Distribution of axon diameters in cortical white matter: an electron-microscopic study on three human brains and a macaque

Biological Cybernetics

Volumn 108, Issue 5, 2014, Pages 541-557

  Liewald, Daniel ^a   Miller, Robert ^b   Logothetis, Nikos ^a   Wagner, Hans Joachim ^c   Schüz, Almut ^a  

^a MAX PLANCK INSTITUTE FOR BIOLOGICAL CYBERNETICS   (Germany)

^b UNIVERSITY OF OTAGO   (New Zealand)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Axon calibre; Conduction time; Diffusion weighted imaging; Electron microscopy; Myelin; White matter

Indexed keywords

CELL MEMBRANES; ELECTRON MICROSCOPES; ELECTRON MICROSCOPY; FIBERS; MAMMALS;

AXON CALIBRE; CONDUCTION VELOCITY; DIFFUSION WEIGHTED IMAGING; MICROSCOPIC STUDY; MYELIN; MYELINATED AXONS; SMALL POPULATION; WHITE MATTER;

BRAIN;

MACACA MULATTA; MAMMALIA;

AGED; ANATOMY AND HISTOLOGY; ANIMAL; BRAIN CORTEX; CYTOLOGY; ELECTRON TOMOGRAPHY; HEMISPHERIC DOMINANCE; HUMAN; MALE; MYELIN SHEATH; NERVE FIBER; RHESUS MONKEY; ULTRASTRUCTURE; VERY ELDERLY; WHITE MATTER;

AGED; AGED, 80 AND OVER; ANIMALS; AXONS; CEREBRAL CORTEX; ELECTRON MICROSCOPE TOMOGRAPHY; FUNCTIONAL LATERALITY; HUMANS; MACACA MULATTA; MALE; MYELIN SHEATH; WHITE MATTER;

EID: 84919794641     PISSN: 03401200     EISSN: 14320770     Source Type: Journal    
DOI: 10.1007/s00422-014-0626-2     Document Type: Article

References (84)

1. Aboitiz F, Ide A, Olivares R (2003) Corpus callosum morphology in relation to cerebral asymmetries in the postmortem human. In: Zaidel E, Iacoboni M (eds) The parallel brain: the cognitive neuroscience of the corpus callosum. MIT Press, Cambridge, pp 33–46
2. Aboitiz FA, Scheibel AB, Fisher RS, Zaidel E (1992) Fiber composition of the human corpus callosum. Brain Res 598:143–153
3. Alexander DC, Hubbard PL, Hall MG, Moore EA, Ptito M, Parker GJM, Dyrby TB (2010) Orientationally invariant indices of axon diameter and density from diffusion MRI. NeuroImage 52:1374–1389
4. Allman J (1999) Evolving brains. Scientific American Library, New York
5. Aroniadou VA, Keller A (1993) The patterns and synaptic properties of horizontal intracortical connections in the rat motor cortex. J Neurophysiol 70:1493–1553
6. Assaf Y, Blumenfeld-Katzir T, Yovel Y, Basser PJ (2008) AxCaliber: a method for measuring axon diameter distribution from diffusion MRI. Magn Reson Med 59:1347–1354
7. Berbel P, Innocenti GM (1988) The development of the corpus callosum in cats: a light- and electron-microscopic study. J Comp Neurol 276:132–156
8. Bischoff A, Thomas PK (1975) Microscopic anatomy of myelinated nerve fibers. In: Dyck JP, Thomas PK, Lambert EH (eds) Peripheral neuropathy. W. B. Saunders Company, Philadelphia, pp 104–130
9. Blinkov SM, Glezer II (1968) Das Zentralnervensystem in Zahlen und Tabellen. VEB Gustav Fischer Verlag, Jena
10. Bojak I, Liley DTJ (2010) Axonal velocity distributions in neural field equations. PLoS Comput Biol 6(1) e1000653 www.ploscompbiol.org
11. Braitenberg V (1978) Cell assemblies in the cerebral cortex. In: Heim R, Palm G (eds) Theoretical approaches to complex systems. Lecture notes in biomathematics (21). Springer, Berlin, Heidelberg, pp 171–188
12. Braitenberg V, Schüz A (1991) Anatomy of the Cortex. Statistics and Geometry. $$2^{{\rm nd}}$$2nd (1998) Statistics and geometry of neuronal connectivity. Springer, Berlin, Heidelberg
13. Bringuier V, Vhavane F, Glaeser L, Frégnac Y (1999) Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. Science 29(283):695–699
14. Büchel C, Raedler T, Sommer M, Sach M, Weiller C, Koch MA (2004) White matter asymmetry in the human brain: a diffusion tensor MRI study. Cerebral cortex 14:945–951. doi:10.1093/cercor/bhh055
15. Bürgel U (1999) Kartierung langer Faserbahnen im adulten menschlichen Gehirn. Geschlechtsunterschiede, Lateralisation und Variabilität. Dissertation at the Faculty of Medicine, Heinrich-Heine-Universität Düsseldorf
16. Buzsáki G, Logothetis N, Singer W (2013) Scaling brain size, keeping timing: evolutionary preservation of brain rhythms. Neuron 80(3):751–764
17. Cragg B (1979) Overcoming the failure of electronmicroscopy to preserve the brain’s extracellular space. Neurosci Lett 15(2–3):301–306
18. Caminiti R, Ghaziri H, Galuske R, Hof PR, Innocenti GM (2009) Evolution amplified processing with temporally dispersed slow neuronal connectivity in primates. Proc Natl Acad Sci 106(46). doi:10.1073/pnas.0907655106
19. Caminiti R, Carducci F, Piervicenzi C, Battaglia-Mayer A, Confalcone G, Visco-Comandini F, Pantano P, Innocenti GM (2013) Diameter, length, speed and conduction delay of callosal axons in macaque monkeys and humans: comparing data from histology and magnetic resonance imaging diffusion tractography. J Neurosci 33(36):14501–14511
20. Cowley AR (1983) Influence of fiber tracts on the CT appearance of cerebral edema: anatomic-pathologic correlation. AJNR Am J Neuroradiol 1983(4):915–925
21. Dawson WW, Hawthorne MN, Jenkins RL, Goldston RT (1982) giant neural systems in the inner retina and optic nerve of small whales. J Comp Neurol 205:1–7
22. DeFelipe J, Conley M, Jones EG (1985) Long-range focal collateralization of axons arising from cortico-cortical cells in the monkey sensory-motor cortex. J Neurosci 6:3749–3766
23. Dyrby TB, SØgaard LV, Hall MG, Ptito M, Alexander DC (2013) Contrast and stability of the axon diameter index from microstructure imaging with diffusion MRI. Magn Reson Med 70:711–721
24. Ferraya Moyano H, Molina JC (1980) Axonal projections and conduction properties of olfactory peduncle neurons in the rat. Exp Brain Res 39:241–248
25. Fisken RA, Garey LJ, Powell TPS (1975) The intrinsic, association and commissural connections of area 17 of the visual cortex. Philos Trans R Soc Lond B 272:487–536
26. Gasser HS, Grundfest H (1939) Axon diameters in relation to the spike dimensions and the conduction velocity in mammalian A fibers. Am J Physiol 127(2):393–414
27. Gluhbegovic N, Williams TH (1980) The human brain. A photographic guide. Harper and Row, Publishers, Hagerstown
28. Gonzaléz-Burgos G, Barrionuevo G, Lewis DA (2000) Horizontal synaptic connections in monkey prefrontal cortex: an In vitro electrophysiological study. Cereb Cortex 10:82–92
29. Guo X, Aoyama M, Sugita S (2001) Quantitative anatomy of the optic nerve of the horse (Thoroughbred). J Vet Med Sci 63:971–975
30. Häggqvist G (1936) Analyse der Faserverteilung in einem Rückenmarkquerschnitt (Th 3). Z Mikrosk Anat Forsch 39:1–34
31. Hildebrand C, Hahn (1978) Relation between myelin sheath thickness and axon size in spinal cord white matter of some vertebrate species. J Neurol Sci 38:421–434
32. Hoffmeister B, Jänig W, Lisney SJ (1991) A proposed relationship between circumference and conduction velocity of unmyelinated axons from normal and regenerated cat hindlimb cutaneous nerves. Neuroscience 42:603–611
33. Hrabetová S, Nicholson C (2007) Biophysical properties of brain extracellular space explored with ion-selective microelectrodes, integrative optical imaging and related techniques. In: Michael AC, Borland LM (eds) Electrochemical methods for neuroscience, Chapter 10. CRC Press, Boca Raton (FL) http://www.ncbi.nlm.nih.gov/books/NBK2581/
34. Hursh JB (1939) Conduction velocity and diameter of nerve fibres. Am J Physiol 127:131–139
35. Innocenti GM (1986) General organization of callosal connections in the cerebral cortex. In: Jones EG, Peters A (eds) Cerebral cortex, vol 5. Plenum Press, New York, London, pp 291–353
36. Innocenti GM, Vercelli A, Caminiti R (2013) The diameter of cortical axons depends both on the area of origin and target. Cereb Cortex 24(8):2178–2188. doi:10.1093/cercor/bht070
37. Izhikevich EM (2006) Polychronization: computation with spikes. Neural Comput 18:245–282
38. Jerison HJ (1991) Brain size and the evolution of mind. Fifth James Arthus Lecture, American Museum of Natural History, New York
39. LaMantia AS, Rakic P (1990) Cytological and quantitative characteristics of four cerebral commissures in the rhesus monkey. J Comp Neurol 291:520–537
40. Leenen LPH, MeekJ Posthuma PR, Nieuwenhuys R (1985) A detailed morphometrical analysis of the pyramidal tract of the rat. Brain Res 359:65–80
41. Liu XB, Schumann CM (2014) optimization of electron microscopy for human brains with long-term fixation and fixed-frozen sections. Acta Neuropathol Commun 2:42
42. Logothetis NK (2003) The underpinnings of the BOLD functional magnetic resonance imaging signal. J Neurosci 23(10):3963–3971
43. Makris N, Worth AJ, Sorensen AG, Papadimitriou GM, Wu O, Reese TG, Wedeen VJ, Davis TL, Stakes JW, Caviness VS, Kaplan E, Rosen BR, Pandya DN, Kennedy DN (1997) Morphometry of in vivo human white matter association pathways with diffusion-weighted magnetic resonance imaging. Ann Neurol 42(6):951–962
44. Makris N, Kennedy DN, McInerey S, Sorensen AG, Wang R, Caviness VS Jr, Pandya DN (2005) Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. Cereb cortex 15:854–869
45. Miller R (1975) Distribution and properties of commissural and other neurons in the cat sensorimotor cortex. J Comp Neurol 164:119–132
46. Miller R (1987) Representation of brief temporal patterns, Hebbian synapses, and the left-hemisphere dominance for phoneme recognition. Psychobiology 15(3):241–247
47. Miller R (1991) Cortico-hippocampal interplay and the representation of objects in the brain. Springer, Berlin
48. Miller R (1994) What is the contribution of axonal conduction delay to temporal structure in brain dynamics? In: Pantev C, Elbert T, Lütkenhöner B (eds) Oscillatory event-related brain dynamics. Plenum Press, New York, London, pp 53–57
49. Miller R (1996) Axonal conduction time and human cerebral laterality. A psychobiological theory. Harwood Academic Publishers, Australia
50. Miller R (2008) A neurodynamic theory on schizophrenia (and related disorders). Lulu Enterprises, Morrinsville
51. Mohajerani MH, McVea DA, Fingas M, Murphy TH (2010) Mirrored bilateral slow-wave cortical activity within local circuits revealed by fast bihemispheric voltage-sensitive dye imaging in anesthetized and awake mice. J Neurosci 30(10):3745–3751
52. Munk MHJ, Nowak LG, Nelson JI, Bullier J (1995) Structural basis of synchronization. II. Effects of cortical lesions. J Neurophysiol 74(6):2401–2414
53. Nieuwenhuys R, Voogd J, van Huijzen C (2008) The human central nervous system: a synopsis and atlas (Google eBook), 4th edn. Springer, Berlin Heidelberg
54. Nieuwenhuys R, ten Dinkelaar HJ, Nicholson C (1998) The central nervous system of vertebrates, vol 1. Springer, Berlin
55. Olivares R, Montiel J, Aboitiz F (2001) Species differences and similarities in the fine structure of the mammalian corpus callosum. Brain Behavior Evol 57:98–105
56. Palay LS, Chan-Palay V (1974) Cereb Cortex. Springer, Berlin
57. Partadiredja G, Miller R, Oorschot DE (2003) The number, size, and type of axons in rat subcortical white matter on left and right sides: a stereological, ultrastructural study. J Neurocyt 32:1165–1179
58. Park H-J, Westin C-F, Kubicki M, Maier SE, Niznikiewicz M, Baer A, Frumin M, Kikinis R, Jolesz FA, McCarley RW, Shenton ME (2004) White matter hemisphere asymmetries in healthy subjects and in schizophrenia: a diffusion tensor MRI study. NeuroImage 23:213–223
59. Perge JA, Koch K, Miller R, Sterling P, Balasubramanian V (2009) How the optic nerve allocates space, energy capacity, and information. J Neurosci 29:7917–7928
60. Perge JA, Niven JE, Mugnaini E, Balasubramanian V, Sterling P (2012) Why do axons differ in caliber? J Neurosci 32(2):626–638
61. Peters A, Palay SL, Webster H deF (1991) The fine structure of the nervous system. Oxford University Press, New York
62. Pouille F, Scanziani M (2001) Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293:1159–1163
63. Ringo JL, Doty RW, Demeter S, Simard PY (1994) Time is of the essence: a conjecture that hemispheric specialization arises from interhemispheric conduction delay. Cereb Cortex 4:331–343
64. Ritz R, Gerstner W, Fuentes U, van Hemmen JL (1994) A biologically motivated and analytically soluble model of collective oscillations in the cortex. II. Application to binding and pattern segmentation. Biol Cybern 71:349–358
65. Roberts JA, Robinson PA (2008) Modeling distributed axonal delays in mean-field brain dynamics. Phys Rev 78:051901
66. Rolheiser T, Stamatakis EA, Tyler LK (2011) Dynamic processing in the human language system: synergy between the arcuate fascicle and extreme capsule. J Neurosci 31(47):16949–16957. doi:10.1523/JNEUROSCI.2725-11.2011
67. Roxin A, Brunel N, Hansel D (2005) Role of delays in shaping spatiotemporal dynamics of neuronal activity in large networks. Phys Rev Lett 94:238103
68. Schüz A, Braitenberg V (2002) The human cortical white matter: quantitative aspects of cortico-cortical long-range connectivity. In: Schüz A, Miller R (eds) Cortical areas: unity and diversity. Taylor and Francis, London, pp 377–385
69. Schüz A, Demianenko GP (1995) Constancy and variability in cortical structure. A study on synapses and dendritic spines in hedgehog and monkey. J Brain Res 36(1):113–122
70. Schüz A, Preißl H (1996) Basic connectivity of the cerebral cortex and some considerations on the corpus callosum. Neurosci Biobehav Rev 20(4):567–570
71. Schüz A, Sultan F (2009) Brain connectivity and brain size. In: Squire LR (ed) Encyclopedia of neuroscience, vol 2. Academic Press, Oxford, pp 317–326
72. Sultan F (2000) Exploring a critical parameter of timing in the mouse cerebellar microcircuitry: the parallel fibre diameter. Neurosci Lett 280:41–44
73. Swadlow HA, Rosene DL, Waxman SG (1978) Characteristics of interhemispheric impulse conduction between prelunate gyri of the rhesus monkey. Exp Brain Res 33:455–467
74. Swadlow HA, Waxman SG, Geschwind N (1980) Small-diameter non-myelinated axons in the primate corpus callosum. Arch Neurol 37:114–115
75. Swadlow HA (2000) Information flow along neocortical axons. In: Miller R (ed) Time and the Brain. Harwood Academic Publishers, Australia, pp 131–155
76. Tomasi S, Caminiti R, Innocenti GM (2012) Areal differences in diameter and length of corticofugal projections. Cereb Cortex 22:1464–1472
77. Tomassy GS, Berger DR, Chen H-H, Kasthuri N, Hayworth KJ, Vercelli A, Seung HS, Lichtman JW, Arlotta P (2014) Distinct profiles of myelin distribution along single axons of pyramidal neurons in the neocortex. Science 433:319–324
78. Ungerleider LG, Gaffan D, Pelak VS (1989) Projections from the inferior temporal cortex to prefrontal cortex via the uncinate fascicle in rhesus monkey. Exp Brain Res 76:417–484
79. Wang SH, Shultz JR, Burish MJ, Harrison KH, Hof PR, Towns LC, Wagers MW, Wyatt KD (2008) Functional trade-offs in white matter axonal scaling. J Neurosci 28(15):4047–4056
80. Wakana S, Jiang H, Nagae-Poetscher LM, Zijl PCM, Mori S (2003) Fiber tract-based atlas of human white matter anatomy. Radiology 230(1):77–87
81. Williams PL, Wendell-Smith CP (1971) Some additional parametric variations between peripheral nerve fibre populations. J Anat 109(3):505–526
82. Yeterian EH, Pandya DN, Tomaiuolo F, Petrides M (2012) The cortical connectivity of the prefrontal cortex in the monkey brain. Cortex 48:58–81
83. Zhang K, Sejnowski TJ (2000) A universal scaling law between gray matter and white matter of cerebral cortex. Proc Natl Acad Sci 97(10):5621–5626
84. Zikopoulos B, Barbas H (2010) Changes in prefrontal axons may disrupt the network in autism. J Neurosci 30(44):14595–14609