Distribution of calbindin-D28k, neuronal nitric oxide synthase, and nicotinamide adenine dinucleotide phosphate diaphorase (NADPH-d) in the lateral nucleus of the sheep amygdaloid complex

Anatomy and Embryology

Volumn 211, Issue 6, 2006, Pages 707-720

  Bombardi, Cristiano ^a   Grandis, Annamaria ^a   Chiocchetti, Roberto ^a   Lucchi, Maria Luisa ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Anatomy; Histochemistry; Immunohistochemistry; Non pyramidal neurons; Temporal lobe

Indexed keywords

CALBINDIN; NEURONAL NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

AMYGDALOID NUCLEUS; ARTICLE; CELL SIZE; CELL STRUCTURE; CELLULAR DISTRIBUTION; ENZYME LOCALIZATION; IMMUNOCOMPETENT CELL; IMMUNOFLUORESCENCE; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; SPINDLE CELL; STATISTICAL SIGNIFICANCE; TEMPORAL LOBE; THALAMUS LATERAL NUCLEUS;

AMYGDALA; ANIMALS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; FEMALE; IMMUNOHISTOCHEMISTRY; MODELS, BIOLOGICAL; NADPH DEHYDROGENASE; NEURONS; NEUROPIL; NITRIC OXIDE SYNTHASE TYPE I; SHEEP; TEMPORAL LOBE; TISSUE DISTRIBUTION;

OVIS ARIES;

EID: 33845367444     PISSN: 03402061     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00429-006-0133-x     Document Type: Article

References (100)

1. Aggleton JP (1992) The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction. Wiley-Liss, New York
2. Aggleton JP (2000) The amygdala: a functional analysis. 2nd edn. Oxford University Press, New York
3. Ahern GP, Klyachko VA, Jackson MB (2002) cGMP and S-nitrosylation: two routes for modulation of neuronal exitability by NO. Trends Neurosci 25:510-517
4. Alheid GF, de Olmos JS, Beltramino CA (1995) Amygdala and extended amygdala. In: Paxinos G (ed) The rat nervous system. Academic, Orlando, pp 495-578
5. Amaral DG, Avendaño C, Benoit R (1989) Distribution of somatostatin-like immunoreactivity in the monkey amygdala. J Comp Neurol 284:294-313
6. Amaral DG, Price JL, Pitkänen A, Garmichael ST (1992) Anatomical organization of the primate amygdaloid complex. In: Aggleton JP (ed) The amygdala. Wiley-Liss, New York, pp 1-66
7. Baimbridge KG, Celio MR, Rogers JH (1992) Calcium binding proteins in the nervous system. Trends Neurosci 15:303-308
8. Bauer EP, LeDoux JE (2004) Heterosynaptic long-term potentiation of inhibitori interneurons in the lateral amygdala. J Neurosci 24:9507-9512
9. Berdel B, Moryś J (2000) Expression of calbindin-D28k and parvalbumin during development of rat's basolateral amygdaloid complex. Int J Dev Neurosci 18:501-513
10. Berger F, Gage FH, Vijayaraghaven S (1998) Nicotinic receptor-induced apoptotic cell death of hippocampal progenitor cells. J Neurosci 18:6871-6881
11. Bertini G, Peng ZC, Bentivoglio M (1996) The chemical heterogeneity of cortical interneurons: nitric oxide synthase vs. calbindin and parvalbumin immunoreactivity in the rat. Brain Res Bull 39:261-266
12. Brady DR, Carey RG, Mufson EJ (1992) Reduced nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d) profiles in the amygdala of human and new world monkey (Saimiri Sciureus). Brain Res 577:236-248
13. Bredt DS, Snyder SH (1989) Nitric oxide mediates glutamate-linked enhancement of cGMP levels in cerebellum. Proc Natl Acad Sci USA 86:9030-9033
14. Bredt DS, Snyder SH (1992) Nitric oxide, a novel neuronal messenger. Neuron 8:3-11
15. 28k, calretinin, and parvalbumin-immunoreactive neurons in the human cerebral cortex. Exp Neurol 182:220-231
16. Carlsen J (1988) Immunocytochemical localization of glutamate decarboxylase in the rat basolateral amygdaloid nucleus, with special reference to GABAercic innervation of amygdalostriatal projection neurons. J Comp Neurol 273:513-526
17. Celio MR (1990) Calbindin-D28k and parvalbumin in the rat nervous system. Neuroscience 35:375-475
18. Chapman PF, Chattarji S (2000) Synaptic plasticity in the amygdala. In: Aggleton JP (ed) The amygdala: a functional analysis. Oxford University Press, New York, pp 117-153
19. 28k. Proc Natl Acad Sci 92:5144-5148
20. Contestabile A, Monti B, Contestabile A, Ciani E (2003) Brain nitric oxide and its dual role in neurodegeneration/neuroprotection: understanding molecular mechanisms to devise drug approaches. Curr Med Chem 10:2147-2174
21. Davis KL, Martin E, Turko IV, Murad F (2001) Novel effects of nitric oxide. Ann Rev Pharmacol Toxicol 41:203-236
22. Dawson VL, Dawson TM (1996) Nitric oxide actions in neurochemistry. Neurochem Int 29:97-110
23. Dawson TM, Bredt DS, Fotuki M, Hwang PM, Snyder SH (1991) Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc Natl Acad Sci USA 88:7797-7801
24. de Olmos JS, Beltramino CA, Alheid G (2004) Amygdala and extended amygdala of the rat: a cytoarchitectonical, fibroarchitectonical, and chemoarchitectonical survey. In: Paxinos G (ed) The rat nervous system, 3rd edn. Academic, San Diego, pp 509-603
25. Dowd DR (1995) Calcium regulation of apoptosis. In: Means AR (ed) Advances in second messenger and phosphoprotein research, vol 30. Raven Press, New York, pp 225-280
26. Dowd DR, MacDonald PN, Komm BS, Haussler MR, Miesfeld RL (1992) Stable expression of the calbindin-D28k complementary DNA interferes with the apoptotic pathway in lymphocytes. Mol Endocrinol 6:1843-1848
27. Dun NJ, Huang R, Dun SL, Förstermann U (1994) Infrequent co-localization of nitric oxide synthase and calcium binding proteins immunoreactivity in rat neocortical neurons. Brain Res 666:289-294
28. Dutar P, Potir B, Lamour Y, Emson PC, Senut MC (1991) Loss of calbindin-D28k immunoreactivity in hippocampal slices from aged rats: a role for calcium? Eur J Neurosci 3:839-849
29. Eleftheriou BE (1972) The neurobiology of the amygdala. Plenum, New York
30. Eyles DW, Mc Grath, Reynolds GP (2002) Neuronal calcium-binding proteins and schizophrenia. Schizophr Res 57:27-34
31. Fuller TA, Russchen FT, Price JL (1987) Sources of presumptive glutamatergic/aspartergic afferents to the rat ventral striatopallidal region. J Comp Neurol 258:317-338
32. Garthwaite J (1991) Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci 14:60-67
33. Garthwaite J, Charles SL, Chess-Williams R (1988) Endothelium-derived relaxing factor release on activation of NMDA receptors suggest role as intercellular messenger in the brain. Nature 336:385-388
34. German DC, Manaye K, Smith WK (1989) Midbrain dopaminergic cell loss in Parkinson's disease: computer visualization. Ann Neurol 26:507-514
35. German DC, Manaye KF, Sonsalla PK, Brooks BA (1992) Midbrain dopaminergic cell loss in Parkinson's disease and MPTP-induced parkinsonism: sparing of calbindin-D28k-containing cells. Ann NY Acad Sci 648:42-62
36. Geula C, Schatz CR, Mesulam MM (1993) Differential localization of NADPH-diaphorase and calbindin-D28k within the cholinergic neurons of the basal forebrain, striatum and brainstem in the rat, monkey, baboon and human. Neuroscience 54:461-476
37. Giraldi-Guimarães A, Tenório F, Brüning G, Mayer B, Mendez-Otero R, Cavalcante LA (1999) Nitric oxide synthase expression in the Opossum superior collicolus: a histochemical, immunohistochemical and biochemical study. Brain Behav Evol 199:303-313
38. Gustafson EL, Card P, Moore RY (1986) Neuropeptide Y localization in the rat amygdaloid complex. J Comp Neurol 251:349-362
39. 2+-binding proteins in human neurodegenerative disorders. TINS 15:259-264
40. Iacopino AM, Christakos S (1990) Specific reduction of calcium-binding protein (28-kilodalton calbindin-D) gene expression in aging and neurodegenerative diseases. Proc Natl Acad Sci USA 87:4078-4082
41. Johnson JL, Sudheimer KD, Davis KK, Winn BM (2002) An atlas of the sheep brain. http://www.brains.rad.msu.edu ; http://www.brainmuseum.org ; http://www.msu.edu/user/brains/sheepatlas/index.html
42. Joo KM, Chung YH, Shin CM, Lee YJ, Cha CI (2004) Region-specific alteration of neuronal nitric oxide synthase (nNOS) expression in the amygdala of the aged rats. Brain Res 999:231-236
43. 28k-deficient mice. Synapse 33:172-180
44. Jouvenceau A, Potier B, Poindessous-Jazat F, Dutar P, Slama A, Epelbaum J, Billard JM (2002) Decrease in calbindin content significantly alters LTP but not NMDA receptor and calcium channel properties. Neuropharmacology 42:444-458
45. 28k immunoreactivity in the rat amygdaloid complex and colocalization with y-aminobutyric acid. J Comp Neurol 426:441-467
46. LeDoux JE (2000) Emotion circuits in the brain. Ann Rev Neuroscience 23:155-184
47. LeDoux JE (2003) The emotional brain, fear, and the amygdala. Cell Mol Neurobiol 23:727-738
48. Lee JE, Ahn CH, Lee JY, Chung ES, Jeon CJ (2004) Nitric oxide and calcium-binding protein-containing neurons in the hamster visual cortex. Mol Cells 18:30-39
49. 28k immunoreactivity from dentate granule cells in human temporall lobe epilepsy. Neuroscience 76:377-385
50. Mascagni F, McDonald AJ (2003) Immunohistochemical characterization of cholecystokinin containing neurons in the rat basolateral amygdala. Brain Res 976:171-184
51. Mattson MP, Rychlik B, Chu C, Christakos S (1991) Evidence for calcium-reducing and excito-protective roles for the calcium-binding protein calbindin-D28k in cultured hippocampal neurons. Neuron 6:41-51
52. McDonald AJ (1982) Neurons of the lateral and basolateral amygdaloid nuclei: a Golgi study in the rat. J Comp Neurol 212:293-312
53. McDonald AJ (1984) Neuronal organization of the lateral and basolateral amygdaloid nuclei in the rat. J Comp Neurol 222:589-606
54. McDonald AJ (1985a) Immunohistochemical identification of gamma-aminobutyric acid containing neurons in the rat basolateral amygdala. Neuroscience Lett 53:203-207
55. McDonald AJ (1985b) Morphology of peptide-containing neurons in the rat basolateral amygdaloid nucleus. Brain Res 338:186-191
56. McDonald AJ (1989) Coexistence of somatostatin with neuropeptide Y, but not with cholecystokinin or vasoactive intestinal peptide, in neuron of the rat amygdala. Brain Res 500:37-45
57. McDonald AJ (1992) Cells types and intrinsic connections of the amygdala. In: Aggleton JP (ed) The amygdala: neurobiological aspects of emotion, memory and mental dysfunction. Wiley-Liss, New York, pp 67-96
58. McDonald AJ (1996) Glutamate and aspartate immunoreactive neurons of rat basolateral amygdala: colocalization of excitatory amino acids and projections to the limbic circuit. J Comp Neurol 365:367-379
59. McDonald AJ (1997) Calbindin-D28k immunoreactivity in the rat amygdala. J Comp Neurol 383:231-244
60. McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Prog Neurobiol 55:257-332
61. McDonald AJ (2003) Is there an amygdala and how far does it extend? An anatomical perspective. Ann NY Acad Sci 285:1-21
62. 28k. Neuroscience 102:413-425
63. McDonald AJ, Mascagni F (2001) Colocalization of calcium-binding proteins and GABA in neurons of the rat basolateral amygdala. Neuroscience 105:681-693
64. McDonald AJ, Mascagni F (2002) Immunohistochemical characterization of somatostatin containing interneurons in the rat basolateral amygdala. Brain Res 943:237-244
65. McDonald AJ, Payne DR, Mascagni F (1993) Identification of putative nitric oxide producing neurons in the rat amygdala using NADPH-diaphorase histochemistry. Neuroscience 52:97-106
66. McDonald AJ, Mascagni F, Augustine JR (1995) Neuropeptide Y and somatostatin-like immunoreactivity in neurons of the monkey amygdala. Neuroscience 66:959-982
67. Meffert MK, Calakos NC, Scheller RH, Schulman H (1996) Nitric oxide modulates synaptic vesicle docking fusion reactions. Neuron 16:1229-1236
68. Millhouse OE, de Olmos J (1983) Neuronal configurations in lateral and basolateral amygdala. Neuroscience 10:1269-1300
69. Mizukawa K, McGeer PL, Vincent SR, McGeer EG (1988) Ultrastructure of reduced nicotinamide adenine dinucleotide phosphate (NADPH) diaphorase-positive neurons in the cat cerebral cortex, amygdala and caudate nucleus. Brain Res 452:286-292
70. Mizukawa K, Vincent S, McGeer PL, McGeer EG (1989) Distribution of reduced-nicotinamide-adenine-dinucleotide-phosphate diaphorase-positive cells and fibers in the cat central nervous system. J Comp Neurol 279:281-311
71. 28k expression. Proc Natl Acad Sci USA 93:8028-8033
72. Moncada S, Higgs R, Furchgott (1997) International Union of Pharmacology Nomenclature in Nitric Oxide Research. Pharmacol Rev 49:137-142
73. Muller JF, Mascagni F, McDonald AJ (2003) Synaptic connections of distinct interneuronal populations in the rat basolateral amygdalar nucleus. J Comp Neurol 456:217-236
74. Nelson RJ, Kriegsfeld LJ, Dawson V, Dawson T (1997) Effects of nitric oxide on neuroendocrine function and behaviour. Front Neuroendocrinol 18:463-491
75. Paré D (2003) Role of the basolateral amygdala in memory consolidation. Prog Neurobiol 70:409-420
76. Paré D, Quirk GJ, LeDoux JE (2004) New vistas on amygdala networks in conditioned fear. J Neurophysiol 92:1-9
77. Phillips RG, Meier TJ, Giuli LC, McLaughlin JR, Ho DY, Sapolsky RM (1999) Calbindin-D28k gene transfer via herpes simplex virus amplicon vector decreases hippocampal damage in vivo following neurotoxic insults. J Neurochem 73:1200-1205
78. Pitkänen A (2000) Connectivity of the rat amygdaloid complex. In: Aggleton JP (ed) The amygdala: a functional analysis. Oxford University Press, New York, pp 31-115
79. Pitkänen 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
80. 28k immunoreactivity in the monkey temporal lobe: the amygdaloid complex. J Comp Neurol 331:199-224
81. Pitkänen A, Amaral DG (1993b) Distribution of parvalbumin- immunoreactive cells and fibers in the monkey temporal lobe: the amygdaloid complex. J Comp Neurol 331:14-36
82. Pitkänen 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
83. Pitkänen A, Kemppainen S (2002) Comparison of the distribution of calcium-binding proteins and intrinsic connectivity in the lateral nucleus of the rat, monkey, and human amygdala. Pharmacol Biochem Behav 71:369-377
84. Pitkänen A, Jolkkonen E, Kemppainen S (2000) Anatomical heterogeneity of the rat amygdaloid complex. Folia Morphol 59:1-23
85. Price JL, Russchen FT, Amaral DG (1987) The limbic region. II: the amygdaloid complex. In: Björklund A, Hökfelt T, Swanson LW (eds) Handbook of chemical neuroanatomy, vol 5. Integrated systems of CNS, Part I. Elsevier, Amsterdam, pp 279-388
86. Rodrigues SM, Schafe GE, LeDoux JE (2004) Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 44:75-91
87. Sah P, Faber ESL, Lopez de Armentia M, Power J (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev 83:803-834
88. Satoh K, Arai R, Ikemoto K, Narita M, Nagai T, Ohshima H, Kitahama K (1995) Distribution of nitric oxide synthase in the central nervous system of Macaca fuscata: subcortical regions. Neuroscience 66:685-696
89. Schafe GE, Rodrigues SM, Schoute AM, LeDoux JE (2002) A role for neuronal nitric oxide synthase (nNOS) in auditory pavlovian fear conditioning. In: SFN 32nd Annual Meeting of Neuroscience, November 2-7, Orlando, FL
90. Schafe GE, Bauer EP, Rosis S, Farb CR, Rodrigues SM, LeDoux JE (2005) Memory consolidation of pavlovian fear conditioning requires nitric oxide signaling in the lateral amygdala. Eur J Neurosci 22:201-211
91. Scharfman HE, Schwartzkroin PA (1989) Protection of dentate hilar cells from prolonged stimulation by intracellular calcium chelation. Science 246:249-262
92. Setzer M, Ulfig N (1999) Differential expression of calbindin and calretinin in the human fetal amygdala. Microsc Res Tech 46:1-17
93. Shetty AK, Turner TA (1995) Intracerebroventriculoar kainic acid administration in adult rat alters hippocampal calbindin and non phosphorylated neurofilament expression. J Comp Neurol 363:581-599
94. Sims KS, Williams RS (1990) The human amygdaloid complex: a cytologic and histochemical atlas using Nissl, myelin, acetylcholinesterase and nicotinamide adenine dinucleotide phosphate diaphorase staining. Neuroscience 36:449-472
95. Smith Y, Paré D (1994) Intra-amygdaloid projections of the lateral nucleus in the cat: PHA-L anterograde labeling combined with post-embedding GABA and glutamate immunocytochemistry. J Comp Neurol 342:232-248
96. Sorvari H, Soininen H, Pitkänen A (1996) Calbindin-D28k- immunoreactive cells and fibres in the human amygdaloid complex. Neuroscience 75:421-443
97. Sorvari H, Miettinen R, Soininen H, Paljärvi L, Karkola K, Pitkänen A (1998) Calretinin-immunoreactive terminals make synapses on calbindin D28k-immunoreactive neurons in the lateral nucleus of the human amygdala. Brain Res 783:355-358
98. Susswein AJ, Katzoff A, Miller N, Hurwitz I (2004) Nitric oxide and memory. Neuroscientist 10:153-162
99. Vincent SR, Kimura H (1992) Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46:755-784
100. Yamada T, McGeer PL, Baibridge KG, McGeer EG (1990) Relative sparing in Parkinson's disease of substantia nigra dopamine neurons containing calbindin-D28k. Brain Res 526:303-307