurgery, Department of Functional Neurosurgery, Xuanwu HospitalCapital Medical UniversityBeijingChina

Personalised recommendations