Hippocampal CA1 interneurons: An in vivo intracellular labeling study

Journal of Neuroscience

Volumn 15, Issue 10, 1995, Pages 6651-6665

  Sik, Attila ^a,b   Penttonen, Markku ^a,c   Ylinen, Aarne ^a,d   Buzsáki, György ^a  

^a RUTGERS UNIVERSITY   (United States)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^d UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

axonal tree; biocytin; calbindin; calretinin; GABA(A); GABA(B); hippocampus; inhibition; interneurons; network; parvalbumin; synapses

Indexed keywords

BIOCYTIN; CALBINDIN; CALRETININ; PARVALBUMIN;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; INHIBITORY POSTSYNAPTIC POTENTIAL; NERVE CELL NETWORK; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0028810185     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.15-10-06651.1995     Document Type: Article

References (80)

1. Aika Y, Ren JQ, Kosaka K, Kosaka T (1994) Quantitative analysis of GABA-like immunoreactivity and parvalbumin containing neurons in the CA1 region of the rat hippocampus using a stereological method, the disector. Exp Brain Res 99:267-276.
2. Alger BE, Nicoll RA (1982) Feed-forward dendritic inhibition in rat hippocampal pyramidal cells studied in vitro. J Physiol (Lond) 328: 105-123.
3. Alonso A, Kohler C (1982) Evidence for separate projections of hippocampal pyramidal and non-pyramidal neurons to different parts of the septum in the rat brain. Neurosci Lett 31:209-214.
4. Amaral D, Witter M (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31:571-591.
5. Andersen P, Eccles JC, Loyning Y (1963) Recurrent inhibition in the hippocampus with identification of the inhibitory cell and its synapse. Nature 198:540-542.
6. Baimbridge KG, Miller JJ (1982) Immunocytochemical localization of calcium-binding protein in cerebellum, hippocampal formation and olfactory bulb of the rat. Brain Res 245:223-229.
7. Baude A, Nuesser Z, Roberts JDB, Mulvihill E, Mcllhinney RAJ, Somogyi P (1993) The metebotropic glutamate receptor (mGluR1a) is concentrated at perisynaptic membrane membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11:771-787.
8. Bragin A, Jandó G, Nádasdy 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.
9. Buckmaster PS, Schwartzkroin PA (1995) Interneurons and inhibition in the dentate gyrus of the rat in vivo. J Neurosci 15:774-789.
10. Buhl E, Halasy K, Somogyi P (1994) Hippocampal unitary inhibitory postsynaptic potentials: diverse sources and number of synaptic release sites. Nature 368:823-828.
11. Buzsáki G (1984) Feed-forward inhibition in the hippocampal formation. Prog Neurobiol 22(1):31-153.
12. Buzsáki G, Eidelberg E (1982) Direct afferent excitation and long-term potentiation of hippocampal interneurons. J Neurophysiol 48:597-607.
13. Buzsáki G, Chrobak JJ (1995) Temporal structure in spatially organized neuronal ensembles: a role for interneuron networks. Curr Opin Neurobiol 5:504-510.
14. Buzsáki G, Leung L, Vanderwolf CH (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res Rev 6:139-171.
15. Buzsáki G, Horvath Z, Urioste R, Hetke J, Wise K (1992) High-frequency network oscillation in the hippocampus. Science 256:1025-1027.
16. Celio MR (1986) Parvalbumin in most γ-aminobutyric acid-containing neurons of the rat cerebral cortex. Science 231:995-997.
17. Faber DS, Young, WS, Legende P, Korn H (1992) Intrinsic quantal variability due to stochastic properties of receptor-transmitter interactions. Science 258:1494-1.
18. Finch DM, Nowlin NL, Babb TL (1983) Demonstration of axonal projection of neurons in the rat hippocampus and subiculum by intracellular injection of HRP. Brain Res 271:201-216.
19. Fraser DD, Mac Vicar BA (1991) Low-threshold transient calcium current in rat hippocampal lacunosum-moleculare interneurons: kinetics and modulation by neurotransmitters. J Neurosci 11:2812-2820.
20. Freund TF, Gulyás AI, Acsady L, Gorcs T, Tóth K (1990) Serotonergic control of the hippocampus via local inhibitory interneurons. Proc Natl Acad Sci USA 87:8501-8505.
21. Gulyás AI, Tóth K, Danos P, Freund TF (1991) Subpopulations of GABAergic neurons containing parvalburnin, calbindin D28k, and cholecystokinin in the rat hippocampus. J Comp Neurol 312:371-378.
22. Gulyás IA, Mietinen R, Jacobowitz MD, Freud TF (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 1:1-27.
23. 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.
24. Gulyás AI, Miles R, Sik A, Tóth K, Tamamaki N, Freund TF (1993b) Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 366:683-687.
25. Halasy K, Somogyi P (1993) Subdivision in the multiple GABAergic innervation of granule cells in the dentate gyrus of the rat hippocampus. Eur J Neurosci 5:411-429.
26. Han ZS, Buhl EH, Lörinczi 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.
27. Kawaguchi Y, Hama K (1987a) Two subtypes of non-pyramidal cells in rat hippocampal formation identified by intracellular recording and HRP injection. Brain Res 411:190-195.
28. Kawaguchi Y, Hama K (1987b) Fast-spiking non-pyramidal cells in the hippocampal CA3 region, dentate gyrus and subiculum of rats. Brain Res 425:351-355.
29. Kawaguchi Y, Katsumaru H, Kisaka T, Heizmann CW, Hama K (1987) Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin. Brain Res 416:369-374.
30. Kosaka T, Wu JY, Benoit R (1988) GABAergic neurons containing somatostatin-like immunoreactivity in the rat hippocampus and dentate gyrus. Exp Brain Res 71:388-398.
31. Kunkel DD, Lacaille J, Schwartzkroin PA (1988) Ultrastructure of stratum lacunosum-moleculare interneurons of hippocampal CA1 region. Synapse 2:382-394.
32. Lacaille CJ (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.
33. Lacaille CJ, Schwartzkroin AP (1988a) Stratum lacunosum-moleculare interneurons of hippocampal CA1 region. I. Intracellular response characteristics, synaptic responses, and morphology. Neuroscience 8:1400-1410.
34. Lacaille CJ, Schwartzkroin AP (1988b) Stratum lacunosum-moleculare interneurons of hippocampal CA1 region. II. Intrasomatic and intradendritic recordings of local circuit synaptic interactions. Neuroscience 8:1411-1424.
35. Lacaille J, Williams S (1990) Membrane properties of interneurons in stratum oriens-alveus of the CA1 region of rat hippocampus in vitro. Neuroscience 36:349-359.
36. Lacaille JC, Mueller A, 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.
37. Leung LS, Yim CY (1991) Intrinsic membrane potential oscillations in hippocampal neurons in vitro. Brain Res 553:261-274.
38. 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 the rat hippocampus. Exp Brain Res 90:519-525.
39. 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.
40. Llinás RR (1988) The intrinsic electrophysiological properties of mammalian neurons: insight into central nervous system function. Science 242::1654-1664.
41. Lopes da Silva FH, Witter MP, Boeijinga PH, Lohman AHM (1990) Anatomic organization and physiology of the limbic cortex. Physiol Rev 70:453-511.
42. McBain CJ (1994) Hippocampal inhibitory neuron activity in the etevated potassium model of epilepsy. J Neurophysiol 72:2653-2863.
43. McBain CJ, Dingledine R (1993) Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurons of rat hippocampus. J Physiol (Lond) 462:373-392.
44. 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.
45. Michelson HB, Wong RKS (1991) Excitatory synaptic responses mediated by GABA receptors in the hippocampus. Science 253:1420-1423.
46. Miettinen, R, Gulyás AI, Baimbridge GK, Jacobowitz MD, Freund FT (1992) Calretinin is present in non-pyramidal cells of the rat hippocampus - II. Co-existence with other calcium binding proteins and GABA. Neuroscience 1:29-43.
47. Miles R, Poncer JC (1993) Metabotropic glutamate receptors mediate a post-tetanic excitation of hippocampal inhibitory neurones. J Physiol (Lond) 463:461-473.
48. Miles R, Tóth K, Gulyás AI, Hájos N, Freund TF (1994) Distinct functional roles for somatic and dendritic inhibition in hippocampus. Soc Neurosci Abstr 20:710.
49. Misgeld U, Frotscher M (1986) Postsynaptic-GABAergic inhibition of non-pyramidal neurons in the guinea-pig hippocampus. Neuroscience 19:193-206.
50. Nicoll RA (1994) Cajal's rational psychology. Nature 368:808-809.
51. Otis TS, de Koninck Y, Mody I (1994) Lasting potentiation of inhibition is associated with an increased number of γ-aminobutiric acid type A receptors activated during miniature inhibitory postsynaptic currents. Proc Natl Acad Sci USA 91:7698-7702.
52. Ramón y Cajal S (1911) Histologie du Systéme Nerveux de l'Homme et des Vertebrés. Paris: Maloine.
53. Ribak CE, Seress L, Peterson GM, Seroogy KB, Fallon JH, Schmued LC (1986) A GABAergic inhibitory component within the hippocampal commissural pathway. J Neurosci 6:3492-3.
54. Rogers JH (1989) Two calcium binding proteins mark many chick sensory neurons. Neuroscience 31:679-711.
55. Sah P, Hestrin S, Nicill RA (1990) Properties of excitatory postsynaptic currents recorded in vitro from rat hippocampal interneurons. J Physiol (Lond) 430:605-616.
56. Scharfman HE, Kunkel DD, Schwartzkroin PA (1990) Synaptic connections of dentate granule cells and hilar neurons: results of paired intracellular recordings and intracellular horseradish peroxidase injections. Neuroscience 37:693-707.
57. Schwartzkroin PA, Mathers LH (1978) Physiological and morphological identification of a nonpyramidal cell type. Brain Res 157:1-10.
58. Schwartzkroin PA, Kunkel DD (1985) Morphology of identified interneurons in the CA1 regions of guinea pig hippocampus. J Comp Neurol 232:205-218.
59. Seeburg PH (1993) The molecular biology of mammalian glutamate receptor channels. Trends Neurosci 16:369-365.
60. Sik A, Tamamaki N, Freund TF (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.
61. Sik A, Ylinen A, Penttonen M, Buzsaki G (1994a) Inhibitory CA1-CA3-hilar region feedback in the hippocampus. Science 265:1722-1724.
62. Sik A, Penttonen M, Ylinen A, Horvath Z, Buzsáki G (1994b) Intracellularly labeled hippocampal interneurons in vivo. Soc Neurosci Abstr 19:148.15.
63. 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.
64. Sloviter RS, Nilaver G (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.
65. Soltész I, Deschenes 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.
66. 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 137-142.
67. Somogyi P, Hodgson AJ, Smith AD, Nunzi MG, Gorio A, Wu JY (1984) Different populations of GABAergic neurons in the visula cortex and hippocampus of the cat containing somatostatin- or cholecystokinin-immunoreactive material. J Neurosci 4:2590-2603.
68. Struble RG, Desmond NL, Levy WB (1978) Anatomical evidence of interlamellar inhibition in the fascia dentata. Brain Res 152:580-585.
69. Tamamaki N, Nojyo Y (1990) Disposition of the slab-like modules formed by axon branches originating from single CA1 pyramidal neurons in the rat hippocampus. J Comp Neurol 291:509-519.
70. Tamamaki N, Nojyo Y (1991) Crossing fiber arrays in the rat hippocampus as demonstrated by three-dimensional reconstruction. J Comp Neurol 303:435-442.
71. Tamamaki N, Nojyo Y (1995) Preservation of reciprocal connections between the subiculum, field CA1 and the entorhinal cortex in the rats. J Comp Neurol, in press.
72. Tamamaki, N, Abe K, Nojyo Y (1988) Three-dimensional analysis of the whole axonal arbors originating from single CA2 pyramidal neurons in the rat hippocampus with the aid of a computer graphic technique. Brain Res 452:255-272.
73. Thompson SM, Gähwiler BH (1989) Activity-dependent disinhibition. I. Repetitive stimulation reduces IPSP driving force and conductance in the hippocampus in vitro. J Neurophysiol 61:501-511.
74. Tóth K, Freund TF (1992) Calbindin D28k-containing nonpyramidal cells in the rat hippocampus: their immunoreactivity for GABA and projection to the medial septum. Neuroscience 49:793-805.
75. Tóth K, Borhegyi Z, Freund TF (1993) Postsynaptic targets of GABAergic hippocampal neurons in the medial septum-diagonal band of Broca complex. J Neurosci 13:3712-3724.
76. Traub RD, Miles R (1991) Neuronal networks of the hippocampus. Cambridge: Cambridge UP.
77. Traub RD, Jefferys JGR, Miles R, Whittington MA, Toth K (1994) A branching dendritic model of a rodent CA3 pyramidal neurone. J Physiol (Lond) 481:79-95.
78. Whittington MA, Traub RD, Jefferys JGR (1995) Metabotropic receptor activation drives synchronized 40 Hz oscillations in networks of inhibitory interneurons. Nature 373:612-615.
79. Ylinen A, Bragin A, Nadasdy Z, Jando G, Szabo I, Sik A, Buzsáki G (1995a) Sharp wave associated high frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15:30-46.
80. Ylinen A, Soltész I, Bragin A, Penttonen M, Sik A, Buzsáki G (1995b) Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells and basket cells. Hippocampus 5:78-90, 1995.