Connectivity of Transplants in the Cerebellum: A Model of Developmental Differences in Neuroplasticity

  • Monica M. Oblinger
  • Gopal D. Das
Part of the Proceedings in Life Sciences book series (LIFE SCIENCES)

Abstract

The problem of mammalian central nervous system (CNS) regeneration has been a cynosure for neurobiologists for nearly a century. Different types of central neurons have been shown to differ in their response to direct injury. Some, namely, the weakly myelinated monoaminergic systems, maintain considerable reGenerative capacity through adulthood (reviewed in Björklund and Stenevi 1979). Others, such as the long myelinated systems of the spinal cord, exhibit nearly none. While the current consensus on the capacity of most intrinsic CNS neurons to exhibit true regeneration remains pessimistic, demonstrations of a similar response, compensatory sprouting of residual fibers in response to partial denervation, have gained general acceptance. Clearly, in many respects, these forms of a sprouting response are inherently similar since both involve the active elongation of axons.

Keywords

Sugar Formalin Dopamine Assure Noradrenaline 

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References

  1. Altman, J. (1969). Autoradiographic and histoloGical studies of postnatal neuroGenesis. III. DatinG the time of proDuction and onset of Differentiation of cerebellar microneurons in the rat. J. Comp. Neurol. 136, 269–294.PubMedCrossRefGoogle Scholar
  2. Altman, J. (1972a). Postnatal Development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer. J. Comp. Neurol. 145, 399–464.PubMedCrossRefGoogle Scholar
  3. Altman, J. (1972b). Postnatal Development of the cerebellar cortex in the rat. III. Maturation of the components of the Granular layer. J. Comp. Neurol. 145, 465–514.PubMedCrossRefGoogle Scholar
  4. Altman, J., Bayer, S. A. (1978). Prenatal Development of the cerebellar system in the rat. II. CytoGenesis and histoGenesis of the inferior olive, pontine Gray and the precerebellar reticular nuclei. J. Comp. Neurol. 179, 49–76.PubMedCrossRefGoogle Scholar
  5. Altman, J., Winfree, A. T. (1977). Postnatal Development of Purkinje cell perikarya V. Spatial orGanization of Purkinje cell perikarya. J. Comp. Neurol. 171, 1–16.PubMedCrossRefGoogle Scholar
  6. Altobelli, R. (1914). Innesti cerebrali. Gazz. Int. MeD Chir. 17, 25.Google Scholar
  7. AnGaut, P., AlvarDo-Mallart, R. M., Sotelo, C. (1982). Ultrastructural eviDence for compensatory sproutinG of climbinG and mossy afferents to the cerebellar hemisphere after ipsilateral peDunculotomy in the newborn rat. J. Comp. Neurol. 205, 101–111.PubMedCrossRefGoogle Scholar
  8. Benfrey, M., Aguayo, A. J. (1982). Extensive elongation of axons from rat brain into peripheral nerve Grafts. Nature (London) 296, 150–152.CrossRefGoogle Scholar
  9. Björklund, A., Johansson, B., Stenevi, U., Svendgaard, N.-A.A. (1975). Reestablishment of functional connections by reGeneratinG central adrenergic and cholinergic axons. Nature (London) 253, 446–448.CrossRefGoogle Scholar
  10. Björklund, A., Stenevi, U. (1971). Growth of central catecholamine neurons into smooth muscle Grafts in the rat mesencephalon. Brain Res. 31, 1–20.PubMedCrossRefGoogle Scholar
  11. Björklund, A., Stenevi, U. (1979). Regeneration of monoaminergic and cholinergic neurons in the mammalian central nervous system. Physiol. Rev. 59, 62–100.PubMedGoogle Scholar
  12. Black, M. M., Lasek, R. J. (1979). SlowinG of the rate of axonal regeneration DurinG Growth and maturation. Exp. Neurol. 63, 108–119.PubMedCrossRefGoogle Scholar
  13. BloeDel, J. R. (1973). Cerebellar afferent systems: A review. ProG. Neurobiol. 2, 1–68.CrossRefGoogle Scholar
  14. BroDai, A., Kawamura, K. (1980). Olivocerebellar proJection: A review. ADvan. Anat. Embryol. Cell Biol. 64, 1–137.Google Scholar
  15. Clemente, C. D. (1955). Structural regeneration in the mammalian central nervous system and the role of neuroGlia and connective tissue. In: Regeneration in the Central Nervous System. Windle, W. F. (ed.). SprinGfielD, III.: Charles C. Thomas.Google Scholar
  16. Clemente, C. D. (1964). Regeneration in the vertebrate central nervous system. Int. Rev. Neurobiol. 6, 257–301.PubMedCrossRefGoogle Scholar
  17. Cotman, C. W., Lynch, G. S. (1976). Reactive synaptoGenesis in the adult nervous system. In: Neuronal RecoGnition. BaronDes, S. H. (ed.). London: Chapman & Hall.Google Scholar
  18. Cotman, C. W., Matthews, D. A., Taylor, D., Lynch, G. S. (1973). Synaptic rearranGement in the Dentate Gyrus: Histochemical eviDence of aDJustments after lesions in immature and adult rats. Proc. Nat. AcaD. Sci. USA 70, 3473–3477.PubMedCrossRefGoogle Scholar
  19. Cotman, C. W., Nieto-SampeDro, M., Harris, E. W. (1981). Synapse replacement in the nervous system of adult vertebrates. Physiol. Rev. 61, 684–784.PubMedGoogle Scholar
  20. Crépel, F. (1971). Maturation of climbinG fiber responses in the rat. Brain Res. 35, 272–276.PubMedCrossRefGoogle Scholar
  21. Crépel, F., Mariani, J., Delhaye-BouchauD, N. (1976). EviDence for a multiple innervation of Purkinje cells by climbinG fibers in the immature rat cerebellum. J. Neurobiol. 8, 567–578.CrossRefGoogle Scholar
  22. Das, G. D. (1974). Transplantation of embryonic neural tissue in the mammalian brain. I. Growth and Differentiation of neuroblasts from various regions of the embryonic brain in the cerebellum of neonate rats. TIT J. Life Sci. 4, 93–124.PubMedGoogle Scholar
  23. Das, G. D. (1975). Differentiation of DenDrites in the transplanteD neuroblasts in the mammalian brain. In: Physiology and Pathology of DenDrites. Kreutzberg, G. W. (ed.). Advances in NeuroloGy, Vol. 12. New York: Raven Press, pp. 181–199.Google Scholar
  24. Das, G. D. (1979). Neural transplants in the brain of the rat: Nature of DeGenerative chanGes in the host brain and the transplant. Anat. Rec. 193, 517.Google Scholar
  25. Das, G. D., Altman, J. (1971). TransplanteD precursors of nerve cells: Their fate in the cerebellums of young rats. Science 173, 637–638.PubMedCrossRefGoogle Scholar
  26. Das, G. D., Altman, J. (1972). StuDies on the transplantation of DevelopinG neural tissue in the mammalian brain. I. Transplantation of cerebellar slabs into the cerebellum of neonate rats. Brain Res. 38, 233–249.PubMedCrossRefGoogle Scholar
  27. Das, G. D., Hallas, B. H., Das, K. G. (1979). Transplantation of neural tissues in the brains of laboratory mammals: Technical Details and comments. Experientia 35, 143–153.PubMedCrossRefGoogle Scholar
  28. Das, G. D., Hallas, B. H., Das, K. G. (1980). Transplantation of brain tissue in the brain of the rat. I. Growth characteristics of transplants from embryos of Different aGes. Am. J. Anat. 158, 135–145.PubMedCrossRefGoogle Scholar
  29. Das, G. D., Houlé, J., Oblinger, M. M., Ross, D. (1983). Survivability of Different embryonic neural tissues transplanteD to the neonate rat brain. In preparation.Google Scholar
  30. Das, G. D., Nornes, H. O. (1972). NeuroGenesis in the cerebellum of the rat: An autoraDioGrapic study. Z. Anat. EntwicklunGsGesch. 138, 155–165.PubMedCrossRefGoogle Scholar
  31. Das, G. D., Nornes, H. O., Hine, R. J., Pfaffenroth, M. J. (1973). Experimental studies on the postnatal Development of the brain. II. Cytoarchitectural regeneration in the DevelopinG cerebellum of the rabbit. TIT J. Life Sci. 3:29–65.PubMedGoogle Scholar
  32. Devor, M. (1976). Neuroplasticity in the rearranGement of olfactory tract fibers after neonatal transection in hamsters. J. Comp. Neurol. 166, 49–72.PubMedCrossRefGoogle Scholar
  33. Dunn, E. (1917). Primary and seconDary finDinGs in a series of attempts to transplant cerebral cortex in the albino rat. J. Comp. Neurol. 27, 565–582.CrossRefGoogle Scholar
  34. Emson, P. C., Björklund, A., Stenevi, U. (1976). Possible regeneration of γ-aminobutyric aciD containinG fibres into iriDes transplanteD into the central nervous system. Nature (London) 259, 567–570.CrossRefGoogle Scholar
  35. Emson, P. C., Björklund, A., Stenevi, U. (1977). Evaluation of the reGenerative capacity of central Dopaminergic, noradrenergic and cholinergic neurones usinG iris implants as tarGets. Brain Res. 135, 87–105.PubMedCrossRefGoogle Scholar
  36. Fink, R. P., Heimer, L. (1967). Two methoDs for selective silver impreGnation of DeGeneratinG axons and their synaptic enDinGs in the central nervous system. Brain Res. 4, 369–374.PubMedCrossRefGoogle Scholar
  37. Gall, C., Lynch, G. (1978). RapiD axon sproutinG in the neonatal rat hippocampus. Brain Res. 153, 357–362.PubMedCrossRefGoogle Scholar
  38. Gall, C., McWilliams, R., Lynch, G. (1979). The effect of collateral sproutinG on the Density of innervation of normal tarGet sites: Implications for theories on the reGulation of the size of DevelopinG synaptic Domains. Brain Res. 175, 37–47.PubMedCrossRefGoogle Scholar
  39. Glees, P. (1955). StuDies on cortical regeneration with special reference to central implants. In: Regeneration in the Central Nervous System. Windle, W. F. (ed.). SprinGfielD, III: Charles C. Thomas.Google Scholar
  40. Gould, B. B. (1980). OrGanization of afferents from the brain stem nuclei to the cerebellar cortex in the cat. ADvan. Anat. Embryol. Cell Biol. 62, 1–79.CrossRefGoogle Scholar
  41. Gutmann, E., Guttman, L., Medawar, P. B., Young, J. Z. (1942). The rate of regeneration of nerve. J. Exp. Biol. 19, 14–44.Google Scholar
  42. Hallas, B. H., Oblinger, M. M., Das, G. D. (1980a). Heterotopic neural transplants in the cerebellum of the rat: Their afferents. Brain Res. 196, 242–246.PubMedCrossRefGoogle Scholar
  43. Hallas, B. H., Das, G. D., Das, K. G. (1980b). Transplantation of brain tissue in the brain of rat. II. Growth characteristics of transplants in hosts of Different aGes. Am. J. Anat. 158, 147–159.PubMedCrossRefGoogle Scholar
  44. HenDrickson, A. E., Cowan, M. (1971). ChanGes in the rate of axoplasmic transport DurinG postnatal Development of the rabbit’s optic nerve and tract. Exp. Neurol. 30, 403–422.PubMedCrossRefGoogle Scholar
  45. Jaeger, C. B., Lund, R. D. (1980a). Transplantation of embryonic occipital cortex to the brain of newborn rats: A light microscopic study of orGanization and connectivity of the transplants. J. Comp. Neurol. 194, 571–597.PubMedCrossRefGoogle Scholar
  46. Jaeger, C. B., Lund, R. D. (1980b). Transplantation of embryonic occipital cortex to the brain of newborn rats. Exp. Brain Res. 40, 265–272.PubMedCrossRefGoogle Scholar
  47. Jaeger, C. B., Lund, R. D. (1981). Transplantation of embryonic occipital cortex to the brain of newborn rats: A GolGi study of mature and DevelopinG transplants. J. Comp. Neurol. 200, 213–230.PubMedCrossRefGoogle Scholar
  48. Kalil, R. E., Schneider, G. E. (1975). Abnormal symaptic connections of the optic tract in the thalamus after miDbrain lesions in newborn hamsters. Brain Res. 100, 690–698.PubMedCrossRefGoogle Scholar
  49. Kalil, R. E., Reh, T. (1979). ReGrowth of severed axons in the neonatal central nervous system: Establishment of normal connections. Science 205, 1158–1161.PubMedCrossRefGoogle Scholar
  50. Kao, C. C., ShimiGer, Y., Perkins, L. C., Freeman, L. W. (1970). Experimental use of cultureD cerebellar cortical tissue to inhibit the collaGenous scar followinG spinal cord transection. J. Neurosurg. 33, 127–139.PubMedCrossRefGoogle Scholar
  51. Komiya, Y. (1980). SlowinG with aGe of the rate of slow axonal flow in bifurcatinG axons of the rat Dorsal root Ganglion cells. Brain Res. 183, 477–480.PubMedCrossRefGoogle Scholar
  52. Komiya, Y. (1981). Axonal regeneration in bifurcatinG axons of Dorsal root Ganglion cells. Exp. Neurol. 73, 824–826.PubMedCrossRefGoogle Scholar
  53. Kromer, L. F. (1980). Glial scar formation in the brain of adult rats is inhibiteD by implants of embryonic CNS tissue. Soc. Neurosci. Abst. 6, 235.9.Google Scholar
  54. Kromer, L. F., Björklund, A., Stenevi, U. (1980). Innervation of embryonic hippo-campal implants by reGeneratinG axons of cholinergic septal neurons in the adult rat. Brain Res. 210, 153–171.CrossRefGoogle Scholar
  55. Kromer, L. F., Björklund, A., Stenevi, U. (1981). Regeneration of the septohippo-campal pathways in adult rats is promoteD by utilizinG embryonic hippocampal implants as briDGes. Brain Res. 210, 173–200.PubMedCrossRefGoogle Scholar
  56. LarramenDi, L. M. H. (1969). Analysis of synaptoGenesis in the cerebellum of the mouse. In: NeurobioloGy of Cerebellar Evolution and Development. Llinas, R. (ed.). ChicaGo: Am. Med. Assoc.Google Scholar
  57. Larsell, O., Jansen, J. (1972). The Comparative Anatomy and HistoloGy of the Cerebellum: The Human Cerebellum, Cerebellum Connections and Cerebellar Cortex. Minneapolis: Univ. Minnesota Press.Google Scholar
  58. Lasek, R. J. (1981). The Dynamic orDerinG of neuronal cytoskeletons. Neurosci. Res. ProG. Bull. 19, 7–32. CambriDGe, Mass.: M.I.T. Press.Google Scholar
  59. Le Gros Clark, W. E. (1942). The problem of neuronal regeneration in the central nervous system. I. The influence of spinal GanGlia and nerve fraGments Grafted in the brain. J. Anat. (London) 77, 20–48.Google Scholar
  60. Le Gros Clark, W. E. (1943). The problem of neuronal regeneration in the central nervous system. II. The insertion of peripheral nerve stumps into the brain. J. Anat. (London) 77, 251–259.Google Scholar
  61. LeonG, S. K. (1976). An experimental study of the corticofuGal system followinG cerebral lesions in the albino rats. Exp. Brain Res. 26, 235–247.PubMedCrossRefGoogle Scholar
  62. Lund, R. D. (1978). Development and Plasticity of the Brain. New York: OxforD Univ. Press.Google Scholar
  63. Lund, R. D., Hauschka, S. D. (1976). TransplanteD neural tissue Develops connections with host rat brain. Science 193, 582–584.PubMedCrossRefGoogle Scholar
  64. Lund, R. D., Lund, J. S. (1976). Plasticity in the DevelopinG visual system: The effects of retinal lesions maDe in young rats. J. Comp. Neurol. 169, 133–154.PubMedCrossRefGoogle Scholar
  65. Lund, R. D., CunninGham, T. S., Lund, J. S. (1973). MoDifieD optic proJections after unilateral eye removal in young rats. Brain Behav. Evol. 8, 51–72.PubMedCrossRefGoogle Scholar
  66. Lynch, G. W., Gall, C., Cotman, C. W. (1977). Temporal parameters of axon sproutinG in the adult brain. Exp. Neurol. 54, 179–183.PubMedCrossRefGoogle Scholar
  67. Matsushita, M., Hosoya, Y., IkeDa, M. (1979). Anatomical orGanization of the spino-cerebellar system in the cat, as stuDieD by retroGraDe transport of horseraDish peroxiDase. J. Comp. Neurol. 184, 81–106.PubMedCrossRefGoogle Scholar
  68. Moyer, E. K., Kimmel, D. L., Winborne, L. W. (1953). Regeneration of sensory spinal roots in young and senile rats. J. Comp. Neurol. 98, 283–388.PubMedCrossRefGoogle Scholar
  69. Mustari, M. J., Lund, R. D. (1976). An aberrant crosseD visual corticotectal pathway in albino rats. Brain Res. 112, 37–42.PubMedCrossRefGoogle Scholar
  70. Nadler, J. V., Cotman, C. W., Lynch, G. S. (1977). Histochemical eviDence of altereD Development of cholinergic fibers in the rat Dentate Gyrus followinG lesions. J. Comp. Neurol. 171, 561–588.PubMedCrossRefGoogle Scholar
  71. Oblinger, M. M., Das, G. D. (1980a). Connectivity of neocortical transplants in the rat cerebellar hemisphere. Anat. Rec. 196, 138.Google Scholar
  72. Oblinger, M. M., Das, G. D. (1980b). Afferent and efferent connections of neocortical transplants in the cerebellum of adult hosts. Soc. Neurosci. Abst. 6, 224.4.Google Scholar
  73. Oblinger, M. M., Das, G. D. (1981). NeuroGenesis in the brain stem of the rabbit: An autoraDioGraphic study. J. Comp. Neurol. 197, 45–62.PubMedCrossRefGoogle Scholar
  74. Oblinger, M. M., Das, G. D. (1982). Connectivity of neural transplants in adult rats: Analysis of afferents and efferents of neocortical transplants in the cerebellar hemisphere. Brain Res. 249, 31–49.PubMedCrossRefGoogle Scholar
  75. Oblinger, M. M., Das, G. D. (1983). AGe Differences in the maGnituDe of afferent fiber inGrowth to cortical transplants in the cerebellar hemisphere. In preparation.Google Scholar
  76. Oblinger, M. M., Hallas, B. H., Das, G. D. (1980). Neocortical transplants in the cerebellum of the rat: Their afferents and efferents. Brain Res. 189, 228–232.PubMedCrossRefGoogle Scholar
  77. Perlow, M. J., Freed, W. J., Hoffer, B. J., Seiger, Å, Olson, L., Wyatt, R. J. (1979). Brain Grafts reDuce motor abnormalities proDuceD by Destruction of niGrostriatal Dopamine system. Science 204, 643–647.PubMedCrossRefGoogle Scholar
  78. Pestronk, A., Drachman, D. B., Griffin, J. W. (1980). Effects of aGinG on nerve sproutinG and reGeneration. Exp. Neurol. 70, 65–82.PubMedCrossRefGoogle Scholar
  79. Pickel, V. M., Krebs, H., Bloom, F. E. (1973). Proliferation of norepinephrine-containinG axons in rat cerebellar cortex after peDuncle lesions. Brain Res. 59, 169–179.PubMedCrossRefGoogle Scholar
  80. Puro, D. G., WooDwarD, D. J. (1977a). Maturation of evokeD climbinG fiber input to rat cerebellar Purkinje cells. (I.). Exp. Brain Res. 28, 85–100.PubMedGoogle Scholar
  81. Puro, D. G., WooDwarD, D. J. (1977b). Maturation of evokeD mossy fiber input to rat cerebellar Purkinje cells (II.). Exp. Brain Res. 28, 427–441.PubMedGoogle Scholar
  82. Ramón J Cajal, S. R. (1928). Degeneration and Regeneration of the Nervous System. London: OxforD Univ. Press.Google Scholar
  83. Ranson, S. W. (1909). Transplantation of the spinal Ganglion into the brain. Q. Bull Northwestern Univ. Med. Sch. 11, 176–178.Google Scholar
  84. RicharDson, P. M., McGuinness, U. M., Aguayo, A. J. (1982). Peripheral nerve autografts to the rat spinal corD: StuDies with axonal tracinG methoDs. Brain Res. 237, 147–162.PubMedCrossRefGoogle Scholar
  85. Ross, D. T., Das, G. D. (1980). Histogenesis of embryonic neocortex transplanteD into the cerebellum of neonatal hosts. Anat. Rec. 196, 160.Google Scholar
  86. Saltykow, S. (1905). Versuche über Gehirnplantation, zugleich ein BeitraG zur Kenntnis Der VorGanGe an den ZellinGen Gehirnelementen. Arch. Psychiatr. Nervenkr. (Berlin). 40, 329–388.CrossRefGoogle Scholar
  87. Schneider, G. F. (1973). Early lesions of superior colliculus: Factors affectinG the formation of abnormal retinal proJections. Brain Behav. Evol. 8, 73–109.PubMedCrossRefGoogle Scholar
  88. Seiger, Å, Olson, L. (1975). Brain tissue transplanteD to the anterior chamber of the eye. (3). Substitution of lackinG central noraDrenaline input by host iris sympathetic fibers in the isolateD cerebral cortex DevelopeD in oculo. Cell Tissue Res. 159, 325–338.PubMedCrossRefGoogle Scholar
  89. Shimono, T., Nosaka, S., Saskai, K. (1976). Electrophysiological study of the postnatal Development of neuronal mechanisms in the rat cerebellar cortex. Brain Res. 108, 279–294.PubMedCrossRefGoogle Scholar
  90. Sotelo, C., Privat, A. (1978). Synaptic remodelinG of the cerebellar circuitry in mutant mice and experimental cerebellar malformations. Acta Neuropathol. (Berlin) 43, 19–34.CrossRefGoogle Scholar
  91. Stenevi, U., Björklund, A. (1978). Transplantation techniques for the study of regeneration in the central nervous system. ProG. Brain Res. 48, 101–112.PubMedCrossRefGoogle Scholar
  92. Stenevi, U., Björklund, A., Svendgaard, N.-A.A. (1976). Transplantation of central and peripheral monoamine neurons to the adult rat brain: Techniques and conditions for survival. Brain Res. 114, 1–20.PubMedCrossRefGoogle Scholar
  93. SuGar, O., Gerard, R. W. (1940). Spinal cord regeneration in the rat. J. Neurophysiol. 3, 1–19.Google Scholar
  94. Svendgaard, N.-A.A. Björklund, A., Stenevi, U. (1975). ReGenerative properties of central monoamine neurons. ADvan. Anat. Embryol. Cell Biol. 51, 1–77.Google Scholar
  95. Svendgaard, N.-A.A., Björklund, A., Stenevi, U. (1976). Regeneration of central cholinergic neurons in the adult rat brain. Brain Res. 102, 1–22.PubMedCrossRefGoogle Scholar
  96. Tello, F. (1911a). Un experimento sobre la influencia Del neurotropismo en 1a reGene-racion De la corteza cerebral. Rev. Clin. MaDr. 5, 292–294.Google Scholar
  97. Tello, F. (1911b). La influencia Del neurotropismo en la reGeneracion De los centros nerviosos. Trab. Lab. Invest. Biol. Univ. MaDr. 9, 123–159.Google Scholar
  98. Walberg, F. (1972). Cerebellovestibular relations: Anatomy. ProGr. Brain Res. 37, 361–376.CrossRefGoogle Scholar
  99. Wenzel, J., Barlehner, E. (1969). Zur Regeneration Des Cortex cerebri bei mus musculus. II. MorpholoGische BefunDe reGenerativer VorGanGe nach Replantation eines Cortexabschnittes. Zeit. Mikro. Anat. Forsch. 81, 32–70.Google Scholar
  100. Windle, W. F. (1956). Regeneration of axons in the vertebrate central nervous system. Physiol. Rev. 36, 426–440.Google Scholar
  101. Yamamoto, M., Chan-Palay, V., Steinbusch, H. W. M., Palay, S. L. (1980). Hyperinnervation of arresteD Granule cells proDuceD by the transplantation of monoamine-containinG neurons into the fourth ventricle of rat. Anat. Embryol. 159, 1–15.PubMedCrossRefGoogle Scholar
  102. Zimmer, J. (1973). ExtenDeD commissural and ipsilateral proJections in postnatally DeentorhinateD hippocampus and fascia Dentata Demonstrated in rats by silver impreGnation. Brain Res. 64, 293–311.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1983

Authors and Affiliations

  • Monica M. Oblinger
    • 1
  • Gopal D. Das
    • 2
  1. 1.Department of AnatomyCase Western Reserve University School of MedicineClevelandUSA
  2. 2.Department of Biological SciencesPurdue UniversityWest LafayetteUSA

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