A Template and Probabilistic Atlas of the Human Sensorimotor Tracts using Diffusion MRI

Cerebral Cortex

Volumn 28, Issue 5, 2018, Pages 1685-1699

  Archer, Derek B ^a   Vaillancourt, David E ^a,b,c   Coombes, Stephen A ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c J Crayton Pruitt Family Department of Biomedical Engineering   (United States)

Author keywords

diffusion; movement; sensorimotor; tractography; white matter template

Indexed keywords

ADULT; AGED; ALGORITHM; BRAIN CORTEX; BRAIN MAPPING; CASE REPORT; CEREBROVASCULAR ACCIDENT; CONNECTOME; DIAGNOSTIC IMAGING; DIFFUSION WEIGHTED IMAGING; FEMALE; HUMAN; INFORMATION PROCESSING; MALE; NERVE TRACT; PHYSIOLOGY; PROBABILITY; WHITE MATTER; YOUNG ADULT;

ADULT; AGED; ALGORITHMS; BRAIN MAPPING; CEREBRAL CORTEX; CONNECTOME; DATASETS AS TOPIC; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; HUMANS; MALE; NEURAL PATHWAYS; PROBABILITY; STROKE; WHITE MATTER; YOUNG ADULT;

EID: 85056287595     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhx066     Document Type: Article

References (82)

1. Andersson JL, Sotiropoulos SN. 2015. Non-parametric representation and prediction of single- and multi-shell diffusionweighted MRI data using Gaussian processes. Neuroimage. 122:166-176.
2. Andersson JL, Sotiropoulos SN. 2016. An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. Neuroimage. 125:1063-1078.
3. Archer DB, Misra G, Patten C, Coombes SA. 2016. Microstructural properties of premotor pathways predict visuomotor performance in chronic stroke. Hum Brain Mapp. 37:2039-2054.
4. Barnard JW, Woolsey CN. 1956. A study of localization in the corticospinal tracts of monkey and rat. J Comp Neurol. 105 (1):25-50.
5. Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW. 2007. Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage. 34(1):144-155.
6. Behrens TE, Jenkinson M, Robson MD, Smith SM, Johansen-Berg H. 2006. A consistent relationship between local white matter architecture and functional specialisation in medial frontal cortex. Neuroimage. 30(1):220-227.
7. Behrens TE, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CA, Boulby PA, Barker GJ, Sillery EL, Sheehan K, Ciccarelli O, et al. 2003a. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci. 6(7):750-757.
8. Behrens TE, Woolrich MW, Jenkinson M, Johansen-Berg H, Nunes RG, Clare S, Matthews PM, Brady JM, Smith SM. 2003b. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med. 50(5): 1077-1088.
9. Caeyenberghs K, Leemans A, Geurts M, Taymans T, Linden CV, Smits-Engelsman BC, Sunaert S, Swinnen SP. 2010. Brainbehavior relationships in young traumatic brain injury patients: DTI metrics are highly correlated with postural control. Hum Brain Mapp. 31(7):992-1002.
10. Clatworthy PL, Williams GB, Acosta-Cabronero J, Jones SP, Harding SG, Johansen-Berg H, Baron JC. 2010. Probabilistic tractography of the optic radiations-an automated method and anatomical validation. Neuroimage. 49(3):2001-2012.
11. Coleman KA, Baker GE, Mitrofanis J. 1997. Topography of fibre organisation in the corticofugal pathways of rats. J Comp Neurol. 381(2):143-157.
12. Coombes SA, Corcos DM, Pavuluri MN, Vaillancourt DE. 2012. Maintaining force control despite changes in emotional context engages dorsomedial prefrontal and premotor cortex. Cereb Cortex. 22(3):616-627.
13. Coombes SA, Corcos DM, Sprute L, Vaillancourt DE. 2010. Selective regions of the visuomotor system are related to gain-induced changes in force error. J Neurophysiol. 103(4): 2114-2123.
14. Coombes SA, Corcos DM, Vaillancourt DE. 2011. Spatiotemporal tuning of brain activity and force performance. Neuroimage. 54(3):2226-2236.
15. Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, et al. 2006. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage. 31(3):968-980.
16. Dum RP, Strick PL. 1991. The origin of corticospinal projections from the premotor areas in the frontal lobe. J Neurosci. 11 (3):667-689.
17. Dum RP, Strick PL. 2005. Frontal lobe inputs to the digit representations of the motor areas on the lateral surface of the hemisphere. J Neurosci. 25(6):1375-1386.
18. Feinberg DA, Moeller S, Smith SM, Auerbach E, Ramanna S, Gunther M, Glasser MF, Miller KL, Ugurbil K, Yacoub E. 2010. Multiplexed echo planar imaging for sub-second whole brain FMRI and fast diffusion imaging. PLoS One. 5(12): e15710.
19. Frazier JA, Chiu S, Breeze JL, Makris N, Lange N, Kennedy DN, Herbert MR, Bent EK, Koneru VK, Dieterich ME, et al. 2005. Structural brain magnetic resonance imaging of limbic and thalamic volumes in pediatric bipolar disorder. Am J Psychiatry. 162(7):1256-1265.
20. Fries W, Danek A, Scheidtmann K, Hamburger C. 1993. Motor recovery following capsular stroke. Role of descending pathways from multiple motor areas. Brain. 116(Pt 2):369-382.
21. Galea MP, Darian-Smith I. 1994. Multiple corticospinal neuron populations in the macaque monkey are specified by their unique cortical origins, spinal terminations, and connections. Cereb Cortex. 4(2):166-194.
22. Goldstein JM, Seidman LJ, Makris N, Ahern T, O'Brien LM, Caviness VS Jr, Kennedy DN, Faraone SV, Tsuang MT. 2007. Hypothalamic abnormalities in schizophrenia: sex effects and genetic vulnerability. Biol Psychiatry. 61(8):935-945.
23. Groisser BN, Copen WA, Singhal AB, Hirai KK, Schaechter JD. 2014. Corticospinal tract diffusion abnormalities early after stroke predict motor outcome. Neurorehabil Neural Repair. 28(8):751-760.
24. He SQ, Dum RP, Strick PL. 1993. Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere. J Neurosci. 13(3): 952-980.
25. He SQ, Dum RP, Strick PL. 1995. Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere. J Neurosci. 15(5 Pt 1):3284-3306.
26. Heffner RS, Masterton RB. 1983. The role of the corticospinal tract in the evolution of human digital dexterity. Brain Behav Evol. 23(3-4):165-183.
27. Hou J, Xiang Z, Yan R, Zhao M, Wu Y, Zhong J, Guo L, Li H, Wang J, Wu J, et al. 2016. Motor recovery at 6 months after admission is related to structural and functional reorganization of the spine and brain in patients with spinal cord injury. Hum Brain Mapp. 37(6):2195-2209.
28. Hua K, Zhang J, Wakana S, Jiang H, Li X, Reich DS, Calabresi PA, Pekar JJ, van Zijl PC, Mori S. 2008. Tract probability maps in stereotaxic spaces: analyses of white matter anatomy and tract-specific quantification. Neuroimage. 39(1):336-347.
29. Jang SH. 2009. The role of the corticospinal tract in motor recovery in patients with a stroke: a review. NeuroRehabilitation. 24(3):285-290.
30. Jang SH, Kim SY. 2016. Injury of the corticospinal tract in patients with mild traumatic brain injury: a diffusion tensor tractography study. J Neurotrauma. 33:1790-1795.
31. Jang SH, Seo JP. 2015. Aging of corticospinal tract fibers according to the cerebral origin in the human brain: a diffusion tensor imaging study. Neurosci Lett. 585:77-81.
32. Jaspers E, Byblow WD, Feys H, Wenderoth N. 2015. The corticospinal tract: a biomarker to categorize upper limb functional potential in unilateral cerebral palsy. Front Pediatr. 3: 112.
33. Jbabdi S, Sotiropoulos SN, Haber SN, Van Essen DC, Behrens TE. 2015. Measuring macroscopic brain connections in vivo. Nat Neurosci. 18(11):1546-1555.
34. Jbabdi S, Sotiropoulos SN, Savio AM, Grana M, Behrens TE. 2012. Model-based analysis of multishell diffusion MR data for tractography: how to get over fitting problems. Magn Reson Med. 68(6):1846-1855.
35. Jenkinson M, Bannister P, Brady M, Smith S. 2002. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 17(2): 825-841.
36. Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM. 2012. Fsl. Neuroimage. 62(2):782-790.
37. Jenkinson M, Smith S. 2001. A global optimisation method for robust affine registration of brain images. Med Image Anal. 5(2):143-156.
38. Johansen-Berg H, Rushworth MF. 2009. Using diffusion imaging to study human connectional anatomy. Annu Rev Neurosci. 32:75-94.
39. Jones DK, Knosche TR, Turner R. 2013. White matter integrity, fiber count, and other fallacies: the do's and don'ts of diffusion MRI. Neuroimage. 73:239-254.
40. Keizer K, Kuypers HG. 1989. Distribution of corticospinal neurons with collaterals to the lower brain stem reticular formation in monkey (Macaca fascicularis). Exp Brain Res. 74(2): 311-318.
41. Lehericy S, Ducros M, Krainik A, Francois C, Van de Moortele PF, Ugurbil K, Kim DS. 2004a. 3-D diffusion tensor axonal tracking shows distinct SMA and pre-SMA projections to the human striatum. Cereb Cortex. 14(12):1302-1309.
42. Lehericy S, Ducros M, Van de Moortele PF, Francois C, Thivard L, Poupon C, Swindale N, Ugurbil K, Kim DS. 2004b. Diffusion tensor fiber tracking shows distinct corticostriatal circuits in humans. Ann Neurol. 55(4):522-529.
43. Lemon RN, Griffiths J. 2005. Comparing the function of the corticospinal system in different species: organizational differences for motor specialization? Muscle Nerve. 32(3):261-279.
44. Leunissen I, Coxon JP, Geurts M, Caeyenberghs K, Michiels K, Sunaert S, Swinnen SP. 2013. Disturbed cortico-subcortical interactions during motor task switching in traumatic brain injury. Hum Brain Mapp. 34(6):1254-1271.
45. Lindenberg R, Renga V, Zhu LL, Betzler F, Alsop D, Schlaug G. 2010. Structural integrity of corticospinal motor fibers predicts motor impairment in chronic stroke. Neurology. 74(4): 280-287.
46. Lindenberg R, Zhu LL, Ruber T, Schlaug G. 2012. Predicting functional motor potential in chronic stroke patients using diffusion tensor imaging. Hum Brain Mapp. 33(5):1040-1051.
47. Luppino G, Matelli M, Camarda R, Rizzolatti G. 1994. Corticospinal projections from mesial frontal and cingulate areas in the monkey. Neuroreport. 5(18):2545-2548.
48. Maier MA, Armand J, Kirkwood PA, Yang HW, Davis JN, Lemon RN. 2002. Differences in the corticospinal projection from primary motor cortex and supplementary motor area to macaque upper limb motoneurons: an anatomical and electrophysiological study. Cereb Cortex. 12(3):281-296.
49. Makris N, Goldstein JM, Kennedy D, Hodge SM, Caviness VS, Faraone SV, Tsuang MT, Seidman LJ. 2006. Decreased volume of left and total anterior insular lobule in schizophrenia. Schizophr Res. 83(2-3):155-171.
50. Mayka MA, Corcos DM, Leurgans SE, Vaillancourt DE. 2006. Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: a meta-analysis. Neuroimage. 31(4):1453-1474.
51. Misra G, Coombes SA. 2015. Neuroimaging evidence of motor control and pain processing in the human midcingulate cortex. Cereb Cortex. 25(7):1906-1919.
52. Misra G, Ofori E, Chung JW, Coombes SA. 2016. Pain-related suppression of beta oscillations facilitates voluntary movement. Cereb Cortex. (in press).
53. Moeller S, Yacoub E, Olman CA, Auerbach E, Strupp J, Harel N, Ugurbil K. 2010. Multiband multislice GE-EPI at 7 tesla, with 16-fold acceleration using partial parallel imaging with application to high spatial and temporal whole-brain fMRI. Magn Reson Med. 63(5):1144-1153.
54. Morecraft RJ, Ge J, Stilwell-Morecraft KS, McNeal DW, Hynes SM, Pizzimenti MA, Rotella DL, Darling WG. 2015. Vulnerability of the medial frontal corticospinal projection accompanies combined lateral frontal and parietal cortex injury in rhesus monkey. J Comp Neurol. 523(4):669-697.
55. Muggeo VM. 2003. Estimating regression models with unknown break-points. Stat Med. 22(19):3055-3071.
56. Newton JM, Ward NS, Parker GJ, Deichmann R, Alexander DC, Friston KJ, Frackowiak RS. 2006. Non-invasive mapping of corticofugal fibres from multiple motor areas-relevance to stroke recovery. Brain. 129(Pt 7):1844-1858.
57. Nudo RJ, Masterton RB. 1990a. Descending pathways to the spinal cord, III: sites of origin of the corticospinal tract. J Comp Neurol. 296(4):559-583.
58. Nudo RJ, Masterton RB. 1990b. Descending pathways to the spinal cord, IV: some factors related to the amount of cortex devoted to the corticospinal tract. J Comp Neurol. 296(4): 584-597.
59. Park CH, Kou N, Boudrias MH, Playford ED, Ward NS. 2013. Assessing a standardised approach to measuring corticospinal integrity after stroke with DTI. Neuroimage Clin. 2: 521-533.
60. Park JK, Kim BS, Choi G, Kim SH, Choi JC, Khang H. 2008. Evaluation of the somatotopic organization of corticospinal tracts in the internal capsule and cerebral peduncle: results of diffusion-tensor MR tractography. Korean J Radiol. 9(3): 191-195.
61. Plow EB, Cunningham DA, Varnerin N, Machado A. 2015. Rethinking stimulation of the brain in stroke rehabilitation: why higher motor areas might be better alternatives for patients with greater impairments. Neuroscientist. 21(3): 225-240.
62. Potter-Baker KA, Varnerin NM, Cunningham DA, Roelle SM, Sankarasubramanian V, Bonnett CE, Machado AG, Conforto AB, Sakaie K, Plow EB. 2016. Influence of corticospinal tracts from higher order motor cortices on recruitment curve properties in stroke. Front Neurosci. 10:79.
63. Rouiller EM, Yu XH, Moret V, Tempini A, Wiesendanger M, Liang F. 1998. Dexterity in adult monkeys following early lesion of the motor cortical hand area: the role of cortex adjacent to the lesion. Eur J Neurosci. 10(2):729-740.
64. Sach M, Winkler G, Glauche V, Liepert J, Heimbach B, Koch MA, Buchel C, Weiller C. 2004. Diffusion tensor MRI of early upper motor neuron involvement in amyotrophic lateral sclerosis. Brain. 127(Pt 2):340-350.
65. Schaechter JD, Fricker ZP, Perdue KL, Helmer KG, Vangel MG, Greve DN, Makris N. 2009. Microstructural status of ipsilesional and contralesional corticospinal tract correlates with motor skill in chronic stroke patients. Hum Brain Mapp. 30 (11):3461-3474.
66. Schaechter JD, Perdue KL, Wang R. 2008. Structural damage to the corticospinal tract correlates with bilateral sensorimotor cortex reorganization in stroke patients. Neuroimage. 39(3): 1370-1382.
67. Schulz R, Park CH, Boudrias MH, Gerloff C, Hummel FC, Ward NS. 2012. Assessing the integrity of corticospinal pathways from primary and secondary cortical motor areas after stroke. Stroke; a journal of cerebral circulation. 43(8): 2248-2251.
68. Setsompop K, Gagoski BA, Polimeni JR, Witzel T, Wedeen VJ, Wald LL. 2012. Blipped-controlled aliasing in parallel imaging for simultaneous multislice echo planar imaging with reduced g-factor penalty. Magn Reson Med. 67(5): 1210-1224.
69. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, et al. 2004. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage. 23(Suppl 1):S208-S219.
70. Sotiropoulos SN, Jbabdi S, Xu J, Andersson JL, Moeller S, Auerbach EJ, Glasser MF, Hernandez M, Sapiro G, Jenkinson M, et al. 2013a. Advances in diffusion MRI acquisition and processing in the human connectome project. Neuroimage. 80:125-143.
71. Sotiropoulos SN, Moeller S, Jbabdi S, Xu J, Andersson JL, Auerbach EJ, Yacoub E, Feinberg D, Setsompop K, Wald LL, et al. 2013b. Effects of image reconstruction on fiber orientation mapping from multichannel diffusion MRI: reducing the noise floor using SENSE. Magn Reson Med. 70(6): 1682-1689.
72. Stinear CM, Barber PA, Petoe M, Anwar S, Byblow WD. 2012. The PREP algorithm predicts potential for upper limb recovery after stroke. Brain. 135(Pt 8):2527-2535.
73. Stinear CM, Barber PA, Smale PR, Coxon JP, Fleming MK, Byblow WD. 2007. Functional potential in chronic stroke patients depends on corticospinal tract integrity. Brain. 130(Pt 1): 170-180.
74. Tovar-Moll F, Evangelou IE, Chiu AW, Auh S, Chen C, Ehrmantraut M, Ohayon JM, Richert N, Bagnato F. 2015. Diffuse and focal corticospinal tract disease and its impact on patient disability in multiple sclerosis. J Neuroimaging. 25(2):200-206.
75. Travis AM. 1955. Neurological deficiencies after ablation of the precentral motor area in Macaca mulatta. Brain. 78(2): 155-173.
76. van Baarsen KM, Kleinnijenhuis M, Jbabdi S, Sotiropoulos SN, Grotenhuis JA, van Cappellen van Walsum AM. 2016. A probabilistic atlas of the cerebellar white matter. Neuroimage. 124(Pt A):724-732.
77. Van Essen DC, Smith SM, Barch DM, Behrens TE, Yacoub E, Ugurbil K. 2013. The WU-Minn human connectome project: an overview. Neuroimage. 80:62-79.
78. Vos SB, Jones DK, Viergever MA, Leemans A. 2011. Partial volume effect as a hidden covariate in DTI analyses. Neuroimage. 55(4):1566-1576.
79. Wakana S, Caprihan A, Panzenboeck MM, Fallon JH, Perry M, Gollub RL, Hua K, Zhang J, Jiang H, Dubey P, et al. 2007. Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage. 36(3):630-644.
80. Wedeen VJ, Wang RP, Schmahmann JD, Benner T, Tseng WY, Dai G, Pandya DN, Hagmann P, D'Arceuil H, de Crespigny AJ. 2008. Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. Neuroimage. 41(4): 1267-1277.
81. Woolrich MW, Jbabdi S, Patenaude B, Chappell M, Makni S, Behrens T, Beckmann C, Jenkinson M, Smith SM. 2009. Bayesian analysis of neuroimaging data in FSL. Neuroimage. 45(Suppl 1):S173-S186.
82. Zhu LL, Lindenberg R, Alexander MP, Schlaug G. 2010. Lesion load of the corticospinal tract predicts motor impairment in chronic stroke. Stroke; a journal of cerebral circulation. 41 (5):910-915.