Gap junctions linking the dendritic network of GABAergic interneurons in the hippocampus

Journal of Neuroscience

Volumn 20, Issue 4, 2000, Pages 1519-1528

  Fukuda, Takaichi ^a   Kosaka, Toshio ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Electron microscopy; GABA; Gap junctions; Hippocampus; Oscillation; Parvalbumin; Synchronization

Indexed keywords

4 AMINOBUTYRIC ACID; PARVALBUMIN;

ANIMAL TISSUE; ARTICLE; CELL ULTRASTRUCTURE; CORTICAL SYNCHRONIZATION; DENDRITE; ELECTRON MICROSCOPY; GAP JUNCTION; HIPPOCAMPUS; IMAGE RECONSTRUCTION; IMMUNOCYTOCHEMISTRY; INTERNEURON; MALE; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; RAT; SYNAPSE; THREE DIMENSIONAL IMAGING;

EID: 0034652245     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-04-01519.2000     Document Type: Article

References (57)

1. Ali AB, Thomson AM (1998) Facilitating pyramid to horizontal oriensalveus interneurone inputs: dual intracellular recordings in slices of rat hippocampus. J Physiol (Lond) 507:185-199.
2. 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.
3. Brightman MW, Reese TS (1969) Junctions between intimately apposed cell membranes in the vertebrate brain. J Cell Biol 40:648-677.
4. 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.
5. Buhl EH, Han Z-S, Lörinczi 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.
6. Buhl EH, Tamás G, Fisahn A (1998) Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. J Physiol (Lond) 513:117-126.
7. 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.
8. Cobb SR, Halasy K, Vida I, Nyiri G, Tamás G, Buhl EH, Somogyi P (1997) Synaptic effects of identified interneurons innervating both interneurons and pyramidal cells in the rat hippocampus. Neuroscience 79:629-648.
9. De Zeeuw CI, Lang EJ, Sugihara I, Ruigrok TJH, Eisenman LM, Mugnaini E, Llinás R (1996) Morphological correlates of bilateral synchrony in the rat cerebellar cortex. J Neurosci 16:3412-3426.
10. Fukuda T, Aika Y, Heizmann CW, Kosaka T (1996) Dense GABAergic input on somata of parvalbumin-immunoreactive GABAergic neurons in the hippocampus of the mouse. Neurosci Res 26:181-194.
11. Fukuda T, Aika Y, Heizmann CW, Kosaka T (1998) GABAergic axon terminals at perisomatic and dendritic inhibitory sites show different immunoreactivities against two GAD isoforms, GAD67 and GAD65, in the mouse hippocampus: a digitized quantitative analysis. J Comp Neurol 395:177-194.
12. Galarreta M, Hestrin S (1999) A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402:72-75.
13. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75-79.
14. Gray CM, König P, Engel AK, Singer W (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338:334-337.
15. Gulyás AI, Miles R, Sik A, Tóth K, Tamamaki N, Freund TF (1993) Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 366:683-687.
16. Halasy K, Buhl EH, Lörinczi Z, Tamás G, Somogyi P (1996) Synaptic target selectivity and input of GABAergic basket and bistratified interneurons in the CA1 area of the rat hippocampus. Hippocampus 6:306-329.
17. Jahr CE, Nicoll RA (1982) An intracellular analysis of dendrodendritic inhibition in the turtle in vitro olfactory bulb. J Physiol (Lond) 326:213-234.
18. 2+-binding parvalbumin in rat testis: characterization, localization, and expression during development. J Biol Chem 262:7314-7320.
19. Katsumaru H, Kosaka T, Heizmann CW, Hama K (1988a) Immunocytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus. Exp Brain Res 72:347-362.
20. Katsumaru H, Kosaka T, Heizmann CW, Hama K (1988b) Gap junctions on GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus (CA1 region). Exp Brain Res 72:363-370.
21. Knowles WD, Schwartzkroin PA (1981) Local circuit synaptic interactions in hippocampal brain slices. J Neurosci 1:318-322.
22. Kosaka T (1983a) Gap junctions between nonpyramidal cell dendrites in the rat hippocampus (CA1 and CA3 regions). Brain Res 271:157-161.
23. Kosaka T (1983b) Neuronal gap junctions in the polymorph layer of the rat dentate gyrus. Brain Res 277:347-351.
24. Kosaka T, Hama K (1985) Gap junctions between non-pyramidal cell dendrites in the rat hippocampus (CA1 and CA3 regions): a combined Golgi-electron microscopy study. J Comp Neurol 231:150-161.
25. Kosaka T, Nagatsu I, Wu J-Y, Hama K (1986) Use of high concentration of glutaraldehyde for immunocytochemistry of transmitter-synthesizing enzymes in the central nervous system. Neuroscience 18:975-990.
26. 2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res 419:119-130.
27. 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.
28. Llinás R, Baker R, Sotelo C (1974) Electrotonic coupling between neurons in cat inferior olive. J Neurophysiol 37:560-571.
29. 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.
30. Michelson HB, Wong RKS (1994) Synchronization of inhibitory neurons in the guinea-pig hippocampus in vitro. J Physiol (Lond) 477:5-45.
31. Miles R, Tóth K, Gulyás AI, Hájos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815-823.
32. Miltner WHR, Braun C, Arnold M, Witte H, Taub E (1999) Coherence of gamma-band EEG activity as a basis for associative learning. Nature 397:434-436.
33. Obata K, Kojima N, Nishiye H, Inoue H, Shirao T, Fujita SC, Uchizono K (1987) Four synaptic vesicle-specific proteins: identification by monoclonal antibodies and distribution in the nervous tissue and the adrenal medulla. Brain Res 404:169-179.
34. Obata K, Fukuda T, Konishi S, Ji F-Y, Mitoma H, Kosaka T (1999) Synaptic localization of the 67,000 molecular wt isoform of glutamate decarboxylase and transmitter function of GABA in the mouse cerebellum lacking the 65,000 molecular wt isoform. Neuroscience 93:1475-1482.
35. Oertel WH, Schmechel DE, Tappaz ML, Kopin IJ (1981) Production of a specific antiserum to rat brain glutamic acid decarboxylase by injection of an antigen-antibody complex. Neuroscience 6:2689-2700.
36. Pinching AJ, Powell TPS (1971) The neuropil of the glomeruli of the olfactory bulb. J Cell Sci 9:347-377.
37. Price JL, Powell TPS (1970) The morphology of the granule cells of the olfactory bulb. J Cell Sci 7:91-123.
38. Rafols JA, Valverde F (1973) The structure of the dorsal lateral geniculate nucleus in the mouse. A Golgi and electron microscopic study. J Comp Neurol 150:303-332.
39. Rall W, Shepherd GM, Reese TS, Brightman MW (1966) Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. Exp Neurol 14:44-56.
40. Rodriguez E, George N, Lachaux J-P, Martineric J, Renault B, Varela FJ (1999) Perception's shadow: long-distance synchronization of human brain activity. Nature 397:430-433.
41. Sik A, Penttonen M, Ylinen A, Buzsáki G (1995) Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J Neurosci 15:6651-6665.
42. Singer W, Gray CM (1995) Visual feature integration and temporal correlation hypothesis. Annu Rev Neurosci 18:555-586.
43. Skinner FK, Zhang L, Perez Velazquez JL, Carllen PL (1999) Bursting in inhibitory interneuronal network: a role for gap-junctional coupling. J Neurophysiol 81:1274-1283.
44. Sloper JJ (1972) Gap junctions between dendrites in the primate neocortex. Brain Res 44:641-646.
45. Sloper JJ, Powell TPS (1978) Dendrodendritic and reciprocal synapses in the primate motor cortex. Proc R Soc Lond [Biol] 203:23-38.
46. Soltesz 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.
47. 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 259:37-142.
48. Sotelo C, Korn H (1978) Morphological correlates of electrical and other interactions through low-resistance pathways between neurons of the vertebrate central nervous system. Int Rev Cytol 55:67-107.
49. Sotelo C, Llinás R, Baker R (1974) Structural study of inferior olivary nucleus of the cat: morphological correlates of electron coupling. J Neurophysiol 37:541-559.
50. Steriade M, Contreras D, Amzica F, Timofeev I (1996) Synchronization of fast (30-40 Hz) spontaneous oscillations in intrathalamic and thalamocortical networks. J Neurosci 16:2788-2808.
51. Traub RD (1995) Model of synchronized population bursts in electrically coupled interneurons containing active dendritic conductances. J Comput Neurosci 2:283-289.
52. Traub RD, Miles R (1995) Pyramidal cell-to-inhibitory cell spike transduction explicable by active dendritic conductances in inhibitory cell. J Comput Neurosci 2:291-298.
53. Traub RD, Whittington MA, Colling SB, Buzsáki G, Jefferys JGR (1996a) Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J Physiol (Lond) 493:471-484.
54. Traub RD, Whittington MA, Stanford IM, Jefferys JGR (1996b) A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature 383:621-624.
55. Traub RD, Spruston N, Soltesz I, Konnerth A, Whittington MA, Jefferys JGR (1998) Gamma-frequency oscillations: a neuronal population phenomenon, regulated by synaptic and intrinsic cellular processes, and inducing synaptic plasticity. Prog Neurobiol 55:563-575.
56. Whittington MA, Traub RD, Jefferys JGR (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373:612-615.
57. Ylinen A, Bragin A, Nádasdy Z, Jandó G, Szabó I. Sik A, Buzsáki G (1995) Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15:30-46.