Quantification of Brain Images Using Korean Standard Templates and Structural and Cytoarchitectonic Probabilistic Maps

한국인 뇌 표준판과 해부학적 및 세포구축학적 확률뇌지도를 이용한 뇌영상 정량화

  • Lee, Jae-Sung (Departments of Nuclear Medicine, Seoul National University) ;
  • Lee, Dong-Soo (Departments of Nuclear Medicine, Seoul National University) ;
  • Kim, Yu-Kyeong (Departments of Nuclear Medicine, Seoul National University) ;
  • Kim, Jin-Su (Departments of Nuclear Medicine, Seoul National University) ;
  • Lee, Jong-Min (Department of Biomedical Engineering, Hanyang University) ;
  • Koo, Bang-Bon (Department of Biomedical Engineering, Hanyang University) ;
  • Kim, Jae-Jin (Department of Neuropsychiatry, Yonsei University) ;
  • Kwon, Jun-Soo (Department of Neuropsychiatry, Seoul National University) ;
  • Yoo, Tae-Woo (Department of Family Medicine, Seoul National University) ;
  • Chang, Ki-Hyun (Department of Diagnostic Radiology, Seoul National University) ;
  • Kim, Sun-I. (Department of Biomedical Engineering, Hanyang University) ;
  • Kang, Hye-Jin (Departments of Nuclear Medicine, Seoul National University) ;
  • Kang, Eun-Joo (Departments of Nuclear Medicine, Seoul National University)
  • Published : 2004.06.30

Abstract

Purpose: Population based structural and functional maps of the brain provide effective tools for the analysis and interpretation of complex and individually variable brain data. Brain MRI and PET standard templates and statistical probabilistic maps based on image data of Korean normal volunteers have been developed and probabilistic maps based on cytoarchitectonic data have been introduced. A quantification method using these data was developed for the objective assessment of regional intensity in the brain images. Materials and Methods: Age, gender and ethnic specific anatomical and functional brain templates based on MR and PET images of Korean normal volunteers were developed. Korean structural probabilistic maps for 89 brain regions and cytoarchitectonic probabilistic maps for 13 Brodmann areas were transformed onto the standard templates. Brain FDG PET and SPGR MR images of normal volunteers were spatially normalized onto the template of each modality and gender. Regional uptake of radiotracers in PET and gray matter concentration in MR images were then quantified by averaging (or summing) regional intensities weighted using the probabilistic maps of brain regions. Regionally specific effects of aging on glucose metabolism in cingulate cortex were also examined. Results: Quantification program could generate quantification results for single spatially normalized images per 20 seconds. Glucose metabolism change in cingulate gyrus was regionally specific: ratios of glucose metabolism in the rostral anterior cingulate vs. posterior cingulate and the caudal anterior cingulate vs. posterior cingulate were significantly decreased as the age increased. 'Rostral anterior'/'posterior' was decreased by 3.1% per decade of age ($P<10^{-11}$, r=0.81) and 'caudal anterior'/'posterior' was decreased by 1.7% ($P<10^{-8}$, r=0.72). Conclusion: Ethnic specific standard templates and probabilistic maps and quantification program developed in this study will be useful for the analysis of brain image of Korean people since the difference in shape of the hemispheres and the sulcal pattern of brain relative to age, gender, races, and diseases cannot be fully overcome by the nonlinear spatial normalization techniques.

목적: 다수의 뇌 자료를 기반으로 구성된 통계적 화률뇌지도는 복잡하고 개인적인 편차가 큰 뇌의 형태학적, 기능적 특성을 분석하는데 유용하다. 특히 최근에 한국인의 정상 MR 영상을 기반으로 한 구조적 기능적 뇌 표준판과 구조적 확률뇌지도가 완성되었으며. 부검뇌의 조직절편을 활용한 세포구축학적 확률뇌지도가 도입되었다. 이 연구에서는 이들 자료를 활용하여 뇌 영상의 국소계수를 객관적으로 측정하기 위한 정량화 기법을 개발하였으며, 이를 이용하여 정상 한국인의 뇌 영상자료를 분석하였다. 대상 및 방법 : T1 MRI와 FDG PET에 대한 뇌 표준판을 성별, 연령별로 개발하였으며, 한국인 정상 MR 영상으로 만들어진 89개 뇌 영역의 구조적 확률뇌지도와 독일 율리히 연구센터에서 도입한 13개 브로드만 영역에 대한 세포구축학적 확률뇌지도를 뇌 표준판 위로 각각 비선형 변환하였다. 확률뇌지도에 정의된 각 뇌 영상의 국소계수는 확률에 의한 가중평균 또는 가중합으로 구하였다. 확률뇌지도를 이용한 예비 연구로 정상 노화에 따른 포도당대사의 변화가 대상회 내에서 전 후 위치에 따라 다르게 나타나는 가를 조사하였다. 결과: SPM과의 연계된 사용을 고려하여 Matlab 상에서 작성된 정량화 프로그램은 20초 미만에 1개의 공간정규화된 영상을 처리할 수 있었다. 대상회 포도당 대사에 대한 분석에서 후대상회에 대한 문측-전대상회 및 미측-전대상회의 계수 비는 정상 노화에 따라 매우 유의하게 감소하였다. 즉. 문측-전대상회/후대상회는 매 10년마다 3.1%씩 감소하였으며($P<10^{-11}$, r=0.81) 미측-전대상회/후대상회는 1.7%씩 감소하였다($P<10^{-8}$, r=0.72). 문측-전대상회와 미측-전대상회의 계수비 감소 역시 유의하였다(P<0.0005. r=0.52, 1.5%/year). 결론: 서양인 뇌에 기반한 확률뇌지도는 그동안 제한적으로만 사용되어 왔으나 한국인 뇌 표준판과 확률뇌지도 및 이 연구에서 개발한 정량화 기법은 일반에 공개하기로 하여 더욱 널리 쓰이게 되면 국내 뇌 연구 활성화에 기여할 것으로 기대 된다.

Keywords

References

  1. Toga AW, Thompson PM. Maps of the brain. Anat Rec 2001; 265:37-53 https://doi.org/10.1002/ar.1057
  2. Evans AC, Collins DL, Mills SR, Brown ED, Kelly RL, Peters TM. 3D statistical neuroanatomical models from 305 MRI volumes. Proc IEEE Nucl Sci Symp Med Imag Conf 1993:1813-7
  3. Amunts K, Zilles K. Advances in cytoarchitectonic mapping of the human cerebral cortex. Neuroimaging Clin N Am 2001;11:151-69
  4. Mazziotta JC, Toga AW, Evans A, Fox P, Lancaster J. A probabilistic atlas of the human brain: theory and rationale for its development. Neuroimage 1995;2:89-101 https://doi.org/10.1006/nimg.1995.1012
  5. Kim JS, Lee DS, Lee BI, Lee JS, Shin HW, Chung J-K et al. Probabilistic anatomical labeling of brain structures using statistical probabilistic anatomical maps. Korean J Nucl Med 2002;36:317-24
  6. Lee JS, Wong DF, Zhou Y, Hoehn-Saric R. Localization of neural substrates of worry using $H_{2}$$^{15}O$ PET and probabilistic brain atlas. J Cereb Blood Flow Metab 2003:23(suppl. 1);713 [Abstract]
  7. Friston, KJ, Holmes AP, Worsley KJ, Poline J-P, Frith CD, Frackowiak RSJ. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 1995;2:189-210 https://doi.org/10.1002/hbm.460020402
  8. Talairach J, Tournoux P. Co-planar stereotaxic atlas of the human brain: 3-dimensional proportional system-an approach to cerebral imaging. New York: Thieme Medical Publishers; 1988
  9. Fox PT, Perlmutter JS, Raichle ME. A stereotactic method of anatomical localization for positron emission tomography. J Comput Assist Tomogr 1985;9:141-53 https://doi.org/10.1097/00004728-198501000-00025
  10. Brett M, Johnsrude IS, Owen AM. The problem of functional localization in the human brain. Nat Rev Neurosci 2002;3:243-9 https://doi.org/10.1038/nrn756
  11. Kang KW, Lee DS, Cho JH, Lee JS, Yeo JS, Lee SK, et al. Quantification of F-18 FDG PET images in temporal lobe epilepsy patients using probabilistic brain atlas. Neuroimage 2001;14(1 Pt 1):1-6 https://doi.org/10.1006/nimg.2001.0783
  12. Lee DS, Lee JS, Kang KW, Jang MJ, Lee SK, Chung JK, et al. Disparity of perfusion and glucose metabolism of epileptogenic zones in temporal lobe epilepsy demonstrated by SPM/SPAM analysis on $^{15}O$ water PET, $[^{18}F]$FDG-PET, and $[^{99m}Tc]$-HMPAO SPECT. Epilepsia 2001;42:1515-22 https://doi.org/10.1046/j.1528-1157.2001.21801.x
  13. Lee SK, Lee DS, Yeo JS, Lee JS, Kim YK, Jang MJ, et al. FDG-PET images quantified by probabilistic atlas of brain and surgical prognosis of temporal lobe epilepsy. Epilepsia 2002;43:1032-8 https://doi.org/10.1046/j.1528-1157.2002.29701.x
  14. Kang E, Lee DS, Lee JS, Kang H, Hwang CH, Oh SH, et al. Developmental hemispheric asymmetry of interregional metabolic correlation of the auditory cortex in deaf subjects. Neuroimage 2003;19:777-83 https://doi.org/10.1016/S1053-8119(03)00118-6
  15. Lee HY, Paeng JC, Lee DS, Lee JS, Oh CW, Cho MJ, et al. Efficacy assessment of cerebral arterial bypass surgery using statistical parametric mapping and probabilistic brain atlas on basal/acetazolamide brain perfusion SPECT. J Nucl Med 2004; 45:202-6
  16. Lee JS, Lee DS, Kang KW, Kim J, Kim YK, Kang E et al. Development of age, gender and ethnic specific anatomical and functional standard brain templates. HBM02 Conf, 2002 [Abstract]
  17. Koo BB, Lee JM, Kim JS, Lee JS, Kim IY, Kim JJ et al., Developing a Korean standard brain atlas on the basis of statistical and probabilistic approach and visualization too for functional image analysis. Korean J Nucl Med 2003;37:162-70
  18. Lee JS, Park KS, Lee DS, Chung J-K, Lee MC, Development of IDL-based software for multimodal image registration. Korean J Nucl Med 2001;35:30P [Abstract]
  19. Yoon U, Lee JM, Kim JJ, Lee SM, Kim IY, Kwon JS, et al. Modified magnetic resonance image based parcellation method for cerebral cortex using successive fuzzy clustering and boundary detection. Ann Biomed Eng 2003;31:441-7 https://doi.org/10.1114/1.1557973
  20. Kim JJ, Crespo-Facorro B, Andreasen NC, O'Leary DS, Zhang B, Harris G, et al. An MRI-based parcellation method for the temporal lobe. Neuroimage 2000;11:271-88 https://doi.org/10.1006/nimg.2000.0543
  21. Crespo-Facorro B, Kim JJ, Andreasen NC, O'Leary DS, Wiser AK, Bailey JM, et al. Human frontal cortex: an MRI-based parcellation method. Neuroimage 1999;10:500-19 https://doi.org/10.1006/nimg.1999.0489
  22. Geyer S, Ledberg A, Schleicher A, Kinomura S, Schormann T, Burgel U, et al. Two different areas within the primary motor cortex of man. Nature 1996;382:805-7 https://doi.org/10.1038/382805a0
  23. Geyer S, Schleicher A, Zilles K. Areas 3a, 3b, and 1 of human primary somatosensory cortex. Neuroimage 1999;10:63-83 https://doi.org/10.1006/nimg.1999.0440
  24. Amunts K, Schleicher A, Burgel U, Mohlberg H, Uylings HB, Zilles K. Broca's region revisited: cytoarchitecture and intersubject variability. J Comp Neurol 1999;412:319-41 https://doi.org/10.1002/(SICI)1096-9861(19990920)412:2<319::AID-CNE10>3.0.CO;2-7
  25. Amunts K, Malikovic A, Mohlberg H, Schormann T, Zilles K. Brodmann's areas 17 and 18 brought into stereotaxic space-where and how variable? Neuroimage 2000;11:66-84
  26. Grefkes C, Geyer S, Schormann T, Roland P, Zilles K. Human somatosensory area 2: observer-independent cytoarchitectonic mapping, interindividual variability, and population map. Neuroimage 2001;14:617-31 https://doi.org/10.1006/nimg.2001.0858
  27. Morosan P, Rademacher J, Schleicher A, Amunts K, Schormann T, Zilles K. Human primary auditory cortex: cytoarchitectonic subdivisions and mapping into a spatial reference system. Neuroimage 2001; 13:684-701
  28. Schormann T, Zilles K. Three-dimensional linear and nonlinear transformations: an integration of light microscopical and MRI data. Hum Brain Mapp 1998;6:339-47 https://doi.org/10.1002/(SICI)1097-0193(1998)6:5/6<339::AID-HBM3>3.0.CO;2-Q
  29. Kim JS, Lee JS, Lee DS, Zilles K, Chung J-K, Lee MC. Nonlinear transformation of cytoarchitectural probabilistic maps of human brain onto Korean standard templates using elastic transformation with full-multigrid. Korean J Nucl Med 2003;37:45P [Abstract]
  30. Petit-Taboue MC, Landeau B, Desson JF, Desgranges B, Baron JC. Effects of healthy aging on the regional cerebral metabolic rate of glucose assessed with statistical parametric mapping. Neuroimage 1998;7:176-84 https://doi.org/10.1006/nimg.1997.0318
  31. Willis MW, Ketter TA, Kimbrell TA, George MS, Herscovitch P, Danielson AL, et al. Age, sex and laterality effects on cerebral glucose metabolism in healthy adults. Psychiatry Res 2002;114:23-37 https://doi.org/10.1016/S0925-4927(01)00126-3
  32. White LE, Lucas G, Richards A, Purves D. Cerebral asymmetry and handedness. Nature 1994;368:197-8 https://doi.org/10.1038/368197a0
  33. Amunts K, Jancke L, Mohlberg H, Steinmetz H, Zilles K. Interhemispheric asymmetry of the human motor cortex related to handedness and gender. Neuropsychologia 2000;38:304-12 https://doi.org/10.1016/S0028-3932(99)00075-5
  34. Thompson PM, Cannon TD, Narr KL, van Erp T, Poutanen VP, Huttunen M, et al. Genetic influences on brain structure. Nat Neurosci 2001;4:1253-8 https://doi.org/10.1038/nn758
  35. Amunts K, Schlaug G, Jäncke L, Steinmetz H, Schleicher A, Dabringhaus A, et al. Motor cortex and hand motor skills: structural compliance in the human brain. Hum Brain Mapp 1997;5:206-15 https://doi.org/10.1002/(SICI)1097-0193(1997)5:3<206::AID-HBM5>3.0.CO;2-7
  36. Zilles K, Kawashima R, Dabringhaus A, Fukuda H, Schormann T. Hemispheric shape of European and Japanese brains: 3-D MRI analysis of intersubject variability, ethnical, and gender differences. Neuroimage 2001;13:262-71
  37. Kochunov P, Fox P, Lancaster J, Tan LH, Amunts K, Zilles K, et al. Localized morphological brain differences between English-speaking Caucasians and Chinese-speaking Asians: new evidence of anatomical plasticity. Neuroreport 2003;14:961-4 https://doi.org/10.1097/00001756-200305230-00011
  38. Lancaster JL, Woldorff MG, Parsons LM, Liotti M, Freitas CS, Rainey L, et al. Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp 2000;10:120-31 https://doi.org/10.1002/1097-0193(200007)10:3<120::AID-HBM30>3.0.CO;2-8
  39. Horwitz B, Amunts K, Bhattacharyya R, Patkin D, Jeffries K, Zilles K. Braun AR. Activation of Broca's area during the production of spoken and signed language: a combined cytoarchitectonic mapping and PET analysis. Neuropsychologia 2003;41:1868-76
  40. Bodegard A, Geyer S, Herath P, Grefkes C, Zilles K, Roland PE. Somatosensory areas engaged during discrimination of steady pressure, spring strength, and kinesthesia. Hum Brain Mapp 2003;20:103-15 https://doi.org/10.1002/hbm.10125