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Neural Transplantation in Parkinson's Disease

Published online by Cambridge University Press:  18 September 2015

V. Mehta ,
J. Spears  and
I. Mendez
V. Mehta
Affiliation:
Neural Transplantation Laboratory, Department of Surgery, Division of Neurosurgery, Dalhousie University, Halifax
J. Spears
Affiliation:
Neural Transplantation Laboratory, Department of Surgery, Division of Neurosurgery, Dalhousie University, Halifax
I. Mendez*
Affiliation:
Neural Transplantation Laboratory, Department of Surgery, Division of Neurosurgery, Dalhousie University, Halifax
*
Neural Transplantation Laboratory, Room 12D, Sir Charles Tupper Medical Building, Dalhousie University, Halifax, Nova Scotia, Canada B3H 4H7
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Abstract:

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Parkinson's disease is a neurodegenerative disorder that affects about 1% of Canadians between the ages of fifty and seventy. The medical management for these patients consists of drug therapy that is initially effective but has limited long term benefits and does not alter the progressive course of the disease. The recalcitrance of longstanding Parkinson's disease to medical management has prompted the use of alternative surgical therapies. Many neurosurgical procedures have been utilized in order to improve the disabling symptoms these patients harbour. Although most of the current procedures involve making destructive lesions within various basal ganglia nuclei, neural transplantation attempts to reconstitute the normal nigrostriatal pathway and restore striatal dopamine. The initial success of neural transplantation in the rodent and primate parkinsonian models has led to its clinical application in the treatment of parkinsonian patients. Currently, well over one hundred patients throughout the world have been grafted with fetal tissue in an effort to ameliorate their parkinsonian symptoms. Although the results of neural transplantation in clinical trials are promising, a number of issues need to be resolved before this technology can become a standard treatment option. This review focuses on the current status of neural transplantation in Parkinson's disease within the context of other surgical therapies in current use.

Type
Review Articles
Information
Canadian Journal of Neurological Sciences , Volume 24 , Issue 4 , November 1997 , pp. 292 - 301
Copyright
Copyright © Canadian Neurological Sciences Federation 1997

References

REFERENCES

1.Barbeau, A, Mars, H, Gillo-Joffroy, L, et al. A proposed classification of dopa-induced dyskinesia. In: Barbeau, A, Macdowell, FH, eds. L-Dopa and Parkinsonism. Philadelphia: Davis, 1970: 118–123.Google Scholar
2.Rajput, AH, Stern, W, Laverly, WH. Chronic low dose levodopa therapy in Parkinson’s disease: an argument for delaying levodopa therapy. Neurology 1984; 34: 991–997.CrossRefGoogle ScholarPubMed
3.Freed, WJ, Hoffer, BJ Olson, et al. Transplantation of catecholamine-containing tissues to restore the functional capacity of the damaged nigrostriatal system. In: Sladek, JR Jr, Gash, DM, eds. Neural Transplants. Development and Function. New York: Plenum Press, 1984: 737–402.Google Scholar
4.Sladek, JR Jr, Gash, DM. Review article. Nerve-cell grafting in Parkinson’s disease. J Neurosurg 1988; 68: 337–351.CrossRefGoogle ScholarPubMed
5.Fisher, LJ, Gage, FH. Intracerebral transplantation: basic and clinical applications to the neostriatum. FASEB 1994; 8: 489–496.CrossRefGoogle Scholar
6.Hitchcock, ER. Current trends in neural transplantation. Neurol Res 1995; 17: 33–37.CrossRefGoogle ScholarPubMed
7.Lindvall, O. Neural Transplantation.Cell Transplantation 1995; 4: 391–400.CrossRefGoogle ScholarPubMed
8.Olanow, CW, Kordower, JH, Freeman, TB. Fetal nigral transplantation as a therapy for Parkinson’s disease. Trends Neurosci 1996; 19: 102–109.CrossRefGoogle ScholarPubMed
9.Freed, WJ. Intracerebral adrenal medulla grafts: a review. Exp Neurol 1990; 110: 139–166.CrossRefGoogle ScholarPubMed
10.Thompson, WG. Successful brain grafting. NY Med J 1890; 51: 701.Google Scholar
11.Saltykow, S. Versuche uber Gehirn replantation, Zugleich ein Beitrag zur Kenntniss reactiver Vorgange an den zelligen Gehirneelementen. Arch Psychiatr Nervenkr 1905; 40: 329–388.CrossRefGoogle Scholar
12.Dunn, E. Primary and secondary findings in a series of attempts to transplant cerebral cortex in albino rats. J Comp Neurol 1917; 22: 565–582.Google Scholar
13.Legros Clark, WE. Neuronal differentiation in implanted foetal cortical tissue. J Neurol Psychiatry 1940; 3: 263–284.CrossRefGoogle Scholar
14.May, RM. Connexions entre des cellules cerebrales et des muscles de la cause dans leur greffe blephoplastique intraoculaire simultaneechez la souris. Anat Microsc Morphol Exp 1949; 38: 145.Google Scholar
15.Flenko, B, Szentagothai, J. Oestrogen sensitive nervous structures in the hypothalamus. Acta Endocrinol 1957; 26: 121–127.Google Scholar
16.Halasz, B, Pupp, L, Uhlarik, S, et al. Growth of hypophysectomized rats bearing pituitary transplant in the hypothalamus. Acta Physiol Hung 1963; 23: 287–292.Google ScholarPubMed
17.Halasz, B, Pupp, L, Uhlarik, S, et al. Further studies on the hormone secretion of the anterior pituitary transplanted into the hypophysiotrophic areas of the rat hypothalamus. Endocrinology 1965; 77: 343–355.CrossRefGoogle Scholar
18.Das, GD. Transplantation of embryonic neural tissue in the mammalian brain. Growth and differentiation of neuroblasts from various regions of the embryonic brain in the cerebellum of neonate rats. J Life Sci 1974; 4: 93–124.Google ScholarPubMed
19.Lund, R, Hauscha, S. Transplanted neural tissue develops connections with host rat brain. Science 1976; 193: 582–584.CrossRefGoogle ScholarPubMed
20.Bjorklund, A, Kramer, LF, Stenevi, U. Cholinergic reinervation of rat hippocampus by septal implants is stimulated by perforant path lesion. Brain Res 1979; 173: 57–64.CrossRefGoogle Scholar
21.Bjorklund, A, Stenevi, U. Reconstruction of the nigrostriatal dopamine pathway by intracerebral nigral transplants. Brain Res 1979; 177: 555–560.CrossRefGoogle ScholarPubMed
22.Bjorklund, A, Stenevi, U. Reformation of the severed septohippocampal cholinergic pathway in the adult rat by transplanted septal neurons. Cell Tissue Res 1977; 185: 289–302.CrossRefGoogle ScholarPubMed
23.Bjorklund, A, Stenevi, U, Svendgaard, NA. Growth of transplanted monoaminergic neurones into the adult hippocampus along the perforant path. Nature 1976; 262: 787–790.CrossRefGoogle ScholarPubMed
24.Bjorklund, A, Dunnett, SB, Stenevi, U, et al. Reinnervation of the denervated striatum by substantia nigra transplants. Functional consequences as revealed by pharmacological and sensorimotor testing. Brain Res 1980; 199: 307–333.CrossRefGoogle ScholarPubMed
25.Perlow, MJ, Freed, WJ, Hoffer, BJ, et al. Brain grafts reduce motor abnormalities produced by destruction of nigro-striatal dopamine system. Science 1979; 204: 643–647.CrossRefGoogle Scholar
26.Freed, WJ, Perlow, MJ, Karoum, F, et al.Restoration of dopaminergic function by grafting of fetal rat substantia nigra to the caudate nucleus: long-term behavioural, biochemical, and histochemical studies. Ann Neurol 1980; 8: 510–519.CrossRefGoogle Scholar
27.Freed, WJ, Morihisa, JM, Spoor, E, et al. Transplanted adrenal chromaffin cells in rat brain reduce lesion induced rotational behaviour. Nature 1981; 292: 351–352.CrossRefGoogle ScholarPubMed
28.Redmond, DE Jr, Sladek, JR Jr, Roth, RH, et al. Fetal neuronal grafts in monkeys given methylphenyltetrahydropyridine. Lancet 1986; 1: 1125–1127.CrossRefGoogle ScholarPubMed
29.Sladek, JR Jr, Redmond, DE Jr, Collier, TJ, et al. Fetal dopamine neural grafts: extended reversal of methylphenyltetrahydropyridine-induced parkinsonism in monkeys. Prog Brain Res 1988; 78: 497–506.CrossRefGoogle ScholarPubMed
30.Sladek, JR Jr, Collier, TJ, Haber, SN, et al. Survival and growth of fetal catecholamine neurons transplanted into primate brain. Brain Res Bull 1986; 17: 809–818.CrossRefGoogle ScholarPubMed
31.Stevens, JR, Phillips, I, Freed, WJ, Poltorak, M. Cerebral transplants for seizures: preliminary results. Epilepsia 1988; 29: 731–737.CrossRefGoogle ScholarPubMed
32.Holmes, GL, Thompson, JL, Huh, K, Stuart, JD, Carl, GF. Effects of neural transplantation on seizures in the immature genetically epilepsy prone rat. Exp Neurol 1992; 116: 52–63.CrossRefGoogle ScholarPubMed
33.Deckel, AW, Robinson, RG, Coyle, JT, Sanberg, PRReversal of longterm locomotor abnormalities in the kainic acid model of Huntington’s disease by day 18 fetal striatal implants. Eur J Pharmacol 1983; 93: 287–288.CrossRefGoogle ScholarPubMed
34.FineA, A,Dunnett, SB, Bjorklund, A, Iversen, SD. Cholinergic ventral forebrain grafts into the neocortex improve passive avoidance memory in a rat model of Alzheimer–s disease. Proc Natl Acad Sci USA 1985; 82: 5227–5230.CrossRefGoogle Scholar
35.Bregman, BS. Spinal cord transplants permit the growth of serotonergic axons across the site of neonatal spinal cord transection. Dev Brain Res 1987; 34: 265–279.CrossRefGoogle Scholar
36.Das, GD. Neural transplantation in the spinal cord of adult rats. J Neurol Sci 1983; 62: 191–210.CrossRefGoogle ScholarPubMed
37.Wurtman, RJ, Pohorecky, LA, Baliga, BS. Adrenocortical control of the biosynthesis of epinephrine and proteins in the adrenal medulla. Pharmacol Rev 1972; 24: 411–426.Google ScholarPubMed
38.Unsicker, K, Rieffert, B, Ziegler, W. Effects of cell culture conditions, nerve growth factor, dexamethasone and cyclic AMP on adrenal chromaffin cells in vitro. Adv Biochem Pharmacol 1980; 25: 51–59.Google ScholarPubMed
39.Winn, SR, Wahlberg, L, Tresro, PA, et al. An encapsulated dopamine-releasing polymer alleviates experimental Parkinsonian in rats. Exp Neurol 1989; 105: 244–250.CrossRefGoogle Scholar
40.Stromberg, I, Herrera-Marschitz, M, Hultgren, L, et al. Adrenal medullary implants in the dopamine denervated rat striatum. l. Acute catecholamine levels in grafts and host caudate as determined by HPLC-electrochemistry and fluorescence histochemical image analysis. Brain Res 1984; 297: 41–51.CrossRefGoogle Scholar
41.Stromberg, I, Herrera-Marschitz, M, Ungerstedt, U, et al. Chronic implants of chromaffin tissue into the dopamine-denervated striatum. Effects of NGF on graft survival, fibre growth and rotational behaviour. Exp Brain Res 1985; 60: 335–349.Google ScholarPubMed
42.Brown, VJ, Dunnett, SB. Comparison of adrenal and foetal nigral grafts on drug-induced rotation in rats with 6-OHDA lesions. Exp Brain Res 1989; 78: 214–218.CrossRefGoogle Scholar
43.Backlund, EO, Granberg, PO, Hamberger, B, et al. Transplantation of adrenal medullary tissue to striatum in parkinsonism. First clinical trials. J Neurosurg 1985; 62: 169–173.CrossRefGoogle ScholarPubMed
44.Lindvall, O, Backlund, EO, Farde, L, et al. Transplantation in Parkinson’s disease: two cases of adrenal medullary grafts to putamen. Ann Neurol 1987; 22: 457–468.CrossRefGoogle ScholarPubMed
45.Madrazo, I, Drucker-Colin, R, Diaz, V, et al. Open microsurgical autograft of adrenal medulla to the right caudate nucleus in Parkinson’s disease: a report of two cases. N Engl J Med 1987; 316: 831–834.CrossRefGoogle Scholar
46.Allen, GS, Burns, RS, Tulipan, NBet al.Adrenal medullary transplantation to the caudate nucleus in Parkinsons disease. Initial results in 18 patients. Arch Neurol 1989; 46: 487–491.CrossRefGoogle Scholar
47.Bakay, RAE. Preliminary report on adrenal medullary grafting from the American Association of Neurological Surgeons GRAFT project. Restorative Neurol Neurosci 1989; 1: 158.Google Scholar
48.Flores, EG. Is autologous transplant of adrenal medulla into the striatum an effective therapy for Parkinson’s disease? Restorative Neurol Neurosci 1990; 1: 182.Google Scholar
49.Kelly, PJ, Ahlskog, JE, Van Heerden, JA, et al. Adrenal medullary autograft transplantation into the striatum of Parkinson’s disease. Mayo Clin Proc 1989; 64: 282–290.CrossRefGoogle Scholar
50.Goetz, CG, Stebbins, GT, Klawans, , et al. United Parkinson Foundation Neural Transplantation Registry (1991) United Parkinson Foundation Neurotransplantation Registry on adrenal medullary transplants: presurgical, and 1 and 2 year follow-up. Neurology 1991; 41: 1719–1722.CrossRefGoogle Scholar
51.Apuzzo, MLJ, Neal, JH, Waters, CH, et al. Utilization of unilateral and bilateral sterotactically placed adrenomedullary-striatal autografts in parkinsonian humans: rationale, techniques, and observations 1990; 26: 746–757.Google Scholar
52.Jiang, N, Jiang, C, Tang, Z, et al. Human foetal brain transplant trials in the treatment of Parkinsonism. Acta Acad Medicin Shangai 1987; 14 (1): 77.Google Scholar
53.Lindvall, O, Rehncrona, S, Gustavii, B, et al. Fetal dopamine-rich mesencephalic grafts in Parkinson’s disease. Lancet 1988; 2: 1483–1484.CrossRefGoogle ScholarPubMed
54.Lindvall, O, Rehncrona, S, Brundin, P, et al. Human fetal dopamine neurons grafted into the striatum in two patients with severe Parkinson’s disease: a detailed account of methodology and a 6 month follow-up. Arch Neurol 1989; 46: 615–631.CrossRefGoogle ScholarPubMed
55.Lindvall, O, Brundin, P, Widner, H, et al. Grafts of fetal dopamine neurons survive and improve motor function in Parkinson’s disease. Science 1990; 247: 547.CrossRefGoogle ScholarPubMed
56.Lindvall, O, Widner, H, Rehncrona, S, et al. Transplantation of fetal dopamine neurons in Parkinson’s disease: one year clinical and neurophysiological observations in two patients with putaminal implants. Ann Neurol 1992; 31: 155–165.CrossRefGoogle ScholarPubMed
57.Lindvall, O, Sawle, G, Widner, H, et al.Evidence for long-term survival and function of dopaminergic grafts in progressive Parkinson’s disease. Ann Neurol 1994; 35: 172–180.CrossRefGoogle ScholarPubMed
58.Madrazo, I, Leon, V, Torres, C, et al. Transplantation of fetal substantia nigra and adrenal medulla to the caudate nucleus in two patients with Parkinson’s disease. N Engl J Med 1988; 318: 51.Google Scholar
59.Madrazo, I, Franco-Bourland, R, Ostrosky-Solis, F, et al. Fetal homotransplants (ventral mesencephalon and adrenal tissue) to the striatum of parkinsonian patients. Arch Neurol 1990; 47: 1281–1285.CrossRefGoogle Scholar
60.Madrazo, I, Franco-Bourland, R, Aguilera, M, et al. Fetal ventral mesencephalon brain homotransplantation in Parkinson’s disease: the Mexican experience. In: Lindvall, O, Bjorklund, A, Widner, H, eds. Intracerebral Transplantation in Movement Disorders. Restorative Neurology, Vol 4, Amsterdam: Elsevier, 1991: 123–129.Google Scholar
61.Madrazo, I, Franco-Bourland, R, Ostrosky-Solis, F, et al. Neural transplantation (auto-adrenal, fetal nigral and fetal adrenal) in Parkinsons disease. The Mexican experience. Prog Brain Res 1990b; 82: 593–602.CrossRefGoogle ScholarPubMed
62.Molina, H, Quinones, R, Alvarez, L, et al. Transplantation of human fetal mesencephalic tissue in caudate nucleus as treatment for Parkinson’s disease: the Cuban experience. In: Lindvall, O, Bjorklund, A, Widner, H. eds. Intracerebral Transplantation in Movement Disorders. Restorative Neurology, Vol. 4, Amsterdam: Elsevier, 1991: 99–110.Google Scholar
63.Hitchcock, ER, Clough, C, Hughes, R, Kenny, B. Embryos and Parkinson’s disease. Lancet 1988; 1: 1274.CrossRefGoogle ScholarPubMed
64.Hitchcock, ER, Kenny, BG, Clough, CG, et al. Stereotactic implantation of foetal mesencephalon (STIM): the UK experience. In: Dunnett, SB, Richards, S-J, eds. Neural Transplantation: From Molecular Basis to Clinical Applications. Progress in Brain Research. Amsterdam: Elsevier, 1990: 723–728.Google Scholar
65.Henderson, BTH, Clough, CG, Hughes, RC, Hitchcock, ER, Kenny, BG. Implantation of human fetal ventral mesencephalon to the right caudate nucleus in advanced Parkinson’s disease. Arch Neurol 1991; 48: 822–827.CrossRefGoogle Scholar
66.Freed, CR, Breeze, RE, Rosenberg, NL, et al. Transplantation of human fetal dopamine cells for Parkinson’s disease: results at 1 year. Arch Neurol 1990; 47: 505–512.CrossRefGoogle ScholarPubMed
67.Freed, CR, Breeze, RE, Rosenberg, NL, et al. Survival of implanted fetal dopamine cells and neurologic improvement 12 to 46 months after transplantation for Parkinson’s disease. N Engl J Med 1992; 327: 1549–1555.CrossRefGoogle ScholarPubMed
68.Lopez-Lozano, JJ, Bravo, G, BreraB, B,et al. Long-term follow-up in 10 Parkinson’s disease patients subjected to fetal brain grafting into a cavity in the caudate nucleus: the clinica Puerta de Hierro experience. Transplant Pro 1995; 27; 1: 1395–1400.Google Scholar
69.Freeman, TB, Olanow, CW, Hauser, RA, et al. Bilateral fetal nigral transplantation into the postcommissural putamen in Parkinson’s disease. Ann Neurol 1995; 38 (3): 379–388.CrossRefGoogle ScholarPubMed
70.Widner, H, Tetrud, J, Rehncrona, S, et al. Bilateral fetal mesencephalic grafting in two patients with Parkinsonism induced by l-methyl-4-phenyl-l,2,3,6-tetrahydropyridine (MPTP). N Engl J Med 1992; 327: 1556–1563.CrossRefGoogle Scholar
71.Peschanski, M, Defer, G, Guyen, JP, et al. Bilateral motor improvement and alteration of L-dopa effect in two patients with Parkinson’s disease following intrastriatal transplantation of foetal ventral mesencephalon. Brain 1994; 117: 487–499.CrossRefGoogle ScholarPubMed
72.Spencer, DD, Robbins, RJ, Naftolin, F, et al. Unilateral transplantation of human fetal mesencephalic tissue into the caudate nucleus of patients with Parkinson’s disease. N Engl J Med 1992; 327: 1541–1548.CrossRefGoogle ScholarPubMed
73.Kordower, JH, Freeman, TB, Snow, BJ, et al. Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinson’s disease. N Engl J Med 1995; 332: 1118–1124.CrossRefGoogle Scholar
74.Freed, CR, Breeze, RE, Leehey, MA, et al. Eight years experience with fetal neurotransplantation in patients with advanced Parkinson’s disease. Soc Neurosci Abst 1996; 22 (2): 481.3.Google Scholar
75.Wu, CY, De Zhou, M, Bao, X-F, et al. The combined method of transplantation of foetal substantia nigra and stereotactic thalamotomy for Parkinson’s disease. Br J Neurosurg 1994; 8: 709–716.CrossRefGoogle ScholarPubMed
76.Langston, JW, Widner, H, Goetz, CG, et al. Core assessment program for intracerebral transplantation (CAPIT). Mov Disord 1992; 7: 2–13.CrossRefGoogle ScholarPubMed
77.Freeman, TB, Spence, MS, Boss, BD, et al. Development of dopaminergic neurons in the human substantia nigra. Exp Neurol 1991; 113: 344–353.CrossRefGoogle ScholarPubMed
78.Verney, C, Zecevic, N, Nikolic, B, et al. Early evidence of catecholaminergic cell groups in 5 and 6 week old human embryos using tyrosine hydroxylase and dopamine-B-hydroxylase immunocytochemistry. Neurosci Lett 1991; 131: 121–124.CrossRefGoogle Scholar
79.Freeman, TB, Sanberg, PR, Navelt, GM, et al. Influence of donor age on the survival of solid and suspension intraparenchymal human embryonic micrografts. Cell Transplant 1995; 4: 141–145.CrossRefGoogle Scholar
80.German, DC, Schlosselberg, DS, Woodward, DJ. Three dimensional computer reconstruction of midbrain dopaminergic neuronal population from mouse to man. J Neural Transm 1983; 57: 243–254.CrossRefGoogle ScholarPubMed
81.Brundin, P, Strecker, RE, Widner, H, et al. 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 1988; 70: 192–208.CrossRefGoogle Scholar
82.Gash, DM, Bresjanac, M, Junn, F, et al. Trophic mechanisms mediating functional recovery following intrastriatal implantation. In: Dunnett, SB, Bjorklund, A, eds. Functional Neural Transplantation. New York: Raven Press, 1994: 140.Google Scholar
83.Yurek, DM, Lu, W, Hipkens, S, Wiegand, SJ. BDNF enhances the functional reinnervation of the striatum by grafted fetal dopamine neurons. Exp Neurol 1996; 137: 105–118.CrossRefGoogle ScholarPubMed
84.Mott, JL, Eken, S, Bowenkamp, K, et al. Effects of glial cell linederived neurotrophic factor on dopaminergic transplants to the 6-OHDA denervated striatum. Soc Neurosci Abst 1996; 22(2): 592.10.Google Scholar
85.Zastrow, DJ, Zawada, WM, Clarkson, , et al. Preincubation with growth factors improves survival of early mesencephalic grafts in hemiparkinsonian rats. Soc Neurosci Abst 1996; 22(2): 592.17.Google Scholar
86.Sanford, E, Hong, M, Poirier, R, Guido, M, Mendez, I. Effect of the neurotrophic factor GDNF on transplanted dopaminergic cells treated acutely at the time of transplantation and during hibernation. Soc Neurosci Abst 1996; 22(3): 767.12.Google Scholar
87.Nakao, N, Frodl, EM, Duan, WM, Widner, H, Brundin, P. Lazoroids improve the survival of grafted rat embryonic dopamine neurons. Proc Natl Acad Sci USA 1994; 91: 12408–12414.CrossRefGoogle ScholarPubMed
88.Othberg, A, Keep, M, Brundin, P, Lindvall, O. Tirilazad mesylate increases survival of embryonic dopaminergic neurons in vitro. Soc Neurosci Abst 1996; 22(2): 592.12.Google Scholar
89.Nikkhah, G, Cunningham, MG, Jodicke, A, Knappe, U, Bjorklund, A. Improved graft survival and striatal reinnervation by microtrans-plantation of fetal nigral cell suspensions in the rat Parkinson’s model. Brain Res 1994: 633; 133–143.CrossRefGoogle Scholar
90.Schnell, L, Schwab, ME. Axonal regeneration in the rat spinal cord produced an antibody against myelin-associated growth inhibitors. Nature 1990; 343: 269–272.CrossRefGoogle Scholar
91.Schwab, ME. Myelin-associated inhibitors of neurite growth and regeneration in the CNS. Trends Neurosci 1990; 13: 452–455.CrossRefGoogle ScholarPubMed
92.Schwab, ME, Kapfhammer, JP, Bandtlow, CE. Inhibitors of neurite growth. Ann Rev Neurosci 1993; 16: 565–595.CrossRefGoogle ScholarPubMed
93.Alexander, GE, Delong, MR. Microstimulation of the primate neostriatum. II. Somatotopic organization of striatal microexcitable zones and their relation to neuronal response properties. J Neurophysiol 1985; 53: 1417–1430.CrossRefGoogle ScholarPubMed
94.Kish, SJ, Shannak, K, Hornykiewicz, O. Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson’s disease. Pathophysiologic and clinical implications. N Engl J Med 1988; 318: 876–880.CrossRefGoogle ScholarPubMed
95.Brooks, DJ, Ibanez, V, Sawle, GV, et al. Differing patterns of striatal l8F-dopa uptake in Parkinson’s disease, multiple system atrophy, and progressive supranuclear palsy. Ann Neurol 1990; 28: 547–555.CrossRefGoogle ScholarPubMed
96.Mendez, I, Sadi, D, Hong, M. Reconstruction of the nigrostriatal pathway by simultaneous intrastriatal and intranigral dopaminergic transplants. J Neurosci 1996; 16(22): 7216–7227.CrossRefGoogle ScholarPubMed
97.Brundin, P, Strecker, RE, Widner, H, et al. Human fetal dopaminergic neurons grafted in a rat model of Parkinson’s disease: immunological aspects, spontaneous and drug-induced behaviour, and dopamine release. Exp Brain Res 1988; 70: 192–208.CrossRefGoogle Scholar
98.Widner, H, Brundin, P, Bjorklund, A, et al. Survival and immunogenicity of dissociated allogenic fetal neural dopamine rich grafts when implanted in the brains of adult mice. Exp Brain Res 1989; 76: 187–197.CrossRefGoogle ScholarPubMed
99.Grabowska, A, Lampson, LA. Expression of class I and II major histocompatibility (MHC) antigens in the developing CNS. J Neural Transpla Plast 1992; 3: 204–205.CrossRefGoogle Scholar
100.Boyer, KL, Ansani, A, Chan, WC, et al. Immunological response to injury and grafting in the central nervous system. J Neural Transpla Plast 1992; 3: 202–203.CrossRefGoogle Scholar
101.Freund, TF, Bolam, JP, Bjorklund, A, et al. Efferent synaptic connections of grafted dopaminergic neurons reinnervating the host neostriatum: a tyrosine hydroxylase immunocytochemical study. J Neurosci 1985; 5: 603–616.CrossRefGoogle ScholarPubMed
102.Clarke, DJ, Brundin, P, Strecker, RE, et al. Human fetal dopamine neurons grafted in a rat model of Parkinson’s disease: ultrastructural evidence for synapse formation using tyrosine hydroxylase immunocytochemistry. Exp Brain Res 1988; 73: 115–126.CrossRefGoogle Scholar
103.Mendez, I, Elisevich, K, Flumerfelt, B. Dopaminergic innervation of substance P-containing striatal neurons by fetal nigral grafts: an ultrastructural double-labeling immunocytochemical study. J Comp Neurol 1991; 308: 66–78.CrossRefGoogle ScholarPubMed
104.Doucet, G, Murata, Y, Brundin, P, et al. Host afferents into intrastriatal transplants of fetal ventral mesencephalon. Exp Neurol 1989; 106: 1–19.CrossRefGoogle ScholarPubMed
105.Robertson, HA. Synergistic interactions of D1-and D2-selective dopamine agonists in animal models for Parkinson’s disease: sites of action and implications for the pathogenesis of dyskinesias. Can J Neurol Sci 1992; 19: 147–152.CrossRefGoogle ScholarPubMed
106.Kondoh, T, Lae, WC. Glutamate uptake blockade induces striatal dopamine release in 6-Hydroxydopamine rats with intrastriatal grafts: evidence for host modulation of transplanted dopamine neurons. Exp Neurol 1994; 127: 191–198.CrossRefGoogle ScholarPubMed
107.Bjorklund, A, Stenevi, U, Dunnett, SB, Gage, FH. Cross-species neural grafting in a rat model of Parkinson’s disease. Nature 1982; 298: 652–654.CrossRefGoogle Scholar
108.Freeman, TB, Brandeis, L, Pearson, J, Flamm, ES. Cross species grafts of embryonic rabbit mesencephalic tissue survive and cause behavioural recovery in the presence of chronic immunosuppression. In: Azmitia, EC, Bjorklund, A, eds. Cell and Tissue Transplantation into the Adult Brain. Ann NY Acad Sci, 1987: 699–702.Google Scholar
109.Huffaker, TK, Boss, BD, Morgan, NT, et al. Xenografting of fetal pig ventral mesencephalon corrects motor asymmetry in the rat model of Parkinson’s disease. Exp Brain Res 1989; 77: 329–336.CrossRefGoogle ScholarPubMed
110.Stromberg, I, Adams, C, Bygdeman, M, et al. Long-term effects of human to rat mesencephalic xenografts on rotational behaviour, striatal dopamine receptor binding and mRNA levels. Brain Res Bull 1995; 38: 221–233.CrossRefGoogle ScholarPubMed
111.Anton, R, Kordower, JH, Maidment, NT, et al. Neural-targeted gene therapy for rodent and primate hemiparkinsonism. Exp Neurol 1994; 127: 207–218.CrossRefGoogle ScholarPubMed
112.Reynolds, BA, Weiss, S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992; 255: 1707–1710.CrossRefGoogle ScholarPubMed
113.Tasker, RR, Siqueira, J, Hawrylyshyn, P, et al. What happened to VIM thalmotomy for Parkinson’s disease? Appl Neurophysiol 1983; 46: 68–83.Google Scholar
114.Fox, MW, Ahlskog, JE, Kelly, PJ. Stereotactic ventrolateralis thalamotomy for medically refractable tremor in post-levodopa era of Parkinson’s disease patients. J Neurosurg 1991; 75: 723–730.CrossRefGoogle ScholarPubMed
115.Jankovic, J, Candoso, F, Grossman, R, et al. Outcome after stereotactic thalamotomy for Parkinsonian, essential, and other types of tremor. Neurosurgery 1995; 37: 680–687.CrossRefGoogle ScholarPubMed
116.Matsumoto, K. Reappraisal of ventrolateral thalamotomy for Parkinson’s disease. In: Tasker, RR, ed. Neurosurgery: State of the Art Reviews. Vol 2(1) Stereotactic Surgery. Philadelphia: Hanley and Belfus, 1987: 209–234.Google Scholar
117.Kelly, PJ, Gillingham, FJ. The long term results of stereotaxic surgery and L-dopa therapy in patients with Parkinson’s disease: a 10-year follow up study. J Neurosurg 1980; 53: 332–337.CrossRefGoogle Scholar
118.Benabid, AL, Pollak, P, Seigneuret, E, et al. Chronic VIM thalamic stimulation in Parkinson’s disease, essential tremor and extrapyramidal dyskinesias. Acta Neurochir 1993; 58: 39–44.Google Scholar
119.Delong, MR. Primate models of movement disorders of basal ganglia origin. Trends Neurosci 1990; 13: 281–285.CrossRefGoogle ScholarPubMed
120.Bergman, H, Wichmann, T, Delong, MR. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 1990; 249: 1436–1438.CrossRefGoogle ScholarPubMed
121.Laitinen, LV, Bergenheim, T, Hariz, MI. Leksell’s posteroventral pallidotomy in the treatment of Parkinson’s disease. J Neurosurg 1992; 76: 53–61.CrossRefGoogle ScholarPubMed
122.Svennilson, E, Torvik, A, Lowe, R, et al. Treatment of parkinsonism by stereotactic thermolesions in the pallidal region: a clinical evaluation of 81 cases. Acta Psychiatr Neurol Scand 1960; 35: 358–377.CrossRefGoogle Scholar
123.Ceballos-Baumann, AO, Obeso, JA, Vitek, JL, et al. Restoration of thalamocortical activity after posteroventral pallidotomy in Parkinson’s disease. Lancet 1994; 344: 814–815.CrossRefGoogle ScholarPubMed
124.Lozano, AM, Lang, AE, Galvez-Jimnez, N, et al. Effect of Gpi pallidotomy on motor function in Parkinson’s disease. Lancet 1995; 346: 1383–1387.CrossRefGoogle ScholarPubMed
125.Benabid, AL. Deep brain stimulation in Parkinson’s disease: present state and outlook. Mediview, 4th International Congress of Movement Disorders 1996: 2.Google Scholar