A golgi study of the short-axon interneurons of the cell layer and inner plexiform layer of the medial cortex of the lizard Podarcis hispanica

Journal of Comparative Neurology

Volumn 385, Issue 4, 1997, Pages 565-598

  Luis De La Iglesia, José A ^a   Lopez Garcia, Carlos ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Fascia dentata; Hilar cells; Hippocampus; Neuron morphology; Reptiles

Indexed keywords

ARTICLE; BRAIN CORTEX; CELL POPULATION; CYTOARCHITECTURE; DENTATE GYRUS; GOLGI COMPLEX; HIPPOCAMPUS; IMMUNOREACTIVITY; INTERNEURON; LIZARD; NERVE ENDING; NONHUMAN; ONTOGENY; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL;

ANATOMY, ARTISTIC; ANIMALS; AXONS; CEREBRAL CORTEX; DENTATE GYRUS; FEMALE; GOLGI APPARATUS; INTERNEURONS; LIZARDS; MALE;

EID: 1842301112     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19970908)385:4<565::AID-CNE5>3.0.CO;2-1     Document Type: Article

References (93)

1. Al-Hussein, S., and S. Al-Ali (1995) A Golgy study of cell types in the dentate gyrus of the adult human brain. Cell. Mol. Neurobiol. 15:207-220.
2. Amaral, D.G. (1978) A Golgi study of the cell types in the hilar region of the hippocampus in the rat. J. Comp. Neurol. 182:851-914.
3. Berbel, P. (1986) Chromation at low temperatures improves impregnation of neurons in Golgi-aldehyde methods. J. Neurosci. Methods 17:255-259.
4. Berbel, P.J. (1988) Cytology of medial and dorso-medial cortices in lizards: A Golgi study. In W.K. Schwerdtfeger and W. Smeets (eds): The Forebrain of Reptiles. Current Concepts on Structure and Function. Basel: Karger, pp. 12-19.
5. Berbel, P.J., F.J. Martínez-Guijarro, and C. Lopez-Garcia (1987) Intrinsic organization of the medial cerebral cortex of the lizard Lacerta pityusensis. A Golgi study. J. Morphol. 194:275-286.
6. Bernabeu, A., F.J. Martínez-Guijarro, J.A. Luis de la Iglesia, and C. Lopez-Garcia (1994) An axosomatic and axodendritic multipolar neuron in the lizard cerebral cortex. J. Anat. 184:567-582.
7. Blanton, M.G., J.M. Shen, and A.R. Kriegstein (1987) Evidence for the inhibitory neurotransmitter gamma-aminobutyric acid in aspiny and sparsely spiny nonpyramidal neurons of the turtle dorsal cortex. J. Comp. Neurol. 259:277-297.
8. Colonnier, M. (1964) The tangential organization of the visual cortex. J. Comp. Neurol. 98:327-344.
9. Dávila, J.C., S. Guirado, A. de la Calle, and F. Marín-Girón (1985) Electron microscopy of the medial cortex of the lizard Psammodromus algirus. J. Morphol. 185:327-338.
10. Dávila, J.C., S. Guirado, and A. de la Calle (1988) Immunocytochemical localization of somatostatin in the cerebral cortex of lizards. Brain Res. 447:52-59.
11. Dávila, J.C., A. de la Calle, A. Gutiérrez, M. Megías, M.J. Andreu, and S. Guirado (1991) Distribution of neuropeptide Y (NPY) in the cerebral cortex of the lizards Psammodromus algirus and Podarcis hispanica: Colocalization of NPY, somatostatin, and GABA. J. Comp. Neurol. 308:397-408.
12. Dávila, J.C., M. Megías, A. de la Calle, and S. Guirado (1993) Subpopulations of GABA neurons containing somatostatin, neuropeptide Y, and parvalbumin in the dorsomedial cortex of the lizard Psammodromus algirus. J. Comp. Neurol. 336:161-173.
13. Dávila, J.C., M. Megías, M.J. Andreu, M.A. Real, and S. Guirado (1995) NADPH diaphorase-positive neurons in the lizard hippocampus: A distinct subpopulation of GABAergic interneurons. Hippocampus 5:60-70.
14. Deller, T., and C. Leranth (1990) Synaptic connections of neuropeptide Y (NPY) immunoreactive neurons in the hilar area of the rat hippocampus. J. Comp. Neurol. 300:433-447.
15. Desfilis, E. (1989) Tipología neuronal del cortex dorsal de Podarcis hispanica. Minor Thesis. Univ. de Valencia.
16. Ebbesson, S.O.E., and T.J. Voneida (1969) The cytoarchitecture of the pallium in the Tegu lizard (Tupinambis nigropunctatus. Brain Behav. Evol. 2:431-466.
17. Frotscher, M., L. Seress, W.K. Schwerdtfeger, and E. Buhl (1991) The mossy cells of the fascia dentata: A comparative study of their fine structure and synaptic connections in rodents and primates. J. Comp. Neurol. 312:145-163.
18. García-Verdugo, J.M., P. Berbel-Navarro, J. Regídor-García, and C. Lopez-Garcia (1984) Ultrastructure of neuronal cell bodies in the medial cortex of Lacerta galloti. J. Hirnforsch. 25:187-196.
19. García-Verdugo, J.M., I. Farinas, A. Molowny, and C. Lopez-Garcia (1986) Ultrastructure of putative migrating cells in the cerebral cortex of Lacerta galloti. J. Morphol. 189:189-197.
20. Guirado, S., A. de la Calle, J.C. Dávila, and F. Marín-Girón (1984) Light microscopy of the medial wall of the cerebral cortex of the lizard Psammodromus algirus. J. Morphol. 181:319-331.
21. Gulyás, A.I., T.J. Görcs, and T.F. Freund (1990) Innervation of different peptide-containing neurons in the hippocampus by GABAergic septal afferents. Neuroscience 37:31-44.
22. Halasy, K., and P. Somogyi (1993) Subdivisions in the multiple GABAergic innervation of granule cells in the dentate gyrus of the rat hippocampus. Eur. J. Neurosci. 5:411-429.
23. Han, Z.-S., E.H. Buhl, Z. Lörinczi, and P. Somogyi (1993) A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of the rat hippocampus. Eur. J. Neurosci. 5:395-410.
24. Hazlett, J.C., and N. Farkas (1978) Short axon molecular layer neurons in the opossum fascia dentata: AGolgi study. Brain Res. 143:319-331.
25. Holm, I.E., F.A. Geneser, and J. Zimmer (1992) Somatostatin- and neuropeptide Y-like immunoreactivity in the dentate area, hippocampus, and subiculum of the domestic pig. J. Comp. Neurol. 322:390-408.
26. Hoogland, P.V., and E. Vermeulen van der Zee (1993) Medial cortex of the lizard Gekko gecko: A hodological study with emphasis on regional specialization. J. Comp. Neurol. 331:326-338.
27. Katsumaru, H., T. Kosaka, C.W. Heizmann, and K. Hama (1988) Immunocytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus. Exp. Brain Res. 72:347-362.
28. 2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res. 419:119-130.
29. Kosaka, T., J.Y. Wu, and R. Benoit (1988) GABAergic neurons containing somatostatin-like immunoreactivity in the rat hippocampus and dentate gyrus. Exp. Brain Res. 71:388-398.
30. Kriegstein, A.R., and B.W. Connors (1986) Cellular physiology of the turtle visual cortex: Synaptic properties and intrinsic circuitry. J. Neurosci. 6:178-191.
31. Kriegstein, A.R., J.M. Shen, G.M. Lee, and M.G. Blanton (1988) Development of inhibitory function during corticogenesis in the turtle. In W.K. Schwerdtfeger and W. Smeets (eds): The Forebrain of Reptiles. Current Concepts of Structure and Function. Basel: Karger, pp. 131-141.
32. Lacey, D.J. (1978) The organization of the hippocampus of the Fence lizard: A light microscopic study. J. Comp. Neurol. 182:247-264.
33. Leranth, C., A.J. Malcolm, and M. Frotscher (1990) Afferent and efferent synaptic connections of somatostatin-immunoreactive neurons in the rat fascia dentata. J. Comp. Neurol. 295:111-122.
34. Lopez-Garcia, C., P.L. Tineo, and J. del Corral (1984) Increase of the neuron number in some cerebral cortical areas of a lizard, Podarcis hispanica, (Steind., 1870), during postnatal periods of life. J. Hirnforsch. 25:255-259.
35. Lopez-Garcia, C., F.J. Martínez-Guijarro, P. Berbel, and J.M. García-Verdugo (1988a) Long-spined polymorphic neurons of the medial cortex of lizards: A Golgi, Timm, and electron-microscopic study. J. Comp. Neurol. 272:409-423.
36. Lopez-Garcia, C., A. Molowny, J.M. Garcia-Verdugo, and I. Ferrer (1988b) Delayed postnatal neurogenesis in the cerebral cortex of lizards. Brain Res. 471:167-174.
37. Lopez-Garcia, C., A. Molowny, F.J. Martínez-Guijarro, J.M. Blasco-Ibáñez, J.A. Luis de la Iglesia, A. Bernabeu, and J.M. García-Verdugo (1992) Lesion and regeneration in the medial cerebral cortex of lizards. Histol. Histopathol. 7:725-746.
38. Lorente de Nó, R. (1934) Studies on the structure of the cerebral cortex. II. Continuation of the study of the Ammonic System. J. Psychol. Neurol. 46:113-177.
39. Luis de la Iglesia, J.A. (1994) Las neuronas principales del cortex medial de la lagartija Podarcis hispanica: Estudio con el método de Golgi. Minor Thesis. Univ. of Valencia.
40. Luis de la Iglesia, J.A. (1995) Las neuronas del cortex medial de la lagartija Podarcis hispanica. Estudio con el método de Golgi. Doctoral Thesis. Univ. of Valencia.
41. Luis de la Iglesia, J.A., and C. Lopez-Garcia (1997) A Golgi study of the principal projection neurons of the medial cortex of the lizard Podarcis hispanica. J. Comp. Neurol. 385:528-564.
42. Luis de la Iglesia, J.A., F.J. Martínez-Guijarro, and C. Lopez-Garcia (1994) Neurons of the medial cortex outer plexiform layer of the lizard Podarcis hispanica: Golgi and immunocytochemical studies. J. Comp. Neurol. 341:184-203.
43. Martínez-García, F., M. Amiguet, W.K. Schwerdtfeger, F.E. Olucha, and M.J. Lorente (1990) Interhemispheric connections through the pallial commissures in the brain of Podarcis hispanica and Gallotia stehlinii (Reptilia, Lacertidae). J. Morphol. 205:17-31.
44. 28K, and parvalbumin in the cerebral cortex of the lizard Podarcis hispanica. J. Comp. Neurol. 322:449-460.
45. Martínez-Guijarro, F.J., and T.F. Freund (1992b) GABA-immunoreactive basal forebrain afferents innervate GABA-immunoreactive non-pyramidal cells in the cerebral cortex of the lizard Podarcis hispanica. Neuroscience 51:425-437.
46. Martínez-Guijarro, F.J., A. Molowny, and C. Lopez-Garcia (1987) Timmstaining is correlated with the density of Timm-positive presynaptic structures in the cerebral cortex of lizards. Histochemistry 86:315-319.
47. Martínez-Guijarro, F.J., E. Desfilis, and C. Lopez-Garcia (1990) Organization of the dorsomedial cortex in the lizard Podarcis hispanica. In W.K. Schwerdtfeger and P. Germroth (eds): The Forebrain in Non-mammals. New Aspects of Structure and Development. Berlin: Springer-Verlag, pp. 77-92.
48. Martínez-Guijarro, F.J., E. Soriano, J.A. del Río, and C. Lopez-Garcia (1991) Parvalbumin-immunoreactive neurons in the cerebral cortex of the lizard Podarcis hispanica. Brain Res. 547:339-343.
49. Martínez-Guijarro, F.J., E. Soriano, J.A. del Río, J.M. Blasco-Ibáñez, and C. Lopez-Garcia (1993) Parvalbumin-containing neurons in the cerebral cortex of the lizard Podarcis hispanica: Morphology, ultrastructure, and coexistence with GABA. somatostatin, and neuropeptide Y. J. Comp. Neurol. 336:447-467.
50. Martínez-Guijarro, F.J., J.M. Blasco-Ibáñez, and T.F. Freund (1994a) Serotoninergic innervation of nonprincipal cells in the cerebral cortex of the lizard Podarcis hispanica. J. Comp. Neurol. 340:2-13.
51. Martínez-Guijarro, F.J., J.M. Blasco-Ibáñez, and C. Lopez-Garcia (1994b) Postnatal increase of GABA- and PV-IR cells in the cerebral cortex of the lizard Podarcis hispanica. Brain Res. 634:168-172.
52. Medina, L., E. Marti, C. Artero, A. Fasolo, and L. Puelles (1992) Distribution of neuropeptide Y-like immunoreactivity in the brain of the lizard Gallotia galloti, J. Comp. Neurol. 319:387-405.
53. Miettinen, R., and T.F. Freund (1992) Neuropeptide Y-containing interneurons in the hippocampus receive synaptic input from median raphe and gabaergic septal afferents. Neuropeptides 22:185-193.
54. Minelli, G. (1966) Architettura delle corteccie di alcuni Rettili (Lacerta muralis, Lacerta viridis, Testudo graeca, Crocodylus acutus). Arch. Zool. Ital. 51:543-573.
55. Molowny, A., and C. Lopez-Garcia (1978) Estudio citoarquitectónico de la corteza cerebral de reptiles. III. Localization histoquímica de metales pesados y definición de subregiones Timm-positivas en la corteza de Lacerta, Chalcides, Tarentola y Malpolon. Trab. Inst. Cajal Inv. Biol. 70:55-74.
56. Molowny, A., C. Lopez-Garcia, and F. Marín-Girón (1972) Estudio citoarquitectónico de la corteza cerebral de reptiles. I. Áreas y núcleos corticales en Lacerta galloti, Chalcides sp. y Tarentola mauritanica. Trab. Inst. Cajal Inv. Biol. 24:125-158.
57. Nacher, J., C. Ramirez, A. Molowny, and C. Lopez-Garcia (1996) Ontogeny of somatostatin immunoreactive neurons in the medial cerebral cortex and other cortical areas of the lizard Podacis hispanica. J. Comp. Neurol. 374:118-135.
58. Nitsch, R., I. Bergmann, K. Kuppers, G. Mueller, and M. Frotscher (1990a) Late appearance of parvalbumin-immunoreactivity in the development of GABAergic neurons in the rat hippocampus. Neurosci. Lett. 118:147-150.
59. Nitsch, R., C. Leranth, and M. Frotscher (1990b) Most somatostatinimmunoreactive neurons in the rat fascia dentata do not contain the calcium-binding protein parvalbumin. Brain Res. 528:327-329.
60. Northcutt, R.G. (1967) Architectonic studies of the telencephalon ofIguana iguana. J. Comp. Neurol. 130:109-148.
61. Olucha, F.E., F. Martínez-García, L. Poch, W.K. Schwerdtfeger, and C. Lopez-Garcia (1988) Projections from the medial cortex in the brain of lizards: Correlation of anterograde and retrograde transport of horseradish peroxidase with Timm staining. J. Comp. Neurol. 276:469-480.
62. Ramón, P. (1891) El Encéfalo de los Reptiles. Barcelona: Tipografía de la Casa Provincial de Caridad, pp. 1-30.
63. Ramön, P. (1896) Estructura del encéfalo del camaleón. Revista Trimestral Micrográfica 1:16-82.
64. Ramön y Cajal, P. (1917) Nuevo estudio del encéfalo de los reptiles. I. Trab. Lab. Inv. Biol. Univ. Madrid 15:83-99.
65. Ramön y Cajal, S. (1904a) Estructura comparada de la corteza cerebral. In Textura del Sistema Nervioso del Hombre y de los Vertebrados. Vol. II. Madrid: Imprenta y librería de Nicolás Moya.
66. Ramön y Cajal, S. (1904b) Focos olfativos cuaternarios o asta de Ammon y fascia dentata. In Textura del Sistema Nervioso del Hombre y de los Vertebrados. Vol. II. Madrid: Imprenta y librería de Nicolás Moya.
67. Ramón y Cajal, S. (1911) Histologie du Système Nerveux de l'Homme et des Vertebres. Paris: A. Maloine.
68. Regidor, J. (1978) Tipología neuronal y organización de la corteza cerebral de Lacerta galloti (Dum. y Bib.). Estudio con los métodos de Golgi. Las Palmas: Excma. Mancom. Cabildos. Plan Cultural.
69. Regidor, J., J.M. Martín-Trujillo, C. Lopez-Garcia, and F. Marín-Girón (1974) Estudio citoarquitectónico de la corteza cerebral de reptiles. II. Tipología dendritica y distribución neuronal en areas corticales de Lacerta galloti. Trab. Inst. Cajal Inv. Biol. 66:1-32.
70. Ribak, C.E., and L. Stress (1983) Five types of basket cell in the hippocampal dentate gyrus: A combined Golgi and electron microscopic study. J. Neurocytol. 12:577-597.
71. Ribak, C.E., L. Seress, and D.O. Amaral (1985) The development, ultrastructure and synaptic connections of the mossy cells of the dentate gyrus. J. Neurocytol. 14:835-857.
72. Ribak, C.E., L. Seress, and C. Leranth (1993) Electron microscopic immunocytochemical study of the distribution of parvalbumin-containing neurons and axon terminals in the primate dentate gyrus and Ammon's horn. J. Comp. Neurol. 327:298-321.
73. Scharfman, H.E. (1991) Dentate hilar cells with dendrites in the molecular layer have lower thresholds for synaptic activation by perforant path than granule cells. J. Neurosci. 11:1660-1673.
74. Schwerdtfeger, W.K., and C. Lopez-Garcia (1986) GABAergic neurons in the cerebral cortex of the brain of a lizard (Podarcis hispanica). Neurosci. Lett. 68:117-121.
75. Schwerdtfeger, W.K., and M.J. Lorente (1988a) GABA-immunoreactive neurons in the medial and dorsomedial cortices of the lizard telencephalon. Some data on their structure, distribution and synaptic relations, In W.K. Schwerdtfeger and W. Smeets (eds): The Forebrain of Reptiles. Current Concepts on Structure and Function. Basel: Karger, pp. 110-121.
76. Schwerdtfeger, W.K., and M.J. Lorente (1988b) Laminar distribution and morphology of gamma-aminobutyric acid (GABA)-immunoreactive neurons in the medial and dorsomedial areas of the cerebral cortex of the lizard Podarcis hispanica. J. Comp. Neurol. 278:473-485.
77. Seress, L., and J. Pokorny (1981) Structure of the granular layer of the rat dentate gyrus. A light microscopic and Golgi study. J. Anat. 133:181-195.
78. Seress, L., and C.E. Ribak (1983) GABAergic cells in the dentate gyrus appear to be local circuit and projection neurons. Exp. Brain Res. 150:173-182.
79. Seress, L., and C.E. Ribak (1984) Direct commissural connections to the basket cells of the hippocampal dentate gyrus: Anatomical evidence for feed-forward inhibition. J. Neurocytol. 13:215-225.
80. 28k-immunoreactive neurons in the human hippocampal formation. J. Comp. Neurol. 337:208-230.
81. Seroogy, K.B., L. Seress, and C.E. Ribak (1983) Ultrastructure of commissural neurons of the hilar region in the hippocampal dentate gyrus. Exp. Neurol. 82:594-608.
82. Soriano, E., and M. Frotscher (1989) A GABAergic axo-axonic cell in the fascia dentata controls the main excitatory hippocampal pathway. Brain Res. 503:170-174.
83. Soriano, E., and M. Frotscher (1993a) GABAergic innervation of the rat fascia dentata: A novel type of interneuron in the granule cell layer with extensive axonal arborization in the molecular layer. J. Comp. Neurol. 334:385-396.
84. Soriano, E., and M. Frotscher (1993b) Spiny nonpyramidal neurons in the CA3 region of the rat hippocampus are glutamate-like immunoreactive and receive convergent mossy fiber input. J. Comp. Neurol. 333:435-448.
85. Soriano, E., A. Cobas, and A. Fairen (1989) Neurogenesis of glutamic acid decarboxylase immunoreactive cells in the hippocampus of the mouse. II. Area dentata. J. Comp. Neurol. 281:603-611.
86. Soriano, E., R. Nitsch, and M. Frotscher (1990) Axo-axonic chandelier cells in the rat fascia dentata: Golgi-electron microscopy and immunocytochemical studies. J. Comp. Neurol. 293:1-25.
87. Stensaas, L.J. (1967) The development of hippocampal and dorsolateral pallial regions of the cerebral hemisphere in fetal rabbits. III. Twenty-nine millimeter stage, marginal lamina. J. Comp. Neurol. 130:149-162.
88. Stensaas, L.J. (1968) The development of hippocampal and dorsolateral pallial regions of the cerebral hemisphere in fetal rabbits. VI. Ninety millimeter stage, cortical differentiation. J. Comp. Neurol. 132:93-108.
89. Swanson, L.W., C. Köhler, and A. Björklund (1987) The limbic region. I. The septohippocampal system. In A. Björklund, T. Höktelt, and L. Swanson (eds): Handbook of Chemical Neuroanatomy. Vol. 5. Integrated Systems of the CNS. Part I. Amsterdam: Elsevier, pp. 125-277.
90. Ulinski, P.S. (1977) Intrinsic organization of snake medial cortex: An electron microscopic and Golgi study. J. Morphol. 152:247-280.
91. Ulinski, P.S. (1990) The cerebral cortex of reptiles. In E.G. Jones and A. Peters (eds): Cerebral Cortex. Vol. 8A. Comparative Structure and Evolution of Cerebral Cortex, Part I. New York: Plenum Press, pp. 139-215.
92. Wouterlood, F.G. (1981) The structure of the mediodorsal cerebral cortex in the lizard Agama agama: A Golgi study. J. Comp. Neurol. 196:443-458.
93. Wouterlood, F.G., V.E. Alones, and A.H.M. Lohman (1981) An electron microscopic study of the mediodorsal cerebral cortex in the lizard Agama agama. Anat. Embryol. 163:185-200.