Distribution of butyrylcholinesterase in the human amygdala and hippocampal formation

Journal of Comparative Neurology

Volumn 393, Issue 3, 1998, Pages 374-390

  Darvesh, S ^a,b   Grantham, D L ^a   Hopkins, D A ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Alzheime's diseaser; Central nervous system; Cholinesterases; Pseudocholinesterase

Indexed keywords

CHOLINESTERASE;

ADULT; AGED; AMYGDALOID NUCLEUS; ARTICLE; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; HIPPOCAMPUS; HISTOCHEMISTRY; HUMAN; HUMAN TISSUE; MALE; NEUROPIL; PRIORITY JOURNAL; TISSUE DISTRIBUTION;

ACETYLCHOLINESTERASE; AGED; AGED, 80 AND OVER; AMYGDALA; BRAIN MAPPING; BUTYRYLCHOLINESTERASE; DENTATE GYRUS; FEMALE; HIPPOCAMPUS; HUMANS; MALE; MIDDLE AGED; ORGAN SPECIFICITY;

EID: 0032513557     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980413)393:3<374::AID-CNE8>3.0.CO;2-Z     Document Type: Article

References (101)

1. Aggleton, J.P. (1992) The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. New York: Wiley-Liss Inc.
2. Amaral, D.G. and R. Insausti (1988) Distribution of somatostatin immunoreactivity in the human dentate gyrus. J. Neurosci. 8:3306-3316.
3. Amaral, D.G. and R. Insausti (1990) Hippocampal formation. In G. Paxinos (ed): The Human Nervous System. San Diego: Academic Press, pp. 711-755.
4. Amaral, D.G., J.L. Price, A. Pitkänen, and S. Thomas (1992) Anatomical organisation of the primate amygdaloid complex. In J.P. Aggleton (ed): The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. New York: Wiley-Liss Inc., pp. 1-66.
5. Appleyard, M.E. (1992) Secreted acetylcholinesterase: Nonclassical aspects of a classic enzyme. Trends Neurosci. 15:485-490.
6. Appleyard, M.E. (1995) Acetylcholinesterase induces long-term potentiation in CA1 pyramidal cells by a mechanism dependent on metabotropic glutamate receptors. Neurosci. Lett. 190:25-28.
7. Arendt, R., V. Bigl, F. Walther, and M. Sonntag (1984) Decreased ratio of CSF cholinesterase to butyrylcholinesterase activity in Alzheimer's disease. Lancet 1:173.
8. Arendt, T., M.K. Brückner, M. Lange, and V. Bigl (1992) Changes in acetylcholinesterase and butyrylcholinesterase in Alzheimer's disease resemble embryonic development: A study of molecular forms. Neurochem. Int. 21:381-396.
9. Bakst, I. and D.G. Amaral (1984) The distribution of acetylcholinesterase in the hippocampal formation of the monkey. J. Comp. Neurol. 225:344-371.
10. Ball, M.J. (1977) Neuronal loss, neurofibrillary tangles, and granulovacuolar degeneration in the hippocampus with aging and dementia. Acta Neuropathol. (Berl.) 36:111-118.
11. Balasubramanian, A.S. and C.D. Bhanumathy (1993) Noncholinergic functions of cholinesterases. FASEB J. 7:1354-1358.
12. Bartus, R.T., R.L.I. Dean, B. Beer, and A.S. Lippa (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217:408-417.
13. Benzing, W.C., E.J. Mufson, and D.M. Armstrong (1993) Immunocytochemical distribution of peptidergic and cholinergic fibers in the human amygdala: Their depletion in Alzheimer's disease and morphologic alteration in nondemented elderly with numerous senile plaques. Brain Res. 625:125-138.
14. Bhatt, D.K. and H.B. Tewari (1978) Histochemical mapping of acetylcholinesterase and butyrylcholinesterase in the medulla oblongata and pons of squirrel (Funambulus palmarum). J. Neurosci. Res. 3:419-439.
15. Bouras, C., P.J. Magistretti, J.H. Morrison, and J. Constantinidis (1987) An immunohistochemical study of pro-somatostatin-derived peptides in the human brain. Neuroscience 22:781-800.
16. Braak, H. (1974) On the structure of the human archicortex: I. The cornu Ammonis. A Golgi and pigment architectonic study. Cell Tissue Res. 152:349-383.
17. Braak, H. and E. Braak (1983) Neuronal subtypes in the basolateral amygdaloid nuclei of man. Brain Res. Bull. 11:349-365.
18. Brockhaus, H. (1938) Zur anatomie des Mendelkerngebietes. J. Psychol. Neurol. 49:1-36.
19. Brockhaus, H. (1940) Die Cyto-und Myeloarchitektonik des Cortex claustralis un des Claustrum beim Menschen. J. Psychol. Neurol. 49:249-348.
20. Cavanagh, J.B., R.H.S. Thompson, and G.R. Webster (1954) The localization of pseudo-cholinesterase activity in nervous tissue. Q. J. Exp. Physiol. 39:185-197.
21. Chan-Palay, V., C. Köhler, U. Haesler, W. Lang, and G. Yasargil (1986) Distribution of neurons and axons immunoreactive with antisera against neuropeptide Y in the normal human hippocampus. J. Comp. Neurol. 248:360-375.
22. Checler, F., J. Grassi, and J.-P. Vincent (1994) Cholinesterases display genuine aryl acylamidase activity but are totally devoid of intrinsic peptidase activities. J. Neurochem. 62:756-763.
23. Chubb, I.W., E. Raniers, G.H. White, and A.J. Godgson (1983) The enkephalins are amongst the peptides hydrolyzed by purified acetylcholinesterase. Neuroscience 10:1369-1377.
24. Coyle, J.T., D.L. Price, and M.R. DeLong (1983) Alzheimer's disease: A disorder of cortical cholinergic innervation. Science 219:1184-1190.
25. Crosby, E.C. and T. Humphrey (1941) Studies of the vertebrate telencephalon: II. The nuclear pattern of the anterior olfactory nucleus tuberculum olfactorium and the amygdaloid complex in adult man. J. Comp. Neurol. 74:309-352.
26. Darvesh, S., A. Smereczynsky, and D.A. Hopkins (1992) Distribution of butyrylcholinesterase in the rat brain. Neurosci. Abstr. 18:1505.
27. Darvesh, S., D. Grantham, and D.A. Hopkins (1996) Distribution of butyrylcholinesterase in normal human forebrain. Neurosci. Abstr. 22:201.
28. De Lacalle, S., C. Lim, T. Sobreviela, E.J. Mufson, L.B. Mufson, and C.B. Saper (1994) Cholinergic innervation in the human hippocampal formation including the entorhinal cortex. J. Comp. Neurol. 345:321-344.
29. de Olmos, J.S. (1990) Amygdala. In G. Paxinos (ed): The Human Nervous System. San Diego: Academic Press, pp. 583-710.
30. Desmedt, J.E. and G. LaGrutta (1957) The effect of selective inhibition of pseudocholinesterase on the spontaneous and evoked activity of the cat's cerebral cortex. J. Physiol. (Lond.) 136:20-40.
31. Foldes, F.F., E.K. Zsigmond, V.M. Foldes, and E.G. Erdös (1962) The distribution of acetylcholinesterase and butyrylcholinesterase in the human brain. J. Neurochem. 9:559-572.
32. Friede, R.L. (1965) Enzyme histochemical studies of senile plaques. J. Neuropathol. Exp. Neurol. 24:477-491.
33. Friede, R.L. (1967) A comparative histochemical mapping of the distribution of butyrylcholinesterase in the brains of four species of mammals including man. Acta Anat. (Basel) 66:161-177.
34. Gallagher, M. and P.J. Colombo (1995) Aging: The cholinergic hypothesis of cognitive decline. Curr. Opin. Neurobiol. 5:161-168.
35. Gatley, S.J. (1991) Activities of the enantiomers of cocaine and some related compounds as substrates and inhibitors of plasma butyrylcholinesterase. Biochem. Pharmacol. 41:1249-1254.
36. George, S.T. and A.S. Balasubramanian (1981) The aryl acylamidases and their relationship to cholinesterases in human serum, erythrocyte and liver. Eur. J. Biochem. 121:177-186.
37. Geula, C. and M.-M. Mesulam (1989) Special properties of cholinesterases in the cerebral cortex of Alzheimer's disease. Brain Res. 498:185-189.
38. Geula C. and M.-M. Mesulam (1995) Cholinesterases and the pathology of Alzheimer disease. Alzheimer Dis. Assoc. Disord. 2:23-28.
39. Giacobini, E., P.L. Griffini, T. Maggi, G. Mascellani, and R. Mandelli (1996) Butyrylcholinesterase: Is it important for cortical acetylcholine regulation? Neurosci. Abstr. 22:203.
40. Graybiel, A.M. and C.W. Ragsdale (1982) Pseudocholinesterase staining in the primary visual pathway of the macaque monkey. Nature 299:439-442.
41. Green, R.C. and M.-M. Mesulam (1988.) Acetylcholinesterase fiber staining in the human hippocampus and parahippocampal gyrus. J. Comp. Neurol. 273:488-499.
42. Greenfield, S.A. (1991) A noncholinergic action of acetylcholinesterase (AChE) in the brain from neuronal secretion to the generation of movement. Cell. Mol. Neurobiol. 11:55-77.
43. Hartz-Shütt, C.G. and J.K. Mai (1991) Cholinesterase-aktivität im menschlichen Striatum unter besonderer Berücksichtigung der Insulae terminales. J. Hirnforsch. 32:317-342.
44. Herzog, A.G. and T.L. Kemper (1980) Amygdaloid changes in aging and dementia. Arch. Neurol. 37:625-629.
45. Hilpert, P. (1928) Der Mandelkern des Menschen: I. Cytoarchitektonik und Faserverbindungen. J. Psychol. Neurol. 36:44-74.
46. Hyman, B.T., G.W. Van Hoesen, A.R. Damasio, and C.L. Barnes (1984) Alzheimer's disease: Cell specific pathology isolates the hippocampal formation. Science 225:1168-1170.
47. Johnston, J.B. (1923) Further contributions to the study of the evolution of the forebrain. J. Comp. Neurol. 35:337-481.
48. Karnovsky, M.J. and L. Roots (1964) A 'direct-coloring' thiocholine method for cholinesterases. J. Histochem. Cytochem. 12:219-232.
49. Kemper, T.L. (1983) Organization of the neuropathology of the amygdala in Alzheimer's disease. Banbury Rep. 15:31-35.
50. Khachaturian, Z.S. (1985) Diagnosis of Alzheimer's disease. Arch. Neurol. 42:1097-1105.
51. Kostovic, I. and P.S. Goldman-Rakic (1983) Transient cholinesterase staining in the mediodorsal nucleus of the thalamus and its connections in the developing human and monkey brain. J. Comp. Neurol. 219:431-447.
52. Kromer Vogt, L.J., B.T. Hyman, G. W. Van Hoesen, and A.R. Damasio (1990) Pathological alterations in the amygdala in Alzheimer's disease. Neuroscience 37:377-385.
53. Lauer, E.W. (1945) The nuclear pattern of fiber connections of certain basal telencephalic centers in the macaque. J. Comp. Neurol. 82:215-254.
54. Lawrence, A.D. and B.J. Sahakian (1995) Alzheimer disease, attention and the cholinergic system. Alzheimer Dis. Assoc. Disord. 9:43-49.
55. Layer, P.G. (1991) Cholinesterases during development of the avian nervous system. Cell. Mol. Neurobiol. 11:7-33.
56. Layer, P.G. (1995) Nonclassic roles of Cholinesterases in the embryonic brain and possible links to Alzheimer disease. Alzheimer Dis. Assoc. Disord. 9:29-36.
57. Lockridge, O. (1982) Substance P hydrolysis by human serum cholinesterase. J. Neurochem. 39:106-110.
58. Lockridge, O., N. Mottershaw-Jackson, H. Eckerson, and B.N. La Du (1980) Hydrolysis of diacetylmorphine (heroin) by human serum cholinesterase. J. Pharmacol. Exp. Ther. 215:1-8.
59. Lorente de Nó, R. (1934) Studies on the structure of the cerebral cortex: II. Continuation of the study of the ammonic system. J. Psychol. Neurol. 46:113-177.
60. Lotstra, F. and J. Vanderhaeghen (1987) Distribution of immunoreactive cholecystokinin in the human hippocampus. Peptides 8:911-920.
61. Mai, J.K., J. Triepel, and J. Metz (1987) Neurotensin in the human brain. Neuroscience 22:499-524.
62. Mellgren, S.I., W. Harkmark, and B. Srebro (1977) Some enzyme histochemical characteristics of the human hippocampus. Cell Tissue Res. 181:459-471.
63. Mesulam, M.-M. and C. Geula (1991) Acetylcholinesterase-rich neurons of the human cerebral cortex: Cytoarchitectonic and ontogenic patterns of distribution. J. Comp. Neurol. 306:193-220.
64. Mesulam, M.-M. and C. Geula (1994) Butyrylcholinesterase reactivity differentiates the amyloid plaques of aging from those of dementia. Ann. Neurol. 36:722-727.
65. Mesulam, M.-M., L.B. Hersh, D.C. Mash, and C. Geula (1992) Differential cholinergic innervation within functional subdivisions of the human cerebral cortex: A choline acetyltransferase study. J. Comp. Neurol. 318:316-328.
66. Michel, J.-P., N. Sakamoto, N. Kopp, and J. Pearson (1986) Neurotensin immunoreaetive structures in the human infant striatum, septum, amygdala and cerebral cortex. Brain Res. 397:93-102.
67. Milner, B. (1970) Memory and the medial temporal regions of the brain. In K.H. Pribram and D.E. Broadbent (eds): Biology of Memory. New York: Academic Press, pp. 29-50.
68. Mirra, S.S., A. Heyman, D. McKeel, S.M. Sumi, B.J. Crain, L.M. Brownlee, F.S. Vogel, J.P. Hughes, G. van Belle, L. Berg, and participating CERAD neuropathologists (1991) The Consortium to Establish a Registry for Alzheimer's Disease (CERAD): Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41:479-486.
69. Mirra, S.S., M.N. Hart, and R.D. Terry (1993) Making the diagnosis of Alzheimer's disease: A primer for practicing pathologists. Arch. Pathol. Lab. Med. 117:132-144.
70. Morán, M.A. and P. Gómez-Ramos (1992) Cholinesterase histochemistry in the human brain: Effect of various fixation and storage conditions. J. Neurosci. Methods 43:49-54.
71. Morán, M.A., E.J. Mufson, and P. Gómez-Ramos (1994) Cholinesterases co-localize with sites of neurofibrillary degeneration in aged and Alzheimer's brains. Acta Neuropathol. (Berl.) 87:284-292.
72. Mufson, E.J., R. Benoit, and M.-M. Mesulam (1988) Immunohistochemical evidence for a possible somatostatin-containing amygdalostriatal pathway in normal and Alzheimer's disease brain. Brain Res. 453:117-128.
73. Nance, D.M. , D.A. Hopkins, and D. Bieger (1987) Re-investigation of the innervation of the thymus gland in mice and rats. Brain Behav. Immun. 1:134-147.
74. Navaratnam, V. and R.P. Lewis (1975) Effects of vagotomy on the distribution of cholinesterases in the cat medulla oblongata. Brain Res. 100:599-613.
75. Nitecka, L. and O. Narkiewicz (1976) Localization of acetylcholinesterase activity in the amygdaloid body of man. Acta Neurobiol. Exp. 36:333-352.
76. Okinaka, S., M. Yoshikawa, M. Uono, T. Muro, T. Mozai, A. Igata, H. Tanabe, S. Ueda, and M. Tomonaga (1961) Distribution of cholinesterase activity in the human cerebral cortex. Am. J. Phys. Med. 40:135-145.
77. Op Den Velde, W. and F.C. Stam (1976) Some cerebral proteins and enzyme systems in Alzheimer's presenile and senile dementia. J. Am. Geriatr. Soc. 24:12-16.
78. Perry, E.K., R.H. Perry, G. Blessed, and E. Tomlinson (1978) Changes in brain Cholinesterases in senile dementia of Alzheimer type. Neuropathol. Appl. Neurobiol. 4:273-277.
79. Price, J.L., F.T. Russchen, and D.G. Amaral (1987) The limbic region: II. The amygdaloid complex. In A. Björklund, T. Hökfelt, and L. W. Swanson (eds): Handbook of Neuroanatomy, Vol. 5, Integrated Systems of the CNS, part I. Amsterdam: Elsevier, pp. 279-381.
80. Ramón y Cajal, S. (1968) The Structure of Ammon's Horn. Springfield, IL: Charles C. Thomas.
81. Ransmayr, G., P. Cervera, E. Hirsch, M. Ruberg, L.B. Hersh, C. Duyckaerts, J.-J. Hauw, C. Delumeau, and Y. Agid (1989) Choline acetyltransferase-like immunoreactivity in the hippocampal formation of control subjects and patients with Alzheimer's disease. Neuroscience 32:701-714.
82. Rao, R.V. and A.S. Balasubramanian (1990) Localization of the peptidase activity of human serum butyrylcholinesterase in a 50-kDa fragment obtained by limited α-chymotrypsin digestion. Eur. J. Biochem. 188:637-643.
83. Robertson, R.T. and F. Mostamand (1988) Development of nonspecific cholinesterase-containing neurons in the dorsal thalamus of the rat. Brain Res. Dev. Brain Res. 41:43-60.
84. Robertson, R.T., C.L. Lieu, K. Lee, and C. Gorenstein (1986) Distribution of 'nonspecific' cholinesterase-containing neurons in the dorsal thalamus of the rat. Brain Res. 368:116-124.
85. Sakamoto, N., J.-P. Michel, N. Kopp, M. Tohyama, and J. Pearson (1987) Substance P- and enkephalin-immunoreactive neurons in the hippocampus and related areas of the human infant brain. Neuroscience 22:801-811.
86. Sethi, J.S. and R.K. Tanwar (1984) Distributive pattern of butyrylcholinesterase in the fore- and mid-brain of the mouse. Cell. Mol. Biol. 30:365-375.
87. Silver, A. (1974) The Biology of Cholinesterases. Amsterdam: Elsevier.
88. Sims, K.S. and R.S. Williams (1990) The human amygdaloid complex: Cytologic and histochemical atlas using Nissl, myelin, acetylcholinesterase and nicotinamide adenine dinucleotide phosphate diaphorase staining. Neuroscience 36:449-472.
89. Small, D.H., S. Michaelson, and G. Sberna (1996) Nonclassic actions of cholinesterases: Role in cellular differentiation, tumorigenesis and Alzheimer's disease. Neurochem. Int. 28:453-483.
90. Soreq, H. and H. Zakut (1993) Human Cholinesterases and Anticholinesterases. San Diego: Academic Press.
91. Squire, L.E., J.G. Ojemann, F.M. Miezin, S.E. Petersen, T.O. Videen, and M.E. Paichle (1992) Activation of the hippocampus in normal humans: A functional anatomical study of memory. Proc. Natl. Acad. Sci. USA 89:1837-1841.
92. Svendsen, C.N. and E.D. Bird (1985) Acetylcholinesterase staining of the human amygdala. Neurosci. Lett. 54:313-318.
93. Tago, H., H. Kimura, and T. Maeda (1986) Visualization of detailed acetylcholinesterase fiber and neuron staining in rat brain by a sensitive histochemical procedure. J. Histochem. Cytochem. 34:1431-1438.
94. Tago, H., T. Maeda, P.L. McGeer, and H. Kimura (1992) Butyrylcholinesterase-rich neurons in rat brain demonstrated by a sensitive histochemical method. J. Comp. Neurol. 325:301-312.
95. Ulrich, J., W. Meier-Ruge, A. Probst, E. Meier, and S. Ipsen (1990) Senile plaques. Staining for acetylcholinesterase and A4 protein: A comparative study in the hippocampus and entorhinal cortex. Acta Neuropathol. (Berl.) 80:624-628.
96. Unger, J.W., T.H. McNeill, L.L. Lapham, and R.W. Hamill (1988) Neuropeptides and neuropathology in the amygdala in Alzheimer's disease: Relationship between somatostatin, neuropeptide Y and regional distribution of neuritic plaques. Brain Res. 452:293-302.
97. Van Hoesen, G.W. and A.R. Damasio (1987) Neural correlates of cognitive impairment in Alzheimer's disease. In F. Plum (ed): Handbook of Physiology, Sect. 1, Vol. V, part 2. Washington, D.C.: American Physiology Society, pp. 871-898.
98. Vigny, M., V. Gisiger, and J. Massoulié (1978) 'Nonspecific' cholinesterase and acetylcholinesterase in rat tissues: Molecular forms, structural and catalytic properties, and significance of the two enzyme systems. Proc. Natl. Acad. Sci. USA 75:2588-2592.
99. Wright, C.I., C. Geula, and M.-M. Mesulam (1993) Neuroglial cholinesterases in the normal brain and in Alzheimer's disease: Relationship to plaques, tangles, and patterns of selective vulnerability. Ann. Neurol. 34:373-384.
100. Zech, M. and B. Bogerts (1985) Methionine-enkephalin and substance P in the basal ganglia of normals, Parkinson patients, Huntington patients, and schizophrenics. A quantitative immunohistochemical study. Acta Neuropathol. (Berl.) 68:32-38.
101. Zech, M., G.W. Roberts, B. Bogerts, T.J. Crow, and J.M. Polak (1986) Neuropeptides in the amygdala of controls, schizophrenics and patients suffering from Huntington's chorea: An immunohistochemical study. Acta Neuropathol. (Berl.) 71:259-266.