Immunostaining for substance P receptor labels GABAergic cells with distinct termination patterns in the hippocampus

Journal of Comparative Neurology

Volumn 378, Issue 3, 1997, Pages 320-336

  Acsady L ^a   Katona, I ^a   Gulyas A I ^a   Shigemoto, R ^b   Freund, T F ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

colocalization; interneurons; neuropeptides; receptors; tachykinins

Indexed keywords

4 AMINOBUTYRIC ACID; BIOCHEMICAL MARKER; CALBINDIN; CALRETININ; CHOLECYSTOKININ; NEUROPEPTIDE; NEUROPEPTIDE Y; PARVALBUMIN; SOMATOSTATIN; SUBSTANCE P; TACHYKININ;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; DENTATE GYRUS; GRANULE CELL; HIPPOCAMPUS; INTERNEURON; MALE; NERVE CELL; NEUROCHEMISTRY; NEUROENDOCRINOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 1842334512     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19970217)378:3<320::AID-CNE2>3.3.CO;2-I     Document Type: Article

References (84)

1. Acsády, L., D. Arabadzisz, and T.F. Freund (1996a) Correlated morphological and neurochemical features identify different subsets of VIP-immunoreactive interneurons in rat hippocampus. Neuroscience 73:299-315.
2. Acsády, L., T.J. Göres, and T.F. Freund (1996b) Different populations of VIP-immunoreactive interneurons are specialized to control pyramidal cells or interneurons in the hippocampus. Neuroscience 73:317-334.
3. Amaral, D.G., (1978) A Golgi study of cell types in the hilar region of the hippocampus in the rat. J. Comp. Neurol. 182:851-914.
4. Baimbridge, K.G., and J.J. Miller (1982) Immunohistochemical localization of calcium-binding protein in the cerebellum, hippocampal formation and olfactory bulb of the rat. Brain Res. 245:223-229.
5. Baude, A., Z. Nusser, J.D. Roberts, E. Mulvihill, R.A. McIlhinney, and P. Somogyi (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. Beaulieu, C., G. Campistron, and C. Crevier (1994) Quantitative aspects of the GABA circuitry in the visual cortex of adult rat. J. Comp. Neurol. 339:559-572.
7. Blasco-Ibanez, J.M., and T.F. Freund (1995) Synaptic input of horizontal interneurons in stratum oriens of the hippocampal CA1 subfield: Structural basis of feedback activation. Eur. J. Neurosci. 7:2170-2180.
8. Bragin, A., G. Jando, Z. Nadasdy, J. Hetke, K. Wise, and G. Buzsáki (1995) Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci. 15:47-60.
9. Buckmaster, P.S., and P.A. Schwartzkroin (1995) Interneurons and inhibition in the dentate gyrus of the rat in vivo. J. Neurosci. 15:774-789.
10. Buckmaster, P.S., D.D. Kunkel, R.J. Robbins, and P.A. Schwartzkroin (1994) Somatostatin-immunoreactivity in the hippocampus of mouse, rat, guinea pig, and rabbit. Hippocampus 4:167-180.
11. Buhl, E.H., K. Halasy, and P. Somogyi (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368:823-828.
12. Buzsáki, G., and J.J. Chrobak (1995) Temporal structure in spatially organized neuronal ensembles: A role for interneuronal networks. Curr. Opin. Neurobiol. 5:504-510.
13. Buzsáki, G., and E. Eidelberg (1982) Direct afferent excitation and long-term potentiation of hippocampal interneurons. J. Neurophysiol. 48:597-607.
14. Buzsáki, G., Z. Horvath, R. Urioste, J. Hetke, and K. Wise (1992) High-frequency network oscillation in the hippocampus. Science 256:1025-1027.
15. Celio, M.R. (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375-475.
16. Cobb, S.R., E.H. Buhl, K. Halasy, O. Paulsen, and P. Somogyi (1995) Synchronization of neural activity in hippocampus by individual GABA-ergic interneurons. Nature 378:75-78.
17. Csiffáry, A., T.J. Gores, and M. Palkovits (1990) Neuropeptide Y innervation of ACTH immunoreactive neurons in the arcuate nucleus of rats: A correlated light and electron microscopic double immunolabelling study. Brain Res. 506:215-222.
18. Davis, S., and C. Köhler (1985) The substance P innervation of the rat hippocampal formation. Anat. Embryol. 173:45-52.
19. Deller, T., and C. Léránth (1990) Synaptic connections of neuropeptide Y (NPY) immunoreactive neurons in the hilar area of the rat hippocampus. J. Comp. Neurol. 300:433-447.
20. Dreifuss, J.J., and M. Raggenbass (1986) Tachykinins and bombesin excite non-pyramidal neurones in rat hippocampus. J. Physiol. 379:417-428.
21. Duggan, A.W., P.J. Hope, B. Jarrott, H.G. Schaible, and S.M. Fleetwood-Walker (1990) Relese spread and persistance of immunoreactive neurokinin A in the dorsal horn of the cat following noxious cutaneous stimulation. Studies with antibody microprobes. Neuroscience 35:195-202.
22. Esclapez, M., and C.R. Houser (1995) Somatostatin neurons are a subpopulation of GABA neurons in the rat dentate gyrus: Evidence from colocalization of pre-prosomatostatin and glutamate decarboxylase messenger RNAs. Neuroscience 64:339-355.
23. Gall, C., and L. Selawski (1984) Supramammillary afferents to guinea pig hippocampus contain substance P-like immunoreactivity. Neurosci. Lett. 51:171-176.
24. Gao, B., and J.M. Fritschy (1994) Selective allocation of GABAA receptors containing the alfa1 subunit to neurochemically distinct subpopulations of rat hippocampal interneurons. Eur. J. Neurosci. 6:837-853.
25. Gulyás, A.I., and T.F. Freund (1996) Calbindin-containing interneurons innervate pyramidal cell dendrites in the hippocampus. Hippocampus, (in press).
26. Gulyás, A.I., T.J. Gores, and T.F. Freund (1990) Innervation of different peptide-containing neurons in the hippocampus by GABAergic septal afferents. Neuroscience 37:31-44.
27. Gulyás, A.I., K. Tóth, P. Danos, and T.F. Freund (1991) Subpopulations of GABAergic neurons containing parvalbumin, calbindin D28k, and cholecystokinin in the rat hippocampus. J. Comp. Neurol. 312:371-378.
28. Gulyás, A.I., R. Miettinen, D.M. Jacobowitz, and T.F. Freund (1992) Calretinin is present in non-pyramidal cells of the rat hippocampus - I. A new type of neuron specifically associated with the mossy fibre system. Neuroscience 48:1-27.
29. Gulyás, A.I., R. Miles, N. Hajos, and T.F. Freund (1993a) Precision and variability in postsynaptic target selection of inhibitory cells in the hippocampal CA3 region. Eur. J. Neurosci. 5:1729-1751.
30. Gulyás, A.I., R. Miles, A. Sík, K. Tóth, N. Tamamaki, and T.F. Freund (1993b) Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 366:683-687.
31. Gulyás, A.I., N. Hájos, and T.F. Freund (1996) Interneurons containing calretinin are specialised to control other interneurons in the rat hippocampus. J.Neurosci 16:3397-3411.
32. Hájos, N., L. Acsády, and T.F. Freund (1996) Target selectivity and neurochemical characteristics of VIP-immonopositive interneurons in the rat dentate gyrus. Eur. J. Neurosci. 8:1415-1431.
33. Han, Z.S., E.H. Buhl, Z. Lôrinczi, 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.
34. Ino, T., K. Itoh, T. Sugimoto, T. Kaneko, H. Kamiya, and N. Mizuno (1989) The supramammillary region of the cat sends substance P-like immunoreactive axons to the hippocampal formation and entorhinal cortex. Neurosci. Lett. 50:259-264.
35. Iritani, S., M. Fujii, and K. Satoh (1989) The distribution of substance P in the cerebral cortex and hippocampal formation: An immunohistochemical study in the monkey and rat. Brain. Res. Bull. 22:295-303.
36. Kaneko, T., R. Shigemoto, S. Nakanishi, and N. Mizuno (1994) Morphological and chemical characteristics of substance P receptor-immunoreactive neurons in the rat neocortex. Neuroscience 60:199-211.
37. Katona, I., L. Acsády, A. Gulácsi, and T.F. Freund (1996) Somatostatin-containing cells in the rat hippocampus: Connectivity and neurochemical heterogeneity. Eur. J. Neurosci. 9(Suppl.): 176.
38. Kawaguchi, Y., H. Katsumaru, T. Kosaka, C.W. Heizmann, and K. Hama (1987) Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin. Brain Res. 416:369-374.
39. Köhler, C., and V. Chan-Palay (1983) Somatostatin-like immunoreactive neurons in the hippocampus: An immunohistochemical study in the rat. Neurosci. Lett. 34:259-265.
40. Köhler, C., L. Eriksson, S. Davies, and V. Chan-Palay (1986) Neuropeptide Y innervation of the hippocampal region in the rat and monkey brain. J. Comp. Neurol. 244:384-400.
41. Köhler, C., L. Eriksson, S. Davies, and V. Chan-Palay (1987) Co-localization of neuropeptide tyrosine and somatostatin immunoreactivity in neurons of individual subfields of the rat hippocampal region. Neurosci. Lett. 78:1-6.
42. Kosaka, T., K. Kosaka, K. Tateishi, Y. Hamaoka, N. Yanaihara, J.Y. Wu, and K. Hama (1985) GABAergic neurons containing CCK-8-like and/or VIP-like immunoreactivities in the rat hippocampus and dentate gyrus. J. Comp. Neurol. 239:420-430.
43. 2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res. 419:119-130.
44. Lacaille, J.C., and P.A. Schwartzkroin (1988a) Stratum lacunosum-moleculare interneurons of hippocampal CA1 region. I. Intracellular response characteristics, synaptic responses, and morphology. J. Neurosci. 8:1400-1410.
45. Lacaille, J.C., and P.A. Schwartzkroin (1988b) Stratum lacunosum-moleculare interneurons of hippocampal CA1 region. II. Intrasomatic and intradendritic recordings of local circuit synaptic interactions. J. Neurosci. 8:1411-1424.
46. Lacaille, J.C., A.L. Mueller, D.D. Kunkel, and P.A. Schwartzkroin (1987) Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: Electrophysiology and morphology. J. Neurosci. 7:1979-1993.
47. Lantos, T.A., T.J. Göres, and M. Palkovits (1995) Immunohistochemical mappings of neuropeptides in the premamillary region of the hypothalamus in rats. Brain Res. Rev. 20:209-249.
48. Léránth, C., and M. Frotscher (1986) Synaptic connections of cholecystokinin-immunoreactive neurons and terminals in the rat fascia dentata: a combined light and electron microscopic study. J. Comp. Neurol. 254:51-64.
49. Léránth, C., and R. Nitsch (1994) Morphological evidence that hypothalamic substance P-containing afferents are capable of filtering the signal flow in the monkey hippocampal formation. J. Neurosci. 14:4079-4094
50. Léránth, 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.
51. Liu, H., J.L. Brown, L. Jasmin, J.E. Maggio, S.R. Vigna, P.W. Mantyh, and A.I. Basbaum (1994) Synaptic relationship between substance P and the substance P receptor: Light and electron microscopic characterization of the mismatch between neuropeptides and their receptors. Proc. Natl. Acad. Sci. USA 91:1009-1013.
52. Ljungdahl, A., T. Hokfelt, and G. Nilsson (1978) Distribution of substance P-like immunoreactivity in the central nervous system of the rat-I. Cell bodies and nerve terminals. Neuroscience 3:861-943.
53. Maglóczky, Z., L. Acsády, and T.F. Freund (1994) Principal cells are the postsynaptic targets of supramammillary afferents in the hippocampus of the rat. Hippocampus 4:322-334.
54. Mantyh, P.W., T. Gates C.R. Mantyh and J.E. Maggio (1989) Autoradiographic localization and characterization of tachykinin receptor binding sites in the rat brain and peripheral tissues. J Neurosci. 9:258-279.
55. Mantyh, P.W., C.J. Allen, J.R. Ghilardi, S.D. Rogers, C.R. Mantyh, H. Liu, A.I. Basbaum, S.R. Vigna, and J.E. Maggio (1995) Rapid endocytosis of a G protein coupled receptor: Substance P-evoked internalization of its receptor in the rat striatum in vivo. Proc. Natl. Acad. Sci. USA 92:2622-2626.
56. McBain, C.J., T.J. DiChiara, and J.A. Kauer (1994) Activation of metabotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission. J. Neurosci. 14:4433-4445.
57. Michelson, H.B., and R.K.S. Wong (1991) Excitatory synaptic responses mediated by GABAA receptors in the hippocampus. Science 253:1420-1423.
58. Miettinen, R., A.I. Gulyás, K.G. Baimbridge, D.M. Jacobowitz, and T.F. Freund (1992) Calretinin is present in non-pyramidal cells of the rat hippocampus - II. Co-existence with other calcium binding proteins and GABA. Neuroscience 48:29-43.
59. Miles, R., K. Tóth, A.I. Gulyás, N. Hájos, and T.F. Freund (1996) Distinct functional roles for somatic and dendritic inhibition in hippocampus. Neuron 16:815-823.
60. Morrison, J.H., R. Benoit, P.J. Magistretti, N. Ling, and F.E. Bloom (1982) Immunohistochemical distribution of pro-somatostatin-related peptides in hippocampus. Neurosci. Lett. 34:137-142.
61. Müller, W., and U. Misgeld (1990) Inhibitory role of dentate hilus neurons in guinea pig hippocampal slice. J. Neurophysiol. 64:46-56.
62. Nakaya, Y., T. Kaneko, R. Shigemoto, S. Nakanishi, and N. Mizuno (1994) Immunohistochemical localization of substance P receptor in the central nervous system of the adult rat. J. Comp. Neurol. 347:249-274.
63. Nunzi, M.G., A. Gorio, F. Milan, T.F. Freund, P. Somogyi, and A.D. Smith (1985) Cholecystokinin-immunoreactive cells form symmetrical synaptic contacts with pyramidal and nonpyramidal neurons in the hippocampus. J. Comp. Neurol. 237:485-505.
64. Ribak, C.E., (1992) Local circuitry of GABAergic basket cells in the dentate gyrus. In Ribak, C.E., Gall, C.M., and Mody I. (eds): The Dentate Gyrus and Its Role in Seizures. Elsevier Science, pp. 29-49.
65. Ribak, C.E., R. Nitsch, and L. Seress (1990) Proportion of parvalbumin-positive basket cells in the GABAergic innervation of pyramidal and granule cells of the rat hippocampal formation. J. Comp. Neurol. 300:449-61.
66. Roberts, G.W., P.L. Woodhams, J.M. Polak, and T.J. Crow (1984) Distribution of neuropeptides in the limbic system of the rat: The hippocampus. Neuroscience 11:35-77.
67. Rogers, J.H. (1989) Two calcium-binding proteins mark many chick sensory neurons. Neuroscience 31:697-709.
68. Scharfman, H.E. ( 1995) Electrophysiological diversity of pyramidal-shaped neurons at the granule cell layer/hilus border of the rat dentate gyrus recorded in vitro. Hippocampus 5:287-305.
69. Seress, L., and C. Léránth (1996) Distribution of substance P-immunoreactive neurons and fibers in the monkey hippocampal formation. Neuroscience 71:633-650.
70. Shigemoto, R., Y. Nakaya, S. Nomura, R. Ogawa-Meguro, H. Ohishi, T. Kaneko, S. Nakanishi, and N. Mizuno (1993) Immunocytochemical localization of rat substance P receptor in striatum. Neurosci. Lett. 153:157-160.
71. Sík, A., M. Penttonen, A. Ylinen, and G. Buzsáki (1995) Hippocampal CA1 interneurons: An in vivo intracellular labeling study. J. Neurosci. 15:6651-6665.
72. Sik, A., M. Penttonen, and G. Buzsáki (1996) Interneurons in the dentate gyrus: An in vivo intracellular study. Eur. J. Neurosci., (in press).
73. Sloviter, R.S., and G. Nilaver (1987) Immunocytochemical localization of GABA-, cholecystokinin-, vasoactive intestinal polypeptide-, and somatostatin-like immunoreactivity in the area dentata and hippocampus of the rat. J. Comp. Neurol. 256:42-60.
74. Soltész, I., and M. Deschenes (1993) Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. J. Neurophysiol. 70:97-116.
75. Somogyi, P., M.G. Nunzi, A. Gorio, and A.D. Smith (1983) A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells. Brain Res. 259:137-142.
76. Somogyi, P., A.J. Hodgson, A.D. Smith, M.G. Nunzi, A. Gorio, and J.Y. Wu (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.
77. Somogyi, P., T.F. Freund, A.J. Hodgson, J. Somogyi, D. Beroukas, and I.W. Chubb (1985) Identified axo-axonic cells are immunoreactive for GABA in the hippocampus and visual cortex of the cat. Brain Res. 332:143-149.
78. Soriano, E., and M. Frotscher (1993) 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.
79. 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.
80. Tóth, K., and T.F. Freund (1992) Calbindin D28k-containing nonpyramidal cells in the rat hippocampus: Their immunoreactivity for GABA and projection to the medial septum. Neuroscience 49:793-805.
81. Tóth, K., Z. Borhegyi, and T.F Freund (1993) Postsynaptic targets of GABAergic hippocampal neurons in the medial septum-diagonal band of Broca complex. J. Neurosci. 13:3712-3724.
82. Whittington, M.A., R.D. Traub, and J.G.R. Jeffrey (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373:612-615.
83. Yanagihara, M., and K. Niimi (1989) Substance P-like immunoreactive projection to the hippocampal formation from the posterior hypothalamus in the cat. Brain Res. Bull. 22:682-694.
84. Ylinen, A., A. Bragin, Z. Nádasdy, G. Jandó, I. Szabó, A. Sík, and G. Buzsáki (1995) Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: Network and intracellular mechanisms. J. Neurosci. 15:30-46.