Ontogeny of human striatal DARPP-32 neurons in fetuses and following xenografting to the adult rat brain

Experimental Neurology

Volumn 137, Issue 1, 1996, Pages 15-25

  Naimi, Souâd ^a,b   Jeny, Roland ^c   Hantraye, Philippe ^d   Peschanski, Marc ^a   Riche, Danielle ^a  

^a INSERM   (France)

^b FACULTÉ DES SCIENCES SEMLALIA   (Morocco)

^c Hopital Esquirol   (France)

^d DIF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOPROTEIN DARPP 32;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; FETUS; HUMAN; HUMAN TISSUE; HUNTINGTON CHOREA; IMMUNOHISTOCHEMISTRY; NERVE TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; RAT; XENOGRAFT;

EID: 0030045705     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1996.0002     Document Type: Article

References (86)

1. BEAL, M. F., N. W. KOWALL, K. J. SWARTZ, R. J. FERRANTE, AND J. B. MARTIN. 1989. Differential sparing of somatostatin/ neuropeptide Y and cholinergic neurons following striatal excitotoxic lesions. Synapse 3: 38-47.
2. BEATTY, W. W., D. P. SALMON, N. BUTTERS, W. C. HEINDEL, AND E. L. GRANHOLM. 1988. Retrograde amnesia in patients with Alzheimer's disease or Huntington's disease. Neurobiol. Aging 9: 181-186.
3. BERENT, S., B. GIORDANI, S. LEHTINEN, D. MARKEL, J. B. PENNEY, H. A. BUCHTEL, S. STAROSTA-RUBINSTEIN, R. HICHWA, AND A. B. YOUNG. 1988. Positron emission tomographic scan investigations of Huntington's disease: Cerebral metabolic correlates of cognitive function. Ann. Neurol. 23: 541-546.
4. BELKADI, A. M., C. GENY, S. NAIMI-SADAOUI, R. JENY, AND M. PESCHANSKI. 1994. Fine structure of human neural xenografts to the rat brain. 5th Int. Symp. on Neural Transplantation, P 61.
5. BJÖRKLUND, A., O. LINDVALL, O. ISACSON, P. BRUNDIN, K. WICTORIN, R. E. STRECKER, D. J. CLARKE, AND S. DUNNETT. 1987. Mechanisms of action of intracerebral neural implants: Studies on nigral and striatal grafts to the lesioned striatum. Trends Neurosci. 10: 509-516.
6. BJÖRKLUND, A., AND S. B. DUNNETT. 1992. Neural transplantation in adults rats. Pages 57-78 in S. B. Dunnett and A. Björklund, Eds., Neural Transplantation: A Practical Approach. The Practical Approach Series. IRL Press, Oxford.
7. BJÖRKLUND, A., S. B. DUNNETT, AND G. NIKKHAH. 1994. Nigral transplants in the rat Parkinson model: Functional limitations and strategies to enhance nigrostriatal reconstruction. Pages 47-68 in S. B. Dunnett and A. Björklund, Eds., Functional Neural Transplantation. Advances in Neuroscience, Vol. 2. Raven Press, New York.
8. 3H]Thymidine autoradiographic analysis of the time of neuron origin in the rhesus monkey. Neuroscience 4: 767-778.
9. BRUNDIN, P., O. ISACSON, AND A. BJÖRKLUND. 1985. Monitoring of cell viability in suspension of embryonic CNS tissue and its use as a criterion for intracerebral graft survival. Brain Res. 331: 251-259.
10. BRUNDIN, P., O. G. NILSSON, R. E. STRECKER, O. LINDVALL, B. ASTEDT, AND A. BJÖRKLUND. 1986. Behavioural effects of human fetal dopamine neurons grafted in a rat model of Parkinson's disease. Exp. Brain Res. 65: 235-240.
11. BRUNDIN, P., R. E. STRECKER, H. WIDNER, D. J. CLARKE, O. G. NILSSON, B. ASTEDT, O. LINDVALL, AND A. BJÖRKLUND. 1988. Human fetal dopamine neurons grafted in a rat model of Parkinson's disease: Immunological aspects, spontaneous and drug-induced behaviour, and dopamine release. Exp. Brain Res. 70: 192-208.
12. BRUNDIN, P. 1992. Dissection, preparation, and implantation of human embryonic brain tissue. Pages 139-160 in S. B. Dunnett and A. Björklund, Eds., Neural Transplantation. A Practical Approach. The Practical Approach Series. IRL Press, Oxford.
13. CAMPBELL, K., K. WICTORIN, AND A. BJÖRKLUND. 1995. Neurotransmitter-related gene expression in intrastriatal striatal transplants. I. Phenotypical characterization of striatal and nonstriatal graft regions. Neuroscience 64: 17-33.
14. CAMPBELL, K., K. WICTORIN, AND A. BJÖRKLUND. 1995. Neurotransmitter-related gene expression in intrastriatal striatal transplants. II. Characterization of efferent projecting graft neurons. Neuroscience 64: 35-47.
15. CLARKE, D. J., S. B. DUNNETT, O. ISACSON, D. J. S. SIRINATHSINGHJI, AND A. BJÖRKLUND. 1988. Striatal grafts in rats with unilateral neostriatal lesions. I. Ultrastructural evidence of afferent synaptic inputs from the host nigrostriatal pathway. Neuroscience 24: 791-801.
16. COOPER, E. R. A. 1946. The development of the human red nucleus and corpus striatum. Brain 69: 34-44.
17. DECKEL, A. W., R. G. ROBINSON, J. T. COYLE, AND P. R. SANBERG. 1983. Reversal of long term locomotor abnormalities in the kainic acid model of Huntington's disease by day 18 fetal striatal implants. Eur. J. Pharmacol. 93: 287-288.
18. DEFONTAINES, B., M. PESCHANSKI, AND B. ONTENIENTE. 1992. Host dopaminergic afferents affect the development of DARPP32 immunoreactivity in transplanted embryonic striatal neurons. Neuroscience 48: 857-869.
19. DIFIGLIA, M., L. SCHIFF, AND A. W. DECKEL. 1988. Neuronal organization of fetal striatal grafts in kainate and sham-lesioned rat caudate nucleus: Light and electron microscopic observations. J. Neurosci. 8: 1112-1130.
20. DUNNETT, S. B., O. ISACSON, D. J. S. SIRINATHSINGHJI, D. J. CLARKE, AND A. BJÖRKLUND. 1988. Striatal grafts in rats with unilateral neostriatal lesions. III. Recovery from dopamine-dependent motor asymmetry and deficits in skilled paw reaching. Neuroscience 24: 813-820.
21. DUNLAP, C. B. 1927. Pathologic changes in Huntington's chorea with special reference to the corpus striatum. Arch. Neurol. Psychiatry 18: 867-943.
22. EMERICH, D. F., E. M. ZUBRICKI, M. T. SHIPLEY, A. B. NORMAN, AND P. R. SANBERG. 1991. Female rats are more sensitive to the locomotor alterations following quinolinic acid induced striatal lesions: Effects of striatal transplants. Exp. Neurol. 111: 369-378.
23. FOSTER, G. A., M. SCHULTZBERG, T. HÖKFELT, M. GOLSTEIN, H. C. HEMMINGS JR., C. C. OUIMET, S. I. WALAAS, AND P. GREENGARD. 1987. Development of a dopamine-and cyclic adenosine 3′:5′-monophosphate-regulated phosphoprotein (DARPP-32) in the prenatal rat central nervous system, and its relationship to the arrival of presumptive dopaminergic innervation. J. Neurosci. 7: 1994-2018.
24. FREED, C. R., R. E. BREEZE, N. L. ROSENBERG, S. A. SCHNECK, T. H. WELLS, J. N. BARRETT, ET AL. 1990. Transplantation of human fetal dopamine cells for Parkinson's disease: Results at 1 year. Arch. Neurol. 47: 505-512.
25. FREED, C. R., R. E. BREEZE, N. L. ROSENBERG, S. A. SCHNECK, E. KRIEK, J. X. QI, ET AL. 1992. Survival of implanted fetal dopamine cells and neurologic improvement 12 to 46 months after transplantation for Parkinson's disease. N. Engl. J. Med. 327: 1549-1555.
26. FRODL, E. M., N. NAKAO, O. LINDVALL, AND P. BRUNDIN. 1994. Neural transplantation in Huntington's disease: Defining parameters crucial for the survival of grafts of human striatal tissue. 5th Int. Symp. on Neural Transplantation, P 154.
27. GENY, CH., S. NAIMI-SADAOUI, R. JENY, A. M. BELKADI, S. L. JULIANO, AND M. PESCHANSKI. 1995. Long term delayed vascularization of human neural transplants to the rat brain. Eur. J. Neurosci. 14: 7553-7562.
28. GIORDANO, M., S. H. HAGENMEYER-HOUSER, AND P. R. SANBERG. 1988. Intraparenchymal fetal striatal transplants and recovery in kainic acid lesioned rats. Brain Res. 446: 183-188.
29. GRAYBIEL, A. M., F. C. LIU, AND S. B. DUNNETT. 1989. Intrastriatal grafts derived from fetal striatal primordia. I. Phenotypy and modular organization. J. Neurosci. 9: 3250-3271.
30. HANTRAYE, P., D. RICHE, M. MAZIÈRE, AND O. ISACSON. 1992. Intrastriatal transplantation of cross-species fetal striatal cells reduces abnormal movements in a primate model of Huntington's disease. Proc. Natl. Acad. Sci. USA 89: 4187-1191.
31. HAYDEN, M. R., W. R. W. MARTIN, A. J. STOESSL, C. CLARK, S. M. J. ADAM, W. AMMANN, R. HARROP, J. ROGERS, T. RUTH, C. SAYRE, AND B. D. PATE. 1986. Positron emission tomography in the early diagnosis of Huntington's disease. Neurology 36: 888-894.
32. HEINDEL, W. C., D. P. SALMON, C. W. SHULTS, P. A. WALICKE, AND N. BUTTERS. 1989. Neuropsychological evidence for multiple implicit memory systems: A comparison of Alzheimer's, Huntington's, and Parkinson's disease patients. J. Neurosci. 9: 582-587.
33. HELM, G. A., P. E. PALMER, N. E. SIMMONS, C. DI PIERRO, AND J. P. BENNETT JR. 1992. Descriptive morphology of developing fetal neostriatal allografts in the rhesus monkey: A correlated light and electron microscopic Golgi study. Neuroscience 50: 163-179.
34. HENDERSON, B. T., C. G. CLOUGH, R. C. HUGHES, E. R. HITCHCOCK, AND B. G. KENNY. 1991. Implantation of human fetal ventral mesencephalon to the right caudate nucleus in advanced Parkinson's disease. Arch. Neurol. 48: 822-827.
35. HEWITT, W. 1958. The development of the human caudate and amygdaloid nuclei. J. Anat. 92: 377-382.
36. HEWITT, W. 1961. The development of the human internal capsule and lentiform nucleus. J. Anat. 95: 191-199.
37. HODGES, J. R., D. P. SALMON, AND N. BUTTERS. 1990. Differential impairment of semantic and episodic memory in Alzheimer's and Huntington's diseases: A controlled prospective study. J. Neurol. Neurosurg. Psychiatry 53: 1089-1095.
38. ISACSON, O., P. BRUNDIN, P. A. T. KELLY, F. H. GAGE, AND A. BJÖRKLUND. 1984. A functional neuronal replacement by grafted neurons in the ibotenic acid lesioned striatum. Nature 311: 458-160.
39. ISACSON, O., P. BRUNDIN, F. H. GAGE, AND A. BJÖRKLUND. 1985. Neural grafting in a rat model of Huntington's disease: Progressive neurochemical changes after neostriatal ibotenate lesions and striatal tissue grafting. Neuroscience 16: 799-817.
40. ISACSON, O., S. B. DUNNETT, AND A. BJÖRKLUND. 1986. Graft-induced behavioural recovery in an animal model of Huntington's disease. Proc. Natl. Acad. Sci. USA 83: 2728-2732.
41. ISACSON, O., D. DAWBARN, P. BRUNDIN, F. H. GAGE, P. C. EMSON, AND A. BJÖRKLUND. 1987. Neural grafting in a rat model of Huntington's disease: Striosomal-like organization of striatal grafts as revealed by acetylcholinesterase histochemistry, immunocytochemistry and receptor autoradiography. Neuroscience 22: 481-497.
42. ISACSON, O., D. RICHE, P. HANTRAYE, M. V. SOFRONIEW, AND M. MAZIÈRE. 1989. A primate model of Huntington's disease: Cross-species implantation of striatal precursor cells to the excitotoxically lesioned baboon caudate-putamen. Exp. Brain Res. 75: 213-220.
43. JENY, R., M. PESCHANSKI, E. CYNOBER, M. KAMMOUN, A. BOUZAGHAR, M. HAMMANI, AND P. CESARO. 1993. Apport de l'échographie dans les prélèvements embryonnaires à visée de greffes intracérébrales dans le traitement de la maladie de Parkinson. J. Echo. Med. Ultras. 14: 19-22.
44. JOHNSTON, J. B. 1923. Further contributions to the study of the evolution of the forebrain. J. Comp. Neurol. 35: 337-112.
45. KUHL, D. E., M. E. PHELPS, C. H. MARKHAM, E. J. METTER, W. H. RIEGE, AND J. WINTER. 1982. Cerebral metabolism and atrophy in Huntington's disease determined by 18FDG and computed tomographic scan. Ann. Neurol. 12: 425-434.
46. KUWERT, T., H. W. LANGE, K. J. LANGEN, H. HERZOG, A. AULICH, AND L. E. FEINENDEGEN. 1990. Cortical and subcortical glucose consumption measured by PET in patients with Huntington's disease. Brain 113: 1405-1423.
47. LABANDEIRA-GARCIA, J. L., K. WICTORIN, E. T. CUNNINGHAM JR, AND A. BJÖRKLUND. 1991. Development of intrastriatal striatal grafts and their afferent innervation from the host. Neuroscience 42: 407-426.
48. LEENDERS, K. L., R. J. S. FRACKOWIAK, N. QUINN, AND C. D. MARSDEN. 1986. Brain energy metabolism and dopaminergic function in Huntington's disease measured in vivo using positron emission tomography. Mov. Disord. 1: 69-77.
49. LINDVALL, O., P. BRUNDIN, H. WIDNER, S. REHNCRONA, B. GUSTAVII, R. FRACKOWIAK, ET AL. 1990. Grafts of fetal dopamine neurons survive and improve motor function in Parkinson's disease. Science 247: 574-577.
50. LINDVALL, O., H. WIDNER, S. REHNCRONA, P. BRUNDIN, P. ODIN, B. GUSTAVII, ET AL. 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.
51. LINDVALL, O., G. SAWLE, H. WIDNER, J. C. ROTHWELL, A. BJÖRKLUND, D. BROOKS, P. BRUNDIN, R. FRACKOWIAK, C. D. MARSDEN, P. ODIN, AND S. REHNCRONA. 1994. Evidence for longterm survival and function of dopaminergic grafts in progressive Parkinson's disease. Ann. Neurol. 35: 172-180.
52. MAYER, E., R. P. HEAVENS, AND D. J. S. SIRINATHSINGHJI. 1990. Autoradiographic localization of D1 and D2 dopamine receptors in primordial striatal tissue grafts in rats. Neurosci. Lett. 109: 271-276.
53. MAZZIOTTA, J. C., M. E. PHELPS, J. J. PAHL, S. C. HUANG, L. R. BAXTER, W. H. RIEGE, J. M. HOFFMAN, D. E. KUHL, A. B. LANTO, J. A. WAPENSKI, AND C. H. MARKHAM. 1987. Reduced cerebral glucose metabolism in asymptomatic subjects at risk for Huntington's disease. N. Engl. J. Med. 316: 357-362.
54. MCALLISTER, J. P., P. D. WALKER, M. C. ZEMANICK, A. B. WEBER, L. I. KAPLAN, AND M. A. REYNOLDS. 1985. Morphology of embryonic neostriatal cell suspensions transplanted into adult neostriata. Dev. Brain Res. 23: 282-286.
55. MCCAUGHEY, W. T. E. 1961. The pathologic spectrum of Huntington's chorea. J. Nerv. Ment. Dis. 133: 91-103.
56. MCHUGH, P. R., AND M. F. FOLSTEIN. 1975. Psychiatric syndromes of Huntington's chorea: A clinical and phenomenologic study. Pages 267-285 in D. F. Benson and D. Blumer, Eds., Psychiatric Aspects of Neurologic Disease. Grune & Stratton, New York.
57. MONTOYA, C. P., S. ASTELL, AND S. B. DUNNETT. 1989. Effects of nigral and striatal grafts on skilled forelimb use in the rat. Pages 459-466 in S. B. Dunnett and S. J. Richards, Eds., Neural Transplantation: From Molecular Basis to Clinical Applications. Progress in Brain Research. Elsevier, Amsterdam.
58. O'RAHILLY, R., AND F. MÜLLER. 1987. Developmental Stages of Human Embryos. Carnegie Inst., Washington, DC.
59. OTSUKA, M., Y. ICHIYA, Y. KUWABARA, S. HOSOKAWA, M. SASAKI, T. FUKUMURA, K. MASUDA, I. GOTO, AND M. KATO. 1993. Cerebral glucose metabolism and striatal F18Dopa uptake by PET in cases of chorea with or without dementia. J. Neurol. Sci. 115: 153-157.
60. OUIMET, C. C., P. E. MILLER, H. C. HEMMINGS JR., S. I. WALAAS, AND P. GREENGARD. 1984. DARPP-32, a dopamine-and adenosine 3′:5′-monophosphate-regulated phosphoprotein enriched in dopamine innervated brain regions. J. Neurosci. 4: 111-124.
61. OUIMET, C. C., A. S. LAMANTIA, P. GOLDMAN-RAKIC, P. RAKIC, AND P. GREENGARD. 1992. Immunocytochemical localization of DARPP-32, a dopamine-and cyclic-AMP-regulated phosphoprotein, in the primate brain. J. Comp. Neurol. 323: 209-218.
62. PAKZABAN, P., T. W. DEACON, L. H. BURNS, AND O. ISACSON. 1993. Increased proportion of acetylcholinesterase-rich zones and improved morphological integration in host striatum of fetal grafts derived from the lateral but not the medial ganglionic eminence. Exp. Brain Res. 97: 13-22.
63. PESCHANSKI, M., G. DEFER, J. P. N'GUYEN, F. RICOLFI, J. C. MONFORT, P. REMY, C. GENY, Y. SAMSON, P. HANTRAYE, R. JENY, A. GASTON, Y. KÉRAVEL, J. D. DEGOS, AND P. CESARO. 1994. Bilateral motor improvement and alteration of L-dopa effect in two patients with Parkinson's disease following intrastriatal transplantation of foetal ventral mesencephalon. Brain 117: 487-499.
64. PESCHANSKI, M., P. CESARO, AND P. HANTRAYE. 1995. Rationale for intrastriatal grafting of striatal neuroblasts in patients with Huntington's disease. Neuroscience 68: 273-285.
65. PILLON, B., B. DUBOIS, A. PLOSKA, AND Y. AGIO. 1991. Severity and specificity of cognitive impairment in Alzheimer's, Huntington's, and Parkinson's diseases and progressive supranuclear palsy. Neurology 41: 634-643.
66. PODOLL, K., P. CASPARY, H. W. LANGE, AND J. NOTH. 1988. Language functions in Huntington's disease. Brain 111: 1475-1503.
67. PRITZEL, M., O. ISACSON, P. BRUNDIN, L. WIKLUND, AND A. BJÖRKLUND. 1986. Afferent and efferent connections of striatal grafts implanted in the ibotenic acid lesioned neostriatum in adult rats. Exp. Brain Res. 65: 112-126.
68. SANBERG, P. R., M. A. HENAULT, AND A. W. DECKEL. 1986. Locomotor hyperactivity: Effects of multiple striatal transplants in an animal model of Huntington's disease. Pharmacol. Biochem. Behav. 25: 297-300.
69. SIRINATHSINGHJI, D. J. S., S. B. DUNNETT, O. ISACSON, D. J. CLARKE, K. KENDRICK, AND A. BJÖRKLUND. 1988. Striatal grafts in rats with unilateral neostriatal lesions. II. In vivo monitoring of GABA release in globus pallidus and substantia nigra. Neuroscience 24: 803-811.
70. SPENCER, D. D., R. J. ROBBINS, F. NAFTOLIN, ET AL. 1992. Unilateral transplantation of human fetal mesencephalic tissue into the caudate nucleus of patients with Parkinson's disease. N. Engl. J. Med. 327: 1541-1548.
71. STARKSTEIN, S. E., S. E. FOLSTEIN, J. BRANDT, G. D. PEARLSON, A. MCDONNEL, AND M. FOLSTEIN. 1989. Brain atrophy in Huntington's disease: ACT scan study. Neuroradiology 31: 156-159.
72. STRÖMBERG, I., M. BYGDEMAN, M. GOLSTEIN, A. STEIGER, AND L. OLSON. 1986. Human fetal substantia nigra grafted to the dopamine denervated striatum of immunosuppressed rats: Evidence for functional reinnervation. Neurosci. Lett. 71: 271-276.
73. TRÖSTER, A. I., D. P. SALMON, D. MCCULLOUGH, AND N. BUTTERS. 1989. A comparison of the category fluency deficits associated with Alzheimer's and Huntington's disease. Brain Lang. 37: 500-513.
74. VALOUSKOVA, V., V. BRACHA, J. BURES, N. HERNANDEZ-MESA, R. MARCIAS-GONZALES, Y. MUZUROVA, AND S. NEMECEK. 1990. Unilateral striatal grafts induce behavioral and electrophysiological asymmetry in rats with bilateral kainate lesions of the caudate nucleus. Behav. Neurosci. 104: 671-680.
75. VONSATTEL, J. P., R. H. MYERS, T. J. STEVENS, R. J. FERRANTE, E. D. BIRD, AND E. P. RICHARDSON JR. 1985. Neuropathological classification of Huntington's disease. J. Neuropathol. Exp. Neurol. 44: 559-577.
76. WALAAS, S. I., AND P. GREENGARD. 1984. DARPP-32, a dopamine-and adenosine 3′:5′-monophosphate-regulated phosphoprotein enriched in dopamine innervated brain regions. I. Regional and cellular distribution in the rat brain. J. Neurosci. 4: 84-98.
77. WARDLAW, J. M., R. J. SELLAR, AND L. J. ABERNETHY. 1991. Measurement of caudate nucleus area a more accurate measurement for Huntington's disease? Neuroradiology 33: 316-319.
78. WICTORIN, K., O. ISACSON, W. FISCHER, F. NOTHIAS, M. PESCHANSKI, AND A. BJÖRKLUND. 1988. Connectivity of striatal grafts implanted into the ibotenic acid lesioned striatum. I. Subcortical afferents. Neuroscience 27: 547-562.
79. WICTORIN, K., AND A. BJÖRKLUND. 1989. Connectivity of striatal grafts implanted into the ibotenic acid lesioned striatum. II. Cortical afferents. Neuroscience 30: 297-311.
80. WICTORIN, K., C. C. OUIMET, AND A. BJÖRKLUND. 1989. Intrinsic organization and connectivity of intrastriatal striatal transplants in rats as revealed by DARPP-32 immunohistochemistry: Specificity of connections with the lesioned host brain. Eur. J. Neurosci. 1: 690-701.
81. WICTORIN, K., R. B. SIMERLY, O. ISACSON, L. W. SWANSON, AND A. BJÖRKLUND. 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.
82. WICTORIN, K., P. BRUNDIN, B. GUSTAVII, O. LINDVALL, AND A. BJÖRKLUND. 1990. Reformation of long axon pathways in adult rat CNS by human forebrain neuroblasts. Nature 347: 556-558.
83. WICTORIN, K. 1992. Anatomy and connectivity of intrastriatal striatal transplants. Prog. Neurobiol. 38: 611-639.
84. WICTORIN, K., P. BRUNDIN, H. SAUER, O. LINDVALL, AND A. BJÖRKLUND. 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.
85. WIDNER, H., J. TETRUD, S. REHNCRONA, B. SNOW, P. BRUNDIN, B. GUSTAVII, A. BJÖRKLUND, O. LINDVALL, AND W. LANGSTON. 1992. Bilateral fetal mesencephalic grafting in two patients with parkinsonism induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). N. Engl. J. Med. 327: 1556-1563.
86. XU, Z. C., C. J. WILSON, AND P. C. EMSON. 1989. Restoration of the corticostriatal projection in rat neostriatal grafts: Electron microscopic analysis. Neuroscience 29: 539-550.