Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2013, Article ID 149060, 7 pages
http://dx.doi.org/10.1155/2013/149060
Review Article

Axon Guidance Mechanisms for Establishment of Callosal Connections

Department of Anatomy, School of Medicine, Keio University, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan

Received 6 June 2012; Revised 30 December 2012; Accepted 21 January 2013

Academic Editor: Giorgio M. Innocenti

Copyright © 2013 Mitsuaki Nishikimi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. B. D. Mitchell and J. D. Macklis, “Large-scale maintenance of dual projections by callosal and frontal cortical projection neurons in adult mice,” Journal of Comparative Neurology, vol. 482, no. 1, pp. 17–32, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. R. Mihrshahi, “The corpus callosum as an evolutionary innovation,” Journal of Experimental Zoology B, vol. 306, no. 1, pp. 8–17, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Biegon, J. L. Eberling, B. C. Richardson et al., “Human corpus callosum in aging and Alzheimer's disease: a magnetic resonance imaging study,” Neurobiology of Aging, vol. 15, no. 4, pp. 393–397, 1994. View at Publisher · View at Google Scholar · View at Scopus
  4. M. G. Funnell, P. M. Corballis, and M. Gazzaniga, “Cortical and subcortical interhemispheric interactions following partial and complete callosotomy,” Archives of Neurology, vol. 57, no. 2, pp. 185–189, 2000. View at Google Scholar · View at Scopus
  5. D. Kamnasaran, “Agenesis of the corpus callosum: lessons from humans and mice,” Clinical and Investigative Medicine, vol. 28, no. 5, pp. 267–282, 2005. View at Google Scholar · View at Scopus
  6. R. M. Fame, J. L. MacDonald, and J. D. Macklis, “Development, specification, and diversity of callosal projection neurons,” Trends in Neurosciences, vol. 34, no. 1, pp. 41–50, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. E. A. Alcamo, L. Chirivella, M. Dautzenberg et al., “Satb2 regulates callosal projection neuron identity in the developing cerebral cortex,” Neuron, vol. 57, no. 3, pp. 364–377, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Silver, S. E. Lorenz, D. Wahlstein, and J. Coughlin, “Axonal guidance during development of the great cerebral commissures: descriptive and experimental studies, in vivo, on the role of preformed glial pathways,” Journal of Comparative Neurology, vol. 210, no. 1, pp. 10–29, 1982. View at Google Scholar · View at Scopus
  9. L. J. Richards, C. Plachez, and T. Ren, “Mechanisms regulating the development of the corpus callosum and its agenesis in mouse and human,” Clinical Genetics, vol. 66, no. 4, pp. 276–289, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. Y. Tagawa, H. Mizuno, and T. Hirano, “Activity-dependent development of interhemispheric connections in the visual cortex,” Reviews in the Neurosciences, vol. 19, no. 1, pp. 19–28, 2008. View at Google Scholar · View at Scopus
  11. C. L. Wang, L. Zhang, Y. Zhou et al., “Activity-dependent development of callosal projections in the somatosensory cortex,” Journal of Neuroscience, vol. 27, no. 42, pp. 11334–11342, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. H. Mizuno, T. Hirano, and Y. Tagawa, “Evidence for activity-dependent cortical wiring: formation of interhemispheric connections in neonatal mouse visual cortex requires projection neuron activity,” Journal of Neuroscience, vol. 27, no. 25, pp. 6760–6770, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. R. R. Sturrock, “Identification of mitotic cells in the central nervous system by electron microscopy of re-embedded semithin sections,” Journal of Anatomy, vol. 138, no. 4, pp. 657–673, 1984. View at Google Scholar · View at Scopus
  14. T. Shu, Y. Li, A. Keller, and L. J. Richards, “The glial sling is a migratory population of developing neurons,” Development, vol. 130, no. 13, pp. 2929–2937, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. T. Shu and L. J. Richards, “Cortical axon guidance by the glial wedge during the development of the corpus callosum,” Journal of Neuroscience, vol. 21, no. 8, pp. 2749–2758, 2001. View at Google Scholar · View at Scopus
  16. T. Shu, A. C. Puche, and L. J. Richards, “Development of midline glial populations at the corticoseptal boundary,” Journal of Neurobiology, vol. 57, no. 1, pp. 81–94, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Silver, M. A. Edwards, and P. Levitt, “Immunocytochemical demonstration of early appearing astroglial structures that form boundaries and pathways along axon tracts in the fetal brain,” Journal of Comparative Neurology, vol. 328, no. 3, pp. 415–436, 1993. View at Publisher · View at Google Scholar · View at Scopus
  18. T. Shu, K. G. Butz, C. Plachez, R. M. Gronostajski, and L. J. Richards, “Abnormal development of forebrain midline glia and commissural projections in Nfia knock-out mice,” Journal of Neuroscience, vol. 23, no. 1, pp. 203–212, 2003. View at Google Scholar · View at Scopus
  19. S. Tole, G. Gutin, L. Bhatnagar, R. Remedios, and J. M. Hébert, “Development of midline cell types and commissural axon tracts requires Fgfr1 in the cerebrum,” Developmental Biology, vol. 289, no. 1, pp. 141–151, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. S. E. Bilasy, T. Satoh, T. Terashima, and T. Kataoka, “RA-GEF-1 (Rapgef2) is essential for proper development of the midline commissures,” Neuroscience Research, vol. 71, no. 3, pp. 200–209, 2011. View at Publisher · View at Google Scholar
  21. C. Sánchez-Camacho, J. A. Ortega, I. Ocaña, S. Alcántara, and P. Bovolenta, “Appropriate Bmp7 levels are required for the differentiation of midline guidepost cells involved in corpus callosum formation,” Developmental Neurobiology, vol. 71, no. 5, pp. 337–350, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Piper, R. X. Moldrich, C. Lindwall et al., “Multiple non-cell-autonomous defects underlie neocortical callosal dysgenesis in Nfib-deficient mice,” Neural Development, vol. 4, no. 1, p. 43, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Piper, G. Barry, J. Hawkins et al., “NFIA controls telencephalic progenitor cell differentiation through repression of the Notch effector Hes1,” Journal of Neuroscience, vol. 30, no. 27, pp. 9127–9139, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Bagri, O. Marín, A. S. Plump et al., “Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain,” Neuron, vol. 33, no. 2, pp. 233–248, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. W. Andrews, A. Liapi, C. Plachez et al., “Robo1 regulates the development of major axon tracts and interneuron migration in the forebrain,” Development, vol. 133, no. 11, pp. 2243–2252, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. T. R. Keeble, M. M. Halford, C. Seaman et al., “The Wnt receptor Ryk is required for Wnt5a-mediated axon guidance on the contralateral side of the corpus callosum,” Journal of Neuroscience, vol. 26, no. 21, pp. 5840–5848, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Shu, K. M. Valentino, C. Seaman, H. M. Cooper, and L. J. Richards, “Expression of the netrin-1 receptor, deleted in colorectal cancer (DCC), is largely confined to projecting neurons in the developing forebrain,” Journal of Comparative Neurology, vol. 416, no. 2, pp. 201–212, 2000. View at Publisher · View at Google Scholar
  28. T. Serafini, S. A. Colamarino, E. D. Leonardo et al., “Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system,” Cell, vol. 87, no. 6, pp. 1001–1014, 1996. View at Publisher · View at Google Scholar · View at Scopus
  29. S. M. Islam, Y. Shinmyo, T. Okafuji et al., “Draxin, a repulsive guidance protein for spinal cord and forebrain commissures,” Science, vol. 323, no. 5912, pp. 388–393, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. H. Zhao, T. Maruyama, Y. Hattori et al., “A molecular mechanism that regulates medially oriented axonal growth of upper layer neurons in the developing neocortex,” Journal of Comparative Neurology, vol. 519, no. 5, pp. 834–848, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. D. K. Unni, M. Piper, R. X. Moldrich et al., “Multiple Slits regulate the development of midline glial populations and the corpus callosum,” Developmental Biology, vol. 365, no. 1, pp. 36–49, 2012. View at Publisher · View at Google Scholar
  32. L. Li, B. I. Hutchins, and K. Kalil, “Wnt5a induces simultaneous cortical axon outgrowth and repulsive axon guidance through distinct signaling mechanisms,” Journal of Neuroscience, vol. 29, no. 18, pp. 5873–5883, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. L. Li, B. I. Hutchins, and K. Kalil, “Wnt5a induces simultaneous cortical axon outgrowth and repulsive turning through distinct signaling mechanisms,” Science Signaling, vol. 3, no. 147, p. pt2, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Niquille, S. Garel, F. Mann et al., “Transient neuronal populations are required to guide callosal axons: a role for semaphorin 3C,” PLoS Biology, vol. 7, no. 10, Article ID e1000230, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. Choe, J. A. Siegenthaler, and S. J. Pleasure, “A cascade of morphogenic signaling initiated by the meninges controls corpus callosum formation,” Neuron, vol. 73, no. 4, pp. 698–712, 2012. View at Publisher · View at Google Scholar
  36. A. Martínez and E. Soriano, “Functions of ephrin/Eph interactions in the development of the nervous system: emphasis on the hippocampal system,” Brain Research Reviews, vol. 49, no. 2, pp. 211–226, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. J. O. Bush and P. Soriano, “Ephrin-B1 regulates axon guidance by reverse signaling through a PDZ-dependent mechanism,” Genes and Development, vol. 23, no. 13, pp. 1586–1599, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Davy and P. Soriano, “Ephrin signaling in vivo: look both ways,” Developmental Dynamics, vol. 232, no. 1, pp. 1–10, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. C. Lindwall, T. Fothergill, and L. J. Richards, “Commissure formation in the mammalian forebrain,” Current Opinion in Neurobiology, vol. 17, no. 1, pp. 3–14, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. S. W. Mendes, M. Henkemeyer, and D. J. Liebl, “Multiple Eph receptors and B-class ephrins regulate midline crossing of corpus callosum fibers in the developing mouse forebrain,” Journal of Neuroscience, vol. 26, no. 3, pp. 882–892, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. C. Plachez and L. J. Richards, “Mechanisms of axon guidance in the developing nervous system,” Current Topics in Developmental Biology, vol. 69, pp. 267–346, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. S. E. Koester and D. D. M. O'Leary, “Axons of early generated neurons in cingulate cortex pioneer the corpus callosum,” Journal of Neuroscience, vol. 14, no. 11, pp. 6608–6620, 1994. View at Google Scholar · View at Scopus
  43. B. G. Rash and L. J. Richards, “A role for cingulate pioneering axons in the development of the corpus callosum,” Journal of Comparative Neurology, vol. 434, no. 2, pp. 147–157, 2001. View at Publisher · View at Google Scholar · View at Scopus
  44. L. C. deAzevedo, C. Hedin-Pereira, and R. Lent, “Callosal neurons in the cingulate cortical plate and subplate of human fetuses,” Journal of Comparative Neurology, vol. 386, no. 1, pp. 60–70, 1997. View at Publisher · View at Google Scholar
  45. M. Piper, C. Plachez, O. Zalucki et al., “Neuropilin 1-Sema signaling regulates crossing of cingulate pioneering axons during development of the corpus callosum,” Cerebral Cortex, vol. 19, supplement 1, pp. i11–i21, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. H. S. Ozaki and D. Wahlsten, “Timing and origin of the first cortical axons to project through the corpus callosum and the subsequent emergence of callosal projection cells in mouse,” Journal of Comparative Neurology, vol. 400, no. 2, pp. 197–206, 1998. View at Publisher · View at Google Scholar
  47. S. O. Chan and K. Y. Chung, “Changes in axon arrangement in the retinofugal [correction of retinofungal] pathway of mouse embryos: confocal microscopy study using single- and double-dye label,” Journal of Comparative Neurology, vol. 406, no. 2, pp. 251–262, 1999. View at Publisher · View at Google Scholar
  48. B. W. Gallarda, D. Bonanomi, D. Müller et al., “Segregation of axial motor and sensory pathways via heterotypic trans-axonal signaling,” Science, vol. 320, no. 5873, pp. 233–236, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. D. T. Plas, J. E. Lopez, and M. C. Crair, “Pretarget sorting of retinocollicular axons in the mouse,” Journal of Comparative Neurology, vol. 491, no. 4, pp. 305–319, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. T. Imai, T. Yamazaki, R. Kobayakawa et al., “Pre-Target axon sorting establishes the neural map topography,” Science, vol. 325, no. 5940, pp. 585–590, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. C. Kudo, I. Ajioka, Y. Hirata, and K. Nakajima, “Expression profiles of EphA3 at both the RNA and protein level in the developing mammalian forebrain,” Journal of Comparative Neurology, vol. 487, no. 3, pp. 255–269, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Nishikimi, K. Oishi, H. Tabata, K. Torii, and K. Nakajima, “Segregation and pathfinding of callosal axons through EphA3 signaling,” Journal of Neuroscience, vol. 31, no. 45, pp. 16251–16260, 2011. View at Publisher · View at Google Scholar
  53. H. Tabata and K. Nakajima, “Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex,” Neuroscience, vol. 103, no. 4, pp. 865–872, 2001. View at Publisher · View at Google Scholar · View at Scopus
  54. B. Knöll, C. Weinl, A. Nordheim, and F. Bonhoeffer, “Stripe assay to examine axonal guidance and cell migration,” Nature Protocols, vol. 2, no. 5, pp. 1216–1224, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. T. Maruyama, M. Matsuura, K. Suzuki, and N. Yamamoto, “Cooperative activity of multiple upper layer proteins for thalamocortical axon growth,” Developmental Neurobiology, vol. 68, no. 3, pp. 317–331, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. G. M. Innocenti, “Growth and reshaping of axons in the establishment of visual callosal connections,” Science, vol. 212, no. 4496, pp. 824–827, 1981. View at Google Scholar · View at Scopus
  57. G. M. Innocenti and D. J. Price, “Exuberance in the development of cortical networks,” Nature Reviews Neuroscience, vol. 6, no. 12, pp. 955–965, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. J. H. Leslie and E. Nedivi, “Activity-regulated genes as mediators of neural circuit plasticity,” Progress in Neurobiology, vol. 94, no. 3, pp. 223–237, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. J. Olavarria and R. C. Van Sluyters, “Callosal connections of the posterior neocortex in normal-eyed, congenitally anophthalmic, and neonatally enucleated mice,” Journal of Comparative Neurology, vol. 230, no. 2, pp. 249–268, 1984. View at Google Scholar · View at Scopus
  60. G. M. Innocenti, D. O. Frost, and J. Illes, “Maturation of visual callosal connections in visually deprived kittens: a challenging critical period,” Journal of Neuroscience, vol. 5, no. 2, pp. 255–267, 1985. View at Google Scholar · View at Scopus
  61. M. G. Hanson and L. T. Landmesser, “Normal patterns of spontaneous activity are required for correct motor axon guidance and the expression of specific guidance molecules,” Neuron, vol. 43, no. 5, pp. 687–701, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. S. Serizawa, K. Miyamichi, H. Takeuchi, Y. Yamagishi, M. Suzuki, and H. Sakano, “A neuronal identity code for the odorant receptor-specific and activity-dependent axon sorting,” Cell, vol. 127, no. 5, pp. 1057–1069, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. K. Itoh, B. Stevens, M. Schachner, and R. D. Fields, “Regulated expression of the neural cell adhesion molecule L1 by specific patterns of neural impulses,” Science, vol. 270, no. 5240, pp. 1369–1372, 1995. View at Google Scholar · View at Scopus
  64. V. Conti, C. Marini, S. Gana, J. Sudi, W. B. Dobyns, and R. Guerrini, “Corpus callosum agenesis, severe mental retardation, epilepsy, and dyskinetic quadriparesis due to a novel mutation in the homeodomain of ARX,” American Journal of Medical Genetics, Part A, vol. 155, no. 4, pp. 892–897, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. G. Friocourt, K. Poirier, S. Rakić, J. G. Parnavelas, and J. Chelly, “The role of ARX in cortical development,” European Journal of Neuroscience, vol. 23, no. 4, pp. 869–876, 2006. View at Publisher · View at Google Scholar · View at Scopus
  66. T. Ren, J. Zhang, C. Plachez, S. Mori, and L. J. Richards, “Diffusion tensor magnetic resonance imaging and tract-tracing analysis of probst bundle structure in netrin1- and DCC-deficient mice,” Journal of Neuroscience, vol. 27, no. 39, pp. 10345–10349, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. H. S. Ozaki and D. Wahlsten, “Cortical axon trajectories and growth cone morphologies in fetuses of acallosal mouse strains,” Journal of Comparative Neurology, vol. 336, no. 4, pp. 595–604, 1993. View at Google Scholar · View at Scopus
  68. R. Lent, D. Uziel, M. Baudrimont, and C. Fallet, “Cellular and molecular tunnels surrounding the forebrain commissures of human fetuses,” Journal of Comparative Neurology, vol. 483, no. 4, pp. 375–382, 2005. View at Publisher · View at Google Scholar · View at Scopus
  69. A. L. S. Donahoo and L. J. Richards, “Understanding the mechanisms of callosal development through the use of transgenic mouse models,” Seminars in Pediatric Neurology, vol. 16, no. 3, pp. 127–142, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. T. Ren, A. Anderson, W. B. Shen et al., “Imaging, anatomical, and molecular analysis of callosal formation in the developing human fetal brain,” Anatomical Record A, vol. 288, no. 2, pp. 191–204, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. J. K. Gupta and R. J. Lilford, “Assessment and management of fetal agenesis of the corpus callosum,” Prenatal Diagnosis, vol. 15, no. 4, pp. 301–312, 1995. View at Google Scholar · View at Scopus
  72. H. C. Sauerwein and M. Lassonde, “Cognitive and sensori-motor functioning in the absence of the corpus callosum: neuropsychological studies in callosal agenesis and callosotomized patients,” Behavioural Brain Research, vol. 64, no. 1-2, pp. 229–240, 1994. View at Publisher · View at Google Scholar · View at Scopus
  73. L. K. Paul, B. Schieffer, and W. S. Brown, “Social processing deficits in agenesis of the corpus callosum: narratives from the Thematic Apperception Test,” Archives of Clinical Neuropsychology, vol. 19, no. 2, pp. 215–225, 2004. View at Publisher · View at Google Scholar · View at Scopus
  74. B. Egaas, E. Courchesne, and O. Saitoh, “Reduced size of corpus callosum in autism,” Archives of Neurology, vol. 52, no. 8, pp. 794–801, 1995. View at Google Scholar · View at Scopus
  75. I. K. Lyoo, G. G. Noam, C. K. Lee, H. K. Lee, B. P. Kennedy, and P. F. Renshaw, “The corpus callosum and lateral ventricles in children with attention-deficit hyperactivity disorder: a brain magnetic resonance imaging study,” Biological Psychiatry, vol. 40, no. 10, pp. 1060–1063, 1996. View at Publisher · View at Google Scholar · View at Scopus
  76. O. Lungu and E. Stip, “Agenesis of corpus callosum and emotional information processing in schizophrenia,” Front Psychiatry, vol. 3, p. 1, 2012. View at Publisher · View at Google Scholar