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Effect of brain shift on the creation of functional atlases for deep brain stimulation surgery

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International Journal of Computer Assisted Radiology and Surgery Aims and scope Submit manuscript

Abstract

Purpose

In the recent past many groups have tried to build functional atlases of the deep brain using intra-operatively acquired information such as stimulation responses or micro-electrode recordings. An underlying assumption in building such atlases is that anatomical structures do not move between pre-operative imaging and intra-operative recording. In this study, we present evidences that this assumption is not valid. We quantify the effect of brain shift between pre-operative imaging and intra-operative recording on the creation of functional atlases using intra-operative somatotopy recordings and stimulation response data.

Methods

A total of 73 somatotopy points from 24 bilateral subthalamic nucleus (STN) implantations and 52 eye deviation stimulation response points from 17 bilateral STN implantations were used. These points were spatially normalized on a magnetic resonance imaging (MRI) atlas using a fully automatic non-rigid registration algorithm. Each implantation was categorized as having low, medium or large brain shift based on the amount of pneumocephalus visible on post-operative CT. The locations of somatotopy clusters and stimulation maps were analyzed for each category.

Results

The centroid of the large brain shift cluster of the somatotopy data (posterior, lateral, inferior: 3.06, 11.27, 5.36 mm) was found posterior, medial and inferior to that of the medium cluster (2.90, 13.57, 4.53 mm) which was posterior, medial and inferior to that of the low shift cluster (1.94, 13.92, 3.20 mm). The coordinates are referenced with respect to the mid-commissural point. Euclidean distances between the centroids were 1.68, 2.44 and 3.59 mm, respectively for low-medium, medium-large and low-large shift clusters. We found similar trends for the positions of the stimulation maps. The Euclidian distance between the highest probability locations on the low and medium-large shift maps was 4.06 mm.

Conclusion

The effect of brain shift in deep brain stimulation (DBS) surgery has been demonstrated using intra-operative somatotopy recordings as well as stimulation response data. The results not only indicate that considerable brain shift happens before micro-electrode recordings in DBS but also that brain shift affects the creation of accurate functional atlases. Therefore, care must be taken when building and using such atlases of intra-operative data and also when using intra-operative data to validate anatomical atlases.

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References

  1. Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme Publishing Group, New York

    Google Scholar 

  2. Schaltenbrand G, Wahren W (1977) Atlas for stereotaxy of the human brain. Thieme Publishing Group, New York

    Google Scholar 

  3. Yelnik J, Bardinet E, Dormont D, Malandain G, Ourselin S, Tandé D, Karachi C, Ayache N, Cornu P, Agid Y (2007) A three-dimensional, histological and deformable atlas of the human basal ganglia. I. Atlas construction based on immunohistochemical and MRI data. Neuroimage 34: 618–638

    Article  PubMed  Google Scholar 

  4. Bardinet E, Bhattacharjee M, Dormont D, Pidoux B, Malandain G, Schüpbach M, Ayache N, Cornu P, Agid Y, Yelnik J (2009) A three-dimensional histological atlas of the human basal ganglia. II. Atlas deformation strategy and evaluation in deep brain stimulation for Parkinson disease. J Neurosurg 110: 208–219

    Article  PubMed  Google Scholar 

  5. Chakravarty MM, Bertrand G, Hodge CP, Sadikot AF, Collins DL (2006) The creation of a brain atlas for image guided neurosurgery using serial histological data. Neuroimage 30(2): 359–376

    Article  PubMed  Google Scholar 

  6. Chakravarty MM, Sadikot AF, Mongia S, Bertrand G, Collins DL (2006) Towards a multi-modal atlas for neurosurgical planning. Lecture notes in computer science (MICCAI), vol 4191, p 389–396

  7. Plaha P, Ben-Shlomo Y, Patel NK, Gill SS (2006) Stimulation of the caudal zona incerta is superior to stimulation of the subthalamic nucleus in improving contralateral parkinsonism. Brain 129: 1732–1747

    Article  PubMed  Google Scholar 

  8. Maks CB, Butson CR, Walter BL, Vitek JL, McIntyre CC (2009) Deep brain stimulation activation volumes and their association with neurophysiological mapping and therapeutic outcomes. Neurol Neurosurg Psychiatry, Online: 16 Jan, 2009. doi:10.1136/jnnp.2007.126219

  9. Andrade-Souza YM, Schwalb JM, Hamani C, Eltahawy H, Hoque T, Saint-Cyr J, Lozano AM (2008) Comparison of three methods of targeting the subthalamic nucleus for chronic stimulation in Parkinson’s disease. Neurosurgery 62(2): 875–883

    Article  PubMed  Google Scholar 

  10. Hamani C, Richter EO, Andrade-Souza Y, Hutchison W, Saint-Cyr JA, Lozano AM (2005) Correspondence of microelectrode mapping with magnetic resonance imaging for subthalamic nucleus procedures. Surg Neurol 63(3): 249–253

    Article  PubMed  Google Scholar 

  11. Tasker RR, Organ LW, Hawrylyshyn PA (1982) The thalamus and midbrain of man. Charles C Thomas, Springfield

    Google Scholar 

  12. Finnis KW, Starreveld YP, Parrent AG, Sadikot AF, Peters TM (2003) Three dimensional database of subcortical dlectrophysiology for dmage-guided stereotactic functional neurosurgery. IEEE Trans Med Imaging 22(11): 93–104

    Article  PubMed  Google Scholar 

  13. Finnis KW, Starreveld YP, Parrent AG, Sadikot AF, Peters TM (2002) Application of a population based electrophysiological database to the planning and guidance of deep brain stereotactic neurosurgery. In: MICCAI

  14. Nowinski WL, Belov D, Benabid AL (2003) An algorithm for rapid calculation of a probabilistic functional atlas of subcortical structures from electrophysiological data collected during functional neurosurgery procedures. Neuroimage 18: 143–155

    Article  PubMed  Google Scholar 

  15. Nowinski WL, Belov D, Pollak P, Benabid AL (2005) Statistical analysis of 168 bilateral subthalamic nucleus implantations by means of the probabilistic functional atlas. Neurosurgery 57(4): 319–330

    Article  PubMed  Google Scholar 

  16. Nowinski WL (2008) Towards construction of an ideal stereotactic brain atlas. Acta Neurochir (Wien) 150(1):1–13; discussion 13:14

    Google Scholar 

  17. Guo T, Finnis KW, Parrent AG, Peters TM (2005) Development and application of functional databases for planning deepbrain neurosurgical procedures. Lecture notes in computer science (MICCAI), vol 3749, pp 835–842

  18. Guo T, Finnis KW, Parrent AG, Peters TM (2006) Visualization and navigation system development and application for stereotactic deep-brain neurosurgeries. Comput Aided Surg 11(5): 231–239

    Article  PubMed  Google Scholar 

  19. Toga AW, Thompson PM, Mori S, Amunts K, Zilles K (2006) Towards multimodal atlases of the human brain. Nat Rev Neurosci 7(12): 952–966

    Article  CAS  PubMed  Google Scholar 

  20. Castro FJ, Pollo C, Cuisenaire O, Villemure J-G, Thiran J-P (2006) Validation of experts versus atlas-based and automatic registration methods for subthalamic nucleus targeting on MRI. Int J Comput Assisted Radiol Surg 1(1): 5–12

    Article  Google Scholar 

  21. Castro FJ, Pollo C, Meuli R, Maeder P, Cuisenaire O, Cuadra MB, Villemure J-G, Thiran J-P (2006) 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(11): 1440–1450

    Article  PubMed  Google Scholar 

  22. D’Haese P-F, Cetinkaya E, Konrad PE, Kao C, Dawant BM (2005) Computer-aided placement of deep brain stimulators: from planning to intraoperative guidance. IEEE Trans Med Imaging 24(11): 1469–1478

    Article  PubMed  Google Scholar 

  23. D’Haese P-F, Pallavaram S, Niermann K, Spooner J, Kao C, Konrad PE, Dawant BM (2005) Automatic selection of DBS target points using multiple electrophysiological atlases. LNCS (MICCAI) 3750: 427–434

    Google Scholar 

  24. Dawant BM, D’Haese P-F, Pallavaram S, Li R, Yu H, Spooner J, Davis T, Kao C, Konrad PE (2007) The VU-DBS project: integrated and computer-assisted planning, intra-operative placement, and post-operative programming of deep-brain stimulators. In: SPIE medical imaging 2007: visualization and image-guided procedures, vol 6509, pp 650–907

  25. Pallavaram S, D’Haese P-F, Kao C, Yu H, Remple M, Neimat JS, Konrad PE, Dawant BM (2008) A new method for creating electrophysiological maps for DBS surgery and their application to surgical guidance. Lecture notes in computer science (MICCAI), Part1, vol 5241, pp 670–677

  26. Guo T, Finnis KW, Deoni SCL, Parrent AG, Peters TM (2006) Comparison of different targeting methods for subthalamic nucleus deep brain stimulation. Lecture notes in computer science (MICCAI), vol 4190, pp 768–775

  27. Gerdes FU, Klein G, Nadjmi M, Schaltenbrand G (1975) X-ray studies of the brain as a basis for stereotaxy (author’s transl). J Neurol 210: 183–190

    Article  CAS  PubMed  Google Scholar 

  28. Hariz MI, Bergenheim AT, Fodstad H (1993) Air-ventriculography provokes an anterior displacement of the third ventricle during functional stereotactic procedures. Acta Neurochir (Wien) 123: 147–152

    Article  CAS  Google Scholar 

  29. Winkler D, Tittgemeyer M, Schwarz J, Preul C, Strecker K, Meixensberger J (2005) The first evaluation of brain shift during functional neurosurgery by deformation field analysis. J Neurol Neurosurg Psychiatry 76: 1161–1163

    Article  CAS  PubMed  Google Scholar 

  30. Miyagi Y, Shima F, Sasaki T (2007) Brain shift: an error factor during implantation of deep brain stimulation electrodes. Neurosurgery 107: 989–997

    Article  Google Scholar 

  31. Khan MF, Mewes K, Gross RE, Škrinjar O (2008) Assessment of brain shift related to deep brain stimulation surgery. Stereotact Funct Neurosurg 86: 44–53

    Article  PubMed  Google Scholar 

  32. Halpern CH, Danish SF, Baltuch GH, Jaggi JL (2008) Brain shift during deep brain stimulation surgery for Parkinson’s disease. Stereotact Funct Neurosurg 86: 37–43

    Article  PubMed  Google Scholar 

  33. Fitzpatrick JM, Konrad PE, Nickele C, Cetinkaya E (2005) Accuracy of customized miniature stereotactic platforms. Stereotact Funct Neurosurg 83: 25–31

    Article  PubMed  Google Scholar 

  34. Balachandran R, Mitchell JE, Dawant BM, Fitzpatrick JM (2009) Accuracy evaluation of MicroTargetingTM platforms for deep-brain stimulation using virtual targets. IEEE Trans Biomed Eng 56(1): 37–44

    Article  PubMed  Google Scholar 

  35. D’Haese P-F, Pallavaram S, Yu H, Spooner J, Konrad PE, Dawant BM (2006) Deformable physiological atlas-based programming of deep brain stimulators: a feasibility study. Lecture notes in computer science (WBIR), vol 4057. Utrecht, The Netherlands, pp 144–150

  36. Rohde GK, Aldroubi A, Dawant BM (2003) The adaptive bases algorithm for intensity-based nonrigid image registration. IEEE Trans Med Imaging 22(11): 1470–1479

    Article  PubMed  Google Scholar 

  37. Maes F, Collignon A, Suetens P (1997) Multimodality image registration by maximization of mutual information. in IEEE Trans Med Imaging 16(2): 187–198

    Article  CAS  Google Scholar 

  38. Wells WM, Viola P, Atsumi H, Nakajima S, Kikinis R (1996) Multi-modal volume registration by maximization of mutual information. Med Image Anal 1(1): 35–52

    Article  PubMed  Google Scholar 

  39. Pluim JP, Maintz JB, Viergever MA (2003) Mutual-information-based registration of medical images: a survey. IEEE Trans Med Imaging 22(8): 986–1004

    Article  PubMed  Google Scholar 

  40. Rosenbaum BP, D’Haese P-F, Yu H, Pallavaram S, Dawant BM, Neimat JS, Konrad PE (2008) Brain shift during deep brain stimulation surgery correlates directly to pneumocephalus and inversely to age. In: American Society of Sterotactic and Functional Neurosurgery (ASSFN) Biennial meeting Vancouver, BC, Canada

  41. Butson CR, McIntyre CC (2008) Current steering to control the volume of tissue activated during deep brain stimulation. Brain Stimul 1(1): 7–15

    Article  Google Scholar 

  42. Pallavaram S, Dawant BM, Koyama T, Yu H, Neimat JS, Konrad PE, D’Haese P-F (2009) Validation of a fully automatic method for the routine selection of the anterior and posterior commissures in MR images. J Stereotact Funct Neurosurg 87: 148–154

    Article  Google Scholar 

  43. The Deep Brain Stimulation for Parkinson’s disease study group (2001) Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson’s disease. N Engl J Med 345:956–963

    Google Scholar 

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Correspondence to Benoit M. Dawant.

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Pallavaram, S., Dawant, B.M., Remple, M.S. et al. Effect of brain shift on the creation of functional atlases for deep brain stimulation surgery. Int J CARS 5, 221–228 (2010). https://doi.org/10.1007/s11548-009-0391-1

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