Development of neurons and fibers containing calcium binding proteins in the pallial amygdala of mouse, with special emphasis on those of the basolateral amygdalar complex

Journal of Comparative Neurology

Volumn 488, Issue 4, 2005, Pages 492-513

  Legaz, Isabel ^a   Olmos, Luis ^b   Real, M Ángeles ^b   Guirado, Salvador ^b   Dávila, José Carlos ^b   Medina, Loreta ^a  

^a UNIVERSITY OF MURCIA   (Spain)

^b UNIVERSITY OF MÁLAGA   (Spain)

Author keywords

Calbindin; Calretinin; GABA; Interneurons; Parvalbumin; Tangential migration

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CALBINDIN; CALCIUM BINDING PROTEIN; CALRETININ; PARVALBUMIN;

ADOLESCENT; AMYGDALOID NUCLEUS; ARTICLE; BRAIN DEVELOPMENT; EMBRYO; ENTOPEDUNCULAR NUCLEUS; FEMALE; IMMUNOCOMPETENT CELL; MOUSE; NERVE FIBER GROWTH; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

AMYGDALA; ANIMALS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CALCIUM-BINDING PROTEINS; GLOBUS PALLIDUS; INTERNEURONS; MICE; NERVE FIBERS; NEURONS; PARVALBUMINS;

EID: 21644486330     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20608     Document Type: Article

References (92)

1. Adolph R, Tranel D, Damasio H, Damasio A. 1994. Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 372:669-672.
2. Aggleton JP. 2000. The amygdala: a functional análisis, 2nd ed. Oxford: Oxford University Press.
3. Alcantara S, Ferrer I. 1995. Postnatal development of calbindin-D28k immunoreactivity in the cerebral cortex of the cat. Anat Embryol 192: 369-384.
4. Alcantara S, de Lecea L, Del Rio JA, Ferrer I, Soriano E. 1996a. Transient colocalization of parvalbumin and calbindin D28k in the postnatal cerebral cortex: evidence for a phenotypic shift in developing nonpyramidal neurons. Eur J Neurosci 8:1329-1339.
5. Alcantara S, Soriano E, Ferrer I. 1996b. Thalamic and basal forebrain afferents modulate the development of parvalbumin and calbindin D28k immunoreactivity in the barrel cortex of the rat. Eur J Neurosci 8:1522-1534.
6. Alheid GF, de Olmos J, Beltramino CA. 1995. Amygdala and extended amygdala. In: Paxinos G, editor. The rat nervous system. San Diego: Academic Press. p 495-578.
7. Amaral DG, Price JL, Pitkänen 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.
8. Anderson SA, Eisenstat DD, Shi L, Rubenstein JLR. 1997. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474-476.
9. Anderson SA, Marín O, Horn C, Jennings K, Rubenstein JLR. 2001. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128:353-363.
10. Ben-Ari Y, Khalilov I, Represa A, Gozlan H. 2004. Interneurons set the tune of developing networks. Trends Neurosci 27:422-427.
11. Berdel B, Morys J. 2000. Expression of calbindin-D28k and parvalbumin during development of rat's basolateral amygdaloid complex. Int J Dev Neurosci 18:501-513.
12. Berger B, Alvarez C. 1996. Neurochemical development of the hippocampal region in the fetal rhesus monkey, III: calbindin-D28k, calretinin and parvalbumin with special mention of Cajal-Retzius cells and the retrosplenial cortex. J Comp Neurol 366:674-699.
13. Bishop KM, Goudreau G, O'Leary DD. 2000. Regulation of area identity in the mammalian neocortex by Emx2 and Pax6. Science 14:344-349.
14. Bulfone A, Puelles L, Porteus MH, Frohman MA, Martin GR, Rubenstein JLR. 1993. Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries. J Neurosci 13:3155-3172.
15. Bulfone A, Smiga SM, Shimamura K, Peterson A, Puelles L, Rubenstein JLR. 1995. T-Brain-1: a homolog of Brachyury whose expression defines molecularly distinct domains within the cerebral cortex. Neuron 15:63-78.
16. Celio MR. 1990. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375-475.
17. Davila JC, Real MA, Olmos L, Legaz I, Medina L, Guirado S. 2005. Embryonic and postnatal development of GABA, calbindin, calretinin, and parvalbumin in the mouse claustral complex. J Comp Neurol 481:42-57.
18. Davis M. 2000. The role of the amygdala in conditioned and unconditioned fear and anxiety. In: Aggleton JP, editor. The amygdala: a functional análisis, 2nd ed. Oxford: Oxford University Press. p 213-287.
19. Del Rio JA, Martínez A, Auladell C, Soriano E. 2000. Developmental history of the subplate and developing white matter in the murine neocortex. Neonatal organization and relationship with the main afferent systems at embryonic and perinatal stages. Cereb Cortex 10: 784-801.
20. Enderlin S, Norman AW, Celio MR. 1987. Ontogeny of the calcium binding protein calbindin D-28k in the rat nervous system. Anat Embryol 177:15-28.
21. File SE. 2000. The amygdala: anxiety and benzodiazepines. In: Aggleton JP, editor. The amygdala: a functional análisis, 2nd ed. Oxford: Oxford University Press. p 195-212.
22. Foster GA. 1998. Chemical neuroanatomy of the prenatal rat brain. A developmental atlas. Oxford: Oxford University Press.
23. Friauf E. 1994. Distribution of calcium-binding protein calbindin-D28k in the auditory system of adult and developing rats. J Comp Neurol 349:193-211.
24. Gallagher M. 2000. The amygdala and associative learning. In: Aggleton JP, editor. The amygdala: a functional analisis, 2nd ed. Oxford: Oxford University Press. p 311-329.
25. Gao WJ, Wormington AB, Newman DE, Pallas SL. 2000. Development of inhibitory circuitry in visual and auditory cortex of postnatal ferrets: immunohistochemical localization of calbindin- and parvalbumin-containing neurons. J Comp Neurol 422:140-157.
26. Gonzalez G, Puelles L, Medina L. 2002. Organization of the mouse dorsal thalamus based on topology, calretinin immnunostaining, and gene expression. Brain Res Bull 57:439-442.
27. Grateron L, Cebada-Sanchez S, Marcos P, Mohedano-Moriano A, Insausti AM, Munoz M, Arroyo-Jimenez MM, Martinez-Marcos A, Artacho-Perula E, Blaizot X, Insausti R. 2003. Postnatal development of calcium-binding proteins immunoreactivity (parvalbumin, calbindin, calretinin) in the human entorhinal cortex. J Chem Neuroanat 26:311-316.
28. Heizmann CW. 1984. Parvalbumin, an intracellular calcium.binding protein: distribution, properties and possible roles in mammalian cells. Experientia 40:910-921.
29. Heizmann CW. 1992. Calcium-binding proteins: bsic concepts and clinical implications. Gen Physiol Biophys 11:411-425.
30. Hogan D, Berman NE. 1994. The development of parvalbumin and calbindin-D28k immunoreactive interneurons in kitten visual cortical areas. Brain Res Dev Brain Res 77:1-21.
31. Holmgren N. 1925. Points of view concerning forebrain morphology in higher vertebrates. Acta Zool 6:413-477.
32. Jacobowitz DM, Abbott LC. 1997. Chemoarchitectonic atlas of the developing mouse brain. Boca Raton: CRC Press.
33. Jimenez D, Lopez-Mascaraque LM, Valverde F, De Carlos JA. 2002. Tangential migration in neocortical development. Dev Biol 244:155-169.
34. Jimenez D, Rivera R, Lopez-Mascaraque L, De Carlos JA. 2003. Origin of the cortical layer I in rodents. Dev Neurosci 25:105-115.
35. 2+ binding proteins and synaptic plasticity. Neurosci Res 16:1-7.
36. Kemppainen S, Pitkänen A. 2000. Distribution of parvalbumin, calretinin, and calbindin-D28k immunoreactivity in the rat amygdaloid complex and colocalization with γ-aminobutyric acid. J Comp Neurol 426:441-467.
37. Korematsu K, Redies C. 1997. Expression of cadherin-8 mRNA in the developing mouse central nervous system. J Comp Neurol 387:291-306.
38. LeDoux JE. 1992. Emotion and the amygdala. In: Aggleton JP, editor. The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction. New York: Wiley-Liss. p 339-352.
39. LeDoux J. 2000. The amygdala and emotion: a view through fear. In: Aggleton JP, editor. The amygdala: a functional análisis, 2nd ed. Oxford: Oxford University Press. p 289-310.
40. LeDoux JE, Farb C, Ruggiero DA. 1990. Topographic organization of neurons in the acoustic thalamus that project to the amygdala. J Neurosci 4:1043-1054.
41. Legaz I, García-López M, Medina L. 2005. Subpallial origin of part of the calbindin-positive neurons of the claustral complex and piriform cortex. Brain Res Bull (in press).
42. Letinic K, Kostovic I. 1998. Postnatal development of calcium-binding proteins calbindin and parvalbumin in human visual cortex. Cereb Cortex 8:660-669.
43. Levitt P, Eagleson KL, Powell EM. 2004. Regulation of neocortical interneuron development and the implications for neurodevelopmental disorders. Trends Neurosci 27:400-406.
44. Linke R, de Lima AD, Schwegler H, Pape HC. 1999. Direct synaptic connections of axons from superior colliculus with identified thalamo-amygdaloid projection neurons in the rat: possible substrates of a subcortical visual pathway to the amygdala. J Comp Neurol 403:158-170.
45. Liu FC, Graybiel AM. 1992. Transient calbindin-D28k-positive systems in the telencephalon: ganglionic eminence, developing striatum and cerebral cortex. J Neurosci 12:674-690.
46. Marín O, Rubenstein JLR. 2001. A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci 2:780-790.
47. Marín O, Rubenstein JLR. 2002. Patterning, regionalization, and cell differentiaton in the forebrain. In: Rossant J, Tam PPL, editors. Mouse development: patterning, morphogenesis, and organogenesis. San Diego: Academic Press. p 75-106.
48. McDonald AJ. 1985. Immunohistochemical identification of gamma-aminobutyric acid containing neurons in the rat basolateral amygdala. Neurosci Lett 53:203-207.
49. McDonald AJ. 1994. Calretinin immunoreactive neurons in the basolateral amygdala of the rat and monkey. Brain Res 667:238-242.
50. McDonald AJ. 1997. Calbindin-D28k immunoreactivity in the rat amygdala. J Comp Neurol 383:231-244.
51. McDonald AJ. 1998. Cortical pathways to the mammalian amygdala. Prog Neurobiol 55:257-332.
52. McDonald AJ, Betette RL. 2001. Parvalbumin containing neurons in the rat basolateral amygdala: morphology and colocalization of calbindin D-28k. Neuroscience 102:413-425.
53. McDonald AJ, Mascagni F. 2001. Colocalization of calcium-binding proteins and GABA in neurons of the rat basolateral amygdala. Neuroscience 105:681-693.
54. Medina L, Legaz I, González G, de Castro F, Rubenstein JLR, Puelles L. 2004. Expression of Dbx1, Neurogenin 2, Semaphorin 5A, Cadherin 8, and Emx1 distinguish ventral and lateral pallial histogenetic divisions in the developing claustroamygdaloid complex. J Comp Neurol 474: 504-523.
55. Meyer G, Soria JM, Martínez-Galán JR, Martín- Clemente B, Fairén A. 1998. Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex. J Comp Neurol 397:493-518.
56. Miyashita-Lin EM, Hevner R, Wassarman KM, Martínez S, Rubenstein JLR. 1999. Early neocortical regionalization in the absence of thalamic innervation. Science 285:906-909.
57. Moon JS, Kim JJ, Chang IY, Chung YY, Yun JY, You HJ, Yoon SP. 2002. Postnatal development of parvalbumin and calbindin D-28k immunoreactivities in the canine anterior cingulate cortex: transient expression in layer V pyramidal cells. Int J Dev Neurosci 20:511.
58. Morys J, Berdel B, Kowianski P, Dziewiatkowski J. 1998. Patterns of synaptophysin changes during the maturation of the amygdaloid body and hippocampal hilus in the rat. Folia Neuropathol 36:13-21.
59. Morys J, Berdel B, Kowianski P, Majak K, Tarnawski M, Wisniewski HM. 1999. Relationship of calcium-binding protein containing neurons and projection neurons in the rat basolateral amygdala. Neurosci Lett 259:91-94.
60. Muller JK, Mascagni F, McDonald AJ. 2003. Synaptic connections of distinct interneuronal subpopulations in the rat basolateral amygdalar nucleus. J Comp Neurol 456:217-236.
61. Nery S, Fishell G, Corbin JG. 2002. The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat Neurosci 5:1279-1277.
62. O'Leary DD, Nakagawa Y. 2002. Patterning centers, regulatory genes and extrinsic mechanisms controlling arealization of the neocortex. Curr Opin Neurobiol 12:14-25.
63. Paxinos G, Ashwell KWS, Törk I. 1994. Atlas of the developing rat nervous system, 2nd ed. San Diego: Academic Press.
64. Pérez-Villegas EM, Olivier C, Spassky N, Poncet C, Cochard P, Zalc B, Thomas JL, Martinez S. 1999. Early specification of oligodendrocytes in the chick embryonic brain. Dev Biol. 216:98-113.
65. Prather MD, Lavenex P, Mauldin-Jourdain ML, Mason WA, Capitanio JP, Mendoza SP, Amaral DG. 2001. Increased social fear and decreased fear of objects in monkeys with neonatal amygdala lesions. Neuroscience 106:653-658.
66. Pitkänen A. 2000. Connectivity of the rat amygdaloid complex. In: Aggleton JP, editor. The Amygdala: A functional analysis. Second Ed. Oxford: Oxford University Press. p. 31-115.
67. Pitkänen A, Amaral DG. 1993a. Distribution of parvalbumin- immunoreactive cells and fibers in the monkey temporal lobe: the amygdaloid complex. J Comp Neurol 331:14-36.
68. Pitkänen A, Amaral DG. 1993b. Distribution of calbindin-D28k immunoreactive cells and fibers in the monkey temporal lobe: the amygdaloid complex. J Comp Neurol 331:199-224.
69. Pleasure SJ, Anderson S, Hevner R, Bagri A, Marin O, Lowenstein DH, Rubenstein JLR. 2000. Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 28:727-740.
70. Price JL, Russchen FT, Amaral DG. 1987. The limbic region. II: The amygdaloid complex. In: Björklund A, Hökfelt T, Swanson LW, editors. Handbook of chemical neuroanatomy, vol 5, Integrated systems of the CNS, Part I. Amsterdam: Elsevier. p 279-388.
71. Puelles L, Rubenstein JLR. 2003. Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci 26:469-476.
72. Puelles L, Sánchez MP, Spreafico R, Fairén A. 1992. Prenatal development of calbindin immunoreactivity in the dorsal thalamus of the rat. Neuroscience 46:135-147.
73. Puelles L, Kuwana E, Puelles E, Bulfone A, Shimamura K, Keleher J, Smiga S, Rubenstein JLR. 2000. Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J Comp Neurol 424:409-438.
74. Puyal J, Devau G, Venteo S, Sans N, Raymond J. 2002. Calcium-binding proteins map the postnatal development of rat vestibular nuclei and their vestibular and cerebellar projections. J Comp Neurol 30:374-391.
75. Remedios R, Subramanian L, Tole S. 2004. LIM genes parcellate the embryonic amygdala and regulate its development. J Neurosci 24: 6986-6990.
76. Reynolds GP, Beasley CL. 2001. GABAergic neuronal subtypes in the human frontal cortex-development and deficits in schizophrenia. J Chem Neuroanat. 22:95-100.
77. Sánchez MP, Frassoni C, Alvarez-Bolado G, Spreafico R, Fairén A. 1992. Distribution and calbindin and parvalbumin in the developing somatosensory cortex and its primordium in the rat: an immunocytochemical study. J Neurocytol 21:717-736.
78. Smith Y, Pare JF, Pare D. 1998. Cat intraamygdaloid inhibitory network: ultrastructural organization of parvalbumin-immunoreactive elements. J Comp Neurol 391:164-179.
79. Smith Y, Pare JF, Pare D. 2000. Differential innervation of parvalbumin-immunoreactive interneurons of the basolateral amygdaloid complex by cortical and intrinsic inputs. J Comp Neurol 416:496-508.
80. Sorvari H, Soininen H, Paljärvi L, Karkola K, Pitkänen A. 1995. Distribution of parvalbumin-immunoreactive cells and fibers in the human amygdaloid complex. J Comp Neurol 360:185-212.
81. Sorvari H, Miettinen R, Soininen H, Pitkänen A. 1996a. Parvalbumin-immunoreactive neurons make inhibitory synapses on pyramidal cells in the human amygdala: a light and electron microscopic study. Neurosci Lett 217:93-96.
82. Sorvari H, Soininen H, Pitkänen A. 1996b. Calbindin-D28k- immunoreactive cells and fibres in the human amygdaloid complex. Neuroscience 75:421-443.
83. Sorvari H, Soininen H, Pitkänen A. 1996c. Calretinin-immunoreactive cells and fibers in the human amygdaloid complex. J Comp Neurol 369:188-208.
84. 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.
85. Swanson LW, Petrovich GD. 1998. What is the amygdala? Trends Neurosci 21:323-330.
86. Ulfig N. 2002. Calcium-binding proteins in the human developing brain. Adv Anat Embryol Cell Biol 165:1-92.
87. Ulfig N, Setzer M, Bohl J. 2003. Ontogeny of the human amygdala. Ann N Y Acad Sci 985:22-33.
88. Xu Q, Cobos I, De la Cruz E, Rubenstein JLR, Anderson SA. 2004. Origins of cortical interneuron subtypes. J Neurosci 24:2612-2622.
89. Yan XX, Cao QL, Luo XG, Garey LJ. 1997. Prenatal development of calbindin D-28k in human visual cortex. Cereb Cortex 7:57-62.
90. Yan YH, Van Brederode JF, Hendrickson AE. 1995. Transient colocalization of calretinin, parvalbumin, and calbindin-D28k in developing visual cortex of monkey. J Neurocytol 24:825-837.
91. Yan YH, Winarto A, Mansjoer I, Hendrickson A. 1996. Parvalbumin, calbindin, and calretinin mark distinct pathways during development of monkey dorsal lateral geniculate nucleus. J Neurobiol 31:189-209.
92. Yoon SP, Chung YY, Chang IY, Kim JJ, Moon JS, Kim HS. 2000. Postnatal development of parvalbumin and calbindin D-28k immunoreactivities in the canine hippocampus. J Chem Neuroanat 19:143-154.