Brain Imaging and Behavior

, 3:332 | Cite as

A Comparison of Voxel-Based Morphometry and Volumetry Methods in the Context of the Neural Basis of Aggression

  • Britt C. Emerton
  • Matthew Jerram
  • Thilo Deckersbach
  • Darin D. Dougherty
  • Carl Fulwiler
  • David A. Gansler
Article

Abstract

The assumption that voxel-based morphometry (VBM) offers an automated substitution for manually-traced volumetry was subjected to empirical evaluation. Data available from a previous volumetry study (Gansler et al. Psychiatry Research: Neuroimaging 171:145–154, 2009) provided the basis for the current study, which assessed for convergence between the methods. Optimized modulated VBM was used to preprocess images (N = 40). Gray matter volume and self-reported aggression associations were tested. Results indicate convergence, as both methods revealed significant negative associations of the left orbitofrontal cortex (OFC) and aggression. VBM detected an additional positive left OFC result not revealed with volumetry, suggesting that VBM may allow greater within-region localization than volumetry. However, the methods differentially deal with error rates and power demands and as such are better conceptualized as complementary than interchangeable.

Keywords

Volumetry Voxel-based morphometry Orbital frontal cortex Aggression 

References

  1. Allen, J. S., Bruss, J., Brown, C. K., & Damasio, H. (2005). Methods for studying the aging brain: volumetric analysis versus VBM. Neurobiology of Aging, 26, 1275–1278.CrossRefGoogle Scholar
  2. American Psychiatric Association. (2000). The Diagnostic and statistical manual of mental disorders (4th ed. Text Revision). Washington DC: American Psychiatric Association.CrossRefGoogle Scholar
  3. Andreasen, N. C., Cizadlo, T., Harris, G., Swayze, V., O’Leary, D. S., Cohen, G., et al. (1993). Voxel processing techniques for the antemortem study of neuroanatomy using magnetic resonance imaging. Journal of Neuropsychiatry and Clinical Neurosciences, 5, 121–130.PubMedGoogle Scholar
  4. Antonucci, A. S., Gansler, D. A., Tan, S., Bhadelia, R., Patz, S., & Fulwiler, C. (2006). Orbitofrontal correlates of aggression and impulsivity in psychiatric patients. Psychiatry Research: Neuroimaging, 147, 213–220.CrossRefPubMedGoogle Scholar
  5. Asami, T., Hayano, F., Nakamura, M., Yamasue, H., Uehara, K., Otsuka, T., et al. (2008). Anterior cingulate cortex volume reduction in patients with panic disorder. Psychiatry and Clinical Neurosciences, 62, 322–330.CrossRefPubMedGoogle Scholar
  6. Ashburner, J., & Friston, K. J. (2000). Voxel-based morphometry—the methods. Neuroimage, 11, 805–821.CrossRefPubMedGoogle Scholar
  7. Ashburner, J., & Friston, K. J. (2001). Why voxel-based morphometry should be used. Neuroimage, 14, 1238–1243.CrossRefPubMedGoogle Scholar
  8. Barbas, H., & Zikopoulos, B. (2006). Sequential and parallel circuits for emotional processing in primate orbitofrontal cortex. In D. H. Zald & S. L. Rauch (Eds.), The Orbitofrontal Cortex (pp. 57–91). Oxford: Oxford University Press.Google Scholar
  9. Baxendale, S. A., Van Paesschen, W., Thompson, P. J., Duncan, J. S., Shorvon, S. D., & Connelly, A. (1997). The relation between quantitative MRI measures of hippocampal structure and the intracarotid amobarbital test. Epilepsia, 38, 998–1007.CrossRefPubMedGoogle Scholar
  10. Bigler, E. D., & Clement, P. F. (1997). Overview of functional neuroanatomy. In E. D. Bigler & P. F. Clement (Eds.), Diagnostic clinical neuropsychology (3rd ed., pp. 1–48). Austin, TX: University of Texas Press.Google Scholar
  11. Blair, R. J. R. (2007). Dysfunctions of medial and lateral orbitofrontal cortex in psychopathy. Annals of the New York Academy of Sciences, 1121, 461–479.CrossRefPubMedGoogle Scholar
  12. Blatter, D. D., Bigler, E. D., Gale, S. D., Johnson, S. C., Anderson, C. V., Burnett, B. M., et al. (1995). Quantitative volumetric analysis of brain MR: normative database spanning 5 decades of life. American Journal of Neuroradiology, 16, 241–251.PubMedGoogle Scholar
  13. Bookstein, F. L. (2001). “Voxel-based morphometry” should not be used with imperfectly registered images. Neuroimage, 14, 1454–1462.CrossRefPubMedGoogle Scholar
  14. Brett, M., Anton, J., Valabregue, R., & Poline, J. (2002, June). Region of interest analysis using an SPM toolbox. Presented at the 8th International Conference on Functional Mapping of the Human Brain, Sendai, Japan.Google Scholar
  15. Chiavaras, M. M., LeGoualher, G., Evans, A., & Petrides, M. (2001). Three-dimensional probabilistic atlas of the human orbitofrontal sulci in standardized stereotaxic space. Neuroimage, 13, 479–496.CrossRefPubMedGoogle Scholar
  16. Coccaro, E., Berman, M., & Kavoussi, R. (1997). Assessment of life history of aggression: development and psychometric characteristics. Psychiatry Research, 73, 147–157.CrossRefPubMedGoogle Scholar
  17. Coccaro, E. F., McCloskey, M. S., Fitzgerald, D. A., & Phan, K. L. (2007). Amygdala and orbitofrontal reactivity to social threat in individuals with impulsive aggression. Biological Psychiatry, 62, 168–178.CrossRefPubMedGoogle Scholar
  18. Collins, D. L., Neelin, P., Peters, T. M., & Evans, A. C. (1994). Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. Journal of Computer Assisted Tomography, 18, 192–205.CrossRefPubMedGoogle Scholar
  19. Crespo-Facorro, B., Kim, J. J., Andreasen, N. C., O’Leary, D. S., Wiser, A. K., Bailey, J. M., et al. (1999). Human frontal cortex: an MRI-based parcellation method. NeuroImage, 10, 500–519.CrossRefPubMedGoogle Scholar
  20. Cui, X. & Li, J. (2005). XjView 4.0 [Computer software] Retrieved April 2008 from http://people.hnl.bcm.tmc.edu/cuixu/xjView
  21. Damasio, H., & Damasio, A. R. (1989). Lesion analysis in neuropsychology. New York: Oxford University Press.Google Scholar
  22. Davatzikos, C. (2004). Why voxel-based morphometric analysis should be used with great caution when characterizing group differences. Neuroimage, 23, 17–20.CrossRefPubMedGoogle Scholar
  23. Di Virgilio, G., Clarke, S., Pizzolato, G., & Schaffner, T. (1999). Cortical regions contributing to the anterior commissure in man. Experimental Brain Research, 124, 1–7.CrossRefGoogle Scholar
  24. Dougherty, D. D., Rauch, S. L., Deckersbach, T., Marci, C., Loh, R., Shin, L. M., et al. (2004). Ventromedial prefrontal cortex and amygdala dysfunction during an anger induction positron emission tomography study in patients with major depressive disorder with anger attacks. Archives of General Psychiatry, 61(8), 795–804.CrossRefPubMedGoogle Scholar
  25. Douaud, G., Gaura, V., Riberio, M. J., Lethimonnier, F., Maroy, R., Verny, C., et al. (2006). Distribution of gray matter atrophy in Huntington’s disease patients: a combined ROI-based and voxel-based morphometric study. Neuroimage, 32, 1562–1575.CrossRefPubMedGoogle Scholar
  26. Duvernoy, H. (1991). The human brain surface, blood supply, and three-dimensional sectional anatomy (2nd ed.). New York: Springer-Verlag/Wien.Google Scholar
  27. Eckert, M. A., Lombardino, L. J., Walczak, A. R., Bonihla, L., Leonard, C. M., & Binder, J. R. (2008). Manual and automated measures of superior temporal gyrus asymmetry: concordant structural predictors of verbal ability in children. Neuroimage, 41, 813–822.CrossRefPubMedGoogle Scholar
  28. Emerton, B. C., Jerram, M., Fulwiler, C., Gansler, D. A. (2008, June). A VBM based exploration of MRI acquisition protocol variance. Poster session presented at the annual meeting of the American Academy of Clinical Neuropsychology, Boston, MA.Google Scholar
  29. Galton, C. J., & Hodges, J. R. (2004). Morphometric brain analysis in the dementias. In M. Rizzo & P. J. Eslinger (Eds.), Principles and practice of behavioral neurology and neuropsychology (pp. 81–89). Philadelphia, PA: W.B. Saunders Company.Google Scholar
  30. Gansler, D. A., McLaughlin, N. C. R., Iguchi, L., Jerram, M., Moore, D. W., Bhadelia, R., et al. (2009). A multivariate approach to aggression and the orbital frontal cortex in psychiatric patients. Psychiatry Research: Neuroimaging, 171, 145–154.CrossRefPubMedGoogle Scholar
  31. Gaser, C. (2006) VBM2 version 1.06 [Computer software] Retrieved April 2007, from http://dbm.neuro.uni-jena.de/additional-functions-in-vbm2
  32. Ghashghaei, H. T., & Barbas, H. (2002). Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience, 115, 1261–1279.CrossRefPubMedGoogle Scholar
  33. Good, C. D., Johnsrude, I. S., Ashburner, J., Henson, R. N., Friston, K. J., & Frackowiak, R. S. (2001). Neuroimage, 14, 21–36.CrossRefPubMedGoogle Scholar
  34. Giuliani, N. R., Calhoun, V. D., Pearlson, G. D., Francis, A., & Buchanan, R. W. (2005). Voxel-based morphometry versus region of interest: a comparison of two methods for analyzing gray matter differences in schizophrenia. Schizophrenia Research, 74, 135–147.CrossRefPubMedGoogle Scholar
  35. Hoptman, M. J., Volavka, J., Weiss, E. M., Czobor, P., Szeszko, P. R., Gerig, G., et al. (2005). Quantitative MRI measures of orbitofrontal cortex in patients with chronic schizophrenia or schizoaffective disorder. Psychiatry Research: Neuroimaging, 140, 133–145.CrossRefPubMedGoogle Scholar
  36. Jack, C. R., Petersen, R. C., Xu, Y. C., O’Brien, P. C., & Tangalos, E. G. (1992a). MR-based hippocampal volumetry in the diagnosis of Alzheimer’s disease. Neurology, 42, 183–188.Google Scholar
  37. Jack, C. R., Sharbrough, F. W., Cascino, G. D., Hischorn, K. A., O’Brien, P. C., & Marsh, W. R. (1992b). Magnetic resonance image-based hippocampal volumetry: correlations with outcome after temporal lobectomy. Annals of Neurology, 31, 138–146.CrossRefGoogle Scholar
  38. Jack, C. R., Petersen, R. C., Xu, Y. C., O’Brien, P. C., Smith, G. E., Ivnik, R. J., et al. (1999). Prediction of AD with MRI-based hippocampal volume in mild cognitive impairment. Neurology, 52, 1397–1403.PubMedGoogle Scholar
  39. Jernigan, T. L., Archibald, S. L., Berhow, M. T., Sowell, E. R., Foster, D. S., & Hesselink, J. R. (1991a). Cerebral structure on MRI, part I: localization of age-related changes. Biological Psychiatry, 29, 55–67.CrossRefGoogle Scholar
  40. Jernigan, T. L., Salmon, D. P., Butters, N., & Hesselink, J. R. (1991b). Cerebral structure on MRI, part II: specific changes in Alzheimer’s and Huntington’s diseases. Biological Psychiatry, 29, 68–81.CrossRefGoogle Scholar
  41. Job, D. E., Whalley, H. C., McConnell, S., Glabus, M., Johnstone, E. C., & Lawrie, S. M. (2002). Structural gray matter differences between first-episode schizophrenics and normal controls using voxel-based morphometry. Neuroimage, 17, 880–889.CrossRefPubMedGoogle Scholar
  42. Job, D. E., Whalley, H. C., McConnell, S., Glabus, M., Johnstone, E. C., & Lawrie, S. M. (2003). Voxel-based morphometry of grey matter densities in subjects at high risk of schizophrenia. Schizophrenia Research, 64, 1–13.CrossRefPubMedGoogle Scholar
  43. Juh, R., Su, M., Lee, C., Suh, T., & Nalcioglu, O. (2006). Investigate between the voxel based morphometry and regions of interest study in Alzheimer’s disease. Medical Physics, 33, 2020.CrossRefGoogle Scholar
  44. Kassubek, J., Juengling, F. D., Kioschies, T., Henkel, K., Karitzky, J., Kramer, B., et al. (2004). Topography of cerebral atrophy in early Huntington’s disease: a voxel based morphometric MRI study. Journal of Neurology, Neurosurgery, & Psychiatry, 75, 213–220.Google Scholar
  45. Kaufman, W. E., & Nagae-Poetscher, L. M. (2004). Structural brain imaging in neurodevelopmental disorders. In M. Rizzo & P. J. Eslinger (Eds.), Principles and practice of behavioral neurology and neuropsychology (pp. 91–114). Philadelphia, PA: W.B. Saunders Company.Google Scholar
  46. Kennedy, K. M., Erickson, K. I., Rodrigue, K. M., Voss, M. W., Colcombe, S. J., Kramer, A. F., et al. (2009). Age-related differences in regional brain volumes: A comparison of optimized voxel-based morphometry to manual volumetry. Neurobiology of Aging (in press).Google Scholar
  47. Kubicki, M., Shenton, M. C., Salisbury, D. F., Hirayasu, Y., Kasai, K., Kikinis, R., et al. (2002). Voxel-based morphometric analysis of gray matter in first episode schizophrenia. Neuroimage, 17, 1711–1719.CrossRefPubMedGoogle Scholar
  48. Lezak, M. D., Howieson, D. B., & Loring, D. W. (2004). The behavioral geography of the brain. In M. D. Lezak, D. B. Howieson & D. W. Loring (Eds.), Neuropsychological assessment (4th ed., pp. 39–85). New York: Oxford University Press.Google Scholar
  49. Luders, E., Gaser, C., Jancke, L., & Schlaug, G. (2004). A voxel-based approach to gray matter asymmetries. Neuroimage, 22, 656–664.CrossRefPubMedGoogle Scholar
  50. Makale, M., Solomon, J., Patronas, N. J., Danek, A., Butman, J. A., & Grafman, J. (2002). Quantification of brain lesions using interactive automated software. Behavior Research Methods, Instruments, & Computers, 34(1), 6–18.Google Scholar
  51. Mechelli, A., Price, C. J., Friston, K. J., & Ashburner, J. (2005). Voxel-based morphometry of the human brain: methods and applications. Current Medical Imaging Reviews, 1, 1–9.CrossRefGoogle Scholar
  52. Medx User’s Guide (2002) [Computer software and manual]. Sensor Systems, Inc.Google Scholar
  53. Raine, A., Lencz, T., Bihrle, S., LaCasse, L., & Colletti, P. (2000). Reduced prefrontal gray matter volume and reduced autonomic activity in antisocial personality disorder. Archives of General Psychiatry, 57, 119–127.CrossRefPubMedGoogle Scholar
  54. Rizzo, M., & Eslinger, P. J. (2004). Overview and introduction. In M. Rizzo & P. J. Eslinger (Eds.), Principles and practice of behavioral neurology and neuropsychology (pp. 3–21). Philadelphia, PA: W.B. Saunders Company.Google Scholar
  55. Rusch, N., Spoletini, I., Wilke, M., Martinotti, G., Bria, P., Trequatrrini, A., et al. (2008). Inferior frontal white matter volume and suicidality in schizophrenia. Psychiatry Research: Neuroimaging, 164, 206–214.CrossRefPubMedGoogle Scholar
  56. Salmond, C. H., Ashburner, J., Vargha-Khadem, F., Connelly, A., Gadian, D. G., & Friston, K. J. (2002). Distributional assumptions in voxel-based morphometry. Neuroimage, 7, 1027–1030.CrossRefGoogle Scholar
  57. Talairach, J., & Tournoux, P. (1988). Co-planar sterotaxic atlas of the human brain: 3-dimensional proportional system, an appraoch to cerebral imaging. New York: Thieme Medical Publishers.Google Scholar
  58. Testa, C., Laakso, M. P., Sbattoli, F., Rossi, R., Beltramello, A., Soininen, H., et al. (2004). A comparison between the accuracy of voxel-based morphometry and hippocampal volumetry in Alzheimer’s disease. Journal of Magnetic Resonance Imaging, 19, 274–282.CrossRefPubMedGoogle Scholar
  59. Tiihonen, J., Rossi, R., Laakso, M. P., Hodgins, S., Testa, C., Perez, J., et al. (2008). Brain anatomy of persistent violent offenders: more rather than less. Psychiatry Research: Neuroimaging, 163, 201–212.CrossRefPubMedGoogle Scholar
  60. Tisserand, D. J., Pruessner, J. C., Sanz Arigita, E. J., van Boxtel, M. P. J., Evans, A. C., Jolles, J., et al. (2002). Regional frontal cortical volumes decrease differentially in aging: an MRI study to compare volumetric approaches and voxel-based morphometry. Neuroimage, 17, 657–669.CrossRefPubMedGoogle Scholar
  61. Tisserand, D. J., van Boxtel, M. P. J., Pruessner, J. C., Hofman, P., Evans, A. C., & Jolle, J. (2004). A voxel-based morphometric study to determine individual differences in gray matter density associated with age and cognitive change over time. Cerebral Cortex, 14, 966–973.CrossRefPubMedGoogle Scholar
  62. Thompson, P. M., Mega, M. S., Woods, R. P., Zoumalan, C. I., Lindshield, C. J., Blanton, R. E., et al. (2001). Cortical change in Alzheimer’s disease detected with a disease-specific population-based brain atlas. Cerebral Cortex, 11, 1–16.CrossRefPubMedGoogle Scholar
  63. Tomaiuolo, F., MacDonald, J. D., Caramanos, Z., Posner, G., Chiavaras, M., Evans, A. C., et al. (1999). Morphology, morphometry and probability mapping of the pars opercularis of the inferior frontal gyrus: an in vivo MRI analysis. European Journal of Neuroscience, 11, 3033–3046.CrossRefPubMedGoogle Scholar
  64. Uchida, R. R., Del-Ben, C. M., Araujo, D., Busatto-Filho, G., Duran, F. L. S., Crippa, J. A. S., et al. (2008). Correlation between voxel based morphometry and manual volumetry in magnetic resonance images of the human brain. Annals of the Brazilian Academy of Sciences, 80, 149–156.Google Scholar
  65. Zald, D. H., & Rauch, S. L. (2006). In D. H. Zald & S. L. Rauch (Eds.), The Orbitofrontal Cortex (preface pages vi–ix). Oxford, United Kingdom: Oxford University Press.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Britt C. Emerton
    • 1
  • Matthew Jerram
    • 1
  • Thilo Deckersbach
    • 2
  • Darin D. Dougherty
    • 2
  • Carl Fulwiler
    • 3
    • 4
  • David A. Gansler
    • 1
    • 4
    • 5
  1. 1.Department of PsychologySuffolk UniversityBostonUSA
  2. 2.Department of PsychiatryHarvard Medical SchoolBostonUSA
  3. 3.Department of PsychiatryUniversity of Massachusetts Medical SchoolBostonUSA
  4. 4.Clinical Neuroscience ServiceLemuel Shattuck HospitalBostonUSA
  5. 5.Department of PsychiatryTufts University School of MedicineBostonUSA

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