Different populations of vasoactive intestinal polypeptide-immunoreactive interneurons are specialized to control pyramidal cells or interneurons in the hippocampus

Neuroscience

Volumn 73, Issue 2, 1996, Pages 317-334

  Acsady L ^a   Gorcs T J ^b   Freund, T F ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

disinhibition; GABA; hippocampus; interneurons; synchronization; VIP

Indexed keywords

4 AMINOBUTYRIC ACID; CALBINDIN; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; INTERNEURON; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE; SYNCHRONIZATION; ULTRASTRUCTURE;

EID: 0029951964     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/0306-4522(95)00609-5     Document Type: Article

References (61)

1. Acsady L., Halasy K. and Freund T. F. (1993) Calretinin is present in non-pyramidal cells of the rat hippocampus - III. Their inputs from the median raphe and medial septal nuclei. Neuroscience 52, 829-841.
2. Acsady L., Arabadizisz D. and Freund T. F. (1996) Correlated morphological and neurochemical features identify different subsets of VIP-immunoreactive interneurons in rat hippocampus. Neuroscience 73, 299-315.
3. Baimbridge K. G. and Miller J. J. (1982) Immunohistochemical localization of calcium-binding protein in the cerebellum, hippocampal formation and olfactory bulb of the rat. Brain Res. 245, 223-229.
4. Bakst I., Morrison J. H. and Amaral D. G. (1985) The distribution of somatostatin-like immunoreactivity in the monkey hippocampal formation. J. comp. Neurol. 236, 423-442.
5. Baude A., Nusser S., Roberts J. D., Mulvihill E., McIlhinney R. A. and Somogyi P. (1993) The metabotropic glutamate receptor (mGluR1 alpha) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11, 771-787.
6. Bragin A., Jando G., Nadasdy Z., Hetke J., Wise K. and Buzsaki G. (1995) Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci. 15, 47-60.
7. Buckmaster P. S., Kunkel D. D., Robbins R. J. and Schwartzkroin P. A. (1994) Somatostatin-immunoreactivity in the hippocampus of mouse, rat, guinea pig, and rabbit. Hippocampus 4, 167-180.
8. Buhl E. H., Halasy K. and Somogyi P. (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites [see comments]. Nature 368, 823-828.
9. Buzsaki G., Horvath Z., Urioste R., Hetke J. and Wise K. (1992) High-frequency network oscillation in the hippocampus. Science 256, 1025-1027.
10. Collingridge G. L., Herron C. E. and Lester R. A. (1988) Synaptic activation of N-methyl-D-aspartate receptors in the Schaffer collateral-commissural pathway of rat hippocampus. J. Physiol., Lond. 399, 283-300.
11. Ferron A., Siggins G. R. and Bloom F. E. (1985) Vasoactive intestinal polypeptide acts synergistically with norepinephrine to depress spontaneous discharge rate in cerebral cortical neurons. Proc. natn. Acad. Sci. U.S.A. 82, 8810-8812.
12. Freedman R., Wetmore C., Stromberg I., Leonard S. and Olson L. (1993) Alpha-bungarotoxin binding to hippocampal interneurons: immunocytochemical characterization and effects on growth factor expression. J. Neurosci. 13, 1965-1975.
13. Freund T. F. and Antal M. (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336, 170-173.
14. Freund T. F., Gulyas A. I., Acsady L., Gorcs T. and Toth K. (1990) Serotonergic control of the hippocampus via local inhibitory interneurons. Proc. natn. Acad. Sci. U.S.A. 87, 8501-8505.
15. Gorcs T. J., Penke B., Boti Z., Katarova Z. and Hamori J. (1993) Immunohistochemical visualization of a metabotropic glutamate receptor. NeuroReport 4, 283-286.
16. Gulyas A. I., Gorcs T. J., Freund T. F. (1990) Innervation of different peptide-containing neurons in the hippocampus by GABAergic septal afferents. Neuroscience 37, 31-44.
17. Gulyas A. I., Miles R., Hajos N. and Freund T. F. (1993) Precision and variability in postsynaptic target selection of inhibitory cells in the hippocampal CA3 region. Eur. J. Neurosci. 5, 1729-1751.
18. Haas H. L. and Gahwiler B. H. (1992) Vasoactive intestinal polypeptide modulates neuronal excitability in hippocampal slices of the rat. Neuroscience 47, 273-277.
19. Han Z. S., Buhl E. H., Lorinczi Z. and Somogyi P. (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.
20. Johansson O., Hökfelt T. and Elde R. P. (1984) Immunohistochemical distribution of somatostatin-like immunoreactivity in the central nervous system of the adult rat. Neuroscience 13, 265-339.
21. Katsumaru H., Kosaka T., Heizmann C. W. and Hama K. (1988) Immunocytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus. Expl Brain Res. 72, 347-362.
22. Kawaguchi Y. and Hama K. (1987) Two subtypes of non-pyramidal cells in rat hippocampal formation identified by intracellular recording and HRP injection. Brain Res. 411, 190-195.
23. 2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res. 419, 119-130.
24. Kosaka T., Wu J. Y. and Benoit R. (1988) GABAergic neurons containing somatostatin-like immunoreactivity in the rat hippocampus and dentate gyrus. Expl Brain Res. 71, 388-398.
25. Lacaille J. C. (1991) Postsynaptic potentials mediated by excitatory and inhibitory amino acids in interneurons of stratum pyramidale of the CA1 region of rat hippocampal slices in vitro. J. Neurophysiol. 66, 1441-1454.
26. Lacaille J. C., Mueller A. L., Kunkel D. D. and Schwartzkroin P. A. (1987) Local circuit interactions between oriens/ alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J. Neurosci. 7, 1979-1993.
27. Lacaille J. C. and Schwartzkroin P. A. (1988) Stratum lacunosum-moleculare interneurons of hippocampal CA1 region - I. Intracellular response characteristics, synaptic responses, and morphology. J. Neurosci. 8, 1400-1410.
28. Lacaille J. C. and Schwartzkroin P. A. (1988) Stratum lacunosum-moleculare interneurons of hippocampal CA1 region - II. Intrasomatic and intradendritic recordings of local circuit synaptic interactions. J. Neurosci. 8, 1411-1424.
29. Leranth C. and Frotscher M. (1983) Commissural afferents to the rat hippocampus terminate on vasoactive intestinal polypeptide-like immunoreactive non-pyramidal neurons. An EM immunocytochemical degeneration study. Brain Res. 276, 357-361.
30. Leranth C., Frotscher M., Tombol T. and Palkovits M. (1984) Ultrastructure and synaptic connections of vasoactive intestinal polypeptide-like immunoreactive non-pyramidal neurons and axon terminals in the rat hippocampus. Neuroscience 12, 531-542.
31. Levey A. I., Edmunds S. E., Koliatsos V., Wiley R. G. and Heilman C. J. (1995) Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulations by cholinergic innervation. J. Neurosci. 15, 4077-4092.
32. Magistretti P. J. and Schorderet M. (1984) VIP and noradrenaline act synergistically to increase cyclic AMP in cerebral cortex. Nature 308, 280-282.
33. McBain C. J., DiChiara T. J. and Kauer J. A. (1994) Activation of metabotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission. J. Neurosci. 14, 4433-4445.
34. Michelson H. B. and Wong R. K. (1991) Excitatory synaptic responses mediated by GABAA receptors in the hippocampus. Science 253, 1420-1423.
35. Miettinen R. and Freund T. F. (1992) Convergence and segregation of septal and median raphe inputs onto different subsets of hippocampal inhibitory interneurons. Brain Res. 594, 263-272.
36. Miettinen R. and Freund T. F. (1992) Neuropeptide Y-containing interneurons in the hippocampus receive synaptic input from median raphe and GABAergic septal afferents. Neuropeptides 22, 185-193.
37. Miles R., Tóth K., Gulyás A. I., Hájos N. and Freund T. F. (1996) Distinct functional roles for somatic and dendritic inhibition in hippocampus. Neuron (in press).
38. Misgeld U. and Frotscher M. (1986) Postsynaptic-GABAergic inhibition of non-pyramidal neurons in the guinea-pig hippocampus. Neuroscience 19, 193-206.
39. Muller W. and Misgeld U. (1990) Inhibitory role of dentate hilus neurons in guinea pig hippocampal slice. J. Neurophysiol. 64, 46-56.
40. Murphy P. C., Grieve K. L. and Sillito A. M. (1993) Effects of vasoactive intestinal polypeptide on the response properties of cells in area 17 of the cat visual cortex. J. Neurophysiol. 69, 1465-1474.
41. Naus C. C., Morrison J. H. and Bloom F. E. (1988) Development of somatostatin-containing neurons and fibers in the rat hippocampus. Brain Res. 468, 113-121.
42. Ramon y Cajal (1968) The Structure of Ammon's Horn. Charles C. Thomas.
43. Ribak C. E., Nitsch R. and Seress L. (1990) Proportion of parvalbumin-positive basket cells in the GABAergic innervation of pyramidal and granule cells of the rat hippocampal formation. J. comp Neurol. 300, 449-461.
44. Roberts G. W., Woodhams P. L., Polak J. M. and Crow T. J. (1984) Distribution of neuropeptides in the limbic system of the rat: the hippocampus. Neuroscience 11, 35-77.
45. Scharfman H. E., Kunkel D. D. and Schwartzkroin P. A. (1990) Synaptic connections of dentate granule cells and hilar neurons: results of paired intracellular recordings and intracellular horseradish peroxidase injections. Neuroscience 37, 693-707.
46. Schmechel D. E., Vickrey B. G., Fitzpatrick D. and Elde R. P. (1984) GABAergic neurons of mammalian cerebral cortex: widespread subclass defined by somatostatin content. Neurosci. Lett. 47, 227-232.
47. Sessler F. M., Grady S. M., Waterhouse B. D. and Moiscs H. C. (1991) Electrophysiological actions of VIP in rat somatosensory cortex. Peptides 12, 715-721.
48. Sik A., Tamamaki N. and Freund T. F. (1993) Complete axon arborization of a single CA3 pyramidal cell in the rat hippocampus, and its relationship with postsynaptic parvalbumin-containing interneurons. Eur. J. Neurosci. 5, 1719-1728.
49. Sik A., Ylinen A., Penttonen M. and Buzsaki G. (1994) Inhibitory CA1-CA3-hilar region feedback in the hippocampus. Science 265, 1722-1724.
50. Sík A., Pentonnen M., Ylinen A, and Buzsáki G. (1995) Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J. Neurosci.
51. Soltesz I. and Mody I. (1994) Patch-clamp recordings reveal powerful GABAergic inhibition in dentate hilar neurons. J. Neurosci. 14, 2365-2376.
52. Somogyi P. and Hodgson A. J. (1985) Antisera to gamma-ammobutync acid - III. Demonstration of GABA in Golgi-impregnated neurons and in conventional electron microscopic sections of cat striate cortex. J. Histochem. Cytochem. 33, 249-257.
53. Somogyi P., Hodgson A. J., Smith A. D., Nunzi M. G., Gorio A. and Wu J. Y. (1984) Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin- or cholecystokinin-immunoreactive material. J. Neurosci. 4, 2590-2603.
54. Spruston N., Schiller Y., Stuart G. and Sakmann B. (1995) Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science 268, 297-300.
55. Toth K., Borhegyi Z. and Freund T. F. (1993) Postsynaptic targets of GABAergic hippocampal neurons in the medial septum-diagonal band of Broca complex. J. Neurosci. 13, 3712-3724.
56. Toth K. and Freund T. F. (1992) Calbindin D28k-containing nonpyramidal cells in the rat hippocampus: their immunoreactivity for GABA and projection to the medial septum. Neuroscience 49, 793-805.
57. Whittington M. A., Traub R. D. and Jefferys J. G. R. (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373, 612-615.
58. Wigstrom H. and Gustafsson B. (1983) Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition. Nature 301, 603-604.
59. Williams S., Samulack D. D., Beaulieu C. and Lacaille J. C. (1994) Membrane properties and synaptic responses of interneurons located near the stratum lacunosum-moleculare/radiatum border of area CA1 in whole-cell recordings from rat hippocampal slices. J. Neurophysiol. 71, 2217-2235.
60. Wilson M. A. and McNaughton B. L. (1993) Dynamics of the hippocampal ensemble code for space [see comments]. Science 261, 1055-1058.
61. Ylinen A., Bragin A., Nadasdy Z., Jando G., Szabo I. and Sik A. (1995) Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J. Neurosci. 15, 30-46.