Distribution of synaptic zinc in the macaque monkey amygdala

Journal of Comparative Neurology

Volumn 489, Issue 2, 2005, Pages 135-147

  Ichinohe, Noritaka ^a   Rockland, Kathleen S ^a  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Alzheimer's disease; Epilepsy; Gradient; Parvalbumin; Plasticity

Indexed keywords

PARVALBUMIN; ZINC;

ALZHEIMER DISEASE; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ELECTRON MICROSCOPY; HISTOLOGY; MACACA; MONKEY; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; OLIVARY NUCLEUS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SEIZURE; SYNAPSE; THALAMUS INTRALAMINAR NUCLEUS; THALAMUS LATERAL NUCLEUS;

AMYGDALA; ANIMALS; IMMUNOHISTOCHEMISTRY; MACACA MULATTA; MICROSCOPY, ELECTRON; NEURONAL PLASTICITY; PARVALBUMINS; SYNAPSES; ZINC;

EID: 22244455053     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20632     Document Type: Article

References (88)

1. Amaral DG, Bassett JL. 1989. Cholinergic innervation of the monkey amygdala: an immunohistochemical analysis with antisera to choline acetyltransferase. J Comp Neurol 281:337-361.
2. Amaral DG, Price JL. 1984. Amygdalo-cortical projections in the monkey (Macaca fascicularis). J Comp Neurol 230:465-496.
3. Amaral DG, Price JL, Pitkanen A, Carmichael ST. 1992. Anatomical organization of the primate amygdaloid complex. In: Aggleton JP, editor. The amygdala. Neurobiological aspects of emotion, memory, and mental dysfunction. New York: Wiley-Liss. p 1-66.
4. Barbas H, Gustafson EL, Greengard P. 1993. Comparison of the immunocytochemical localization of DARPP-32 and 1-1 in the amygdala and hippocampus of the rhesus monkey. J Comp Neurol. 334:1-18.
5. Bayer SA, Altman J. 1991. Neocortical development. Philadelphia: Lippincott Williams & Wilkins.
6. Brady DR, Mufson EJ. 1990. Amygdaloid pathology in Alzheimer's disease: quantitative and quantitative analysis. Dementia 1:5-17.
7. Brashear HR, Godec MS, Carlsen J. 1988. The distribution of neuritic plaques and acetylcholinesterase staining in the amygdala in Alzheimer's disease. Neurology 38:1694-1699.
8. Bush AI, Pettingell WH, Multhaup G, d Paradis M, Vonsattel JP, Gusella JF, Beyreuther K, Masters CL, Tanzi RE. 1994. Rapid induction of Alzheimer A beta amyloid formation by zinc. Science 265:1464-1467.
9. Casanovas-Aguilar C, Christensen MK, Reblet C, Martinez-Garcia F, Perez-Clausell J, Bueno-Lopez JL. 1995. Callosal neurones give rise to zinc-rich boutons in the rat visual cortex. Neuroreport 6:497-500.
10. Casanovas-Aguilar C, Reblet C, Perez-Clausell J, Bueno-Lopez JL. 1998. Zinc-rich afferents to the rat neocortex: projections to the visual cortex traced with intracerebral selenite injections. J Chem Neuroanat 15:97-109.
11. Casanovas-Aguilar C, Miro-Bernie N, Perez-Clausell J. 2002. Zinc-rich neurones in the rat visual cortex give rise to two laminar segregated systems of connections. Neuroscience 110:445-458.
12. Cheng K, Saleem KS, Tanaka K. 1997. Organization of corticostriatal and corticoamygdalar projections arising from the anterior inferotemporal area TE of the macaque monkey: a Phaseolus vulgaris leucoagglutinin study. J Neurosci 17:7902-7925.
13. Choi DW, Koh JY. 1998. Zinc and brain injury. Annu Rev Neurosci 21: 347-375.
14. Christensen MK, Frederickson CJ. 1998. Zinc-containing afferent projections to the rat corticomedial amygdaloid complex: a retrograde tracing study. J Comp Neurol 400:375-390.
15. Christensen MK, Geneser FA. 1995. Distribution of neurons of origin of zinc-containing projections in the amygdala of the rat. Anat Embryol (Berl) 191:227-237.
16. Christensen MK, Frederickson CJ, Danscher G. 1992. Retrograde tracing of zinc-containing neurons by selenide ions: a survey of seven selenium compounds. J Histochem Cytochem 40:575-579.
17. Cote PY, Levitt P, Parent A. 1996. Limbic system-associated membrane protein (LAMP) in primate amygdala and hippocampus. Hippocampus. 6:483-494.
18. Coulter DA. 2000. Mossy fiber zinc and temporal lobe epilepsy: pathological association with altered "epileptic" gamma-aminobutyric acid A receptors in dentate granule cells. Epilepsia 41 Suppl 6:S96-S99.
19. Crosby EC, Humphrey T. 1941. Studies on 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.
20. Cuajungco MP, Faget KY. 2003. Zinc takes the center stage: its paradoxical role in Alzheimer's disease. Brain Res Brain Res Rev 41:44-56.
21. Cuajungco MP, Lees GJ. 1997. Zinc metabolism in the brain: relevance to human neurodegenerative disorders. Neurobiol Dis 4:137-169.
22. Danscher G, 1996. The autometallographic zinc-sulphide method. A new approach involving in vivo creation of nanometer-sized zinc sulphide crystal lattices in zinc-enriched synaptic and secretory vesicles. Histochem J 28:361-373.
23. Danscher G, Norgaard JO, Baatrup E. 1987. Autometallography: tissue metals demonstrated by a silver enhancement kit. Histochemistry 86: 465-469.
24. Daunais JB, Letchworth SR, Sim-Selley LJ, Smith HR, Childers SR, Porrino LJ. 2001. Functional and anatomical localization of mu opioid receptors in the striatum, amygdala, and extended amygdala of the nonhuman primate. J Comp Neurol 433:471-485.
25. De Biasi S, Bendotti C. 1988. A simplified procedure for the physical development of the sulphide silver method to reveal synaptic zinc in combination with immunocytochemistry at light and electron microscopy. J Neurosci Methods 79:87-96.
26. de Olmos J. 1990. Amygdala. In: Paxinos G, editor. The human nervous system. San Diego: Academic Press, p 583-710.
27. de Olmos J, Alheid GF, Beltramino CA. 1985. Amygdala. In: Paxinos G, editor. The rat nervous system, vol 1. Forebrain and midbrain. Sydney: Academic Press, p 223-334.
28. Esclapez M, Tillakaratne NJ, Tobin AJ, Houser CR. 1993. Comparative localization of mRNAs encoding two forms of glutamic acid decarboxylase with nonradioactive in situ hybridization methods. J Comp Neurol 331:339-362.
29. Frederickson CJ, Klitenick MA, Manton WI, Kirkpatrick JB. 1983. Cytoarchitectonic distribution of zinc in the hippocampus of man and the rat. Brain Res 273:335-339.
30. Frederickson CJ, Rampy BA, Reamy-Rampy S, Howell GA. 1992. Distribution of histochemically reactive zinc in the forebrain of the rat. J Chem Neuroanat 5:521-530.
31. Frederickson CJ, Suh SW, Silva D, Frederickson CJ, Thompson RB. 2000. Importance of zinc in the central nervous system: the zinc-containing neuron. J Nutr 130(58 suppl):1471S-1483S.
32. Friedman B, Price JL. 1984. Fiber systems in the olfactory bulb and cortex: a study in adult and developing rats, using the Timm method with the light and electron microscope. J Comp Neurol 223:88-109.
33. Garrett B, Sorensen JC, Slomianka L. 1992. Fluoro-Gold tracing of zinc-containing afferent connections in the mouse visual cortices. Anat Embryol 185:451-459.
34. Ghashghaei HT, Barbas H. 2001. Neural interaction between the basal forebrain and functionally distinct prefrontal cortices in the rhesus monkey. Neuroscience 103:593-614.
35. Gloor P. 1992. Role of the amygdala in temporal epilepsy. In: Aggleton JP, editor. The amygdala: neurobiolgical aspects of emotion, memory, and mental dysfunction. New York: Wiley-Liss. p 505-538.
36. Haberly LB. 1998. Olfactory cortex. In: Shepherd, editor. The synaptic organization of the brain. New York: Oxford University Press. p 377-416.
37. Hannissian SH, Tejwani GA. 1988. Histidine abolishes the inhibition by zinc of naloxone binding to opioid receptors in rat brain. Neuropharmacology 27:1145-1149.
38. Haug FMS. 1973. Heavy metals in the brain. A light microscope study of the rat with Timm's sulphide silver method. Methodological considerations and cytological and regional staining patterns. Adv Anat Embryol Cell Biol 47:1-71.
39. Hudson LP, Munoz DG, Miller L, McLachlan RS, Girvin JP, Blume WT. 1993. Amygdaloid sclerosis in temporal lobe epilepsy. Ann Neurol 33:622-631.
40. Ichinohe N, Rockland KS. 2003. Zinc-Enriched neural system in the monkey cortex. Sixth IBRO World Congress of Neuroscience Abstract, p 314.
41. Ichinohe N, Rockland KS. 2004a. Region specific micromodularity in the uppermost layers in primate cerebral cortex. Cereb Cortex 14:1173-1184.
42. Ichinohe N, Rockland KS. 2004b. Distribution of vesicular zinc in the monkey amygdala. 4th Forum of European Neuroscience Abstract, p 412.
43. Ichinohe N, Fujiyama F, Kaneko T, Rockland KS. 2003. Honeycomb-like mosaic at the border of layers 1 and 2 in the cerebral cortex. J Neurosci 23:1372-1382.
44. Kordower JH, Piecinski P, Rakic P. 1992. Neurogenesis of the amygdaloid nuclear complex in the rhesus monkey. Brain Res Dev Brain Res 68:9-15.
45. Kotter R, Stephan KE, Palomero-Gallagher N, Geyer S, Schleicher A, Zilles K. 2001. Multimodal characterisation of cortical areas by multivariate analyses of receptor binding and connectivity data. Anat Embryol 204:333-350.
46. Kozin SA, Zirah S, Rebuffat S, Hoa GH, Debey P. 2001. Zinc binding to Alzheimer's Abeta(1-16) peptide results in stable soluble complex. Biochem Biophys Res Commun 285:959-964.
47. Kozma M, Szerdahelyi P, Kasa P. 1981. Histoehemical detection of zinc and copper in various neurons of the central nervous system. Acta Histochem 69:12-17.
48. Lee JY, Mook-Jung I, Koh JY. 1999. Histochemically reactive zinc in plaques of the Swedish mutant beta-amyloid precursor protein transgenic mice. J Neurosci 19:RC10.
49. Lovell MA, Robertson JD, Teesdale WJ, Campbell JL, Markesbery WR. 1998. Copper, iron and zinc in Alzheimer's disease senile plaques. J Neurol Sci 158:47-52.
50. McDonald AJ, Mascagni F. 2001. Colocalization of calcium-binding proteins and GABA in neurons of the rat basolateral amygdala. Neuroscience 105:681-693.
51. Mizukawa K, Tseng IM, Otsuka N. 1989. Quantitative electron microscopic analysis of postnatal development of zinc-positive nerve endings in the rat amygdala using Timm's sulphide silver technique. Dev Brain Res 50:197-203.
52. Nishijo H, Ono T, Nishino H. 1988. Topographic distribution of modality-specific amygdalar neurons in alert monkey. J Neurosci 8:3556-3569.
53. Perez-Clausell J. 1996. Distribution of terminal fields stained for zinc in the neocortex of the rat. J Chem Neuroanat 11:99-111.
54. Perez-Clausell J, Danscher G. 1985. Intravesicular localization of zinc in rat telencephalic boutons. A histochemical study. Brain Res 337:91-98.
55. Peters A, Palay SL, Webster HD. 1991. The fine structure of the nervous system: neurons and their supporting cells. New York: Oxford University Press.
56. Pitkanen A, Amaral DG. 1991. Distribution of reduced nicotinamide adenine dinucleotide phosphate diaphorase (NADPH-d) cells and fibers in the monkey amygdaloid complex. J Comp Neurol 313:326-348.
57. Pitkanen A, Amaral DG. 1993a. Distribution of parvalbumin-immunoreactive cells and fibers in the monkey temporal lobe: the amygdaloid complex. J Comp Neurol 331:37-74.
58. Pitkanen A, Amaral DG. 1993b. Distribution of calbindin-D28k immunoreactivity in the monkey temporal lobe: the amygdaloid complex. J Comp Neurol 331:199-224.
59. Pitkanen A, Amaral DG. 1994. The distribution of GABAergic cells, fibers, and terminals in the monkey amygdaloid complex: an immunohistochemical and in situ hybridization study. J Neurosci 14:2200-2224.
60. Pitkanen A, Amaral DG. 1998. Organization of the intrinsic connections of the monkey amygdaloid complex: projections originating in the lateral nucleus. J Comp Neurol 398:431-458.
61. Pitkanen A, Tuunanen J, Kalviainen R, Partanen K, Salmenpera T. 1998. Amygdala damage in experimental and human temporal lobe epilepsy. Epilepsy Res 32:233-253.
62. Price JL, Amaral DG. 1981. An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J Neurosci 1:1242-1259.
63. Price JL, Russchen FT, Amaral DG. 1987. The limbic region. II: The amygdaloid complex. In: Bjorklund A, Hokfelt T, Swanson LW, editors. Handbook of chemical neuroanatomy, vol 5: Integrated systems of the CNS. Part I. Amsterdam: Elsevier, p 279-388.
64. Rachline J, Perin-Dureau F, Le Goff A, Neyton J, Paoletti P. 2005. The micromolar zinc-binding domain on the NMDA receptor subunit NR2B. J Neurosci 25:308-317.
65. Saunders RC, Rosene DL, Van Hoesen GW. 1988. Comparison of the efferents of the amygdala and the hippocampal formation in the rhesus monkey: II, Reciprocal and non-reciprocal connections. J Comp Neurol 271:185-207.
66. Schwaller B, Tetko IV, Tandon P, Silveira DC, Vreugdenhil M, Henzi T, Potier MC, Celio MR, Villa AE. 2004. Parvalbumin deficiency affects network properties resulting in increased susceptibility to epileptic seizures. Mol Cell Neurosci 25:650-663.
67. Sensi SL, Jeng JM. 2004. Rethinking the excitotoxic ionic milieu: the emerging role of Zn(2+) in ischemic neuronal injury. Curr Mol Med 4:87-111.
68. Slomianka L. 1992. Neurons of origin of zinc-containing pathways and the distribution of zinc-containing boutons in the hippocampal region of the rat. Neuroscience 48:325-352.
69. Slomianka L, Ernst E, Ostergaard K. 1997. Zinc-containing neurons are distinct from GABAergic neurons in the telencephalon of the rat. Anat Embryol (Berl) 195:165-174.
70. 2+ ions: modulators of excitatory and inhibitory synaptic activity. Neuroscientist 10:432-442.
71. Smith Y, Pare JF, Pare D. 1998. Cat intraamygdaloid inhibitory network: ultrastructural organization of parvalbumin-immunoreactive elements. J Comp Neurol 391:164-179.
72. Stefanacci L, Suzuki WA, Amaral DG. 1996. Organization of connections between the amygdaloid complex and the perirhinal and parahippocampal cortices in macaque monkeys. J Comp Neurol 375:552-582.
73. Stefanacci L, Amaral DG. 2000. Topographic organization of cortical inputs to the lateral nucleus of the macaque monkey amygdala: a retrograde tracing study. J Comp Neurol 421:52-79.
74. Stefanacci L, Amaral DG. 2002. Some observations on cortical inputs to the macaque monkey amygdala: an anterograde tracing study. J Comp Neurol 451:301-323.
75. Stengaard-Pedersen K. 1982. Inhibition of enkephalin binding to opiate receptors by zinc ions: possible physiological importance in the brain. Pharmacol Toxicol. 50:213-220.
76. Suh SW, Jensen KB, Jensen MS, Silva DS, Kesslak PJ, Danscher G, Frederickson CJ. 2000. Histochemically-reactive zinc in amyloid plaques, angiopathy, and degenerating neurons of Alzheimer's diseased brains. Brain Res 852:274-278.
77. Swanson LW, Petrovich GD. 1998. What is the amygdala? Trends Neurosci 21:323-331.
78. Szerdahelyi P, Kasa P. 1986. Histochemical demonstration of copper in normal rat brain and spinal cord. Evidence of localization in glial cells. Histochemistry 85:341-347.
79. Takeda A, Minami A, Yamaide R, Oku N. 2004. Involvement of amygdalar extracellular zinc in rat behavior for passive avoidance. Neurosci Lett 358:119-122.
80. Tejwani GA, Hanissian SH. 1990. Modulation of mu, delta and kappa opioid receptors in rat brain by metal ions and histidine. Neuropharmacology. 29:445-452.
81. Tsuchiya K, Kosaka K. 1990. Neuropathological study of the amygdala in presenile Alzheimer's disease. J Neurol Sci 100:165-173.
82. Turner BH, Zimmer J. 1984. The architecture and some of the interconnections of the rat's amygdala and lateral periallocortex. J Comp Neurol 227:540-557.
83. Wolf HK, Aliashkevich AF, Blumcke I, Wiestler OD, Zentner J. 1997. Neuronal loss and gliosis of the amygdaloid nucleus in temporal lobe epilepsy. A quantitative analysis of 70 surgical specimens. Acta Neuropathol (Berl) 93:606-610.
84. Woodroofe CC, Masalha R, Barnes KR, Frederickson CJ, Lippard SJ. 2004. Membrane-permeable and -impermeable sensors of the Zinpyr family and their application to imaging of hippocampal zinc in vivo. Chem Biol 11:1659-1666.
85. Yilmazer-Hanke DM, Wolf HK, Schramm J, Elger CE, Wiestler OD, Blumcke I. 2000. Subregional pathology of the amygdala complex and entorhinal region in surgical specimens from patients with pharmacoresistant temporal lobe epilepsy. J Neuropathol Exp Neurol 59:907-920.
86. Yoshiike Y, Tanemura K, Murayama O, Akagi T, Murayama M, Sato S, Sun X, Tanaka N, Takashima A. 2001. New insights on how metals disrupt amyloid beta-aggregation and their effects on amyloid-beta cytotoxicity. J Biol Chem 276:32293-32299.
87. Yu S, Iwatsuki H, Ichinohe N, Mori F, Shoumura K. 2001. "In vivo perfusion Turnbull's reaction' for Fe(II) histochemistry in non-anoxic/non- ischemic and anoxic/ischemic cat brains. Neurosci Lett 308:79-82.
88. Yukie M. 2002. Connections between the amygdala and auditory cortical areas in the macaque monkey. Neurosci Res 42:219-229.