Central Cholinergic Pathways: The Biochemical Evidence

  • F. Fonnum
Part of the Handbook of Experimental Pharmacology book series (HEP, volume 86)

Abstract

The biochemical approach to identifying cholinergic pathways in the brain is based on the determination of cholinergic markers in well-defined anatomical structures. With highly sensitive biochemical methods it is possible to determine the cholinergic markers in small regions, even single cells, and thereby provide an accurate quantitative description of the cholinergic system. As will be seen in this chapter the determination of choline acetyltransferase (ChAT) in combination with chemical or surgical lesions has been of particular importance in gaining such information. The strength of the histochemical approach, particularly the immunocytochemistry of ChAT, has not been in its ability to discover new cholinergic pathways, but to identify and characterize cholinergic cells or cell groups (Chap. 22). The application of immunohistochemical methods at the electron microscopic level may in the future reveal new and exciting details of the central cholinergic nerve terminals.

Keywords

Dopamine Retina Neurol Catecholamine Acetylcholine 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aquilonius SM, Eckernäs SÅ, Gulberg P-G (1981) Topographical localization of choline acetyltransferase within the human spinal cord and with some other species. Brain Res 211:329–340PubMedGoogle Scholar
  2. Bagnoli PA, Beaudet M, Stella M, Cuénod M (1981) Selective retrograde labeling of cholinergic neurons with [3H]choline. J Neurosci 1:691–695PubMedGoogle Scholar
  3. Barrington-Ward SJ, Kilpatric IC, Phillipson OT, Pycock CJ (1984) Evidence that thalamic efferent neurones are non-cholinergic — a study in the rat with special reference to the thalamostriatal pathway. Brain Res 299:146–151PubMedGoogle Scholar
  4. Beesley PY, Emson PC (1975) Distribution of transmitter related enzymes in the rat sensori-motor cortex. Biochem Soc Trans 3:936–939Google Scholar
  5. Ben-Ari Y, Zigmond RE, Shute CCD, Lewis PR (1977) Regional distribution of choline acetyltransferase and acetylcholinesterase within the amygdaloid cortex and stria terminalis system. Brain Res 120:435–445PubMedGoogle Scholar
  6. Brownstein M, Kobayashi R, Palkovits M, Saavedra JM (1976 a) Choline acetyltransferase levels in the diencephalic nuclei of the rat. J Neurochem 24:35–38Google Scholar
  7. Brownstein M, Palkovits M, Tappaz ML, Saavedra JM, Kizer JS (1976 b) Effect of surgical isolation of the hypothalamus on its neurotransmitter content. Brain Res 117:287–295PubMedGoogle Scholar
  8. Burke RE, Fahn S (1985) Choline acetyltransferase activity of the principal vestibular nuclei of rat studied by micropunch technique. Brain Res 328:196–199PubMedGoogle Scholar
  9. Carson KA, Nemeroff CB, Rone MS, Young-Blood WW, Prange AJ Jr, Hanker JS, Kezer JS (1977) Biochemical and histochemical evidence for the existence of a tuberonfundubular cholinergic pathway in the rat. Brain Res 129:169–173PubMedGoogle Scholar
  10. Cheney DL, Lefevre HF, Racagni G (1975) Choline acetyltransferase activity and mass fragmentographic measurements in acetylcholine specific nuclei and tracts of rat brain. Neuropharmacology 14:801–809PubMedGoogle Scholar
  11. Contestabile A, Fonnum F (1983) Cholinergic and GABAergic forebrain projections to the habenula and nucleus interpeduncularis: surgical and kainic acid lesions. Brain Res 275:287–297PubMedGoogle Scholar
  12. Contestabile A, Villani L, Fonnum F (1986 a) Neurochemical and ultrastructural study of the effect of the cholinergic toxin AF 6417 in nucleus interpeduncularis. Brain Res 379:223–231PubMedGoogle Scholar
  13. Contestabile A, Villani L, Fasolo A, Franzoni MF, Gribaudo L, Oktedalen O, Fonnum F (1986 b) Topography of cholinergic and substance P pathways in the habenulo-interpeduncular system of the rat: an immunocytochemical and microchemical approach. Neuroscience (in press)Google Scholar
  14. Coyle JT, Schwartz R (1976) Lesion of striatal neurons with kainic acid model for Huntington’s chorea. Nature 271:178–180Google Scholar
  15. Cuello AC, Emson PC, Paxines C, Jessel T (1978) Substance P containing and cholinergic projections from the habenulae. Brain Res 149:413–429PubMedGoogle Scholar
  16. Damsma BH, Westerink BHC, Horn AS (1985) A simple, sensitive and economic assay for choline and acetylcholine using HPLC, an enzyme reactor, and an electrochemical detector. J Neurochem 45:1649–1653PubMedGoogle Scholar
  17. Demêmes D, Raymond J, Sano A (1983) Selective retrograde labelling of vestibular efferent neurons with [3H]choline. Neuroscience 8:290–295Google Scholar
  18. Eckenstein F, Thoenen H (1983) Cholinergic neurons in the rat cerebral cortex demonstrated by immunohistochemical localization of choline acetyltransferase. Neurosci Lett 36:211–255PubMedGoogle Scholar
  19. Emson PC, Fonnum F (1974) Choline acetyltransferase, acetylcholinesterase and aromatic L-amino acid decarboxylase in single identified nerve cells bodies from snail Helix aspersa. J Neurochem 22:1079–1088PubMedGoogle Scholar
  20. Emson PC, Burrows M, Fonnum F (1974) Levels of glutamate decarboxylase, choline acetyltransferase and acetylcholinesterase in identified motorneurons of the locust. J Neurobiol 5:33–42PubMedGoogle Scholar
  21. Emson PC, Paxinos G, Le Gal La Salle G, Ben Ari Y, Silver A (1979) Choline acetyltransferase and acetylcholinesterase containing projections from the basal forebrain to the amygdaloid complex of the rat. Brain Res 165:271–282PubMedGoogle Scholar
  22. Eva C, Hadjiconstantinou M, Neff NM, Meek JL (1984) Acetylcholine measurement by high performance liquid chromatography using an enzyme-loaded post-column reactor. Anal Biochem 143:320–324PubMedGoogle Scholar
  23. Fibiger HC (1982) The organization and some projections of cholinergic neurons of the mammalian forebrain. Brain Res Rev 4:324–388Google Scholar
  24. Fisher A, Mantione CR, Abraham DJ, Hanin I (1982) Long term central cholinergic hypofunction induced in mice by ethylcholine aziridinium (AF64A) in vivo. J Pharmacol Exp Ther 222:140–145PubMedGoogle Scholar
  25. Flumerfelt BA, Contestabile A (1982) Acetylcholinesterase histochemistry of the habenulo-interpeduncular pathway in the rat and the effect of electrolytic and kainic acid lesions. Anat Embryol (Berl) 163:435–446Google Scholar
  26. Fonnum F (1969 a) Radiochemical micro assays for the determination of choline acetyltransferase and acetylcholinesterase activities. Biochem J 115:465–472PubMedGoogle Scholar
  27. Fonnum F (1969 b) Subcellular localization of choline acetyltransferase in brain. In: Heilbronn E, Winter A (eds) Drugs and cholinergic metabolism in the CNS. FOA, Stockholm, pp 83–96Google Scholar
  28. Fonnum F (1970) Topographical and subcellular localization of choline acetyltransferase in rat hippocampal region. J Neurochem 17:1029–1037PubMedGoogle Scholar
  29. Fonnum F (1972) Application of microchemical analysis and subcellular fractionation technique to the study of neurotransmitters in discrete areas of mammalian brain. Adv Biochem Psychopharmacol 6:75–88PubMedGoogle Scholar
  30. Fonnum F (1975) A rapid radiochemical method of the determination of choline acetyltransferase. J Neurochem 24:407–409PubMedGoogle Scholar
  31. Fonnum F, Contestabile A (1984) Colchicine neurotoxicity demonstrates the cholinergic projection from the supracommissural system to the habenula and nucleus interpeduncularis in the rat. J Neurochem 42:881–884Google Scholar
  32. Fonnum F, Grofová I, Rinvik E, Storm-Mathisen J, Walberg F (1974) Origin and distribution of glutamate decarboxylase in the substantia nigra of the rat. Brain Res 71:77–92PubMedGoogle Scholar
  33. Fonnum F, Walaas I, Iversen E (1977) Localization of GABAergic, cholinergic and aminergic structures in the mesolimbic system. J Neurochem 29:221–230PubMedGoogle Scholar
  34. Freeman JJ, Choi RL, Jenden DY (1975) Plasma choline: its turnover and exchange with brain choline. J Neurochem 24:729–734PubMedGoogle Scholar
  35. Geneser-Jensen FA, Blackstad TW (1971) Distribution of acetylcholinesterase in the hippocampal region of the guinea-pig I. Enthorinal area, parasubiculum and presubiculum. Z Zellforsch 114:460–481PubMedGoogle Scholar
  36. Giller E, Schwartz JH (1971) Choline acetyltransferase in identified neurons of adominal ganglion of Aplysia california. J Neurophysiol 34:93–107PubMedGoogle Scholar
  37. Godfrey DA, Ross CD, Herrmann AD, Matchinsky FM (1980) Distribution and derivation of cholinergic elements in the rat olfactory bulb. Neuroscience 5:273–292PubMedGoogle Scholar
  38. Goldberg AM, McCaman RE (1967) A quantitative microchemical study of choline acetyltransferase and acetylcholinesterase in the cerebellum of several species. Life Sci 6:1493–1500PubMedGoogle Scholar
  39. Goldberg AM, McCaman RE (1973) The determination of picomole amounts of acetylcholine in mammalian brain. J Neurochem 20:1–8PubMedGoogle Scholar
  40. Goldman PS, Nauta WJH (1977) An intricately patterned prefrontocaudate projection in the rhesus monkey. J Comp Neurol 171:369–386Google Scholar
  41. Gordon CR, Krieger NR (1983) Localization of choline acetyltransferase in laminae of the rat olfactory tubercle. J Neurochem 40:79–83PubMedGoogle Scholar
  42. Gordon MN, Finch CE (1985) Topochemical localization of choline acetyltransferase and acetylcholinesterase in mouse brain. Brain Res 308:364–368Google Scholar
  43. Gottesfeld Z, Fonnum F (1977) Transmitter synthesizing enzymes in the hypoglossal nucleus and the cerebellum — effect of acetylpyridine and surgical lesions. J Neurochem 28:237–239PubMedGoogle Scholar
  44. Gottesfeld Z, Jacobowitz DM (1978) Cholinergic projection of the diagonal band to the interpeduncular nucleus of the rat brain. Brain Res 156:329–332PubMedGoogle Scholar
  45. Gottesfeld Z, Jacobowitz DM (1979) Cholinergic projections from the septal-diagonal band area to the habenular nuclei. Brain Res 176:391–394PubMedGoogle Scholar
  46. Graybiel AM, Ragsdale CW (1978) Histochemically distinct compartments in the striatum of human, monkey and cat demonstrated by acetylcholinesterase staining. Proc Natl Acad Sci USA 75:5723–5726PubMedGoogle Scholar
  47. Gwyn DG, Wolstencroft JH, Silver A (1972) The effect of hemisection on the distribution of acetylcholinesterase and choline acetyltransferase in the spinal cord of cat. Brain Res 47:289–301PubMedGoogle Scholar
  48. Hassler R, Nitsch C, Lee HL (1980) The role of eight putative transmitters in the nine types of synapses in rat caudate-putamen. In: Rinne U, Klinger M, Stanson G (ed) Parkinson’s disease — current progress, problems and management. Elsevier, Amsterdam, pp 61–91Google Scholar
  49. Hebb CO, Krnjević K, Silver A (1963) Effect of undercutting on the acetylcholinesterase and choline acetyltransferase activity in the cat’s cerebral cortex. Nature 198:692Google Scholar
  50. Heimer L (1978) The olfactory cortex and the ventral striatum. In: Livingston KE, Hornykiewicz O (eds) Limbic mechanisms. Plenum, New York, pp 95–187Google Scholar
  51. Hiley CR, Burgen ASV (1974) The distribution of muscarinic receptor sites in the nervous system of the dog. J Neurochem 22:159–162PubMedGoogle Scholar
  52. Hodes HI, Rea MA, Felten DL, Aprison MH (1983) Specific binding of the muscarinic antagonist [3H]quinuclidinyl benzilate is not associated with preganglionic motor neurons in the dorsal motor nucleus of the vagus. Neurochem Res 8:73–87PubMedGoogle Scholar
  53. Hoover DB, Hancock JC (1985) Effect of facial nerve transection on acetylcholinesterase, choline acetyltransferase and [3H]quinuclidinyl benzilate binding in rat facial nuclei. Neuroscience 15:481–487PubMedGoogle Scholar
  54. Hoover DB, Jacobowitz DM (1979) Neurochemical and histochemical studies of the effect of a lesion of the nucleus cuneiformis on the cholinergic innervation of discrete areas of the rat brain. Brain Res 170:113–122PubMedGoogle Scholar
  55. Hoover DB, Muth EA, Jacobowitz DM (1978) A mapping of the distribution of acetylcholine, choline acetyltransferase and acetylcholinesterase in discrete areas of rat brain. Brain Res 153:295–306PubMedGoogle Scholar
  56. Israël M, Lesbats B (1981) Chemiluminescent determination of acetylcholine and continuous detection of its release from Torpedo electric organ synapses and synaptosomes. Neurochem Int 3:81–90PubMedGoogle Scholar
  57. Israël M, Whittaker VP (1967) The isolation of mossy fibre endings from the granular layer of the cerebellar cortex. Experientia 21:325–326Google Scholar
  58. Jaffé EH, Cuello AC (1980) The distribution of catecholamines, glutamate decarboxylase and choline acetyltransferase in layers of the rat olfactory bulb. Brain Res 186:232–237PubMedGoogle Scholar
  59. Jacobowitz DM (1974) Removal of discrete fresh regions of the rat brain. Brain Res 80:111–115PubMedGoogle Scholar
  60. Kanazawa I, Sutoo D, Oshima I, Saito S (1979) Effect of transection on choline acetyltransferase, thyrotropin releasing hormone and substance P in the cervical spinal cord. Neurosci Lett 13:325–330PubMedGoogle Scholar
  61. Kása P, Silver A (1969) The correlation between choline acetyltransferase and acetylcholinesterase activity in different areas of the cerebellum of rat and guinea pig. J Neurochem 16:389–396Google Scholar
  62. Kása P, Joó F, Csillik B (1965) Histochemical localization of acetylcholinesterase in the cat cerebellar cortex. J Neurochem 12:31–35PubMedGoogle Scholar
  63. Kataoka K, Nakamura Y, Hassler R (1973) Habenulo-interpeduncular tract: a possible cholinergic neuron in rat brain. Brain Res 62:264–267PubMedGoogle Scholar
  64. Kato T (1984) Enzymatic determination of choline acetyltransferase by coenzyme A cycling and its application to analysis of single mammalian neurons. J Neurochem 42:903–910PubMedGoogle Scholar
  65. Kato T, Murashima YL (1985) Choline acetyltransferase activities in single motor neurons from vertebrate spinal cords. J Neurochem 44:675–679PubMedGoogle Scholar
  66. Kelly PH, Moore KE (1978) Decrease of neocortical choline acetyltransferase after lesion of the globus pallidus in the rat. Exp Neurol 61:479–484PubMedGoogle Scholar
  67. Kim J-S (1978) Transmitters for the afferent and efferent systems of the neostriatum and their possible interactions. Adv Biochem Psychopharmacol 19:217–233PubMedGoogle Scholar
  68. Kobayashi RM, Brownstein M, Saavedra JM, Palkovits M (1975) Choline acetyltransferase content in discrete regions of the rat brain stem. J Neurochem 24:637–640PubMedGoogle Scholar
  69. Kobayashi RM, Palkovits M, Hruska RE, Rothschild R, Yamamura H (1978) Regional distribution of muscarinic cholinergic receptors in rat brain. Brain Res 154:13–23PubMedGoogle Scholar
  70. Koslow SH, Racagni C, Costa E (1974) Mass fragmentographic measurements of norephinephrine, dopamine, serotonin and acetylcholine in seven discrete nuclei of the rat tel-diencephalon. Neuropharmacology 13:1123–1130PubMedGoogle Scholar
  71. Kuhar MJ, Murrin LC (1978) Sodium dependent high affinity choline uptake. J Neurochem 30:15–22PubMedGoogle Scholar
  72. Kuhar MJ, Setting VH, Roth RH, Aghajanian GK (1973) Choline: selective accumulation by central cholinergic neurons. J Neurochem 20:581–593PubMedGoogle Scholar
  73. Kuhar MJ, Dehaven RN, Yamamura HI, Rommelspacher H, Simon JR (1975) Further evidence for cholinergic habenulo-interpeduncular neurons: pharmacologic and functional characteristics. Brain Res 97:265–275PubMedGoogle Scholar
  74. Lehmann NJ, Fibiger HC (1978) Acetylcholinesterase in the substantia nigra and caudate-putamen of the rat: properties and localization in dopaminergic neurons. J Neurochem 30:615–624PubMedGoogle Scholar
  75. Lehmann NJ, Nagy JJ, Atmadja, Fibiger HC (1980) The nucleus basalis magnocellularis is the origin of a cholinergic projection to the neocortex of the rat. Neuroscience 5:1161–1174PubMedGoogle Scholar
  76. Levy A, Kant GJ, Meyerhoff JL, Jarrard LE (1984) Non-cholinergic neurotoxic effects of AF64A in the substantia nigra. Brain Res 305:169–172PubMedGoogle Scholar
  77. Lewis PR, Shute CCD, Silver A (1967) Confirmation from choline acetylase analysis of a massive cholinergic innervation of the rat hippocampus. J Physiol (Lond) 191:215–224Google Scholar
  78. Lowry OH, Passoneau JV (1972) A flexible system of enzymatic analysis. Academic, New YorkGoogle Scholar
  79. Lund-Karlsen R, Fonnum F (1976) The toxic effect of sodium glutamate on rat retina: changes in putative transmitters and their corresponding enzymes. J Neurochem 27:1437–1441Google Scholar
  80. Macrides F, Davis BY, Youngs WM, Nach MS, Margolis FL (1981) Cholinergic and cate-cholaminergic afferents to the olfactory bulb in the hamster. A neuroanatomical, biochemical and histochemical investigation. J Comp Neurol 203:497–516Google Scholar
  81. Malthe-Sørenssen D, Odden E, Walaas I (1980) Selective destruction by kainic acid of neurons innervated by putative glutamergic afferents in septum and nucleus of the diagonal band. Brain Res 182:461–465PubMedGoogle Scholar
  82. Manaker S, Wieczorek CM, Rainbow TC (1986) Identification of sodium-dependent, high-affinity choline uptake sites in rat brain with [3H]hemicholinum-3. J Neurochem 46:483–488PubMedGoogle Scholar
  83. Mantione CR, Fisher A, Hanin I (1981) AF64A neurotoxicity: a potential animal model of central cholinergic hypofunction. Science 213:579–580PubMedGoogle Scholar
  84. Mantione CR, Zigmand MY, Fisher A, Hanin I (1983) Selective presynaptic cholinergic neurotoxicity following intrahippocampal AF64A injection in rats. J Neurochem 41:251–255PubMedGoogle Scholar
  85. Marshall RC, Flumberfelt BA, Gwyn DG (1980) Acetylcholinesterase activity and acetylcholine effects in the cerbello-rubro-thalamic pathway of the cat. Brain Res 190:493–504PubMedGoogle Scholar
  86. McCaman RE, Dewhurst SA (1970) Choline acetyltransferase in individual neurones of Aplysia california. J Neurochem 17:1421–1426PubMedGoogle Scholar
  87. McGeer EG, McGeer PL (1976) Distribution of biochemical changes of Hungtington’s chorea by intrastriatal injections of glutamic and kainic acids. Nature 263:517–512PubMedGoogle Scholar
  88. McGeer PL, McGeer EG, Fibiger HG, Wickson V (1971) Neostriatal choline acetylase and Cholinesterase following selective brain lesions. Brain Res 35:308–314PubMedGoogle Scholar
  89. McKinney M, Struble RG, Prue DL, Coyle JT (1982) Monkey nucleus basalis is enriched with choline acetyltransferase. Neuroscience 7:2363–2368PubMedGoogle Scholar
  90. Mellgren SI, Srebro B (1973) Changes in acetylcholinesterase and distribution of degenerating fibres in the hippocampal region after septal lesions in the rat. Brain Res 52:19–36PubMedGoogle Scholar
  91. Meyer DK, Brownstein MJ (1980) Effect of surgical deafferentation of the supraoptic nucleus on its choline acetyltransferase content. Brain Res 193:566–569PubMedGoogle Scholar
  92. Nieoullon A, Dusticier N (1980) Choline acetyltransferase activity in discrete regions of the cat brain. Brain Res 196:139–149PubMedGoogle Scholar
  93. Nieoullon A, Dusticier N (1981) Decrease in choline acetyltransferase activity in the red nucleus of the cat after cerebellar lesion. Neuroscience 6:1633–1641PubMedGoogle Scholar
  94. Palkovits M (1973) Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res 59:449–450PubMedGoogle Scholar
  95. Palkovits M, Saavedra JM, Kobayashi RM, Brownstein M (1974) Choline acetyltransferase content of limbic nuclei of the rat. Brain Res 79:443–450PubMedGoogle Scholar
  96. Perry EL, Atack JR, Perry RH, Hardy JA, Dodd PC, Edwardson JA, Blessed G, Tomlinson BE, Fairbarn DF (1984) Intralaminar neurochemical distributions in human midtemporal cortex; comparison between Alzheimer’s disease and the normal. J Neurochem 42:1402–1410PubMedGoogle Scholar
  97. Rainbow TC, Parsons B, Wieczerok CM (1984) Quantitative autoradiography of [3H]hemicholinum-3 binding sites in rat brain. Eur J Pharmacol 102:195–196PubMedGoogle Scholar
  98. Ross CD, McDougal DM Jr (1976) The distribution of choline acetyltransferse activity in vertebrate retina. J Neurochem 26:521–526PubMedGoogle Scholar
  99. Ross CD, Godbrey DA, Williams AD, Matschinsky FM (1978) Evidence for a central origin of cholinergic structures in the olfactory bulb. Neurosci Abstr 4:91Google Scholar
  100. Rotter A, Birdsall NJM, Field PM, Raisman G (1979 a) Muscarinic receptors in the central nervous system of the rat. II. Distribution of binding [3H]propylbenzilylcholine mustard in the midbrain and hindbrain. Brain Res Rev 1:167–183Google Scholar
  101. Rotter A, Birdsall NJM, Burgen ASV, Field PM, Hulme EC, Raisman G (1979b) Muscarinic receptors in the central nervous system of the rat. I. Technique for autoradiographic localization of the binding of [3H]propylbenzilylcholine mustard and its distribution in the forebrain. Brain Res Rev 1:141–165Google Scholar
  102. Saelens JK, Edwards-Neale S, Simke JP (1979) Further evidence for cholinergic thalamostriatal neurons. J Neurochem 32:1093–1094PubMedGoogle Scholar
  103. Shute CCD, Lewis PR (1961) The use of Cholinesterase techniques combined with operative procedures to follow neuron pathways in the brain. Bibl Anat 2:34–39Google Scholar
  104. Shute CCD, Lewis PR (1967) The ascending cholinergic reticular system: neocortical, olfactory and subcortical projections. Brain 90:497–520PubMedGoogle Scholar
  105. Simke JP, Saelens JK (1977) Evidence for a cholinergic fibre tract connecting the thalamus with the head of the striatum of the rat. Brain Res 126:487–495PubMedGoogle Scholar
  106. Simon JR, Oderfeld-Nowak B, Felten DL, Aprison MH (1981) Distribution of choline acetyltransferase, acetylcholinesterase, muscarinic receptor binding and choline uptake in discrete areas of the rat medula oblongata. Neurochem Res 6:497–505PubMedGoogle Scholar
  107. Stadler H, Nesselhut T (1986) Single and rapid measurement of acetylcholine and choline by HPLC and enzymatic-electrochemical detection. Neurochem Int 9:127–129PubMedGoogle Scholar
  108. Stanton GB, Orr A (1985) [3H]choline labeling of cerebellothalamic neurons with observations on the cerebello-thalamo-parietal pathway in cats. Brain Res 335:237–243PubMedGoogle Scholar
  109. Storm-Mathisen J (1970) Quantitative histochemistry of acetylcholinesterase in rat hippocampal region correlated to histochemical staining. J Neurochem 17:739–750PubMedGoogle Scholar
  110. Storm-Mathisen J (1972) Glutamate decarboxylase in the rat hippocampal region after lesions of the afferent fibre systems. Brain Res 40:215–235PubMedGoogle Scholar
  111. Vickroy TW, Fibiger HC, Roeske WR, Yamamura HI (1984) Reduced density of sodium-dependent [3H]hemicholinum-3 binding sites in the anterior cerebral cortex of rats following chemical destruction of the nucleus basalis magnocellularis. Eur J Pharmacol 102:369–370PubMedGoogle Scholar
  112. Vickroy TW, Roeske WR, Gehlert DR, Wamsley JK, Yamamura HI (1985) Quantitative light microscope autoradiography of [3H]hemicholinum-3 binding sites in the rat central nervous system: a biochemical marker for mapping the distribution of cholinergic nerve terminals. Brain Res 329:368–373PubMedGoogle Scholar
  113. Villani L, Contestabile A, Fonnum F (1983) Autoradiographic labeling of the cholinergic habenulo-interpeduncular projection. Neurosci Lett 42:261–266PubMedGoogle Scholar
  114. Walaas I, Fonnum F (1978) The effect of parenteral glutamate treatment on the localization of neurotransmitters in the mediobasal hypothalamus. Brain Res 153:549–562PubMedGoogle Scholar
  115. Walaas I, Fonnum F (1979 a) The distribution and origin of glutamate decarboxylase and choline acetyltransferase in ventral pallidum and other basal forebrain regions. Brain Res 177:325–336PubMedGoogle Scholar
  116. Walaas I, Fonnum F (1979 b) The effects of surgical and chemical lesions on neurotransmitter candidates in the nucleus accumbens of the rat. Neuroscience 4:209–216PubMedGoogle Scholar
  117. Wenk H, Meyer U, Bigl V (1976) Zur Histochemie cholinerger Systeme in ZNS. II. Topo-chemische und quantitative Veränderungen cholinerger Transmitterenzyme (AChE, ChAc) im olfactorischen System bei Ratten nach Zwischenhirnläsion. Z Mikrosk Anat Forsch 90:940–958PubMedGoogle Scholar
  118. Wenk H, Meyer U, Bigl V (1977) Centrifugal cholinergic connections in the olfactory system of rats. Neuroscience 2:797–800PubMedGoogle Scholar
  119. Wenk H, Bigl V, Meyer U (1980) Cholinergic projection from magnocellular nuclei of the basal forebrain to cortical areas in rats. Brain Res Rev 2:295–316Google Scholar
  120. Yamamura HI, Kuhar MY, Greenberg D, Snyder SH (1974) Muscarinic cholinergic receptor binding: regional distribution in monkey brain. Brain Res 66:541–546Google Scholar
  121. Youngs WM, Nadi NS, Davis BJ, Margolis FL, Macrides F (1979) Evidence for a cholinergic projection to the olfactory bulb from the magnocellular preoptica area. Neurosci Abstr 5:135Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1988

Authors and Affiliations

  • F. Fonnum

There are no affiliations available

Personalised recommendations