Development of long-distance efferent projections from fetal hippocampal grafts depends upon pathway specificity and graft location in kainate-lesioned adult hippocampus

Neuroscience

Volumn 76, Issue 4, 1997, Pages 1205-1219

  Shetty, A K ^a   Turner, D A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

axon growth; graft host connections; hippocampal grafts; hyperexcitability; neural transplantation; temporal lobe epilepsy

Indexed keywords

KAINIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; MALE; NERVE GRAFT; NERVE GROWTH; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SEPTUM NUCLEUS; TEMPORAL LOBE EPILEPSY;

ANIMALS; ANTIMETABOLITES; BRAIN TISSUE TRANSPLANTATION; BROMODEOXYURIDINE; CARBOCYANINES; CELL SURVIVAL; EXCITATORY AMINO ACID AGONISTS; FETAL TISSUE TRANSPLANTATION; FLUORESCENT DYES; HIPPOCAMPUS; KAINIC ACID; NEURAL PATHWAYS; NEURONS, EFFERENT; RATS; RATS, INBRED F344; STILBAMIDINES;

EID: 0031021796     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(96)00413-7     Document Type: Article

References (66)

1. Abercrombie M. (1946) Estimation of nuclear population from microtome sections. Anat. Rec. 94, 239-246.
2. Altman J. and Bayer S. A. (1990) Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J. comp. Neurol. 301, 325-342.
3. 3H)thymidine autoradiographic study. J. comp. Neurol. 190, 87-114.
4. Ben-Ari Y. (1985) Limbic seizures and brain damage produced by kainic acid: Mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14, 375-403.
5. Bjorklund A. (1991) Neural transplantation - an experimental tool with clinical possibilities. Trends Neurosci. 8, 319-322.
6. Bjorklund A. (1992) Dopaminergic transplants in experimental parkinsonism: cellular mechanisms of graft-induced functional recovery. Curr. Opin. Neurobiol. 2, 683-689.
7. Bjorklund A. and Dunnett S. B. and Nikkhah G. (1994) Nigral transplants in the rat Parkinson model. In Functional Neural Transplantation (eds Dunnett S. B. and Bjorklund A.), pp. 47-69. Raven Press, New York.
8. Buzsaki G., Czopf J., Kondakor I., Bjorklund A. and Gage F. H. (1987) Cellular activity of intracerebrally transplanted fetal hippocampus during behavior. Neuroscience 22, 871-883.
9. Buzsaki G., Ponomareff G., Bayardo F., Shaw T. and Gage F. H. (1988) Suppression and induction of epileptic activity by neuronal grafts. Proc. natn. Acad Sci. U.S.A. 85, 9327-9330.
10. Davies S. J. A., Field P. M. and Raisman G. (1993) Long fiber growth by axons of embryonic mouse hippocampal neurons microtransplanted into the adult rat fimbria. Eur. J. Neurosci. 5, 95-106.
11. Davies S. J. A., Field P. M. and Raisman G. (1994) Long interfascicular axon growth from embryonic neurons transplanted into adult myelinated tracts. J. Neurosci. 14, 1596-1612.
12. Deckel A. W., Moran T. H., Coyle J. T., Sanberg P. R. and Robinson R. G. (1986) Anatomical predictors of behavioral recovery following fetal striatal transplants. Brain Res. 365, 249-258.
13. Dunnett S. B. (1995) Functional repair of striatal systems by neural transplants: evidence of circuit reconstruction. Behav. Brain Res. 66, 133-142.
14. Field P. M., Seeley P. J., Frotscher M. and Raisman G. (1991) Selective innervation of embryonic hippocampal transplants by adult host dentate granule cell axons. Neuroscience 41, 713-727.
15. Freeman J. N., Baisden R. H. and Woodruff M. L. (1995) Fetal ammon's horn transplants improve acquisition of radial arm maze and a low-rate operant schedule in trimethyltin-treated rats. Cell Transplant. 4, 113-122.
16. Gage F. H. and Fisher L. J. (1991) Intracerebral grafting: A tool for the neurobiologist. Neuron 6, 1-12.
17. Garcia A. R., Deacon T. W., Dinsmore J. and Isacson O. (1995) Extensive axonal and glial fiber growth from fetal porcine cortical xenografts in the adult rat cortex. Cell Transplant. 4, 515-527.
18. Granholm A.-C., Bergman H., Dudek E. and Browning M. (1995) Synapsin I in intraocular hippocampal transplants during maturation and aging: effects of brainstem co-grafts. Cell Transplant. 4, 3-12.
19. Granholm A.-C., Eriksdottor-Nilsson M., Stromberg I., Stieg P., Seiger A., Bygdeman M., Geffard M., Oertel W., Dahl D. and Olson L. (1989) Morphological and electrophysiological studies of human hippocampal transplants in the anterior eye chamber of athymic nude rats. Expl Neurol. 104, 162-171.
20. Holmes G. L., Thompson J. L., Huh K., Holmes C. and Carl G. F. (1991) Effect of neural transplants on seizure frequency and kindling in immature rats following kainic acid. Devl Brain Res. 64, 47-56.
21. Isacson O. and Peschanski M. (1992) Is there capacity for anatomical and functional repair in the adult somatosensory thalamus? Expl Neurol. 115, 173-176.
22. Kordower J. H., Freeman T. B., Snow B. J., Vingerhoets F. J. G., Mufson E. J., Sanberg P. R., Hauser R. A., Smith D. A., Nauert G. M., Perl D. P. and Olanow C. W. (1995) Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinson's disease. New Eng. J. Med. 332, 1118-1124.
23. Kromer L. F., Bjorklund A. and Stenevi U. (1981) Innervation of embryonic hippocampal implants by regenerating axons of cholinergic septal neurons in the adult rat. Brain Res. 210, 153-171.
24. Lindvall O. (1991) Prospects of transplantation in human neurodegenerative diseases. Trends Neurosci. 14, 376-384.
25. Lindvall O. (1995) Neural transplantation. Cell Transplant. 4, 393-400.
26. Lindvall O., Widner H., Rehncrona S., Brundin P., Odin P., Gustavii B., Leenders K. L., Sawle G., Rothwell J. C., Bjorklund A. and Marsden C. D. (1992) Transplantation of fetal dopamine neurons in Parkinson's disease: One year clinical and neurophysiological observations in two patients with putaminal implants. Ann. Neurol. 31, 155-165.
27. Lowenstein D. H., Seren M. S. and Longo F. M. (1993) Prolonged increases in neurotrophic activity associated with kainate-induced hippocampal synaptic reorganization. Neuroscience 56, 597-604.
28. Mitchell J., Best N., Sundstrom L. E. and Wheal H. V. (1993) The use of sodium sulfide-fixed brain tissue for immunocytochemical staining of activated microglia and reactive astrocytes. Histochemistry 99, 91-94.
29. Mudrick L. A. and Baimbridge K. G. (1991) Hippocampal neurons transplanted into ischemically lesioned hippocampus: anatomical assessment of survival, maturation and integration. Expl Brain Res. 86, 233-247.
30. Mudrick L. A., Baimbridge K. G. and Peet M. J. (1989) Hippocampal neurons transplanted into ischemically lesioned hippocampus: electroresponsiveness and re-establishment of circuitries. Expl Brain Res. 76, 333-342.
31. Nadler J. V., Perry B. W. and Cotman C. W. (1978) Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature 271, 676-677.
32. Nadler J. V., Perry B. W., Gentry C. and Cotman C. W. (1980) Degeneration of hippocampal CA3 pyramidal cells induced by intraventricular kainic acid. J. comp. Neurol. 192, 333-359.
33. Netto C. A., Hodges H., Sinden J. D., Le Peillet E., Kershaw T., Sowinski P., Meldrum B. S. and Gray J. A. (1993) Effects of fetal hippocampal field grafts on ischemic-induced deficits in spatial navigation in the water maze. Neuroscience 54, 69-92.
34. Nieto-Sampedro M., Whittemore S. R., Needels D. L., Larson J. and Cotman C. W. (1984) The survival of brain transplants is enhanced by extracts from injured brain. Proc. natn. Acad. Sci. U.S.A. 81, 6250-6254.
35. Nikkhah G., Bentlage C., Cunningham M. G. and Bjorklund A. (1994) Intranigral fetal dopamine grafts induce behavioral compensation in the rat Parkinson model. J. Neurosci. 14, 3449-3461.
36. Nothias F. and Peschanski M. (1990) Homotypic fetal transplants into an experimental model of spinal cord neurodegeneration. J comp. Neurol. 301, 520-534.
37. Onifer S. M. and Low W. C. (1990) Spatial memory deficit resulting from ischemia-induced damage to the hippocampus is ameliorated by intra-hippocampal transplants of fetal hippocampal neurons. Prog. Brain Res. 82, 359-366.
38. Paxinos G. and Watson C. (1982) The Rat Brain in Stereotaxic Coordinates. Academic, New York.
39. Pritzel M., Isacson O., Brundin P., Wiklund L. and Bjorklund A. (1986) Afferent and efferent connections of striatal grafts implanted into the ibotenic acid lesioned neostriatum in adult rats. Expl Brain Res. 65, 112-126.
40. Pyapali G. K., Turner D. A. and Madison R. D. (1994) Fetal transplants in rat hippocampus following kainic acid lesions: influence of post-lesion delay on graft survival and integration. Res. Neurol. Neurosci. 6, 113-126.
41. Raisman G. and Ebner F. F. (1983) Mossy fiber projections into and out of hippocampal transplants. Neuroscience 9, 783-801.
42. Schnell L. and Schwab M. E. (1990) Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 343, 269-272.
43. Shetty A. K., Madison R. D., Bradley J. and Turner D. A. (1994) Quantitative graft integration of fetal hippocampal transplants labeled with 5′ bromodeoxyuridine into normal adult hippocampus. Expl Neurol. 126, 205-224.
44. Shetty A. K. and Turner D. A. (1995) Non-phosphorylated neurofilament protein immunoreactivity in adult and developing rat hippocampus: specificity and application in grafting studies. Brain Res. 676, 293-306.
45. Shetty A. K. and Turner D. A. (1995) Enhanced cell survival in fetal hippocampal suspension transplants grafted to adult rat hippocampus following kainate lesions: A three-dimensional graft reconstruction study. Neuroscience 67, 561-582.
46. Shetty A. K. and Turner D. A. (1995) Fetal hippocampal grafts in kainate lesioned hippocampus establish specific connections and reduce aberrant mossy fiber sprouting. Soc. Neurosci. Abstr. 21, 2028.
47. Shihabuddin L. S., Hertz J. A., Holets V. R. and Whittemore S. R. (1995) The adult CNS retains the potential to direct region-specific differentiation of a transplanted neuronal precursor cell line. J. Neurosci. 15, 6666-6678.
48. Sorenson T. and Zimmer J. (1988) Ultrastructural organization of normal and transplanted fascia dentata: II. A quantitative analysis of the synaptic organization of intracerebral and intraocular grafts. J. comp. Neurol. 267, 43-54.
49. Sprick U. (1991) Morphology of embryonic hippocampus transplants and generation of long-distance extrinsic graft fiber connections to the lateral septum and the entorhinal cortex in the mature rat brain. Res. Neurol. Neurosci. 3, 23-34.
50. Stromberg I., Bygdeman M. and Almqvist P. (1992) Target-specific outgrowth from human mesencephalic tissue grafted to cortex or ventricle of immunosuppressed rats. J. comp. Neurol. 315, 445-456.
51. Sunde N. A., Laurberg S. and Zimmer J. (1984) Brain grafts can restore irradiation damaged neuronal connections in the newborn rat. Nature 310, 51-53.
52. Swanson L. W. and Cowan W. M. (1977) An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J. comp. Neurol. 172, 49-84.
53. Tønder N. (1995) Neural transplantation to the normal and lesioned brain: An experimental study of the rat hippocampus. Acta neurol. scand. 91, 6-30.
54. Tønder N., Sorenson J. C., Bakkum E., Danielsen E. and Zimmer J. (1988) Hippocampal neurons grafted to newborn rats establish efferent commissural connections. Expl Brain Res. 72, 577-583.
55. Tønder N., Sorensen T. and Zimmer J. (1990) Grafting of fetal CA3 neurons to excitotoxic, axon-sparing lesions of the hippocampal CA3 area in adult rats. Prog. Brain Res. 83, 391-409.
56. Toth K. and Freund T. F. (1992) Calbindin D28k-containing non-pyramidal cells in the rat hippocampus: their immunoreactivity for GABA and projection to the medial septum. Neuroscience 49, 793-805.
57. Turner D. A., Li X.-G., Pyapali G. K., Ylinen L. and Buzsaki G. (1995) Morphometric and electrical properties of reconstructed CA3 hippocampal neurons recorded in vivo. J. comp. Neurol. 356, 580-594.
58. Turner D. A. and Wheal H. V. (1991) Excitatory synaptic potentials in kainic-acid denervated rat CA1 pyramidal neurons. J. Neurosci. 11, 2786-2794.
59. Wictorin K. (1992) Anatomy and connectivity of intrastriatal striatal transplants. Prog. Neurobiol. 38, 611-639.
60. Wictorin K., Brundin P., Gustavii B., Lindvall O. and Bjorklund A. (1990) Reformation of long axon pathways in adult rat central nervous system by human forebrain neuroblasts. Nature 347, 556-558.
61. Wictorin K., Brundin P., Sauer H., Lindvall O. and Bjorklund A. (1992) Long distance directed axonal growth from human dopaminergic mesencephalic neuroblasts implanted along the nigrostriatal pathway in 6-hydroxydopamine lesioned adult rats. J. comp. Neurol. 323, 475-494.
62. Wictorin K., Simerly R. B., Isacson O., Swanson L. W. and Bjorklund A. (1989) Connectivity of striatal grafts implanted into the ibotenic acid-lesioned striatum. III. Efferent projecting graft neurons and their relation to host afferents within the grafts. Neuroscience 30, 313-330.
63. Woodruff M. L., Baisden R. H. and Nonneman A. J. (1991) Anatomical and behavioral sequelae of fetal brain transplants in rats with trimethyltin-induced neurodegeneration. Neurotoxicology 12, 427-444.
64. Woodruff M. L., Baisden R. H. and Nonneman A. J. (1992) Effects of transplantation of fetal hippocampal or hindbrain tissue into the brains of adult rats with hippocampal lesions on water maze acquisition. Behav. Neurosci. 106, 39-50.
65. Yurek D. and Sladek J. R.Jr. (1990) Dopamine cell replacement: Parkinson's disease. A. Rev. Neurosci. 13, 415-440.
66. Zhou C. F., Raisman G. and Morris R. J. (1985) Specific patterns of fiber outgrowth from transplants to host mice hippocampi, shown immunohistochemically by the use of allelic forms of Thy-1. Neuroscience 16, 819-833.