Distribution of the parvalbumin, calbindin-D28K and calretinin immunoreactivity in globus pallidus of the Brazilian short-tailed opossum (Monodelphis domestica)

Acta Neurobiologiae Experimentalis

Volumn 67, Issue 4, 2007, Pages 421-438

  Domaradzka Pytel, Beata ^a   Majak, Katarzyna ^a   Spodnik, Jan ^a   Olkowicz, Seweryn ^b   Turlejski, Krzysztof ^b   Djavadian, Ruzanna L ^b   Moryś, Janusz ^a  

^a MEDICAL UNIVERSITY OF GDANSK   (Poland)

^b NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

Author keywords

Calbindin; Calretinin; Confocal microscopy; Globus pallidus; Marsupials; Monodelphis; Parvalbumin

Indexed keywords

CALBINDIN; CALRETININ; PARVALBUMIN;

ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GLOBUS PALLIDUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MONODELPHIS DOMESTICA; NERVE CELL; NONHUMAN; OPOSSUM; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ANIMALS; ANTIBODIES; BRAZIL; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CALCIUM-BINDING PROTEINS; FEMALE; GLOBUS PALLIDUS; IMMUNOHISTOCHEMISTRY; MALE; MONODELPHIS; NEURAL PATHWAYS; NEURONS; PARVALBUMINS; SPECIES SPECIFICITY;

EID: 38149063759     PISSN: 00651400     EISSN: 00651400     Source Type: Journal    
DOI: None     Document Type: Article

References (94)

1. Adams I, Brauer K, Arelin C, Hartig W, Fine A, Mader M, Arendt T, Bruckner G (2001) Perineuronal nets in the rhesus monkey and human basal forebrain including basal ganglia. Neuroscience 108: 285-298.
2. Badowska-Szalewska E, Klejbor I, Ludkiewicz B, Morys J (2005) Analysis of calretinin immunoreactiviry in the rat piriform cortex after open field stress during postnatal maturation. Folia Morphol (Warsz) 64: 33-40.
3. Baimbridge KG, Celio MR, Rogers JH (1992) Calcium-binding proteins in the nervous system. Trends Neurosci 15: 303-308.
4. Bano D, Nicotera P (2007) Ca2+ signals and neuronal death in brain ischemia. Stroke 38: 674-676.
5. Barker DA, Dreher B (1998) Spatiotemporal patterns of ontogenetic expression of parvalbumin in the superior colliculi of rats and rabbits. J Comp Neurol 393: 210-30.
6. Beck PD, Pospichal MW, Kaas JH (1996) Topography, architecture, and connections of somatosensory cortex in opossums: evidence for five somatosensory areas. J Comp Neurol 366: 109-133.
7. Bevan MD, Booth PA, Eaton SA, Bolam JP (1998) Selective innervation of neostriatal intemeurons by a subclass of neuron in the globus pallidus of the rat. J Neurosci 18: 9438-9452.
8. Bodian D (1940) Studies on the diencephalons of the Virginia opossum. II. The fiber connections in normal and experimental material. J Comp Neurol 72: 207-297.
9. Burgoyne RD (2007) Neuronal calcium sensor proteins: generating diversity in neuronal Ca2+ signalling. Nat Rev Neurosci 8: 182-193.
10. Calder AJ, Beaver JD, Davis MH, van Ditzhuijzen J, Keane J, Lawrence AD (2007) Disgust sensitivity predicts the insula and pallidal response to pictures of disgusting foods. Eur J Neurosci 25: 3422-3428.
11. Celio MR (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35: 375-475.
12. Chang HT, Wilson CJ, Kitai ST (1981) Single neostriatal efferent axons in the globus pallidus: A light and electron microscopic study. Science 213: 915-918.
13. Cheng G, Marotte LR, Ashwell KW (2003) Cyto-and chemoarchitecture of the hypothalamus of a wallaby (Macropus eugenii) with special emphasis on oxytocin and vasopressinergic neurons. Anat Embryol (Berl) 207: 233-253.
14. Cooper AJ, Stanford IM (2000) Electrophysiological and morphological characteristics of three subtypes of rat globus pallidus neurone in vitro. J.Physiol 527 Pt 2: 291-304.
15. Cooper AJ, Stanford IM (2002) Calbindin D-28k positive projection neurones and calretinin positive interneurones of the rat globus pallidus. Brain Res. 929: 243-251.
16. Cote PY, Sadikot AF, Parent A (1991) Complementary distribution of calbindin D-28k and parvalbumin in the basal forebrain and midbrain of the squirrel monkey. Eur J Neurosci 3: 1316-1329.
17. Cote PY, Levitt P, Parent A (1995) Distribution of limbic system-associated membrane protein immunoreactivity in primate basal ganglia. Neuroscience 69: 71-81.
18. Danscher G (1981) Histochemical demonstration of heavy metals. A revised version of the sulphide silver method suitable for both light and electronmicroscopy. Histochemistry 71: 1-16.
19. Difiglia M, Rafols JA (1988) Synaptic organization of the globus pallidus. J Electron Microsc Tech 10: 247-263.
20. Difiglia M, Pasik P, Pasik T (1982) A Golgi and ultrastructural study of the monkey globus pallidus. J Comp Neurol 212: 53-75.
21. Dino MR, Willard FH, Mugnaini E (1999) Distribution of unipolar brush cells and other calretinin immunoreactive components in the mammalian cerebellar cortex. J Neurocytol 28: 99-123.
22. Djavadian R, Bisti S, Maccarone R, Bartkowska K, Turlejski K (2006) Development and plasticity of the retina in the opossum Monodelphis domestica. Acta Neurobiol Exp (Wars) 66: 179-188.
23. FitzGibbon T, Solomon SG, Goodchild AK (2000) Distribution of calbindin, parvalbumin, and calretinin immunoreactivity in the reticular thalamic nucleus of the marmoset: evidence for a medial leaflet of incertal neurons. Exp Neurol 164: 371-383.
24. Fortin M, Parent A (1994) Calretinin labels a specific neuronal subpopulation in primate globus pallidus. Neuroreport 5: 2097-2100.
25. Frost SB, Milliken GW, Plautz EJ, Masterton RB, Nudo RJ (2000) Somatosensory and motor representations in cerebral cortex of a primitive mammal (Monodelphis domestica): a window into the early evolution of sensorimotor cortex. J Comp Neurol 421: 29-51.
26. Gerfen CR (2004) Basal ganglia. In: The Rat Nervous System (Third Edition). Elsevier, Academic Press, Amsterdam, pp. 455-508.
27. Gerfen CR, Baimbridge KG, Miller JJ (1985) The neostriatal mosaic: Compartmental distribution of calcium-binding protein and parvalbumin in the basal ganglia of the rat and monkey. Proc Natl Acad Sci U S A 82: 8780-8784.
28. Grove EA, Domesick VB, Nauta WJH (1986). Light microscopic evidence of striatal input to intrapallidal neurons of cholinergic cell group Ch4 in the rat: A study employing the anterograde tracer Phaseolus vulgaris leucagglutinin (PHA-L). Brain Res 367: 379-384.
29. Haber SN, Groenewegen HJ, Grove EA, Nauta WJ (1985). Efferent connections of the ventral pallidum: evidence of a dual striato pallidofugal pathway. J Comp Neurol 235: 322-335.
30. Haber SN, Lynd-Balta E, Mitchell SJ (1993) The organization of the descending ventral pallidal projections in the monkey J Comp Neurol 329: 111-128.
31. Hamel EG Jr (1966) A study of the hippocampal formation in the opossum, Didelphis virginiana. In: Evolution of the Forebrain (Hassler R, Stephan H, Eds). Georg Thieme Verlag, Stuttgart, pp. 81-91.
32. Hardman CD, Henderson JM, Finkelstein DI, Horne MK, Paxinos G, Halliday GM (2002) Comparison of the basal ganglia in rats, marmosets, macaques, baboons, and humans: volume and neuronal number for the output, internal relay, and striatal modulating nuclei. J Comp Neurol 445: 238-255.
33. Heath CJ, Jones EG (1971) Interhemispheric pathways in the absence of a corpus callosum. An experimental study of commissural connexions in the marsupial phalanger. J Anat 109: 253-270.
34. Heizmann CW, Braun K (1992) Changes in Ca(2+)-binding proteins in human neurodegenerative disorders. Trends Neurosci 15: 259-264.
35. Hof PR, Glezer II, Conde F, Flagg RA, Rubin MB, Nimchinsky EA, Vogt Weisenhorn DM (1999) Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns. J Chem Neuroanat 16: 77-116.
36. Hontanilla B, Parent A, de las HS, Gimenez-Amaya JM (1998) Distribution of calbindin D-28k and parvalbumin neurons and fibers in the rat basal ganglia. Brain Res Bull 47: 107-116.
37. Hooks MS, Kalivas PW (1995) The role of mesoaccumbenspallidal circuitry in novelty-induced behavioral activation. Neuroscience 64: 587-597.
38. Hoover BR, Marshall JF (2002) Further characterization of preproenkephalin mRNA-containing cells in the rodent globus pallidus. Neuroscience 111: 111-125.
39. Ingham CA, Bolam JP, Wainer BH, Smith AD (1985) A correlated light and electron microscopic study of identified cholinergic basal forebrain neurons that project to the cortex in the rat. J Comp Neurol 239: 176-192.
40. Iwahori N, Mizuno N (1981) A Golgi study on the globus pallidus of the mouse. J Comp Neurol 197: 29-43.
41. Jia C, Halpern M (2004) Calbindin D28k, parvalbumin, and calretinin immunoreactivity in the main and accessory olfactory bulbs of the gray short-tailed opossum, Monodelphis domestica. J Morphol 259: 271-280.
42. Jones EG (2007) The Thalamus (2nd ed.) Cambridge University Press, Cambridge, UK.
43. Kalanithi PS, Zheng W, Kataoka Y, DiFiglia M, Grantz H, Saper CB, Schwartz ML, Leckman JF, Vaccarino FM (2005) Altered parvalbumin-positive neuron distribution in basal ganglia of individuals with Tourette syndrome. Proc Natl Acad Sci U S A 102: 13307-13312.
44. Kalivas PW, Churchill L, Romanides A (1999) Involvement of the pallidal-thalamocortical circuit in adaptive behavior. Ann N Y Acad Sci 877: 64-70.
45. Karlen SJ, Krubitzer L (2006) Phenotypic diversity is the cornerstone of evolution: variation in cortical field size within short-tailed opossums. J Comp Neurol 499: 990-999.
46. Karlen SJ, Krubitzer L (2007) The functional and anatomical organization of marsupial neocortex: Evidence for parallel evolution across mammals. Prog Neurobiol 82: 122-141.
47. Kawaguchi Y, Wilson CJ, Augood SJ, Emson PC (1995) Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 18: 527-535. [Erratum in Trends Neurosci 19: 143.]
48. Kincaid AE, Penney JB Jr, Young AB, Newman SW (1991) Evidence for a projection from the globus pallidus to the entopeduncular nucleus in the rat. Neurosci Lett 128: 121-125.
49. Kita H (2007) Globus pallidus external segment. Prog Brain Res 160: 111-133.
50. Kita H, Kita T (2001) Number, origins, and chemical types of rat pallidostriatal projection neurons. J Comp Neurol 437: 438-448.
51. Kita H, Kitai ST (1987) Efferent projections of the subthalamic nucleus in the rat: Light and electron microscopic analysis with the PHA-L method. J Comp Neurol 260: 435-452.
52. Kita H, Kitai ST (1991) Intracellular study of rat globus pallidus neurons: membrane properties and responses to neostriatal, subthalamic and nigral stimulation. Brain Res 564: 296-305.
53. Kita H, Kitai ST (1994) The morphology of globus pallidus projection neurons in the rat: an intracellular staining study. Brain Res 636: 308-319.
54. Krause WJ, Saunders NR (1994) Brain growth and neocortical development in the opossum. Ann Anat 176:395-407.
55. Lende RA (1963a) Sensory representation in the cerebral cortex of the opossum (Didelphis virginiana). J Comp Neurol 121: 395-403.
56. Lende RA (1963b) Motor representation in the cerebral cortex of the opossum (Didelphis virginiana). J Comp Neurol 121: 405-415.
57. Levesque M, Bedard A, Cossette M, Parent A (2003) Novel aspects of the chemical anatomy of the striatum and its efferents projections. J Chem Neuroanat 26: 271-281.
58. Loo YT (1930) The forebrain of the opossum, Didelphis virginiana. Part I. Gross anatomy. J Comp Neurol 51: 13-64.
59. Loo YT (1931) The forebrain of the opossum, Didelphis virginiana. Part II. Histology. J Comp Neurol 52: 1-148.
60. Martin GF Jr, Hamel EG Jr (1967) The striatum of the opossum, Didelphis virginiana. Description and experimental studies. J Comp Neurol 131: 491-516.
61. Mattson MP (2007) Calcium and neurodegeneration. Aging Cell 6: 337-350.
62. Maurice N, Deniau JM, Menetrey A, Glowinski J, Thierry AM (1997) Position of the ventral pallidum in the rat prefrontal cortex-basal ganglia circuit. Neuroscience 80: 523-534.
63. Mickle JP (1976) Efferent connections of the caudate nucleus in the Virginia opossum. J Comp Neurol 166: 373-385.
64. Mikula S, Manger PR, Jones EG (2007) The thalamus of the monotremes: cyto- and myeloarchitecture and chemical neuroanatomy. Phil Trans R Soc B (Epub ahead of print May 19, 2007).
65. Millhouse OE (1986) Pallidal neurons in the rat. J Comp Neurol 254: 209-227.
66. Morel A, Loup F, Magnin M, Jeanmonod D (2002) Neurochemical organization of the human basal ganglia: anatomofunctional territories defined by the distributions of calcium-binding proteins and SM1-32. J Comp Neurol 443: 86-103.
67. Moriizumi T, Hattori T (1992) Ultrastructural morphology of projections from the medial geniculate nucleus and its adjacent region to the basal ganglia. Brain Res Bull 29: 193-198.
68. Naito A, Kita H (1994) The cortico-pallidal projection in the rat: an anterograde tracing study with biotinylated dextran amine. Brain Res 653: 251-257.
69. Nambu A (2007) Globus pallidus internal segment. Prog Brain Res 160: 135-150.
70. Nambu A, Llinas R (1994) Electrophysiology of globus pallidus neurons in vitro. J Neurophysiol 72: 1127-1139.
71. Nambu A, Llinas R (1997) Morphology of globus pallidus neurones: its correlation with electrophysiology in guinea pig brain slices. J Comp Neurol 377: 85-94.
72. Oswaldo-Cruz E, Rocha-Miranda CE (1968) The Brain of the Opossum (Didelphis marsupialis): A Cytoarchitectonic Atlas in Stereotaxic Coordinates. Instituto de Biofisica Universida de Federal do Rio de Janeiro, pp. 1-99.
73. Paxinos G, Watson C (1998) The Rat Brain in Stereotaxic Coordinates, 4th Edition. Academic Press, San Diego, CA.
74. Parent A, Hazrati LN (1994) Multiple striatal representation in primate substantia nigra. J Comp Neurol 344: 305-320.
75. Parent A, Fortin M, Cote PY, Cicchetti F (1996) Calcium-binding proteins in primate basal ganglia. Neurosci Res 25: 309-334.
76. Park MR, Falls WM, Kitai ST (1982) An intracellular HRP study of the rat globus pallidus. I. Responses and light microscopic analysis. J Comp Neurol 211: 284-294.
77. Pilleri G (1962) On the fine structure and comparative anatomy of the corpus striatum of primitive marsupials and rodents (in German). Acta Anat (Basel) 48: 347-367.
78. Pubols BH, Jr., Pubols LM, DiPette DJ, Sheely JC (1976) Opossum somatic sensory cortex: a microelectrode mapping study. J Comp Neurol 165: 229-245.
79. Rajakumar N, Rushlow W, Naus CC, Elisevich K, Flumerfelt BA (1994) Neurochemical compartmentalization of the globus pallidus in the rat: an immunocytochemical study of calcium-binding proteins. J Comp Neurol 346: 337-348.
80. Resibois A, Rogers JH (1992) Calretinin in rat brain: an immunohistochemical study. Neuroscience 46: 101-134.
81. Rowe MH, Wilson PD, Rapaport DH (1981) Conduction of velocity groups in the optic nerve of the North American opossum (Didelphis virginiana): retinal origins and central projections. J.Comp Neurol 199: 481-493.
82. Sadek AR, Magill PJ, Bolam JP (2007) A single-cell analysis of intrinsic connectivity in the rat globus pallidus. J Neurosci 27: 6352-6362.
83. Saunders NR, Adam E, Reader M, Mollgard K (1989) Monodelphis domestica (grey short-tailed opossum): an accessible model for studies of early neocortical development. Anat Embryol (Berl) 180: 227-236.
84. Schnitzlein HN, Hamel EG Jr, Carey JH, Brown JW, Hoffman HH, Faucette JR, Showers MJ (1973) The interrelations of the striatum with subcortical areas through the lateral forebrain bundle. J Hirnforsch 13: 409-455.
85. Shammah-Lagnado SJ, Alheid GF, Heimer L (1996) Efferent connections of the caudal part of the globus pallidus in the rat. J Comp Neurol 376: 489-507.
86. Smith Y, Bolam JP (1989) Neurons of the substantia nigra reticulata receive a dense GABA-containing input from the globus pallidus in the rat. Brain Res 493: 160-167.
87. Standaert DG, Landwehrmeyer GB, Kerner JA, Penney JB, Jr., Young AB (1996) Expression of NMDAR2D glutamate receptor subunit mRNA in neurochemically identified interneurons in the rat neostriatum, neocortex and hippocampus. Mol.Brain Res 42: 89-102.
88. Stepniewska I, Preuss TM, Kaas JH (2007) Thalamic connections of the dorsal and ventral premotor areas in New World owl monkeys. Neuroscience 147: 727-745.
89. Tsai C (1925) The optic tracts and centers of the opossum, Didelphis virginiana. J Comp Neurol 39: 173-216.
90. Waldvogel HJ, Kubota Y, Fritschy J, Mohler H, Faull RL (1999) Regional and cellular localisation of GABA(A) receptor subunits in the human basal ganglia: An autoradiographic and immunohistochemical study. J Comp Neurol 415: 313-340.
91. Waldvogel HJ, Billinton A, White JH, Emson PC, Faull RL (2004) Comparative cellular distribution of GABAA and GABAB receptors in the human basal ganglia: immunohistochemical colocalization of the alpha 1 subunit of the GABAA receptor, and the GABABR1 and GABABR2 receptor subunits. J Comp Neurol 470: 339-356.
92. Wojcik S, Dziewiatkowski J, Klejbor I, Spodnik JH, Kowianski P, Morys J (2006) The anatomical relationships between the serotonergic afferents and the neurons containing calcium-binding proteins in the rat claustrum. Acta Neurobiol Exp (Wars) 66: 33-42.
93. Xue Y, Chen L, Cui QL, Xie JX, Yung WH (2007) Electrophysiological and behavioral effects of neurotensin in rat globus pallidus: an in vivo study. Exp Neurol 205: 108-115.
94. Zold CL, Larramendy C, Riquelme LA, Murer MG (2007) Distinct changes in evoked and resting globus pallidus activity in early and late Parkinson's disease experimental models. Eur J Neurosci 26: 1267-1279.