Synaptic target selectivity and input of GABAergic basket and bistratified interneurons in the CA1 area of the rat hippocampus

Hippocampus

Volumn 6, Issue 3, 1996, Pages 306-329

  Halasy, Katalin ^a,b   Buhl, Eberhard H ^a,d   Lörinczi, Zoltán ^a,c   Tamás, Gábor ^b   Somogyi, Peter ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF SZEGED   (Hungary)

^c UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

^d MRC Anat Neuropharmacology Unit   (United Kingdom)

Author keywords

Dendritic innervation; Electron microscopy; GABA; Inhibition; Intracellular labeling

Indexed keywords

4 AMINOBUTYRIC ACID; BIOCYTIN;

ANIMAL CELL; ARTICLE; DENDRITE; HIPPOCAMPUS; INNERVATION; INTERNEURON; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPSE;

EID: 0029792662     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-1063(1996)6:3<306::AID-HIPO8>3.0.CO;2-K     Document Type: Article

References (81)

1. Acsády L, Halasy K, Freund TF (1993) Calretinin is present in nonpyramidal cells of the rat hippocampus. III. Their inputs from the median raphe and medial septal nuclei. Neuroscience 52:829-841.
2. Acsády L, Arabadzisz D, Freund TF (1996) Correlated morphological and neurochemical features identify different subsets of VIP-immunoreactive interneurons in rat hippocampus. Neuroscience 73:299-315.
3. Aika Y, Ren JQ, Kosaka K, Kosaka T (1994) Quantitative analysis of GABA-like-immunoreactive and parvalbumin-containing neurons in the CA1 region of the rat hippocampus using a stereological method, the disector. Exp Brain Res 99:267-276.
4. Andersen P, Eccles JC, Loyning Y (1963) Recurrent inhibition in the hippocampus with identification of the inhibitory cell and its synapses. Nature 198:540-542.
5. Andersen P, Eccles JC, Loyning Y (1964) Location of postsynaptic inhibitory synapses on hippocampal pyramids. J Neurophysiol 27:592-607.
6. Arancio O, Korn H, Gulyás A, Freund T, Miles R (1994) Excitatory synaptic connections onto rat hippocampal inhibitory cells may involve a single transmitter release site. J Physiol (Lond) 481:395-405.
7. Blackstad TW, Flood PR (1963) Ultrastructure of hippocampal axosomatic synapses. Nature 198:542-543.
8. Boeijinga PH, Lopes da Silva FH (1988) Differential distribution of beta and theta EEG activity in the entorhinal cortex of the cat. Brain Res 448:272-286.
9. Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsáki G (1995) Gamma (40-100 hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15:47-60.
10. Buhl EH, Halasy K, Somogyi P (1994a) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368:823-828.
11. Buhl EH, Han Z-S, Lorinczi Z, Stezhka VV, Karnup SV, Somogyi P (1994b) Physiological properties of anatomically identified axo-axonic cells in the rat hippocampus. J Neurophysiol 71:1289-1307.
12. Buhl EH, Cobb SR, Halasy K, Somogyi P (1995) Properties of unitary IPSPs evoked by anatomically identified basket cells in the rat hippocampus. Eur J Neurosci 7:1989-2004.
13. Buhl EH, Szilagyi T, Halasy K, Somogyi P (1996) Physiological properties of anatomically identified basket and bistratified cells in the CA1 area of the rat hippocampus. Hippocampus 6:294-305.
14. Buzsáki G, Chrobak JJ (1995) Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr Biol 5:504-510.
15. Buzsáki G, Penttonen M, Bragin A, Nadasdy Z, Chrobak JJ (1995) Possible physiological role of the perforant path-CA1 projection. Hippocampus 5:141-146.
16. Celio MR (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375-475.
17. Charpak S, Pare D, Llinas R (1995) The entorhinal cortex entrains fast CA1 hippocampal oscillations in the anaesthetized guinea-pig: role of the monosynaptic components of the perforant path. Eur J Neurosci 7:1548-1557.
18. Chrobak JJ, Buzsáki G (1994) Selective activation of deep layer (V-VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat. J Neurosci 14:6160-6170.
19. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75-78.
20. Colbert CM, Levy WB (1992) Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by glutamate receptors. J Neurophysiol 68:1-8.
21. Freund TF, Antal M (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336: 170-173.
22. Freund TF, Gulyás AI, Acsády L, Gorcs L, Tóth K (1990) Serotonergic control of the hippocampus via local inhibitory interneurons. Proc Natl Acad Sci USA 87:8501-8505.
23. Gabbiani F, Midtgaard J, Knopfel T (1994) Synaptic integration in a model of cerebellar granule cells. J Neurophysiol 72:999-1009.
24. Gall C (1984) The distribution of cholecystokinin-like immunoreactivity in the hippocampal formation of the guinea pig: localization in the mossy fibers. Brain Res 306:73-83.
25. A receptors containing the α1 subunit to neurochemically distinct subpopulations of rat hippocampal interneurons. Eur J Neurosci 6:837-853.
26. Greenwood RS, Godar E, Reaves TA, Hayward JN (1981) Cholecystokinin in hippocampal pathways. J Comp Neurol 203:335-350.
27. Gulyás AI, Gores TJ, Freund TF (1990) Innervation of different peptide-containing neurons in the hippocampus by GABAergic septal afferents. Neuroscience 37:31-44.
28. Gulyás AI, Tóth K, Danos P, Freund TF (1991) Subpopulations of GABAergic neurons containing parvalbumin, calbindin D28k, and cholecystokinin in the rat hippocampus. J Comp Neurol 312:371-378.
29. Gulyás AI, Miles R, Hajos N, Freund TF (1993a) Precision and variability in postsynaptic target selection of inhibitory cells in the hippocampal CA3 region. Eur J Neurosci 5:1729-1751.
30. Gulyás AI, Miles R, Sík A, Tóth K, Tamamaki N, Freund TF (1993b) Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 366:683-087.
31. Halasy K, Somogyi P (1993) Subdivisions in the multiple GABAergic innervation of granule cells in the dentate gyrus of the rat hippocampus. Eur J Neurosci 5:411-429.
32. Han Z-S, Buhl EH, Lorinczi Z, 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.
33. Harris KM, Marshall PE, Landis DMD (1985) Ultrastructural study of cholecystokinin-immunoreactive cells and processes in area CA1 of the rat hippocampus. J Comp Neurol 233:147-158.
34. Hendry SHC, Jones EG (1985) Morphology of synapses formed by cholecystokinin-immunoreactive axon terminals in regio superior of rat hippocampus. Neuroscience 16:57-68.
35. Hodgson AJ, Penke B, Erdei A, Chubb IW, Somogyi P (1985) Antisera to γ-aminobutyric acid. I. Production and characterization using a new model system. J Histochem Cytochem 33:229-239.
36. Ishizuka N, Weber J, Amaral DG (1990) Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol 295:580-623.
37. Karsumaru H, Kosaka T, Heizmann CW, Hama K (1988) Immunocytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus. Exp Brain Res 72:347-362.
38. Kawaguchi Y, 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.
39. Kawaguchi Y, Hama K (1988) Physiological heterogeneity of nonpyramidal cells in rat hippocampal CA1 region. Exp Brain Res 72:494-502.
40. 2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res 419:119-130.
41. Kosaka T, Wu JY, Benoit R (1988) GABAergic neurons containing somatostatin-like immunoreactiviry in the rat hippocampus and dentate gyrus. Exp Brain Res 71:388-398.
42. Kunkel DD, Schwartzkroin PA (1988) Ultrastructural characterization and GAD co-localization of somatostatin-like immunoreactive neurons in CA1 of rabbit hippocampus. Synapse 2:371-381.
43. Kunkel DD, Lacaille J-C, Schwartzkroin PA (1988) Ultrastructure of stratum lacunosum-moleculare interneurons of hippocampal CA1 region. Synapse 2:382-394.
44. Lacaille J-C, Schwartzkroin PA (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, Schwartzkroin PA (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, Williams S (1990) Membrane properties of interneurons in stratum oriens-alveus of the CA1 region of rat hippocampus in vitro. Neuroscience 36:349-359.
47. Lacaille J-C, Mueller AL, Kunkel DD, Schwartzkroin PA (1987) Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J Neurosci 7:1979-1993.
48. Li X-G, Somogyi P, Tepper JM, Buzsáki G (1992) Axonal and dendritic arborization of an intracellularly labeled chandelier cell in the CA1 region of rat hippocampus. Exp Brain Res 90:519-525.
49. Li X-G, Somogyi P, Ylinen A, Buzsáki G (1994) The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol 339:181-208.
50. Lopes da Silva FH, Witter MP, Boeijinga PH, Lohman AHM (1990) Anatomic organization and physiology of the limbic system. Physiol Rev 70:453-511.
51. 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.
52. McBain CJ, DiChiara TJ, Kauer JA (1994) Activation of metabotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission. J Neurosci 14:4433-4445.
53. Miettinen R, Gulyás AI, Baimbridge KG, Jacobowitz DM, Freund TF (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.
54. Miles R, Tóth K, Gulyás AI, Hajos N, Freund TF (1994) Different functions for dendritic and somatic inhibitory cells of the hippocampus. J Physiol (Lond) 480P:32.
55. Nunzi MG, Gorio A, Milan F, Freund TF, Somogyi P, Smith AD (1985) Cholecystokinin-immunoreactive cells form symmetrical synaptic contacts with pyramidal and non-pyramidal neurons in the hippocampus. J Comp Neurol 237:485-505.
56. Nusser Z, Roberts JDB, Baude A, Richards JG, Sieghart W, Somogyi P (1995) Immunocytochemical localisation of the α1 and β2/3 subunits of the GABAA receptor in relation to specific GABAergic synapses in the dentate gyrus. Eur J Neurosci 7:630-646.
57. Peters A, Palay SL, Webster H (1991) The fine structure of the nervous system. New York: Oxford University Press.
58. Ramón y Cajal S (1893) Estructura del asta de ammon y fascia dentata. Anal Soc Espan Historia Natural 22:53-114.
59. Ribak CE, Vaughn JE, Saito K (1978) Immunocytochemical localization of glutamic acid decarboxylase in neuronal somata following colchicine inhibition of axonal transport. Brain Res 140:315-332.
60. Ryugo DK, Wu MM, Pongstaporn T (1996) Activity-related features of synapse morphology: a study of endbulbs of Held. J Comp Neurol 365:141-158.
61. Schaffer K (1892) Beitrag zur Histologie der Ammonshorn-formation. Arch Mikrosk Anat 39:611-632
62. Schwartzkroin PA, Kunkel DD (1985) Morphology of identified interneurons in the CA1 regions of guinea pig hippocampus. J Comp Neurol 232:205-218.
63. Schwartzkroin PA, Mathers LH (1978) Physiological and morphological identification of a nonpyramidal hippocampal cell type. Brain Res 157:1-10.
64. Schwartzkroin PA, Mueller AL (1987) Electrophysiology of hippocampal neurons. In: Cerebral cortex. Further aspects of cortical function, including hippocampus (Jones EG, Peters A, eds), pp 295-343. New York: Plenum Press.
65. Seress L, Ribak CE (1990) The synaptic connections of basket cell axons in the developing rat hippocampal formation. Exp Brain Res 81:500-508.
66. 28k-immunoreactive neurons in the human hippocampal formation. J Comp Neurol 337:208-230.
67. Sík A, Ylinen A, Penttonen M, Buzsáki G (1994) Inhibitory CA1-CA3-hilar region feedback in the hippocampus. Science 265:1722-1724.
68. Sík A, Penttonen M, Ylinen A, Buzsáki G (1995) Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J Neurosci 15: 6651-6665.
69. Sloviter RS (1989) Calcium-binding protein (calbindin-D28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J Comp Neurol 280:183-196.
70. Soltész I (1995) A brief history of cortico-hippocampal time with a special reference to the direct entorhinal input to CA1. Hippocampus 5:120-124.
71. Soltész I, Deschênes M (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.
72. Soltész I, Smetters DK, Mody I (1995) Tonic inhibition originates from synapses close to the soma. Neuron 14:1273-1283.
73. Somogyi P (1988) Immunocytochemical demonstration of GABA in physiologically characterized, HRP-filled neurons and their postsynaptic targets. In: Molecular neuroanatomy. Techniques in the behavioral and neural sciences (van Leeuwen FW, Bujs RM, Pool CW, Pach O, eds), pp 339-359. Amsterdam: Elsevier.
74. Somogyi P, Nunzi MG, Gorio A, Smith AD (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.
75. Somogyi P, Hodgson AJ, Smith AD, Nunzi MG, Gorio A, Wu J-Y (1984) Different populations of GABAergic neurons in the visual cortex and hippocampus of car contain somatostatin- or cholecystokinin-immunoreactive material. J Neurosci 4:2590-2603.
76. Somogyi P, Freund TF, Hodgson AJ, Somogyi J, Beroukas D, Chubb IW (1985) Identified axo-axonic cells are immunoreactive for GABA in the hippocampus and visual cortex of the cat. Brain Res 332:143-149.
77. A receptor-mediated postsynaptic conductance. J Neurophysiol 68:197-212.
78. Thurbon D, Field A, Redman S (1994) Electrotonic profiles of interneurons in stratum pyramidale of the CA1 region of rat hippocampus. J Neurophysiol 71:1948-1958.
79. 28k-containing nonpyramidal cells in the rat hippocampus: their immunoreactivity for GABA and projection to the medial septum. Neuroscience 49:793-805.
80. Totterdell S, Smirh AD (1986) Cholecystokinin-immunoreactive boutons in synaptic contact with hippocampal pyramidal neurons that project to the nucleus accumbens. Neuroscience 19:181-192.
81. Woodson W, Nitecka L, Ben-Ari Y (1989) Organization of the GABAergic system in the rat hippocampal formation: a quantitative immunocytochemical study. J Comp Neurol 280:254-271.