Spike timing of distinct types of GABAergic interneuron during hippocampal gamma oscillations in vitro

Journal of Neuroscience

Volumn 24, Issue 41, 2004, Pages 9127-9137

  Hájos, Norbert ^a   Pálhalini, János ^a   Mann, Edward O ^b   Nèmeth, Beáta ^a   Paulsen, Ole ^b   Freund, Tamas F ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Carbachol; GABAergic cells; Gamma oscillation; Hippocampus; Phase coupling; Rat

Indexed keywords

CARBACHOL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENTION; BRAIN SLICE; CELL LABELING; CONTROLLED STUDY; CURRENT SOURCE DENSITY ANALYSIS; DENDRITE; DENSITY; DIPOLE; FEEDBACK SYSTEM; GABAERGIC SYSTEM; HIPPOCAMPUS; IN VITRO STUDY; INHIBITION KINETICS; INTERNEURON; MALE; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RADIOFREQUENCY; RAT; SYNAPTIC TRANSMISSION; WAKEFULNESS;

ACTION POTENTIALS; ANIMALS; BIOLOGICAL CLOCKS; CHOLINERGIC AGONISTS; ELECTRIC STIMULATION; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; INTERNEURONS; MALE; NERVE NET; NEURAL INHIBITION; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; RATS; RATS, WISTAR; TIME FACTORS;

EID: 5644277512     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2113-04.2004     Document Type: Article

References (51)

1. Acsády L, Gores TJ, Freund TF (1996) Different populations of vasoactive intestinal polypeptide-immunoreactive interneurons are specialized to control pyramidal cells or interneurons in the hippocampus. Neuroscience 73:317-334.
2. Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, Geiger JR, Jonas P (2002) Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc Natl Acad Sci USA 99:13222-13227.
3. Boddeke HW, Best R, Boeijinga PH (1997) Synchronous 20 Hz rhythmic activity in hippocampal networks induced by activation of metabotropic glutamate receptors in vitro. Neuroscience 76:653-658.
4. 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.
5. Buzsáki G, Chrobak JJ (1995) Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr Opin Neurobiol 5:504-510.
6. Chrobak JJ, Buzsáki G (1998) Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci 18:388-398.
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. Cunningham MO, Davies CH, Buhl EH, Kopell N, Whittington MA (2003) Gamma oscillations induced by kainate receptor activation in the entorhinal cortex in vitro. J Neurosci 23:9761-9769.
9. Csicsvari J, Jamieson B, Wise KD, Buzsáki G (2003) Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311-322.
10. Eeckman FH, Freeman WJ (1990) Correlations between unit firing and EEG in the rat olfactory system. Brain Res 528:238-244.
11. Engel AK, Fries P, Singer W (2001) Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2:704-716.
12. Fell J, Klaver P, Lehnertz K, Grunwald T, Schaller C, Elger CE, Fernandez G (2001) Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nat Neurosci 4:1259-1264.
13. Fisahn A, Pike FG, Buhl EH, Paulsen O (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394:186-189.
14. Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
15. Fries P, Reynolds JH, Rorie AE, Desimone R (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291:1560-1563.
16. Gray CM (1994) Synchronous oscillations in neuronal systems: mechanisms and functions. J Comput Neurosci 1:11-38.
17. Gulyás AI, Miles R, Sik A, Toth K, Tamamaki N, Freund TF (1993) Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 366:683-687.
18. Gulyás AI, Hájos N, Freund TF (1996) Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J Neurosci 16:3397-3411.
19. Gulyás AI, Hájos N, Katona I, Freund TF (2003) Interneurons are the local targets of hippocampal inhibitory cells which project to the medial septum. Eur J Neurosci 17:1861-1872.
20. Hájos N, Mann EO, Freund TF, Paulsen O (2004) Increased oxygen supply enables cholinergically-induced network oscillations in submerged hippocampal slices. Fed European Neurosci Soc Abstr 2:A009.013.
21. Hasselmo ME, Wyble BP, Wallenstein GV (1996) Encoding and retrieval of episodic memories: role of cholinergic and GABAergic modulation in the hippocampus. Hippocampus 6:693-708.
22. Hormuzdi SG, Pais I, LeBeau FE, Towers SK, Rozov A, Buhl EH, Whittington MA, Monyer H (2001) Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36-deficient mice. Neuron 31:487-495.
23. Jonas P, Bischofberger J, Fricker D, Miles R (2004) Interneuron diversity series: fast in, fast out-temporal and spatial signal processing in hippocampal interneurons. Trends Neurosci 27:30-40.
24. Kawaguchi Y (2001) Distinct firing patterns of neuronal subtypes in cortical synchronized activities. J Neurosci 21:7261-7272.
25. Klausberger T, Roberts JD, Somogyi P (2002) Cell type-and input-specific differences in the number and subtypes of synaptic GABA(A) receptors in the hippocampus. J Neurosci 22:2513-2521.
26. Klausberger T, Magill PJ, Marton LF, Roberts JD, Cobden PM, Buzsaki G, Somogyi P (2003) Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421:844-848.
27. Klausberger T, Marton LF, Baude A, Roberts JD, Magill PJ, Somogyi P (2004) Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo. Nat Neurosci 7:41-47.
28. LeBeau FE, Towers SK, Traub RD, Whittington MA, Buhl EH (2002) Fast network oscillations induced by potassium transients in the rat hippocampus in vitro. J Physiol (Lond) 542:167-179.
29. Leung SW (1979) Potentials evoked by alvear tract in hippocampal CA1 region of rats. II. Spatial field analysis. J Neurophysiol 42:1571-1589.
30. Li XG, Somogyi P, Ylinen A, Buzsaki G (1994) The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol 339:181-208.
31. Maccaferri G, Roberts JD, Szucs P, Cottingham CA, Somogyi P (2000) Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro. J Physiol (Lond) 524: 91-116.
32. Marrosu F, Portas C, Mascia MS, Casu MA, Fa M, Giagheddu M, Imperato A, Gessa GL (1995) Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats. Brain Res 671:329-332.
33. McMahon LL, Williams JH, Kauer JA (1998) Functionally distinct groups of interneurons identified during rhythmic carbachol oscillations in hippocampus in vitro. J Neurosci 18:5640-5651.
34. Miles R. Toth K, Gulyás AI, Hájos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815-823.
35. Oka H, Shimono K, Ogawa R, Sugihara H, Taketani M (1999) A new planar multielectrode array for extracellular recording: application to hippocampal acute slice. J Neurosci Methods 93:61-67.
36. Pálhalmi J, Paulsen O, Freund TF, Hajos N (2004) Distinct properties of carbachol- and DHPG-induced network oscillations in hippocampal slices. Neuropharmacology 47:381-389.
37. Paulsen O, Moser EI (1998) A model of hippocampal memory encoding and retrieval: GABAergic control of synaptic plasticity. Trends Neurosci 21:273-278.
38. Pike FG, Goddard RS, Suckling JM, Ganter P, Kasthuri N, Paulsen O (2000) Distinct frequency preferences of different types of rat hippocampal neurones in response to oscillatory input currents. J Physiol (Lond) 529: 205-213.
39. Pouille F, Scanziani M (2004) Routing of spike series by dynamic circuits in the hippocampus. Nature 429:717-723.
40. Shimono K, Brucher F, Granger R, Lynch G, Taketani M (2000) Origins and distribution of cholinergically induced beta rhythms in hippocampal slices. J Neurosci 20:8462-8473.
41. 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.
42. Sik A, Penttonen M, Ylinen A, Buzsáki G (1995) Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J Neurosci 15:6651-6665.
43. Singer W (1993) Synchronization of cortical activity and its putative role in information processing and learning. Annu Rev Physiol 55:349-374.
44. Soltesz I, Bourassa J, Deschenes M (1993) The behavior of mossy cells of the rat dentate gyrus during theta oscillations in vivo. Neuroscience 57:555-564.
45. Traub RD, Bibbig A, Fisahn A, LeBeau FE, Whittington MA, Buhl EH (2000) A model of gamma-frequency network oscillations induced in the rat CA3 region by carbachol in vitro. Eur J Neurosci 12:4093-4106.
46. Traub RD, Kopell N, Bibbig A, Buhl EH, LeBeau FE, Whittington MA (2001a) Gap junctions between interneuron dendrites can enhance synchrony of gamma oscillations in distributed networks. J Neurosci 21:9478-9486.
47. Traub RD, Whittington MA, Buhl EH, LeBeau FE, Bibbig A, Boyd S, Cross H, Baldeweg T (2001b) A possible role for gap junctions in generation of very fast EEG oscillations preceding the onset of, and perhaps initiating, seizures. Epilepsia 42:153-170.
48. Varela F, Lachaux JP, Rodriguez E, Martinerie J (2001) The brainweb: phase synchronization and large-scale integration, Nat Rev Neurosci 2:229-239.
49. Whittington MA, Traub RD (2003) Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci 26:676-682.
50. Whittington MA, Traub RD, Jefferys JG (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373:612-615.
51. Ylinen A, Soltesz I, Bragin A, Penttonen M, Sik A, Buzsáki G (1995) Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells. Hippocampus 5:78-90.