Advertisement

Transplantation of Catecholamine-Containing Tissues to Restore the Functional Capacity of the Damaged Nigrostriatal System

  • William J. Freed
  • Barry J. Hoffer
  • Lars Olson
  • Richard Jed Wyatt

Abstract

One of the ultimate goals of neurobiological research is to develop methods of reconstituting functional capacity following damage to the CNS. Most past efforts have approached this problem with attempts to enhance the function of the remaining, undamaged tissues by providing tropic influences or cellular “drive.”1 Drugs, chemical factors, or behavioral and electrical stimulation have been used. Such treatments might potentially stimulate the functional activity of spared tissues or increase the regrowth of fiber tracts.2, 3 For example, there have been encouraging results in reversing the effects of striatal lesions with the intracerebral administration of nerve growth factor.4

Keywords

Substantia Nigra Lateral Ventricle Adrenal Medulla Rotational Behavior Nigrostriatal System 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Varon, S., 1977, Neural growth and regeneration: A cellular perspective, Exp. Neurol. 54:1.PubMedCrossRefGoogle Scholar
  2. 2.
    Finger, S., and Stein, D. G., 1982, Brain Damage and Recovery: Research and Clinical Perspectives, p. 384, Academic Press, New York.Google Scholar
  3. 3.
    Puchala, E., and Windle, W. F., 1977, The possibility of structural and functional restitution after spinal cord injury: A review, Exp. Neurol. 55:1.PubMedCrossRefGoogle Scholar
  4. 4.
    Hart, T., Chaimas, N., Moore, R. Y., and Stein, D. G., 1978, Effects of nerve growth factor on behavioral recovery following caudate nucleus lesions in rats, Brain Res. Bull. 3:245.PubMedCrossRefGoogle Scholar
  5. 5.
    Seiger, Å., and Olson, L., 1977, Quantitation of fiber growth in transplanted central monoamine neurons, Cell Tissue Res. 179:285.PubMedCrossRefGoogle Scholar
  6. 6.
    Varon, S., 1975, Neurons and glia in neural cultures, Exp. Neurol. 48:93.PubMedCrossRefGoogle Scholar
  7. 7.
    Cotman, C. W., Nieto-Sampedro, M., and Harris, E. W., 1981, Synapse replacement in the nervous system of adult vertebrates, Physiol. Rev. 61:684.PubMedGoogle Scholar
  8. 8.
    Guth, L., 1974, Axonal regeneration and functional plasticity in the central nervous system, Exp. Neurol. 45:606.PubMedCrossRefGoogle Scholar
  9. 9.
    Steward, O., 1982, Assessing the functional significance of lesion-induced neuronal plasticity, Int. Rev. Neurobiol. 23:197.PubMedCrossRefGoogle Scholar
  10. 10.
    Anden, N.-E., Fuxe, K., Hamberger, B., and Hökfelt, T., 1966, A quantitative study of the nigroneostriatal dopamine neuron system in the rat, Acta Physiol. Scand. 67:306.PubMedCrossRefGoogle Scholar
  11. 11.
    Anden, N.-E., Dahlström, A., Fuxe, K., Larsson, K., Olson, L., and Ungerstedt, U., 1966, Ascending monoamine neurons to the telencephalon and diencephalon, Acta Physiol. Scand. 67:313.CrossRefGoogle Scholar
  12. 12.
    Dahlström, A., and Fuxe, K., 1964, Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brain stem neurons, Acta Physiol. Scand. 62:1.Google Scholar
  13. 13.
    Ungerstedt, U., 1971, Stereotaxic mapping of the monoamine pathways in the rat brain, Acta Physiol. Scand. 367:1.Google Scholar
  14. 14.
    Cotzias, G. C., Miller, S. T., Tang, L. C., and Papavasiliov, P. S., 1977, Levodopa, fertility, and longevity, Science 196:549.PubMedCrossRefGoogle Scholar
  15. 15.
    Finch, C. E., 1973, Catecholamine metabolism in the brains of ageing male mice, Brain Res. 52:261.PubMedCrossRefGoogle Scholar
  16. 16.
    Friedhoff, A. J., and Chase, T. N. (eds.), 1982, Güles de la Tourette Syndrome, p. 454, Raven Press, New York.Google Scholar
  17. 17.
    Lloyd, K. G., Hornykeiwicz, O., Davidson, L., Schannak, K., Farley, I., Goldstein, M., Shibuya, M., Kelley, W. N., and Fox, I. N., 1981, Biochemical evidence of dysfunction of brain neurotransmitters in the Lesch-Nyhan syndrome, N. Engl. J. Med. 305:110.CrossRefGoogle Scholar
  18. 18.
    Meltzer, H. Y., and Stahl, S. M., 1976, The dopamine hypothesis of schizophrenia: A review, Schizophr. Bull. 2:19.PubMedGoogle Scholar
  19. 19.
    Moskowitz, M. A., and Wurtman, R. J., 1975, Catecholamines and neurologic diseases, N. Engl. J. Med. 293:332.PubMedCrossRefGoogle Scholar
  20. 20.
    Wyatt, R. J., 1976, Biochemistry and schizophrenia. (IV). The neuroleptics—their mechanism of action: A review of the biochemical literature, Psychopharmacol. Bull. 12:5.PubMedGoogle Scholar
  21. 21.
    Olson, L., and Seiger, Å., 1972, Brain tissue transplanted to the anterior chamber of the eye. I. Fluorescence histochemistry of immature catecholamine and 5-hydroxytryptamine neurons reinnervating the rat iris, Z. Zellforsch. Mikrosk. Anat. 135:175.PubMedCrossRefGoogle Scholar
  22. 22.
    Olson, L., 1970, Fluorescence histochemical evidence for axonal growth and secretion from transplanted adrenal medullary tissue, Histochemie 22:1.PubMedCrossRefGoogle Scholar
  23. 23.
    Olson, L., Seiger, Å., Freedman, R., and Hoffer, B., 1980, Chromaffine cells can innervate brain tissue: Evidence from intraocular double grafts, Exp. Neurol. 70:414.PubMedCrossRefGoogle Scholar
  24. 24.
    Tischler, A. S., and Greene, L. A., 1980, Phenotypic plasticity of pheochromocytoma and normal adrenal medullary cells, in: Histochemistry and Cell Biology of Autonomic Neurons, SIF Cells, and Paraneurons (O. Eranko, S. Soinila, and H. Paivarinta, eds.), pp. 61–68, Raven Press, New York.Google Scholar
  25. 25.
    Unsicker, K., Krisch, B., Otten, U., and Thoenen, H., 1978, Nerve growth factor-induced fiber out-growth from isolated rat adrenal chromaffin cells: Impairment by glucocorticoids, Proc. Natl. Acad. Sci. USA 75:3498.PubMedCrossRefGoogle Scholar
  26. 26.
    Unsicker, K., Rieffert, B., and Ziegler, W., 1980, Effects of cell culture conditions, nerve growth factor, dexamethasone, and cyclic AMP on adrenal chromaffin cells in vitro, in: Histochemistry and Cell Biology of Autonomic Neurons, SIF Cells, and Paraneurons (O. Eranko, S. Sionila, and H. Paivarinta, eds.), pp. 51–59, Raven Press, New York.Google Scholar
  27. 27.
    Wurtman, R. J., Pohorecky, L. A., and Baliga, B. S., 1972, Adrenocortical control of the biosynthesis of epinephrine and proteins in the adrenal medulla, Pharmacol. Rev. 24:411.PubMedGoogle Scholar
  28. 28.
    Björklund, A., Schmidt, R. H., and Stenevi, U., 1980b, Functional reinnervation of the neostriatum in the adult rat by use of intraparenchymal grafting of dissociated cell suspensions from the substantia nigra, Cell Tissue Res. 212:39.PubMedCrossRefGoogle Scholar
  29. 29.
    Perlow, M. J., Kumakura, K., and Guidotti, A., 1980, Prolonged survival of bovine adrenal chromaffin cells in rat cerebral ventricles, Proc. Natl. Acad. Sci. USA 77:5278.PubMedCrossRefGoogle Scholar
  30. 30.
    Murphy, J. E., and Sturm, E., 1923, Conditions determining the transplantability of tissues in the brain, J. Exp. Med. 38:183.PubMedCrossRefGoogle Scholar
  31. 31.
    Das, G. D., Hallas, B. H., and Das, K. G., 1979, Transplantation of neural tissues in the brains of laboratory mammals: Technical details and comments, Experientia 35:143.PubMedCrossRefGoogle Scholar
  32. 32.
    Rosenstein, J. M., and Brightman, M. W., 1978, Intact cerebral ventricle as a site for tissue transplantation, Nature (London) 276:83.CrossRefGoogle Scholar
  33. 33.
    Perlow, M. J., Freed, W. J., Hoffer, B. J., Seiger, A., Olson, L., and Wyatt, R. J., 1979, Brain grafts reduce motor abnormalities produced by destruction of nigrostriatal dopamine system, Science 204:643.PubMedCrossRefGoogle Scholar
  34. 34.
    Freed, W. J., Perlow, M. J., Karoum, F., Seiger, Å., Olson, L., Hoffer, B. J., and Wyatt, R. J., 1980, Restoration of dopaminergic function by grafting of fetal rat substantia nigra to the caudate nucleus: Long-term behavioral, biochemical, and histochemical studies, Ann. Neurol. 8:510.PubMedCrossRefGoogle Scholar
  35. 35.
    Freed, W. J., Morihisa, J. M., Spoor, E., Hoffer, B. J., Olson, L., Seiger, Å., and Wyatt, R. J., 1981, Transplanted adrenal chromaffin cells in rat brain reduce lesion-induced rotational behavior, Nature (London) 292:351.CrossRefGoogle Scholar
  36. 36.
    Morihisa, J. M., Cannon-Spoor, H. E., Wyatt, R. J., and Freed, W. J., 1981, Alteration of drinking behavior by transplantation of kidney cortex to the rat brain, Soc. Neurosci. Abstr. 7:265.Google Scholar
  37. 37.
    Freed, W. J., Spoor, H. E., Sachs, D., and Wyatt, R. J., 1982, Immunological privilege in the brain with respect to functional brain grafts, Soc. Neurosci. Abstr. 8:141.Google Scholar
  38. 38.
    Freed, W. J., and Wyatt, R. J., 1980, Transplantation of eyes to the adult rat brain: Histological findings and light-evoked potential response, Life Sci. 27:503.PubMedCrossRefGoogle Scholar
  39. 39.
    Lund, R. D., and Hauschka, S. D., 1976. Transplanted neural tissue develops connections with host rat brain, Science 193:582.PubMedCrossRefGoogle Scholar
  40. 40.
    Björklund, A., Dunnett, S. B., Stenevi, U., Lewis, M. E., and Iversen, S. D., 1980, Reinnervation of the denervated striatum by substantia nigra transplants: Functional consequences as revealed by pharmacological and sensorimotor testing, Brain Res. 199:307.PubMedCrossRefGoogle Scholar
  41. 41.
    Medawar, P. B., 1948, Immunity to homologous grafted skin. III. The fate of skin homografts transplanted to the brain, to subcutaneous tissue, and to the anterior chamber of the eye, Br. J. Exp. Pathol. 29:58.PubMedGoogle Scholar
  42. 42.
    Stenevi, U., Björklund, A., Dunnett, S. B., and Gage, F. H., 1982, Cross-species neural grafting: Survival and function in an animal model of Parkinson’s disease, Soc. Neurosci. Abstr. 8:748.Google Scholar
  43. 43.
    Falck, B., Hillarp, N.-Å., Thieme, G., and Torp, A., 1962, Fluorescence of catecholamines and related compounds condensed with formaldehyde, J. Histochem. Cytochem. 10:348.CrossRefGoogle Scholar
  44. 44.
    de la Torre, J. C., 1980, An improved approach to histofluorescence using the SPG method for tissue monoamines, J. Neurosci. Methods 3:1.PubMedCrossRefGoogle Scholar
  45. 45.
    Church, A. C., Bunney, B. S., and Krieger, N. R., 1982, Neuronal localization of dopamine-sensitive adenylate cyclase within the rat olfactory tubercule, Brain Res. 234:369.PubMedCrossRefGoogle Scholar
  46. 46.
    Olson, L., Seiger, Å., Hoffer, B., and Taylor, D., 1979, Isolated catecholaminergic projections from substantia nigra and locus coeruleus to caudate, hippocampus, and cerebral cortex formed by intraocular sequential double brain grafts, Exp. Brain Res. 35:47.PubMedCrossRefGoogle Scholar
  47. 47.
    Stenevi, U., Emson, P., and Björklund, A., 1977, Development of dopamine sensitive adenylate cyclase in hippocampus reinnervated by transplanted dopamine neurons: Evidence for new functional contacts, Acta Physiol. Scand. Suppl. 452:39.PubMedGoogle Scholar
  48. 48.
    Karoum, F., Garrison, C. K., Neff, N., and Wyatt, R. J., 1977, Trans-synaptic modulation of dopamine metabolism in the rat superior cervical ganglion, J. Pharmacol. Exp. Ther. 210:654–661.Google Scholar
  49. 49.
    Karoum, F., and Neff, N. H., 1979, Analysis of dopamine and its metabolites in biological materials by mass fragmentography, in: The Neurobiology of Dopamine (A. S. Horn, J. Horf, and B. H. C. Westerink, eds.), pp. 63–76, Academic Press, New York.Google Scholar
  50. 50.
    Coupland, R. E., and MacDougall, I. D. B., 1966, Adrenaline formation in noradrenaline-storing chromaffin cells in vitro induced by corticosterone, J. Endocrinol. 36:317.PubMedCrossRefGoogle Scholar
  51. 51.
    Goochee, C., Rasband, W., and Sokoloff, L., 1980, Computerized densitometry and color coding of 14C deoxyglucose autoradiographs, Ann. Neurol. 7:359.PubMedCrossRefGoogle Scholar
  52. 52.
    Thoenen, H., 1975, Transsynaptic regulation of neuronal enzyme synthesis, in: Handbook of Psychopharmacology, Vol. 3 (L. L. Iversen, S. D. Iversen, and S. H. Synder, eds.), pp. 443–475, Plenum Press, New York.Google Scholar
  53. 53.
    Lewis, P. R., and Shute, C. C. D., 1969, An electron-microscopic study of cholinesterase distribution in rat adrenal medulla, J. Microsc. (Oxford) 89:181.CrossRefGoogle Scholar
  54. 54.
    Freed, W. J., Karoum, F., Spoor, H. E., Morihisa, J. M., Olson, L., and Wyatt, R. J., 1983, Catecholamine content of intracerebral adrenal medulla grafts, Brain Res. 269:184–189.PubMedCrossRefGoogle Scholar
  55. 55.
    Patrick, R. L., and Kirshner, N., 1971, Effect of stimulation on the levels of tyrosine hydroxylase, dopamine β-hydroxylase, and catecholamines in intact and denervated rat adrenal glands, Mol. Pharmacol. 7:87.PubMedGoogle Scholar
  56. 56.
    Snider, S. R., and Carlsson, A., 1972, The adrenal dopamine as an indicator of adrenomedullary hormone biosynthesis, Naunyn-Schmiedebergs Arch. Pharmacol. 275:347.PubMedCrossRefGoogle Scholar
  57. 57.
    Lishajko, F., 1970, Dopamine secretion from the isolated perfused sheep adrenal, Acta Physiol. Scand. 79:405.PubMedCrossRefGoogle Scholar
  58. 58.
    Hökfelt, T., and Ungerstedt, U., 1969, Electron and fluorescence microscopical studies on the nucleus caudatus putamen of the rat after unilateral lesion of the ascending nigro-neostriatal dopamine neurons, Acta Physiol. Scand. 76:415.PubMedCrossRefGoogle Scholar
  59. 59.
    Heybach, J. P., Coover, G. D., and Lints, C. E., 1978, Behavioral effects of neurotoxic lesions of the ascending monoamine pathways in the rat brain, J. Comp. Physiol. Psychol. 92:58.PubMedCrossRefGoogle Scholar
  60. 60.
    Stricker, E. M., and Zigmond, M. J., 1976, Recovery of function after damage to central catecholamine-containing neurons: A neurochemical model for the lateral hypothalamic syndrome, Prog. Psychobiol. Physiol. Psychol. 6:121.Google Scholar
  61. 61.
    Ungerstedt, U., 1971, Adipsia and aphagia after 6-hydroxydopamine induced degeneration of the nigrostriatal dopamine system, Acta Physiol. Scand. 367:95.Google Scholar
  62. 62.
    Ungerstedt, U., 1974, Brain dopamine neurons and behavior, in: Neurosciences: Third Study Program (F. O. Schmitt and F. G. Worden, eds.), pp. 695–703, MIT Press, Cambridge, Mass.Google Scholar
  63. 63.
    Ungerstedt, U., 1980, Behavioral pharmacology reflecting catecholamine neurotransmission, in: Handbook of Experimental Pharmacology, Vol. 54 (L. Szekeres, ed.), pp. 499–519, Springer-Verlag, Berlin.Google Scholar
  64. 64.
    Kornhuber, H. H., 1974, Cerebral cortex, cerebellum, and basal ganglia: An introduction to their motor functions, in: The Neurosciences: Third Study Program (F. O. Schmitt and F. G. Worden, eds.), pp. 267–280, MIT Press, Cambridge, Mass.Google Scholar
  65. 65.
    Ungerstedt, U., 1971, Striatal dopamine release after amphetamine or nerve degeneration revealed by rotational behavior, Acta Physiol. Scand. 367:49.Google Scholar
  66. 66.
    Ungerstedt, U., 1971, Postsynaptic supersensitivity after 6-hydroxydopamine induced degeneration of the nigro-striatal dopamine system, Acta Physiol. Scand. 367:69.Google Scholar
  67. 67.
    Creese, I., and Synder, S. H., 1979, Nigrostriatal lesions enhance striatal 3H-apomorphine and 3H-spiroperidol binding, Eur. J. Pharmacol. 56:277.PubMedCrossRefGoogle Scholar
  68. 68.
    Kreuger, B. K., Forn, J., Walters, J. R., Roth, R. N., and Greengard, P., 1976, Stimulation by dopamine of adenosine cyclic 3′, 5′-monophosphate formation in rat caudate nucleus: Effect of lesions of the nigro-neostriatal pathway, Mol. Pharmacol. 12:639.Google Scholar
  69. 69.
    Schultz, W., and Ungerstedt, U., 1978, Striatal cell supersensitivity to apomorphine in dopaminelesioned rats correlated to behavior, Neuropharmacology 17:349.PubMedCrossRefGoogle Scholar
  70. 70.
    Walsh, M. J., and Silbergeld, E. K., 1979, Rat rotation monitoring for pharmacology research, Pharmacol. Biochem. Behav. 10:433.PubMedCrossRefGoogle Scholar
  71. 71.
    Carman, J. B., Cowan, W. M., Powell, T. P. S., and Webster, K. E., 1965, A bilateral cortico-striate projection, J. Neurol. Neurosurg. Psychiatry 28:71.PubMedCrossRefGoogle Scholar
  72. 72.
    Björklund, H., Seiger, Å., Hoffer, B., and Olson, L., 1982, Trophic effects of brain areas on the developing cerebral cortex. I. Growth and histological organization of intraocular grafts, Dev. Brain Res. 6:131–140CrossRefGoogle Scholar
  73. 73.
    Björklund, A., and Stenevi, U., 1979, Reconstruction of the nigrostriatal dopamine pathway by intracerebral nigral transplants, Brain Res. 177:555.PubMedCrossRefGoogle Scholar
  74. 74.
    Dunnett, S. B., Björklund, A., Stenevi, U., and Iversen, S. D., 1981, Behavioral recovery following transplantation of substantia nigra in rats subjected to 6-OHDA lesions of the nigrostriatal pathway. I. Unilateral lesions, Brain Res. 215:147.PubMedCrossRefGoogle Scholar
  75. 75.
    Björklund, A., Stenevi, U., Dunnett, S. B., and Iversen, S. D., 1981, Functional reactivation of the deafferented neostriatum by nigral transplants, Nature (London) 289:497.CrossRefGoogle Scholar
  76. 76.
    Trendelenburg, U., 1963, Supersensitivity and subsensitivity to sympathomimetic amines, Pharmacol. Rev. 15:225.PubMedGoogle Scholar
  77. 77.
    Trendelenburg, U., 1966, Mechanisms of supersensitivity and subsensitivity to sympathomimetic amines, Pharmacol. Rev. 18:629.PubMedGoogle Scholar
  78. 78.
    Fleming, W. W., 1976, Variable sensitivity of excitable cells: Possible mechanisms and biological significance, in: Reviews of Neuroscience, Vol. 2 (S. Ehrenpreis and I. J. Kopin, eds.), pp. 43–90, Raven Press, New York.Google Scholar
  79. 79.
    Wyatt, R. J., and Freed, W. J., Grafting dopamine-containing cells into the striatal region of substantia nigra lesioned rats, in: Proceedings of World Health Organization’s Study Group on Neuroplasticity and Repair in the Central Nervous System. C. L. Bolis (ed)., Raven Press, N.Y., in pressGoogle Scholar
  80. 80.
    Fink, J. S., and Smith, G. P., 1980, Mesolimbicortical dopamine terminal fields are necessary for normal locomotor and investigatory exploration in rats, Brain Res. 199:359.PubMedCrossRefGoogle Scholar
  81. 81.
    Kelly, P. H., Seviour, P. W., and Iversen, S. D., 1975, Amphetamine and apomorphine responses in the rat following 6-OHDA lesions of the nucleus accumbens septi and corpus striatum, Brain Res. 94:507.PubMedCrossRefGoogle Scholar
  82. 82.
    Fray, P. J., Dunnett, S. B., Iversen, S. D., Björklund, A., and Stenevi, U., Nigral transplants reinnervating the dopamine-depleted neostriatum can sustain intracranial self-stimulation, Science 219:416-419.Google Scholar
  83. 83.
    Dunnett, S. B., Björklund, A., Stenevi, U., and Iversen, S. D., 1981. Behavioral recovery following transplantation of substantia nigra in rats subjected to 6-OHDA lesions of the nigrostriatal pathway. II. Bilateral lesions, Brain Res. 229:457.PubMedCrossRefGoogle Scholar
  84. 84.
    Dunnett, S. B., Björklund, A., Stenevi, U., and Iversen, S. D., 1981, Grafts of embryonic substantia nigra reinnervating the ventrolateral striatum ameliorate sensorimotor impairments and akinesia in rats with 6-OHDA lesions of the nigrostriatal pathway, Brain Res. 229:209.PubMedCrossRefGoogle Scholar
  85. 85.
    Ljungberg, T., and Ungerstedt, U., 1976, Sensory inattention produced by 6-hydroxydopamine-induced degeneration of ascending dopamine neurons in the brain, Exp. Neurol. 53:585.PubMedCrossRefGoogle Scholar
  86. 86.
    Marshall, J. F., and Teitelbaum, P., 1974, Further analysis of sensory inattention following lateral hypothalamic damage in rats, J. Comp. Physiol. Psychol. 86:375.PubMedCrossRefGoogle Scholar
  87. 87.
    Teitelbaum, P., and Epstein, A. N., 1962, The lateral hypothalamic syndrome: Recovery of feeding and drinking after lateral hypothalamic lesions, Psychol. Rev. 691:74.CrossRefGoogle Scholar
  88. 88.
    Goldberg, S. R., Hoffmeister, F., Schlichting, U. U., and Wuttke, W., 1971, A comparison of pentobarbital and cocaine self-administration in rhesus monkeys: Effects of dose and fixed-ratio parameter, J. Pharmacol. Exp. Ther. 179:277.PubMedGoogle Scholar
  89. 89.
    Pickens, R., and Thompson, T., 1968, Cocaine-reinforced behavior in rats: Effects of reinforcement magnitude and fixed-ratio size, J. Pharmacol. Exp. Ther. 161:122.PubMedGoogle Scholar
  90. 90.
    Wuerthele, S. M., Freed, W. J., Olson, L., Morihisa, J., Spoor, L., Wyatt, R. J., and Hoffer, B. J., 1981, Effect of dopamine agonists and antagonists on the electrical activity of substantia nigra neurons transplanted into the lateral ventricle of the rat, Exp. Brain Res. 44:1.PubMedCrossRefGoogle Scholar
  91. 91.
    Groves, P. M., Wilson, C. J., Young, S. J., and Rebec, G. V., 1975, Self-inhibition by dopaminergic neurons, Science 190:522.PubMedCrossRefGoogle Scholar
  92. 92.
    Gale, K., Costa, E., Toffano, G., Hong, J.-S., and Guidotti, A., 1978, Evidence for a role of nigral gamma-aminobutyric acid and substance P in the haloperidol-induced activation of striatal tyrosine hydroxylase, J. Pharmacol. Exp. Ther. 206:29.PubMedGoogle Scholar
  93. 93.
    Buchwald, N. A., Price, D. D., Vernon, L., and Hull, C. D., 1973, Caudate intracellular response to thalamic and cortical inputs, Exp. Neurol. 38:311.PubMedCrossRefGoogle Scholar
  94. 94.
    Woodruff, M. F. A., 1960, The Transplantation of Tissues and Organs, Thomas, Springfield, Ill.Google Scholar
  95. 95.
    de Groot, J., 1959, The Rat Forebrain in Stereotaxic Coordinates, Verh. K. Ned. Akad. Wet. Afd. Natuurkd. 52:1–40.Google Scholar

Copyright information

© Plenum Press, New York 1984

Authors and Affiliations

  • William J. Freed
    • 1
    • 2
  • Barry J. Hoffer
    • 3
  • Lars Olson
    • 4
  • Richard Jed Wyatt
    • 1
    • 2
  1. 1.Preclinical Neurosciences SectionAdult Psychiatry BranchUSA
  2. 2.National Institute of Mental HealthSaint Elizabeths HospitalUSA
  3. 3.Department of PharmacologyUniversity of Colorado Medical CenterDenverUSA
  4. 4.Department of HistologyKarolinska InstituteStockholmSweden

Personalised recommendations