Layer-specific intracortical connectivity revealed with diffusion MRI

Cerebral Cortex

Volumn 24, Issue 2, 2014, Pages 328-339

  Leuze, Christoph W U ^a   Anwander, Alfred ^a   Bazin, Pierre Louis ^a   Dhital, Bibek ^a   Stüber, Carsten ^a   Reimann, Katja ^a   Geyer, Stefan ^a   Turner, Robert ^a  

^a MAX PLANCK INSTITUTE FOR HUMAN COGNITIVE AND BRAIN SCIENCES   (Germany)

Author keywords

Crossing fiber tractography; Diffusion tensor imaging; Layer 1; Stria of Gennari; Visual cortex

Indexed keywords

ADULT; AGED; ARTICLE; BRAIN CORTEX; CYTOARCHITECTURE; DIFFUSION; DIFFUSION WEIGHTED IMAGING; FEMALE; GRAY MATTER; HISTOLOGY; HUMAN; HUMAN TISSUE; MALE; MIDDLE AGED; PRIORITY JOURNAL; VISUAL CORTEX; WHITE MATTER;

CROSSING-FIBER TRACTOGRAPHY; DIFFUSION TENSOR IMAGING; LAYER 1; STRIA OF GENNARI; VISUAL CORTEX;

AGED; CEREBRAL CORTEX; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; HUMANS; MALE; MIDDLE AGED; NEURAL PATHWAYS;

EID: 84893598190     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhs311     Document Type: Article

References (86)

1. Amir Y, Harel M, Malach R. 1993. Cortical hierarchy reflected in the organization of intrinsic connections in macaque monkey visual cortex. J Comp Neurol. 334:19-46.
2. Anderson JC, Martin KA. 2009. The synaptic connections between cortical areas V1 and V2 in macaque monkey. J Neurosci. 29:11283-11293.
3. Anwander A, Pampel A, Knösche TR. 2010. In vivo measurement of cortical anisotropy by diffusion-weighted imaging correlates with cortex type. Proceedings of the 18th Annual Meeting of ISMRM; 2010 May 1-7; Stockholm (Sweden). p. 109.
4. Axer H, Axer M, Krings T, Keyserlingk DG. 2001. Quantitative estimation of 3-D fiber course in gross histological sections of the human brain using polarized light. J Neurosci Methods. 105:121-131.
5. Axer M, Amunts K, Grassel D, Palm C, Dammers J, Axer H, Pietrzyk U, Zilles K. 2011. A novel approach to the human connectome: ultra-high resolution mapping of fiber tracts in the brain. Neuroimage. 54:1091-1101.
6. Axer M, Grassel D, Kleiner M, Dammers J, Dickscheid T, Reckfort J, Hutz T, Eiben B, Pietrzyk U, Zilles K et al. 2011. High-resolution fiber tract reconstruction in the human brain by means of threedimensional polarized light imaging. Front Neuroinform. 5:34.
7. Baillarger J. 1840. Recherches sur la structure de la couche corticale des circonvolutions du cerveau. Mem Acad R Med. 8:149-183.
8. Baratti C, Barnett AS, Pierpaoli C. 1999. Comparative MR imaging study of brain maturation in kittens with T1, T2, and the trace of the diffusion tensor. Radiology. 210:133-142.
9. Behrens TE, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CA, Boulby PA, Barker GJ, Sillery EL, Sheehan K, Ciccarelli O et al. 2003. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci. 6:750-757.
10. Blasdel GG, Lund JS, Fitzpatrick D. 1985. Intrinsic connections of macaque striate cortex: axonal projections of cells outside lamina 4C. J Neurosci. 5:3350-3369.
11. Boucsein C, Nawrot MP, Schnepel P, Aertsen A. 2011. Beyond the cortical column: abundance and physiology of horizontal connections imply a strong role for inputs from the surround. Front Neurosci. 5:32.
12. Braitenberg V. 1962. A note on myeloarchitectonics. J Comp Neurol. 118:141-156.
13. Brauer J, Anwander A, Friederici AD. 2011. Neuroanatomical prerequisites for language functions in the maturing brain. Cereb Cortex. 21:459-466.
14. Brodmann K. 1909. Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Leipzig: Johann Ambrosius Barth Verlag.
15. Burkhalter A. 1993. Development of forward and feedback connections between areas V1 and V2 of human visual cortex. Cereb Cortex. 3:476-487.
16. Cajal SRY. 1911. Histologie du système nerveux de l'homme et des vertébrés. Paris: Maloine.
17. Clark CA, Hedehus M, Moseley ME. 2001. Diffusion time dependence of the apparent diffusion tensor in healthy human brain and white matter disease. Magn Reson Med. 45:1126-1129.
18. Coogan TA, Van Essen DC. 1996. Development of connections within and between areas V1 and V2 of macaque monkeys. J Comp Neurol. 372:327-342.
19. Dammers J, Breuer L, Axer M, Kleiner M, Eiben B, Grassel D, Dickscheid T, Zilles K, Amunts K, Shah NJ et al. 2012. Automatic identification of gray and white matter components in polarized light imaging. Neuroimage. 59:1338-47.
20. D'Arceuil H, Liu C, Levitt P, Thompson B, Kosofsky B, de Crespigny A. 2008. Three-dimensional high-resolution diffusion tensor imaging and tractography of the developing rabbit brain. Dev Neurosci. 30:262-275.
21. D'Arceuil HE, Hotakainen MP, Liu C, Themelis G, de Crespigny AJ, Franceschini MA. 2005. Near-infrared frequency-domain optical spectroscopy and magnetic resonance imaging: a combined approach to studying cerebral maturation in neonatal rabbits. J Biomed Opt. 10:11011.
22. Demyanenko GP, Schachner M, Anton E, Schmid R, Feng G, Sanes J, Maness PF. 2004. Close homolog of L1 modulates area-specific neuronal positioning and dendrite orientation in the cerebral cortex. Neuron. 44:423-437.
23. Dyrby TB, Baare WF, Alexander DC, Jelsing J, Garde E, Sogaard LV. 2011. An ex vivo imaging pipeline for producing high-quality and high-resolution diffusion-weighted imaging datasets. Hum Brain Mapp. 32:544-563.
24. Fatterpekar GM, Naidich TP, Delman BN, Aguinaldo JG, Gultekin SH, Sherwood CC, Hof PR, Drayer BP, Fayad ZA. 2002. Cytoarchitecture of the human cerebral cortex: MR microscopy of excised specimens at 9.4 Tesla. AJNR Am J Neuroradiol. 23:1313-1321.
25. Gallyas F. 1979. Silver staining of myelin by means of physical development. Neurol Res. 1:203-209.
26. Gennari F. 1782. De peculiari structura cerebri nonnulisque ejus morbis. Parma, Italy: Ex Regio.
27. Gilbert CD, Das A, Ito M, Kapadia M, Westheimer G. 1996. Spatial integration and cortical dynamics. Proc Natl Acad Sci USA. 93:615-622.
28. Godement P, Vanselow J, Thanos S, Bonhoeffer F. 1987. A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue. Development. 101:697-713.
29. Han S, Gemmell SJ, Helmer KG, Grigg P, Wellen JW, Hoffman AH, Sotak CH. 2000. Changes in ADC caused by tensile loading of rabbit Achilles tendon: evidence for water transport. J Magn Reson. 144:217-227.
30. Heidemann RM, Anwander A, Feiweier T, Knösche TR, Turner R. 2012. k-space and q-space: combining ultra-high spatial and angular resolution in diffusion imaging using ZOOPPA at 7 T. Neuroimage. 60:967-978.
31. Heidemann RM, Porter DA, Anwander A, Feiweier T, Heberlein K, Knösche TR, Turner R. 2010. Diffusion imaging in humans at 7T using readout-segmented EPI and GRAPPA. Magn Reson Med. 64:9-14.
32. Hoehn-Berlage M, Eis M, Schmitz B. 1999. Regional and directional anisotropy of apparent diffusion coefficient in rat brain. NMR Biomed. 12:45-50.
33. Hubel DH, Wiesel TN. 1972. Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. J Comp Neurol. 146:421-450.
34. Jaermann T, De Zanche N, Staempfli P, Pruessmann KP, Valavanis A, Boesiger P, Kollias SS. 2008. Preliminary experience with visualization of intracortical fibers by focused high-resolution diffusion tensor imaging. AJNR Am J Neuroradiol. 29: 146-150.
35. Jespersen SN, Bjarkam CR, Nyengaard JR, Chakravarty MM, Hansen B, Vosegaard T, Ostergaard L, Yablonskiy D, Nielsen NC, Vestergaard-Poulsen P. 2010. Neurite density from magnetic resonance diffusion measurements at ultrahigh field: comparison with light microscopy and electron microscopy. Neuroimage. 49:205-216.
36. Jespersen SN, Kroenke CD, Ostergaard L, Ackerman JJ, Yablonskiy DA. 2007. Modeling dendrite density from magnetic resonance diffusion measurements. Neuroimage. 34:1473-1486.
37. Jespersen SN, Leigland LA, Cornea A, Kroenke CD. 2012. Determination of axonal and dendritic orientation distributions within the developing cerebral cortex by diffusion tensor imaging. IEEE Trans Med Imaging. 31:16-32.
38. Jones DK, Knösche TR, Turner R. 2012. White matter integrity, fiber count, and other fallacies: the do's and don'ts of diffusion MRI. Neuroimage. doi:10.1016/j.neuroimage.2012.06.081.
39. Kleinnijenhuis M, Sikma KJ, Barth M, Dederen P, Zerbi V, Küsters B, Ruiter D, Slump CH, van Cappellen van Walsum A-M. 2011. Validation of diffusion weighted imaging of cortical anisotropy by means of a histological stain for myelin. Proceedings of the 19th Annual Meeting of ISMRM; 2011 May 7-13; Montreal (Canada). p. 2085.
40. Kuypers HG, Szwarcbart MK, Mishkin M, Rosvold HE. 1965. Occipitotemporal corticocortical connections in the rhesus monkey. Exp Neurol. 11:245-262.
41. Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, Laval-Jeantet M. 1988. Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology. 168:497-505.
42. Le Bihan D, Turner R, Douek P. 1993. Is water diffusion restricted in human brain white matter? An echo-planar NMR imaging study. Neuroreport. 4:887-890.
43. Leergaard TB, White NS, de Crespigny A, Bolstad I, D'Arceuil H, Bjaalie JG, Dale AM. 2010. Quantitative histological validation of diffusion MRI fiber orientation distributions in the rat brain. PloS One. 5:e8595.
44. Leuze C, Dhital B, Anwander A, Pampel A, Heidemann RM, Reimann K, Geyer S, Gratz M, Turner R. 2011. Visualization of the orientational structure of the human stria of Gennari with high-resolution DWI. Proceedings of the 19th Annual Meeting of ISMRM; 2011 May 7-13; Montreal (Canada). p. 2371.
45. Lund JS, Boothe R. 1975. Interlaminar connections and pyramidal neuron organization in the visual cortex, area 17, of the macaque monkey. J Comp Neurol. 159:305-34.
46. Lund JS, Henry GH, MacQueen CL, Harvey AR. 1979. Anatomical organization of the primary visual cortex (area 17) of the cat. A comparison with area 17 of the macaque monkey. J Comp Neurol. 184:599-618.
47. Lund JS, Lund RD, Hendrickson AE, Bunt AH, Fuchs AF. 1975. The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. J Comp Neurol. 164:287-303.
48. Lund JS, Takahashi Y, Levitt JB. 1994. Primary visual cortex in primates. New York: Plenum Press.
49. Lund JS, Yoshioka T. 1991. Local circuit neurons of macaque monkey striate cortex: III. Neurons of laminae 4B, 4A, and 3B. J Comp Neurol. 311:234-258.
50. Maas LC, Mukherjee P, Carballido-Gamio J, Veeraraghavan S, Miller SP, Partridge SC, Henry RG, Barkovich AJ, Vigneron DB. 2004. Early laminar organization of the human cerebrum demonstrated with diffusion tensor imaging in extremely premature infants. Neuroimage. 22:1134-1140.
51. McAuliffe MJ, Lalonde FM, McGarry D, Gandler W, Csaky K, Trus BL. 2001. Medical image processing, analysis and visualization in clinical research. Proceedings of the 14th IEEE Symposium on Computer-Based Medical Systems; 2001 July 26-27; Washington DC (USA), p. 381-386.
52. McKinstry RC, Mathur A, Miller JH, Ozcan A, Snyder AZ, Schefft GL, Almli CR, Shiran SI, Conturo TE, Neil JJ. 2002. Radial organization of developing preterm human cerebral cortex revealed by non-invasive water diffusion anisotropy MRI. Cereb Cortex. 12:1237-1243.
53. McNab JA, Jbabdi S, Deoni SC, Douaud G, Behrens TE, Miller KL. 2009. High resolution diffusion-weighted imaging in fixed human brain using diffusion-weighted steady state free precession. Neuroimage. 46:775-785.
54. McNab JA, Polimeni JR, Wald LL. 2011. Surface based analysis of diffusion orientation for identifying architectonic domains in the in vivo human cortex. Proceedings of the 19th Annual Meeting of ISMRM; 2011 May 7-13; Montreal (Canada). p. 412.
55. Merker B. 1983. Silver staining of cell bodies by means of physical development. J Neurosci Methods. 9:235-241.
56. Mesulam MM. 1979. Tracing neural connections of human-brain with selective silver impregnation-observations on geniculocalcarine, spinothalamic, and entorhinal pathways. Arch Neurol. 36:814-818.
57. Miklossy J, Clarke S, Vanderloos H. 1991. The long-distance effects of brain-lesions-visualization of axonal pathways and their terminations in the human brain by the nauta method. J Neuropathol Exp Neurol. 50:595-614.
58. Miller KL, Stagg CJ, Douaud G, Jbabdi S, Smith SM, Behrens TE, Jenkinson M, Chance SA, Esiri MM, Voets NL et al. 2011. Diffusion imaging of whole, post-mortem human brains on a clinical MRI scanner. Neuroimage. 57:167-181.
59. Mori S, Itoh R, Zhang J, Kaufmann WE, van Zijl PC, Solaiyappan M, Yarowsky P. 2001. Diffusion tensor imaging of the developing mouse brain. Magn Reson Med. 46:18-23.
60. Mufson EJ, Brady DR, Kordower JH. 1990. Tracing neuronal connections in postmortem human hippocampal complex with the carbocyanine dye DiI. Neurobiol Aging. 11:649-653.
61. Peters A. 1994. Primary visual cortex in primates. New York: Plenum Press.
62. Rakic P. 2009. Evolution of the neocortex: a perspective from developmental biology. Nat Rev Neurosci. 10:724-735.
63. Riffert TW, Knösche TR, Anwander A. 2012. Quantification of fiber bundle properties using a decomposition of the fiber orientation distribution function. Proceedings of the 20th Annual Meeting of ISMRM; 2012 May 5-11; Melbourne (Australia). p. 3592.
64. Rockland KS. 1992. Laminar distribution of neurons projecting from area V1 to V2 in macaque and squirrel monkeys. Cereb Cortex. 2:38-47.
65. Rockland KS. 1994. Primary visual cortex in primates. New York: Plenum Press. Rockland KS, Lund JS. 1983. Intrinsic laminar lattice connections in primate visual cortex. J Comp Neurol. 216:303-318.
66. Rockland KS, Virga A. 1989. Terminal arbors of individual "feedback" axons projecting from area V2 to V1 in the macaque monkey: a study using immunohistochemistry of anterogradely transported Phaseolus vulgaris-leucoagglutinin. J Comp Neurol. 285:54-72.
67. Roebroeck A, Galuske R, Formisano E, Chiry O, Bratzke H, Ronen I, Kim DS, Goebel R. 2008. High-resolution diffusion tensor imaging and tractography of the human optic chiasm at 9.4 T. Neuroimage. 39:157-168.
68. Ronen I, Kim KH, Garwood M, Ugurbil K, Kim DS. 2003. Conventional DTI vs. slow and fast diffusion tensors in cat visual cortex. Magn Reson Med. 49:785-790.
69. Sanides F, Vitzthum HG. 1965. Zur Architektonik der menschlichen Sehrinde und den Prinzipien ihrer Entwicklung. Dtsch Z Nervenheilkd. 187:680-707.
70. Seehaus AK, Roebroeck A, Chiry O, Kim DS, Ronen I, Bratzke H, Goebel R, Galuske RA. 2013. Histological validation of DWMRI tractography in human postmortem tissue. Cereb Cortex. 23:442-450.
71. Stejskal EO, Tanner JE. 1965. Spin diffusion measurements: spin echoes in the presence of a time-dependent field gradient. J Chem Phys. 42:288-292.
72. Stepanyants A, Martinez LM, Ferecsko AS, Kisvarday ZF. 2009. The fractions of short-and long-range connections in the visual cortex. Proc Natl Acad Sci USA. 106:3555-3560.
73. Tardif E, Clarke S. 2001. Intrinsic connectivity of human auditory areas: a tracing study with DiI. Eur J Neurosci. 13:1045-1050.
74. Thornton JS, Ordidge RJ, Penrice J, Cady EB, Amess PN, Punwani S, Clemence M, Wyatt JS. 1997. Anisotropic water diffusion in white and gray matter of the neonatal piglet brain before and after transient hypoxia-ischaemia. Mag Reson Imag. 15: 433-440.
75. Tournier JD, Calamante F, Connelly A. 2012. MRtrix: diffusion tractography in crossing fiber regions. Int J Imag Syst Tech. 22:53-66.
76. Tournier JD, Calamante F, Connelly A. 2007. Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. Neuroimage. 35:1459-1472.
77. Trampel R, Ott D, Turner R. 2011. Do the congenitally blind have a stria of Gennari? First intracortical insights in vivo. Cereb Cortex. 21:2075-2081.
78. Tsvetkov VN. 1942. Acta Physicochim. URSS. 16:132.
79. Tuch DS, Reese TG, Wiegell MR, Wedeen VJ. 2003. Diffusion MRI of complex neural architecture. Neuron. 40:885-895.
80. Turner R, Le Bihan D, Maier J, Vavrek R, Hedges LK, Pekar J. 1990. Echo-planar imaging of intravoxel incoherent motion. Radiology. 177:407-414.
81. Vogt C, Vogt O. 1919. Allgemeinere Ergebnisse unserer Hirnforschung. J Psychol Neurol. 25:1-189.
82. Wedeen VJ, Rosene DL, Wang R, Dai G, Mortazavi F, Hagmann P, Kaas JH, Tseng WY. 2012. The geometric structure of the brain fiber pathways. Science. 335:1628-1634.
83. Wedeen VJ, Song S, Wald L, Reese TG, Benner T, Tseng WY. 2004. Diffusion spectrum MRI of cortical architectonics: visualization of cortical layers and segmentation of cortical areas by analysis of planar structure. Proceedings of the 12th Annual Meeting of ISMRM; 2004 May 15-21; Kyoto (Japan). p. 622.
84. 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. 41:1267-1277.
85. Wolman M. 1975. Polarized light microscopy as a tool of diagnostic pathology. J Histochem Cytochem. 23:21-50.
86. Yassa MA, Muftuler LT, Stark CE. 2010. Ultrahigh-resolution microstructural diffusion tensor imaging reveals perforant path degradation in aged humans in vivo. Proc Natl Acad Sci USA. 107:12687-12691.