MRI guidance improves accuracy of stereotaxic targeting for cell transplantation in parkinsonian monkeys

Experimental Neurology

Volumn 193, Issue 1, 2005, Pages 172-180

  Subramanian, Thyagarajan ^a   Deogaonkar, Milind ^a   Brummer, Marijn ^b   Bakay, Roy ^c  

^a LERNER RESEARCH INSTITUTE   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Chicago Institute of Neurosurgery and Neuroresearch   (United States)

Author keywords

Brain atlas; Cell transplantation; Macaca mulatta; MRI; Parkinson's disease; Stereotaxy

Indexed keywords

ACCURACY; ANIMAL MODEL; ARTICLE; BASAL GANGLION; BRAIN NUCLEUS; CAUDATE NUCLEUS; CELL TRANSPLANTATION; CENTRAL NERVOUS SYSTEM; CORPUS STRIATUM; FEMALE; MONKEY; MORPHOLOGY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARKINSONISM; PRIORITY JOURNAL; PUTAMEN; SKULL SURGERY; STEREOTAXIC SURGERY; THREE DIMENSIONAL IMAGING;

EID: 16244412603     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.expneurol.2004.11.032     Document Type: Article

References (91)

1. P. Aebischer, P.A. Tresco, J. Sagen, and S.R. Winn Transplantation of microencapsulated bovine chromaffin cells reduces lesion-induced rotational asymmetry in rats Brain Res. 560 1991 43 49
2. P. Aebischer, P.A. Tresco, S.R. Winn, L.A. Greene, and C.B. Jaeger Long-term cross-species brain transplantation of a polymer-encapsulated dopamine-secreting cell line Exp. Neurol. 111 1991 269 275
3. T. Akai, M. Yamaguchi, E. Mizuta, and S. Kuno Effects of terguride, a partial D2 agonist, on MPTP-lesioned parkinsonian cynomolgus monkeys Ann. Neurol. 33 1993 507 511
4. J.M. Allen, A.J. Cross, J.C. Yeats, M.A. Ghatei, G.P. McGregor, S.P. Close, S. Pay, A.S. Marriott, M.B. Tyers, and T.J. Crow Neuropeptides and dopamine in the marmoset. Effect of treatment with 1-methyl-4-phenyl-1, 2, 3, 6 tetrahydropyridine (MPTP): an animal model for Parkinson's disease? Brain 109 Pt. 1 1986 143 157
5. P. Alvarez-Royo, R.P. Clower, S. Zola-Morgan, and L.R. Squire Stereotaxic lesions of the hippocampus in monkeys: determination of surgical coordinates and analysis of lesions using magnetic resonance imaging J. Neurosci. Methods 38 1991 223 232
6. G. Andringa, S. Eshuis, E. Perentes, R.P. Maguire, D. Roth, M. Ibrahim, K.L. Leenders, and A.R. Cools TCH346 prevents motor symptoms and loss of striatal FDOPA uptake in bilaterally MPTP-treated primates Neurobiol. Dis. 14 2003 205 217
7. L.E. Annett, F.L. Martel, D.C. Rogers, R.M. Ridley, H.F. Baker, and S.B. Dunnett Behavioral assessment of the effects of embryonic nigral grafts in marmosets with unilateral 6-OHDA lesions of the nigrostriatal pathway Exp. Neurol. 125 1994 228 246
8. E.O. Backlund, P.O. Granberg, B. Hamberger, E. Knutsson, A. Martensson, G. Sedvall, A. Seiger, and L. Olson Transplantation of adrenal medullary tissue to striatum in parkinsonism. First clinical trials J. Neurosurg. 62 1985 169 173
9. R.A. Bakay, and C.J. Herring Central nervous system grafting in the treatment of parkinsonism Stereotact. Funct. Neurosurg. 53 1989 1 20
10. R.A. Bakay, K.L. Boyer, C.R. Freed, and A.A. Ansari Immunological responses to injury and grafting in the central nervous system of nonhuman primates Cell Transplant. 7 1998 109 120
11. R.A. Bakay, C.D. Raiser, N.P. Stover, T. Subramanian, M.L. Cornfeldt, A.W. Schweikert, R.C. Allen, and R. Watts Implantation of Spheramine in advanced Parkinson's disease (PD) Front. Biosci. 9 2004 592 602
12. K.S. Bankiewicz, E.H. Oldfield, C.C. Chiueh, J.L. Doppman, D.M. Jacobowitz, and I.J. Kopin Hemiparkinsonism in monkeys after unilateral internal carotid artery infusion of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) Life Sci. 39 1986 7 16
13. K.S. Bankiewicz, J. Bringas, P. Pivirotto, E. Kutzscher, D. Nagy, and M.E. Emborg Technique for bilateral intracranial implantation of cells in monkeys using an automated delivery system Cell Transplant. 9 2000 595 607
14. H. Bergman, T. Wichmann, B. Karmon, and M.R. DeLong The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism J. Neurophysiol. 72 1994 507 520
15. R. Betarbet, R.H. Porter, and J.T. Greenamyre GluR1 glutamate receptor subunit is regulated differentially in the primate basal ganglia following nigrostriatal dopamine denervation J. Neurochem. 74 2000 1166 1174
16. E. Bezard, S. Dovero, C. Prunier, P. Ravenscroft, S. Chalon, D. Guilloteau, A.R. Crossman, B. Bioulac, J.M. Brotchie, and C.E. Gross Relationship between the appearance of symptoms and the level of nigrostriatal degeneration in a progressive 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine- lesioned macaque model of Parkinson's disease J. Neurosci. 21 2001 6853 6861
17. A. Bjorklund Cell replacement strategies for neurodegenerative disorders Novartis Found. Symp. 231 2000 7 15 (discussion 16-20)
18. A. Bjorklund, D. Kirik, C. Rosenblad, B. Georgievska, C. Lundberg, and R.J. Mandel Towards a neuroprotective gene therapy for Parkinson's disease: use of adenovirus, AAV and lentivirus vectors for gene transfer of GDNF to the nigrostriatal system in the rat Parkinson model Brain Res. 886 2000 82 98
19. K.J. Black, M.H. Gado, T.O. Videen, and J.S. Perlmutter Baboon basal ganglia stereotaxy using internal MRI landmarks: validation and application to PET imaging J. Comput. Assist. Tomogr. 21 1997 881 886
20. K.J. Black, J.M. Koller, A.Z. Snyder, and J.S. Perlmutter Template images for nonhuman primate neuroimaging: 2. Macaque NeuroImage 14 2001 744 748
21. K.J. Black, A.Z. Snyder, J.M. Koller, M.H. Gado, and J.S. Perlmutter Template images for nonhuman primate neuroimaging: 1. Baboon NeuroImage 14 2001 736 743
22. G. Bourgeois, M. Magnin, A. Morel, S. Sartoretti, T. Huisman, E. Tuncdogan, D. Meier, and D. Jeanmonod Accuracy of MRI-guided stereotactic thalamic functional neurosurgery Neuroradiology 41 1999 636 645
23. A.F. Cannestra, E.M. Santori, C.J. Holmes, and A.W. Toga A three-dimensional multimodality brain map of the nemestrina monkey Brain Res. Bull. 43 1997 141 148
24. E. Cuny, D. Guehl, P. Burbaud, C. Gross, V. Dousset, and A. Rougier Lack of agreement between direct magnetic resonance imaging and statistical determination of a subthalamic target: the role of electrophysiological guidance J. Neurosurg. 97 2002 591 597
25. T. Deacon, J. Schumacher, J. Dinsmore, C. Thomas, P. Palmer, S. Kott, A. Edge, D. Penney, S. Kassissieh, P. Dempsey, and O. Isacson Histological evidence of fetal pig neural cell survival after transplantation into a patient with Parkinson's disease Nat. Med. 3 1997 350 353
26. D.A. Di Monte, A. McCormack, G. Petzinger, A.M. Janson, M. Quik, and W.J. Langston Relationship among nigrostriatal denervation, parkinsonism, and dyskinesias in the MPTP primate model Mov. Disord. 15 2000 459 466
27. S.G. Diamond, C.H. Markham, R.W. Rand, D.P. Becker, and L.J. Treciokas Four-year follow-up of adrenal-to-brain transplants in Parkinson's disease Arch. Neurol. 51 1994 559 563
28. R. Drucker-Colin, L. Verdugo-Diaz, C. Morgado-Valle, G. Solis-Maldonado, R. Ondarza, C. Boll, G. Miranda, G.J. Wang, and N. Volkow Transplant of cultured neuron-like differentiated chromaffin cells in a Parkinson's disease patient. A preliminary report Arch. Med. Res. 30 1999 33 39
29. M.E. Emborg, and J.H. Kordower Delivery of therapeutic molecules into the CNS Prog. Brain Res. 128 2000 323 332
30. E. Erwin, F.H. Baker, W.F. Busen, and J.G. Malpeli Relationship between laminar topology and retinotopy in the rhesus lateral geniculate nucleus: results from a functional atlas J. Comp. Neurol. 407 1999 92 102
31. K.A. Fowler, M.J. Huerkamp, J.K. Pullium, and T. Subramanian Anesthetic protocol: propofol use in Rhesus macaques (Macaca mulatta) during magnetic resonance imaging with stereotactic head frame application Brain Res. Brain Res. Protoc. 7 2001 87 93
32. S.H. Fox, B. Henry, M. Hill, A. Crossman, and J. Brotchie Stimulation of cannabinoid receptors reduces levodopa-induced dyskinesia in the MPTP-lesioned nonhuman primate model of Parkinson's disease Mov. Disord. 17 2002 1180 1187
33. C.R. Freed, P.E. Greene, R.E. Breeze, W.Y. Tsai, W. DuMouchel, R. Kao, S. Dillon, H. Winfield, S. Culver, J.Q. Trojanowski, D. Eidelberg, and S. Fahn Transplantation of embryonic dopamine neurons for severe Parkinson's disease N. Engl. J. Med. 344 2001 710 719
34. P. Ghosh, M. O'Dell, P.T. Narasimhan, S.E. Fraser, and R.E. Jacobs Mouse lemur microscopic MRI brain atlas NeuroImage 1 1994 345 349
35. J. Guridi, and J.A. Obeso The subthalamic nucleus, hemiballismus and Parkinson's disease: reappraisal of a neurosurgical dogma Brain 124 2001 5 19
36. T. Hashimoto, C.M. Elder, M.S. Okun, S.K. Patrick, and J.L. Vitek Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons J. Neurosci. 23 2003 1916 1923
37. L.L. Howel, L.D. Byrd, A.M. McDonough, P.M. Iuvone, and R.A. Bakay Behavioral evaluation of hemiparkinsonian MPTP monkeys following dopamine pharmacological manipulation and adrenal co-graft transplantation Cell Transplant. 9 2000 609 622
38. O. Isacson, T.W. Deacon, P. Pakzaban, W.R. Galpern, J. Dinsmore, and L.H. Burns Transplanted xenogeneic neural cells in neurodegenerative disease models exhibit remarkable axonal target specificity and distinct growth patterns of glial and axonal fibres Nat. Med. 1 1995 1189 1194
39. P. Jenner, and C.D. Marsden The actions of 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine in animals as a model of Parkinson's disease J. Neural Transm., Suppl. 20 1986 11 39
40. J.H. Jensen, R. Chandra, and H. Yu Quantitative model for the interecho time dependence of the CPMG relaxation rate in iron-rich gray matter Magn. Reson. Med. 46 2001 159 165
41. F.G. Kaddis, E.D. Clarkson, K.P. Bell, P.K. Choi, and C.R. Freed Co-grafts of muscle cells and mesencephalic tissue into hemiparkinsonian rats: behavioral and histochemical effects Brain Res. Bull. 51 2000 203 211
42. K. Kakishita, M.A. Elwan, N. Nakao, T. Itakura, and N. Sakuragawa Human amniotic epithelial cells produce dopamine and survive after implantation into the striatum of a rat model of Parkinson's disease: a potential source of donor for transplantation therapy Exp. Neurol. 165 2000 27 34
43. J.H. Kordower, M.E. Emborg, J. Bloch, S.Y. Ma, Y. Chu, L. Leventhal, J. McBride, E.Y. Chen, S. Palfi, B.Z. Roitberg, W.D. Brown, J.E. Holden, R. Pyzalski, M.D. Taylor, P. Carvey, Z. Ling, D. Trono, P. Hantraye, N. Deglon, and P. Aebischer Neurodegeneration prevented by lentiviral vector delivery of GDNF in primate models of Parkinson's disease Science 290 2000 767 773
44. P. Krack, J. Dostrovsky, I. Ilinsky, K. Kultas-Ilinsky, F. Lenz, A. Lozano, and J. Vitek Surgery of the motor thalamus: problems with the present nomenclatures Mov. Disord. 17 Suppl. 3 2002 S2 S8
45. J.W. Langston, M. Quik, G. Petzinger, M. Jakowec, and D.A. Di Monte Investigating levodopa-induced dyskinesias in the parkinsonian primate Ann. Neurol. 47 2000 S79 S89
46. O. Lindvall Neural transplantation: a hope for patients with Parkinson's disease NeuroReport 8 1997 iii x
47. O. Lindvall, and A. Bjorklund Transplantation strategies in the treatment of Parkinson's disease: experimental basis and clinical trials Acta Neurol. Scand., Suppl. 126 1989 197 210
48. R.R. Lonser, M.E. Corthesy, P.F. Morrison, N. Gogate, and E.H. Oldfield Convection-enhanced selective excitotoxic ablation of the neurons of the globus pallidus internus for treatment of parkinsonism in nonhuman primates J. Neurosurg. 91 1999 294 302
49. K.H. Ma, W.S. Huang, C.H. Chen, S.Z. Lin, S.P. Wey, G. Ting, S.D. Wang, H.W. Liu, and J.C. Liu Dual SPECT of dopamine system using [99mTc]TRODAT-1 and [123I]IBZM in normal and 6-OHDA-lesioned formosan rock monkeys Nucl. Med. Biol. 29 2002 561 567
50. I. Madrazo, B.R. Franco, M. Aguilera, S.F. Ostrosky, M. Madrazo, C. Cuevas, H. Catrejon, Z.G. Guizar, and E. Magallon Autologous adrenal medullary, fetal mesencephalic, and fetal adrenal brain transplantation in Parkinson's disease: a long-term postoperative follow-up J. Neural Transpl. Plast. 2 1991 157 164
51. J.S. Manaster, T. Feuerman, C.P. Reynolds, and C.H. Markham Transplantation of human neuroblastoma cells, catecholaminergic and non-catecholaminergic: effects on rotational behavior in Parkinson's rat model J. Neural Transpl. Plast. 3 1992 139 150
52. I. Mendez, and M. Hong Reconstruction of the striato-nigro-striatal circuitry by simultaneous double dopaminergic grafts: a tracer study using fluorogold and horseradish peroxidase Brain Res. 778 1997 194 205
53. I. Mendez, K.A. Baker, and M. Hong Simultaneous intrastriatal and intranigral grafting (double grafts) in the rat model of Parkinson's disease Brain Res. Brain Res. Rev. 32 2000 328 339
54. D. Nandi, J.F. Stein, and T.Z. Aziz Exploration of the role of the upper brainstem in motor control Stereotact. Funct. Neurosurg. 78 2002 158 167
55. C.W. Olanow, C.G. Goetz, J.H. Kordower, A.J. Stoessl, V. Sossi, M.F. Brin, K.M. Shannon, G.M. Nauert, D.P. Perl, J. Godbold, and T.B. Freeman A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson's disease Ann. Neurol. 54 2003 403 414
56. J. Olzewski The Thalamus of Macaca mulatta. An Atlas for Use With the Stereotaxic Instruments 1952 Karger Basel, New York
57. M. Onofrj, F. Ferracci, T. Fulgente, G. Malatesta, and M.F. Ghilardi Effects of drug manipulations on anterior components of somatosensory evoked potentials in a parkinsonian animal model Drugs Exp. Clin. Res. 20 1994 29 36
58. N.K. Patel, P. Heywood, K. O'Sullivan, S. Love, and S.S. Gill MRI-directed subthalamic nucleus surgery for Parkinson's disease Stereotact. Funct. Neurosurg. 78 2002 132 145
59. G. Paxinos Rhesus Monkey Brain in Stereotaxic Co-ordinates First ed. 1999 Academic Press
60. G. Percheron Ventricular landmarks for thalamic stereotaxy in Macaca J. Med. Primatol. 4 1975 217 244
61. G. Percheron A reliable system of ventricular coordinates for the cartography and stereotaxy of the amygdala (and anterior hippocampus) in macaques J. Neurosci. Methods 75 1997 5 14
62. G. Percheron, and N. Lacourly The lack of precision of thalamic stereotaxy based on Horsley and Clarke cranial coordinates in Macaca (author's transl.) Exp. Brain Res. 18 1973 355 373
63. M. Quik, S. Police, J.W. Langston, and D.A. Di Monte Increases in striatal preproenkephalin gene expression are associated with nigrostriatal damage but not L-DOPA-induced dyskinesias in the squirrel monkey Neuroscience 113 2002 213 220
64. A. Raz, E. Vaadia, and H. Bergman Firing patterns and correlations of spontaneous discharge of pallidal neurons in the normal and the tremulous 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine vervet model of parkinsonism J. Neurosci. 20 2000 8559 8571
65. D.C. Rohrer, G. Nilaver, V. Nipper, and C.A. Machida Genetically modified PC12 brain grafts: survivability and inducible nerve growth factor expression Cell Transplant. 5 1996 57 68
66. P.R. Sanberg, C.V. Borlongan, A.I. Othberg, S. Saporta, T.B. Freeman, and D.F. Cameron Testis-derived Sertoli cells have a trophic effect on dopamine neurons and alleviate hemiparkinsonism in rats Nat. Med. 3 1997 1129 1132
67. J.M. Savola, M. Hill, M. Engstrom, H. Merivuori, S. Wurster, S.G. McGuire, S.H. Fox, A.R. Crossman, and J.M. Brotchie Fipamezole (JP-1730) is a potent alpha2 adrenergic receptor antagonist that reduces levodopa-induced dyskinesia in the MPTP-lesioned primate model of Parkinson's disease Mov. Disord. 18 2003 872 883
68. M.I. Sereno Brain mapping in animals and humans Curr. Opin. Neurobiol. 8 1998 188 194
69. S. Sestini, A. Scotto di Luzio, F. Ammannati, M.T. De Cristofaro, A. Passeri, S. Martini, and A. Pupi Changes in regional cerebral blood flow caused by deep-brain stimulation of the subthalamic nucleus in Parkinson's disease J. Nucl. Med. 43 2002 725 732
70. P.A. Starr, T. Wichmann, C. van Horne, and R.A. Bakay Intranigral transplantation of fetal substantia nigra allograft in the hemiparkinsonian rhesus monkey Cell Transplant. 8 1999 37 45
71. T. Subramanian Cell transplantation for the treatment of Parkinson's disease Semin. Neurol. 21 2001 103 115
72. Subramanian T., Deogaonkar, M., in press. Cell transplantation and gene therapy for the treatment of Parkinson's disease. In: Galvez-Jimenez, N. (Ed.), Scientific Basis for Treatment of Parkinson's Disease. Taylor & Francis Medical Books, London, UK.
73. T. Subramanian, D.F. Emerich, R.A. Bakay, J.M. Hoffman, M.M. Goodman, T.M. Shoup, G.W. Miller, A.I. Levey, G.W. Hubert, S. Batchelor, S.R. Winn, J.A. Saydoff, and R.L. Watts Polymer-encapsulated PC-12 cells demonstrate high-affinity uptake of dopamine in vitro and 18F-Dopa uptake and metabolism after intracerebral implantation in nonhuman primates Cell Transplant. 6 1997 469 477
74. T. Subramanian, K. Venkiteswaran, D. Marchionini, and B. Brummer MRI guidance improves accuracy of stereotactic targeting of cell transplantation and gene therapy in parkinsonian monkeys Neurosci. Abstr. 27 2001 243 245
75. T. Subramanian, D. Marchionini, E.M. Potter, and M.L. Cornfeldt Striatal xenotransplantation of human retinal pigment epithelial cells attached to microcarriers in hemiparkinsonian rats ameliorates behavioral deficits without provoking a host immune response Cell Transplant. 11 2002 207 214
76. C.N. Svendsen, M.A. Caldwell, J. Shen, M.G. ter Borg, A.E. Rosser, P. Tyers, S. Karmiol, and S.B. Dunnett Long-term survival of human central nervous system progenitor cells transplanted into a rat model of Parkinson's disease Exp. Neurol. 148 1997 135 146
77. P.V. Theodosopoulos, W.J. Marks Jr., C. Christine, and P.A. Starr Locations of movement-related cells in the human subthalamic nucleus in Parkinson's disease Mov. Disord. 18 2003 791 798
78. C. Tornatore, B. Baker-Cairns, G. Yadid, R. Hamilton, K. Meyers, W. Atwood, A. Cummins, V. Tanner, and E. Major Expression of tyrosine hydroxylase in an immortalized human fetal astrocyte cell line; in vitro characterization and engraftment into the rodent striatum Cell Transplant. 5 1996 145 163
79. K. Tsao, S. Wilkinson, J. Overman, J. Kieltyka, T. Tollefson, W.C. Koller, R. Pahwa, A.I. Troster, K.E. Lyons, S. Batznitzky, L. Wetzel, and M.A. Gordon Comparison of actual pallidotomy lesion location with expected stereotactic location Stereotact. Funct. Neurosurg. 71 1998 1 19
80. D.C. Van Essen Surface-based atlases of cerebellar cortex in the human, macaque, and mouse Ann. N. Y. Acad. Sci. 978 2002 468 479
81. D.C. Van Essen, J.W. Lewis, H.A. Drury, N. Hadjikhani, R.B. Tootell, M. Bakircioglu, and M.I. Miller Mapping visual cortex in monkeys and humans using surface-based atlases Vision Res. 41 2001 1359 1378
82. R.J. Vermeulen, B. Drukarch, M.C. Sahadat, C. Goosen, E.C. Wolters, and J.C. Stoof The dopamine D1 agonist SKF 81297 and the dopamine D2 agonist LY 171555 act synergistically to stimulate motor behavior of 1-methyl-4-phenyl-1,2, 3,6-tetrahydropyridine-lesioned parkinsonian rhesus monkeys Mov. Disord. 9 1994 664 672
83. R.L. Watts, T. Subramanian, A. Freeman, C.G. Goetz, R.D. Penn, G.T. Stebbins, J.H. Kordower, and R.A. Bakay Effect of stereotaxic intrastriatal cografts of autologous adrenal medulla and peripheral nerve in Parkinson's disease: two-year follow-up study Exp. Neurol. 147 1997 510 517
84. R.L. Watts, C.D. Raiser, N.P. Stover, M.L. Cornfeldt, A.W. Schweikert, R.C. Allen, T. Subramanian, D. Doudet, C.R. Honey, and R.A. Bakay Stereotaxic intrastriatal implantation of human retinal pigment epithelial (hRPE) cells attached to gelatin microcarriers: a potential new cell therapy for Parkinson's disease J. Neural Transm., Suppl. 2003 215 227
85. T. Wichmann, H. Bergman, P.A. Starr, T. Subramanian, R.L. Watts, and M.R. DeLong Comparison of MPTP-induced changes in spontaneous neuronal discharge in the internal pallidal segment and in the substantia nigra pars reticulata in primates Exp. Brain Res. 125 1999 397 409
86. W.K. Winters, and R.W. Adey A Stereotaxic Brain Atlas for Macaca nemestrina 1969 University of California Press Berkley
87. H. Yoshida, I. Date, T. Shingo, K. Fujiwara, Y. Miyoshi, T. Furuta, and T. Ohmoto Evaluation of reaction of primate brain to grafted PC12 cells Cell Transplantation 8 1999 427 430
88. M. Zabek, M. Sobstyl, and H. Koziara Bilateral deep brain stimulation of subthalamic nucleus STN in the surgical treatment of Parkinson's disease Neurol. Neurochir. Pol. 37 2003 447 455 (discussion 455-447)
89. M.J. Zigmond, and E.M. Stricker Parkinson's disease: studies with an animal model Life Sci. 35 1984 5 18
90. T. Zigova, V. Pencea, R. Betarbet, S.J. Wiegand, C. Alexander, R.A. Bakay, and M.B. Luskin Neuronal progenitor cells of the neonatal subventricular zone differentiate and disperse following transplantation into the adult rat striatum Cell Transplant. 7 1998 137 156
91. K. Zilles, G. Schlaug, M. Matelli, G. Luppino, A. Schleicher, M. Qu, A. Dabringhaus, R. Seitz, and P.E. Roland Mapping of human and macaque sensorimotor areas by integrating architectonic, transmitter receptor, MRI and PET data J. Anat. 187 Pt. 3 1995 515 537