Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex

Journal of Chemical Neuroanatomy

Volumn 14, Issue 1, 1997, Pages 1-19

  DeFelipe, Javier ^a  

^a INSTITUTO CAJAL   (Spain)

Author keywords

Calcium binding proteins; Cerebral cortex; Colocalization; GABA; Immunocytochemistry; Neuropeptides; Receptors

Indexed keywords

CALBINDIN; CALRETININ; CELL SURFACE MARKER; CELL SURFACE RECEPTOR; NEUROTRANSMITTER; PARVALBUMIN;

HUMAN; IMMUNOREACTIVITY; INTERNEURON; NEOCORTEX; NERVE CELL; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REVIEW; SPECIES DIFFERENCE; SYNAPSE; TEMPORAL CORTEX;

ADULT; ANIMALS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; HUMANS; NEOCORTEX; NERVE TISSUE PROTEINS; NEURONS; PARVALBUMINS; SYNAPTIC TRANSMISSION;

EID: 0031474097     PISSN: 08910618     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-0618(97)10013-8     Document Type: Review

References (124)

1. Adams L.A., Ang L.C., Munoz D.G. Chromogranin A, a soluble synaptic vesicle protein, is found in cortical neurons other than previously defined peptidergic neurons in the human neocortex. Brain Res. 602:1993;336-341.
2. Alcántara S., de Lecea L., Del Río J.A., Ferrer I., Soriano E. Transient colocalization of parvalbumin and calbindin D28k in the postnatal cerebral cortex: evidence for a phenotypic shift in developing nonpyramidal neurons. Eur. J. Neurosci. 8:1996;1329-1339.
3. Andressen C., Blümcke I., Celio M.R. Calcium-binding proteins: selective markers of nerve cells. Cell Tissue Res. 271:1993;181-208.
4. A receptor with parvalbumin and calbindin D-28K in neurons of the visual cortex and the dorsal lateral geniculate nucleus of the cat. J. Chem. Neuroanat. 8:1994;1-10.
5. Baimbridge K.G., Celio M.R., Rogers J.H. Calcium-binding proteins in the nervous system. Trends Neurosci. 15:1992;303-308.
6. Bertini G., Peng Z.-C., Bentivoglio M. The chemical heterogeneity of cortical interneurons: Nitric oxide synthase vs. calbindin and parvalbumin immunoreactivity in the rat. Brain Res. Bull. 39:1996;261-266.
7. Blümcke I., Hof P.R., Morrison J.H., Celio M.R. Distribution of parvalbumin immunoreactivity in the visual cortex of old world monkeys and humans. J. Comp. Neurol. 301:1990;417-432.
8. Blümcke I., Hof P.R., Morrison J.H., Celio M.R. Parvalbumin in the monkey striate cortex: a quantitative immunoelectron-microscopy study. Brain Res. 554:1991;237-243.
9. Blümcke I., Weruaga E., Kasas S., Hendrickson A.E., Celio M.R. Discrete reduction patterns of parvalbumin and calbindin D-28k immunoreactivity in the dorsal lateral geniculate nucleus and the striate cortex of adult macaque monkeys after monocular enucleation. Vis. Neurosci. 11:1994;1-11.
10. Brückner G., Seeger G., Brauer K., Härtig W., Kacza J., Bigl V. Cortical areas are revealed by distribution patterns of proteoglycan components and parvalbumin in the Mongolian gerbil and rat. Brain Res. 658:1994;67-86.
11. Campbell M.J., Morrison J.H. Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex. J. Comp. Neurol. 282:1989;191-205.
12. Carder R.K., Leclerc S.S., Hendry S.H.C. Regulation of calcium-binding protein immunoreactivity in GABA neurons of macaque primary visual cortex. Cereb. Cortex. 6:1996;271-287.
13. Cauli B., Audinat E., Lambolez B., Angulo M.C., Ropert N., Tsuzuki K., Hestrin S., Rossier J. Molecular and physiological diversity of cortical nonpyramidal cells. J. Neurosci. 17:1997;3894-3906.
14. Celio M.R. Parvalbumin in most γ-aminobutyric acid-containing neurons of the rat cerebral cortex. Science. 231:1986;995-997.
15. Celio M.R. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience. 35:1990;375-475.
16. Celio M.R., Scharer I., Morrison J.H., Norman A.W., Bloom F.E. Calbindin immunoreactivity alternates with cytochrome-c oxidase-rich zones in some layers of the primate visual cortex. Nature. 323:1986;715-717.
17. Condé F., Lund J., Jacobowitz D.M., Baimbridge K.G., Lewis D.A. Local circuit neurons immunoreactive for calretinin, calbindin D-28k or parvalbumin in monkey prefrontal cortex: distribution and morphology. J. Comp. Neurol. 341:1994;95-116.
18. Czeiger D., White E.L. Comparison of the distribution of parvalbumin-immunoreactive and other synapses onto somata of callosal projection neurons in mouse visual and somatosensory cortex. J. Comp. Neurol. 379:1997;198-210.
19. DeFelipe J. Neocortical neuronal diversity: chemical heterogeneity revealed by co-localization studies of classic neurotransmitters, neuropeptides, calcium binding proteins and cell surface molecules. Cereb. Cortex. 3:1993;273-289.
20. DeFelipe J., Fariñas I. The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs. Prog. Neurobiol. 39:1992;563-607.
21. DeFelipe J., Jones E.G. Vertical organization of γ-aminobutyric acid-accumulating intrinsic neuronal systems in monkey cerebral cortex. J. Neurosci. 5:1985;3246-3260.
22. DeFelipe, J., Jones, E.G., 1988. Cajal on the Cerebral Cortex. Oxford University Press, New York.
23. DeFelipe J., Jones E.G. Parvalbumin immunoreactivity reveals layer IV of the monkey cerebral cortex as a mosaic of microzones of thalamic afferent terminations. Brain Res. 562:1991;39-47.
24. DeFelipe J., Jones E.G. High resolution light and electron microscopic immunocytochemistry of co-localized GABA and calbindin D-28k in somata and double bouquet cell axons of monkey somatosensory cortex. Eur. J. Neurosci. 4:1992;46-60.
25. DeFelipe J., Hendry S.H.C., Jones E.G., Schmechel D. Variability in the terminations of GABAergic chandelier cell axons on initial segments of pyramidal cell axons in the monkey sensory-motor cortex. J. Comp. Neurol. 231:1985;364-384.
26. DeFelipe J., Hendry S.H.C., Jones E.G. Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex. Proc. Natl. Acad. Sci. USA. 86:1989;2093-2097.
27. DeFelipe J., Hendry S.H.C., Jones E.G. Synapses of double bouquet cells in monkey cerebral cortex visualized by calbindin immunoreactivity. Brain Res. 503:1989;49-54.
28. DeFelipe J., Hendry S.H.C., Hashikawa T., Molinari M., Jones E.G. A microcolumnar structure of monkey cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons. Neuroscience. 37:1990;655-673.
29. DeFelipe J., Sola R.G., Marco P., del Río M.R., Pulido P., Ramón Y Cajal S. Selective changes in the microorganization of the human epileptogenic neocortex revealed by parvalbumin immunoreactivity. Cereb. Cortex. 3:1993;39-48.
30. de Lima A.D., Morrison J.H. Ultrastructural analysis of somatostatin-immunoreactive neurons and synapses in the temporal and occipital cortex of the macaque monkey. J. Comp. Neurol. 283:1989;212-227.
31. del Río M.R., DeFelipe J. A study of SMI 32-stained pyramidal cells, parvalbumin-immunoreactive chandelier cells and presumptive thalamocortical axons in the human temporal neocortex. J. Comp. Neurol. 342:1994;389-408.
32. del Río M.R., DeFelipe J. A light and electron microscopic study of calbindin D-28k immunoreactive double bouquet cells in the human temporal cortex. Brain Res. 690:1995;133-140.
33. del Río M.R., DeFelipe J. Colocalization of calbindin D-28k, calretinin and GABA immunoreactivities in neurons of the human temporal cortex. J. Comp. Neurol. 369:1996;472-482.
34. del Río M.R., DeFelipe J. Colocalization of parvalbumin and calbindin d-28k in neurons including chandelier cells of the human temporal neocortex. J. Chem. Neuroanat. 12:1997;165-173.
35. del Río M.R., DeFelipe J. Synaptic connections of calretinin-immunoreactive neurons in the human neocortex. J. Neurosci. 17:1997;5143-5154.
36. del Río M.R., DeFelipe J. Double bouquet cell axons in the human temporal neocortex: Relationship to bundles of myelinated axons and colocalization of calretinin and calbindin D-28k immunoreactivities. J. Chem. Neuroanat. 13:1997;243-251.
37. Demeulemeester H., Vandesande F., Orban G.A., Brandon C., Vanderhaeghen J.J. Heterogeneity of GABAergic cells in cat visual cortex. J. Neurosci. 8:1988;988-1000.
38. Demeulemeester H., Vandesande F., Orban G.A., Heizmann C.W., Pochet R. Calbindin D-28K and parvalbumin immunoreactivity is confined to two separate neuronal subpopulations in the cat visual cortex, whereas partial coexistence is shown in the dorsal lateral geniculate nucleus. Neurosci. Lett. 99:1989;9-16.
39. Demeulemeester H., Arckens L., Vandesande F., Orban G.A., Heizmann C.W., Pochet R. Calcium binding proteins and neuropeptides as molecular markers of GABAergic interneurons in the cat visual cortex. Exp. Brain Res. 84:1991;538-544.
40. Dun N.J., Huang R., Dun S.L., Förstermann Infrequent co-localization of nitric oxide synthase and calcium binding proteins immunoreactivity in rat neocortical neurons. Brain Res. 666:1994;289-294.
41. Estrada, C., DeFelipe, J., 1997. Nitric oxide-producing neurons in the neocortex: morphological and functional relationship with the intraparenchymal microvasculature. Cereb. Cortex (in press).
42. Fairén A., Valverde F. A specialized type of neuron in the visual cortex of cat: a Golgi and electron microscope study of chandelier cells. J. Comp. Neurol. 194:1980;761-779.
43. Fairén, A., DeFelipe, J., Regidor, J., 1984. Nonpyramidal neurons. General account. In: Peters, A., Jones, E.G. (Eds.), Cerebral Cortex, vol. 1. Cellular Components of the Cerebral Cortex. Plenum Press, New York, pp. 201-253.
44. Ferrer I., Tuñon T., Soriano E., del Rio A., Iraizoz I., Fonseca M., Guionnet N. Calbindin immunoreactivity in normal human temporal cortex. Brain Res. 572:1992;33-41.
45. Fonseca M., Soriano E. Calretinin-immunoreactive neurons in the normal human temporal cortex and in Alzheimer's disease. Brain Res. 691:1995;83-91.
46. Fonseca M., Soriano E., Ferrer I., Martínez A., Tuñon T. Chandelier cell axons identified by parvalbumin-immunoreactivity in the normal human temporal cortex and in Alzheimer's disease. Neuroscience. 55:1993;1107-1116.
47. Freund T.F., Gulyás A.I. GABAergic interneurons containing calbindin D28k or somatostatin are major targets of GABAergic basal forebrain afferents in the rat neocortex. J. Comp. Neurol. 314:1991;187-199.
48. Freund T.F., Meskenaite V. γ-Aminobutyric acid-containing basal forebrain neurons innervate inhibitory interneurons in the neocortex. Proc. Natl. Acad. Sci. USA. 89:1992;738-742.
49. Freund T.F., Martin K.A.C., Smith A.D., Somogyi P. Glutamate decarboxylase-immunoreactive terminals of Golgi-impregnated axoaxonic cells and of presumed basket cells in synaptic contact with pyramidal neurons of cat's visual cortex. J. Comp. Neurol. 221:1983;263-278.
50. Gabbott P.L.A., Bacon S.J. Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey: I. Cell morphology and morphometrics. J. Comp. Neurol. 364:1996;567-608.
51. Gabbott P.L.A., Bacon S.J. Vasoactive intestinal polypeptide containing neurones in monkey medial prefrontal cortex (mPFC): colocalisation with calretinin. Brain Res. 744:1997;179-184.
52. Gabbott P.L.A., Dickie B.G.M., Vaid R.R., Headlam A.J.N., Bacon S.J. Local-circuit neurones in the medial prefrontal cortex (areas 25, 32 and 24b) in the rat: Morphology and quantitative distribution. J. Comp. Neurol. 377:1997;465-499.
53. Gabbott P.L.A., Jays P.R.L., Bacon S.J. Calretinin neurons in human medial prefrontal cortex (areas 24a,b,c, 32′, and 25). J. Comp. Neurol. 381:1997;389-410.
54. Gonchar Y., Burkhalter A. Three distinct families of GABAergic neurons in rat visual cortex. Cereb. Cortex. 7:1997;347-358.
55. Hashikawa T., Rausell E., Molinari M., Jones E.G. Parvalbumin- and calbindin-containing neurons in the monkey medial geniculate complex: Differential distribution and cortical layer specific projections. Brain Res. 544:1991;335-341.
56. Hayes T.L., Lewis D.A. Nonphosphorylated neurofilament protein and calbindin immunoreactivity in layer III pyramidal neurons of human neocortex. Cereb. Cortex. 2:1992;56-67.
57. Hedlich A., Lüth H.-J., Werner L., Bär B., Hanisch U., Winkelmann GABAergic NADPH-diaphorase-positive Martinottizellen im visuellen Cortexx der Ratte. J. Hirnforsch. 31:1990;681-687.
58. +-binding proteins in human neurodegenerative disorders. Trends Neurosci. 15:1992;259-264.
59. Heizmann, C.W., Braun, K., 1995. Calcium Regulation by Calcium-binding Proteins in Neurodegenerative Disorders. R.G. Landers, Austin.
60. Hendry S.H.C., Carder R.K. Neurochemical compartmentation of monkey and human visual cortex: Similarities and variations in calbindin immunoreactivity across species. Vis. Neurosci. 10:1993;1109-1120.
61. Hendry S.H.C., Jones E.G. GABA neuronal subpopulations in cat primary auditory cortex: co-localization with calcium binding proteins. Brain Res. 543:1991;45-55.
62. Hendry S.H.C., Jones E.G., Emson P.C., Lawson D.E.M., Heizmann C.W., Streit P. Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Exp. Brain Res. 76:1989;467-472.
63. Hof P.R., Bogaert Y.E., Rosenthal R.E., Fiskum G. Distribution of neuronal populations containing neurofilament protein and calcium-binding proteins in the canine neocortex: regional analysis and cell typology. J. Chem. Neuroanat. 11:1996;81-98.
64. Houser, C.R., Vaughn, J.E., Hendry, S.H.C., Jones, E.G., Peters, A., 1984. GABA neurons in the cerebral cortex. In: Jones, E.G., Peters, A. (Eds.), Cerebral Cortex, vol. 2. Functional Properties of Cortical Cells. Plenum Press, New York, pp. 63-89.
65. Huntley G.W., Vickers J.C., Janssen W., Brose N., Heinemann S.F., Morrison J.H. Distribution and synaptic localization of immunocytochemically identified NMDA receptor subunit proteins in sensory-motor and visual cortices of monkey and human. J. Neurosci. 14:1994;3603-3619.
66. Jakab R.L., Goldman-Rakic P., Leranth C. Dual role of susbstance P/GABA axons in cortical neurotransmission: synaptic triads on pyramidal cell spines and basket-like innervation of layer II-III calbindin interneurons in primate prefrontal cortex. Cereb. Cortex. 7:1997;359-373.
67. Johnson J.K., Casagrande V.A. Distribution of calcium-binding proteins within the parallel visual pathways of a primate (Galago crassicaudatus). J. Comp. Neurol. 356:1995;238-260.
68. Jones E.G. Varieties and distribution of non-pyramidal cells in the somatic sensory cortex of the squirrel monkey. J. Comp. Neurol. 160:1975;205-268.
69. Jones E.G. GABAergic neurons and their role in cortical plasticity in primates. Cereb Cortex. 3:1993;361-372.
70. Jones E.G., Hendry S.H.C. Co-localization of GABA and neuropeptides in neocortical neurons. Trends Neurosci. 10:1986;71-76.
71. Jones E.G., Hendry S.H.C. Differential calcium binding protein immunoreactivity distinguishes classes of relay neurons in monkey thalamic nuclei. Eur. J. Neurosci. 1:1989;222-246.
72. Kaneko T., Nakaya Y., Mizuno N. Paucity of glutaminase-immunoreactive nonpyramidal neurons in the rat cerebral cortex. J. Comp. Neurol. 322:1992;181-190.
73. Kaneko T., Shigemoto R., Nakanishi S., Mizuno N. Morphological and chemical characteristics of substance P receptor-immunoreactive neurons in the rat neocortex. Neuroscience. 60:1994;199-211.
74. D28k-immunoreactive neurons in layer V of rat frontal cortex. J. Neurophysiol. 70:1993;387-396.
75. Kawaguchi Y., Kubota Y. Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex. J. Neurosci. 16:1996;2701-2715.
76. Kawaguchi Y., Kubota Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex. 7:1997;476-486.
77. Kisvárday Z.F., Beaulieu C., Eysel U. Network of GABAergic large basket cells in cat visual cortex (area 18): Implication for lateral disinhibition). J. Comp. Neurol. 327:1993;398-415.
78. Kobayashi K., Emson P.C., Mountjoy C.Q. Vicia villosa lectin-positive neurones in human cerebral cortex. Loss in Alzheimer-type dementia. Brain Res. 498:1989;170-174.
79. Kobayashi K., Emson P.C., Mountjoy C.Q., Thornton S.N., Lawson D.E.M., Mann D.M.A. Cerebral cortical calbindin D28K and parvalbumin neurones in Down's syndrome. Neurosci. Lett. 113:1990;17-22.
80. Kondo H., Hashikawa T., Tanaka K., Jones E.G. Neurochemical gradient along the monkey occipito-temporal cortical pathway. Neuroreport. 5:1994;613-616.
81. Kondo M., Sumino R., Okado H. Combinations of AMPA receptor subunit expression in individual cortical neurons correlate with expression of specific calcium-binding proteins. J. Neurosci. 17:1997;1570-1581.
82. Kosaka T., Heizmann C.W. Selective staining of a population of parvalbumin-containing GABAergic neurons in the rat cerebral cortex by lectins with specific affinity for terminal N-acetylgalactosamine. Brain Res. 483:1989;158-163.
83. Kosaka T., Heizmann C.W., Tateishi K., Hamaoka Y., Hama K. An aspect of the organizational principle of the γ-aminobutyric acid-ergic system in the cerebral cortex. Brain Res. 409:1987;403-408.
84. Kosaka T., Heizmann C.W., Barnstable C.J. Monoclonal antibody VC1.1 selectively stains a population of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat cerebral cortex. Exp. Brain Res. 78:1989;43-50.
85. Kosaka T., Isogai K., Barnstable C.J., Heizmann C.W. Monoclonal antibody HNK-1 selectively stains a subpopulation of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat cerebral cortex. Exp. Brain Res. 82:1990;566-574.
86. Kosaka T., Heizmann C.W., Fujita S.C. Monoclonal antibody 473 selectively stains a population of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat cerebral cortex. Exp. Brain Res. 89:1992;109-114.
87. Kubota Y., Kawaguchi Y. Two distinct subgroups of cholecystokinin-immunoreactive cortical interneurons. Brain Res. 752:1997;175-183.
88. Kubota Y., Hattori R., Yui Y. Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex. Brain Res. 649:1994;159-173.
89. Leuba G., Saini K. Colocalization of parvalbumin, calretinin and calbindin D-28k in human cortical and subcortical visual structures. J. Chem. Neuroanat. 13:1997;41-52.
90. Lin R.C., Nicolelis M.A., Zhou H.L., Chapin J.K. Calbindin-containing non-specific thalamocortical projecting neurons in the rat. Brain Res. 711:1996;50-55.
91. Lüth H.J., Fischer J., Celio M.R. Soybean lectin binding neurons in the visual cortex of the rat contain parvalbumin and are covered by glial nets. J. Neurocytol. 21:1992;211-221.
92. Lüth H.J., Blümcke I., Celio M.R. The calcium-binding protein calretinin is localized in a subset of interneurons in the rat cerebral cortex: a light and electron immunohistochemical study. J. Hirnforsch. 1993:1993;93-103.
93. Meskenaite V. Calretinin-immunoreactive local circuit neurons in area 17 of the cynomolgus monkey, Macaca fascicularis. J. Comp. Neurol. 379:1997;113-132.
94. Miettinen M., Pitkänen A., Miettinen R. Distribution of calretinin-immunoreactivity in the rat entorhinal cortex: Coexistence with GABA. J. Comp. Neurol. 378:1997;363-378.
95. Molinari M., Dell'Anna M.E., Rausell E., Leggio M.G., Hashikawa T., Jones E.G. Auditory thalamocortical pathways defined in monkeys by calcium-binding protein immunoreactivity. J. Comp. Neurol. 362:1995;171-194.
96. 3 receptor is present in different subpopulations of GABAergic neurons in the rat telencephalon. J. Neurosci. 17:1997;3157-3167.
97. Morino-Wannier P., Fujita S.C., Jones E.G. GABAergic neuronal populations in monkey primary auditory cortex defined by co-localized calcium binding proteins and surface antigens. Exp. Brain Res. 88:1992;422-432.
98. Peters, A., 1987. Synaptic specificity in the cerebral cortex. In: Edelman, G.M., Gall, W.E., Cowan, W.M. (Eds.), Synaptic Fuction. John Wiley, New York, pp. 373-397.
99. Peters A., Proskauer C.C., Ribak C.E. Chandelier cells in rat visual cortex. J. Comp. Neurol. 206:1982;397-416.
100. Preuss T.M., Kaas J.H. Parvalbumin-like immunoreactivity of layer V pyramidal cells in the motor and somatosensory cortex of adult primates. Brain Res. 712:1996;353-357.
101. Rausell E., Jones E.G. Chemically distinct compartments of the thalamic VPM nucleus in monkeys relay principal and spinal trigeminal pathways to different layers of the somatosensory cortex. J. Neurosci. 11:1991;226-237.
102. Rausell E., Bae C.S., Viñuela A., Huntley G.W., Jones E.G. Calbindin and parvalbumin cells in monkey VPL thalamic nucleus: Distribution, laminar cortical projections, and relations to spinothalamic terminations. J. Neurosci. 12:1992;4088-4111.
103. Ren J.Q., Aika Y., Heizmann C.W., Kosaka T. Quantitative analysis of neurons and glial cells in the rat somatosensory cortex, with special reference to GABAergic neurons and parvalbumin-containing neurons. Exp. Brain Res. 92:1992;1-14.
104. Rogers J.H. Immunohistochemical markers in rat cortex: co-localization of calretinin and calbindin-D28k with neuropeptides and GABA. Brain Res. 587:1992;147-157.
105. Rogers J.H., Résibois A. Calretinin and calbindin-D28k in rat brain: patterns of partial co-localization. Neuroscience. 51:1992;843-865.
106. Sesack S.R., Bressler C.N., Lewis D.A. Ultrastructural associations between dopamine terminals and local circuit neurons in the monkey prefrontal cortex: A study of calretinin-immunoreactive cells. Neurosci. Lett. 200:1995;9-12.
107. Sloper J.J. Dendro-dendritic synapses in the primate motor cortex. Brain Res. 34:1971;186-192.
108. Sloper J.J. Gap junctions between dendrites in the primate neocortex. Brain Res. 44:1972;641-646.
109. Sloper J.J., Powell T.P.S. Gap junctions between dendrites and somata of neurons in the primate sensori-motor cortex. Proc. R. Soc. London B Biol. Sci. 203:1978;39-47.
110. Somogyi P. A specific 'axo-axonal' interneuron in the visual cortex of the rat. Brain Res. 136:1977;345-350.
111. Somogyi P., Cowey A. Combined Golgi and electron microscopic study on the synapses formed by double bouquet cells in the visual cortex of the cat and monkey. J. Comp. Neurol. 195:1981;547-566.
112. Somogyi P., Freund T.F., Cowey A. The axo-axonic interneuron in the cerebral cortex of the rat, cat and monkey. Neuroscience. 7:1982;2577-2607.
113. Staiger J.F., Zilles K., Fruend T. Distribution of GABAergic elements postsynaptic to ventroposteromedial thalamic projections in layer IV of rat barrel cortex. Eur. J. Neurosci. 8:1996;2273-2285.
114. Standaert D.G., Landwehrmeyer G.B., Kerner J.A., Penney J.B., Young A.B. Expression of NMDAR2D glutamate receptor subunit mRNA in neurochemically identified interneurons in the rat neostriatum, neocortex and hippocampus. Mol. Brain Res. 42:1996;89-102.
115. van Brederode J.F.M., Mulligan K.A., Hendrickson A.E. Calcium-binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex. J. Comp. Neurol. 298:1990;1-22.
116. van Brederode J.F.M., Helliesen M.K., Hendrickson A.E. Distribution of the calcium-binding proteins parvalbumin and calbindin-D28k in the sensorimotor cortex of the rat. Neuroscience. 44:1991;157-171.
117. Vickers J.C., Huntley G.W., Edwards A.M., Moran T., Rogers S.W., Heinemann S.F., Morrison J.H. Quantitative localization of AMPA/kainate and kainate glutamate receptor subunit immunoreactivity in neurochemically identified subpopulations of neurons in the prefrontal cortex of the macaque monkey. J. Neurosci. 13:1993;2982-2992.
118. Vissavajjhala P., Janssen G.M., Hu Y., Gazzaley A.H., Moran T., Hof P.R., Morrison J.H. Synaptic distribution of the AMPA-GluR2 subunit and its colocalization with calcium-binding proteins in rat cerebral cortex: An immunohistochemical study using a GluR2-specific monoclonal antibody. Exp. Neurol. 142:1996;296-312.
119. White, E.L., 1989. Cortical Circuits: Synaptic Organization of the Cerebral Cortex. Structure, Function and Theory. Birkhäuser, Boston.
120. Williams S.M., Goldman-Rakic P.S., Leranth C. The synaptology of parvalbumin-immunoreactive neurons in the primate prefrontal cortex. J. Comp. Neurol. 320:1992;353-369.
121. Wintergerst E.S., Faissner A., Celio M.R. The proteoglycan DSD-1-PG occurs in perineuronal nets around parvalbumin-immunoreactive interneurons of the rat cerebral cortex. Int. J. Dev. Neurosci. 14:1996;249-255.
122. Yan Y.-H., van Brederode J.F.M., Hendrickson A.E. Transient co-localization of calretinin, parvalbumin, and calbindin-D28K in developing visual cortex of monkey. J. Neurocytol. 24:1995;825-837.
123. Yan X.X., Jen L.S., Garey L.J. NADPH-diaphorase-positive neurons in primate cerebral cortex colocalize with GABA and calcium-binding proteins. Cereb. Cortex. 6:1996;524-529.
124. Yoshioka T., Hendry S.H.C. Compartmental organization of layer IVA in human primary visual cortex. J. Comp. Neurol. 359:1995;213-220.