Surface-Based Display of Volume-Averaged Cerebellar Imaging Data
Jörn Diedrichsen, Ewa Zotow, Jörn Diedrichsen, Ewa Zotow
Abstract
The paper presents a flat representation of the human cerebellum, useful for visualizing functional imaging data after volume-based normalization and averaging across subjects. Instead of reconstructing individual cerebellar surfaces, the method uses a white- and grey-matter surface defined on volume-averaged anatomical data. Functional data can be projected along the lines of corresponding vertices on the two surfaces. The flat representation is optimized to yield a roughly proportional relationship between the surface area of the 2D-representation and the volume of the underlying cerebellar grey matter. The map allows users to visualize the activation state of the complete cerebellar grey matter in one concise view, equally revealing both the anterior-posterior (lobular) and medial-lateral organization. As examples, published data on resting-state networks and task-related activity are presented on the flatmap. The software and maps are freely available and compatible with most major neuroimaging packages.
Conflict of interest statement
Competing Interests: The authors have declared that no competing interests exist.
Figures
![Fig 1. Representation of individual fingers in…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4521932/bin/pone.0133402.g001.jpg)
![Fig 2. Surfaces defined on a group-averaged…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4521932/bin/pone.0133402.g002.jpg)
![Fig 3. Distortion of the flatmap in…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4521932/bin/pone.0133402.g003.jpg)
![Fig 4. Surface-based mapping pipeline for cerebellar…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4521932/bin/pone.0133402.g004.jpg)
![Fig 5. Probabilistic atlas of the cerebellar…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4521932/bin/pone.0133402.g005.jpg)
![Fig 6. Atlas of cerebellar-cortical connectivity.](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4521932/bin/pone.0133402.g006.jpg)
![Fig 7. Functional activity maps from the…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4521932/bin/pone.0133402.g007.jpg)
References
- Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage. 1999;9(2):179–94. 10.1006/nimg.1998.0395
- Van Essen DC. Surface-based atlases of cerebellar cortex in the human, macaque, and mouse. Ann N Y Acad Sci. 2002;978:468–79.
- Van Essen DC, Dickson J, Harwell J, Hanlon D, Anderson CH, Drury HA. An Integrated Software System for Surface-based Analyses of Cerebral Cortex. Journal of American Medical Informatics Association. 2001;41:1359–78.
- Van Essen DC. Surface-based approaches to spatial localization and registration in primate cerebral cortex. Neuroimage. 2004;23 Suppl 1:S97–107.
- Fischl B, Sereno MI, Tootell RB, Dale AM. High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp. 1999;8(4):272–84.
- Van Essen DC. A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. Neuroimage. 2005;28(3):635–62.
- Tucholka A, Fritsch V, Poline JB, Thirion B. An empirical comparison of surface-based and volume-based group studies in neuroimaging. Neuroimage. 2012;63(3):1443–53. 10.1016/j.neuroimage.2012.06.019
- Oosterhof NN, Wiestler T, Downing PE, Diedrichsen J. A comparison of volume-based and surface-based multi-voxel pattern analysis. Neuroimage. 2011;56(2):593–600. 10.1016/j.neuroimage.2010.04.270
- Braitenberg V, Atwood RP. Morphological observations on the cerebellar cortex. The Journal of comparative neurology. 1958;109(1):1–33.
- Sultan F, Braitenberg V. Shapes and sizes of different mammalian cerebella. A study in quantitative comparative neuroanatomy. Journal fur Hirnforschung. 1993;34(1):79–92.
- Sereno MI, Diedrichsen J, Tachrout M, Silva G, De Zeeuw CI, editors. Reconstruction and unfolding of the human cerbellar cortex from high-resolution post-mortem MRI. Annual meeting of the Society for Neuroscience 2014; Washington, DC.
- Diedrichsen J. A spatially unbiased atlas template of the human cerebellum. Neuroimage. 2006;33(1):127–38.
- Ashburner J, Friston KJ. Unified segmentation. Neuroimage. 2005;26(3):839–51.
- Ashburner J. A fast diffeomorphic image registration algorithm. Neuroimage. 2007;38(1):95–113. 10.1016/j.neuroimage.2007.07.007
- Klein A, Andersson J, Ardekani BA, Ashburner J, Avants B, Chiang MC, et al. Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. Neuroimage. 2009;46(3):786–802. 10.1016/j.neuroimage.2008.12.037
- Diedrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani N. A probabilistic MR atlas of the human cerebellum. Neuroimage. 2009;46(1):39–46. 10.1016/j.neuroimage.2009.01.045
- Wiestler T, McGonigle DJ, Diedrichsen J. Integration of sensory and motor representations of single fingers in the human cerebellum. J Neurophysiol. 2011;105(6):3042–53. 10.1152/jn.00106.2011
- Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BT. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106(5):2322–45. 10.1152/jn.00339.2011
- Van Essen DC, Smith SM, Barch DM, Behrens TE, Yacoub E, Ugurbil K. The WU-Minn Human Connectome Project: an overview. Neuroimage. 2013;80:62–79. 10.1016/j.neuroimage.2013.05.041
- Barch DM, Burgess GC, Harms MP, Petersen SE, Schlaggar BL, Corbetta M, et al. Function in the human connectome: task-fMRI and individual differences in behavior. Neuroimage. 2013;80:169–89. 10.1016/j.neuroimage.2013.05.033
- Andersson JL, Smith SM, Jenkinson M, editors. FNIRT—FMRIB's Non-linear Image Registration Tool. Organization for Human Brain Mapping; 2008.
- Friston K, Holmes AP, Ashburner J. Statistical parameter mapping (SPM). 1999.
- Yeo BT, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M, et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106(3):1125–65. 10.1152/jn.00338.2011
- Glasser MF, Sotiropoulos SN, Wilson JA, Coalson TS, Fischl B, Andersson JL, et al. The minimal preprocessing pipelines for the Human Connectome Project. Neuroimage. 2013;80:105–24. 10.1016/j.neuroimage.2013.04.127
- Worsley KJ, Marrett S, Neelin P, Vandal AC, Friston KJ, Evans AC. A unified statistical approach for determining significant voxels in images of cerebral activation. Hum Brain Mapp. 1996;12:900–18.
- Diedrichsen J. Cerebellar toolbox (SUIT). 2015. Available from: . 10.6084/m9.figshare.1485637.
- Schmahmann JD, Doyon J, McDonald D, Holmes C, Lavoie K, Hurwitz AS, et al. Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space. Neuroimage. 1999;10(3 Pt 1):233–60. 10.1006/nimg.1999.0459
- Larsell O. [The corpus cerebelli in birds & mammals.]. Arch Sci Biol (Bologna). 1958;42(1):90–104.
- Larsell O, Jansen J. The comparative anatomy and histology of the cerebellum The human cerebellum, cerebellar connections and cerebellar cortex. Minneapolis: The University of Minnesota Press; 1972.
- Balsters JH, Cussans E, Diedrichsen J, Phillips KA, Preuss TM, Rilling JK, et al. Evolution of the cerebellar cortex: the selective expansion of prefrontal-projecting cerebellar lobules. Neuroimage. 2010;49(3):2045–52. 10.1016/j.neuroimage.2009.10.045
- Badre D. Cognitive control, hierarchy, and the rostro-caudal organization of the frontal lobes. Trends Cogn Sci. 2008;12(5):193–200. 10.1016/j.tics.2008.02.004
- Grodd W, Hülsmann E, Lotze M, Wildgruber D, Erb M. Sensorimotor mapping of the human cerebellum: fMRI evidence of somatotopic organization. Hum Brain Mapp. 2001;13(2):55–73.
- Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage. 2009;44(2):489–501. 10.1016/j.neuroimage.2008.08.039
- E KH, Chen SH, Ho MH, Desmond JE. A meta-analysis of cerebellar contributions to higher cognition from PET and fMRI studies. Hum Brain Mapp. 2014;35(2):593–615. 10.1002/hbm.22194
- Salmi J, Pallesen KJ, Neuvonen T, Brattico E, Korvenoja A, Salonen O, et al. Cognitive and motor loops of the human cerebro-cerebellar system. Journal of Cognitive Neuroscience. 2010;22(11):2663–76. 10.1162/jocn.2009.21382
- Stoodley CJ. The cerebellum and cognition: evidence from functional imaging studies. Cerebellum. 2012;11(2):352–65. 10.1007/s12311-011-0260-7
- Lee GP, Meador KJ, Loring DW, Allison JD, Brown WS, Paul LK, et al. Neural substrates of emotion as revealed by functional magnetic resonance imaging. Cognitive and Behavioral Neurology. 2004;17(1):9–17.
- Liotti M, Mayberg HS, Brannan SK, McGinnis S, Jerabek P, Fox PT. Differential limbic–cortical correlates of sadness and anxiety in healthy subjects: implications for affective disorders. Biological psychiatry. 2000;48(1):30–42.
- Schraa-Tam CK, Rietdijk WJ, Verbeke WJ, Dietvorst RC, van den Berg WE, Bagozzi RP, et al. fMRI activities in the emotional cerebellum: a preference for negative stimuli and goal-directed behavior. Cerebellum. 2012;11(1):233–45. 10.1007/s12311-011-0301-2
- Shaikh AG, Marti S, Tarnutzer AA, Palla A, Crawford TO, Straumann D, et al. Ataxia telangiectasia: a "disease model" to understand the cerebellar control of vestibular reflexes. J Neurophysiol. 2011;105(6):3034–41. 10.1152/jn.00721.2010
- Jack A, Pelphrey KA. Neural Correlates of Animacy Attribution Include Neocerebellum in Healthy Adults. Cerebral cortex. 2014. 10.1093/cercor/bhu146
- Van Overwalle F, Baetens K, Marien P, Vandekerckhove M. Social cognition and the cerebellum: a meta-analysis of over 350 fMRI studies. Neuroimage. 2014;86:554–72. 10.1016/j.neuroimage.2013.09.033
- McDermott KB, Petersen SE, Watson JM, Ojemann JG. A procedure for identifying regions preferentially activated by attention to semantic and phonological relations using functional magnetic resonance imaging. Neuropsychologia. 2003;41(3):293–303.
- Binder JR, Frost JA, Hammeke TA, Cox RW, Rao SM, Prieto T. Human brain language areas identified by functional magnetic resonance imaging. The Journal of Neuroscience. 1997;17(1):353–62.
- Tukey JW. Exploratory data analysis: Addison-Wesley; 1977.
- Tufte ER. The visual display of quantitative information. Cheshire, CT: Graphics Press; 1983.
- Voogd J. Cerebellum and precerebellar nuclei In: Paxinos G, Mai J, editors. Human Nervous System. 2nd Edition ed: Elsevier; 2004. p. 321–92.
- Sugihara I, Shinoda Y. Molecular, topographic, and functional organization of the cerebellar cortex: a study with combined aldolase C and olivocerebellar labeling. J Neurosci. 2004;24(40):8771–85. 10.1523/jneurosci.1961-04.2004
- Andersson G, Oscarsson O. Climbing fiber microzones in cerebellar vermis and their projection to different groups of cells in the lateral vestibular nucleus. Experimental brain research. 1978;32(4):565–79.
- Glickstein M, Sultan F, Voogd J. Functional localization in the cerebellum. Cortex; a journal devoted to the study of the nervous system and behavior. 2011;47(1):59–80. 10.1016/j.cortex.2009.09.001
- De Zeeuw CI, Simpson JI, Hoogenraad CC, Galjart N, Koekkoek SK, Ruigrok TJ. Microcircuitry and function of the inferior olive. Trends Neurosci. 1998;21(9):391–400. S0166-2236(98)01310-1 [pii].
- Ashburner J, Friston KJ. Voxel-based morphometry—the methods. Neuroimage. 2000;11(6 Pt 1):805–21.
- Buckner RL. The cerebellum and cognitive function: 25 years of insight from anatomy and neuroimaging. Neuron. 2013;80(3):807–15. 10.1016/j.neuron.2013.10.044
- Diedrichsen J, Maderwald S, Kuper M, Thurling M, Rabe K, Gizewski ER, et al. Imaging the deep cerebellar nuclei: a probabilistic atlas and normalization procedure. Neuroimage. 2011;54(3):1786–94. 10.1016/j.neuroimage.2010.10.035
- Timmann D, Konczak J, Ilg W, Donchin O, Hermsdorfer J, Gizewski ER, et al. Current advances in lesion-symptom mapping of the human cerebellum. Neuroscience. 2009;162(3):836–51. 10.1016/j.neuroscience.2009.01.040
- Andersen BB, Gundersen HJ, Pakkenberg B. Aging of the human cerebellum: a stereological study. The Journal of comparative neurology. 2003;466(3):356–65. 10.1002/cne.10884
Source: PubMed