Cell type-specific synaptic dynamics of synchronized bursting in the juvenile CA3 rat hippocampus

Journal of Neuroscience

Volumn 24, Issue 43, 2004, Pages 9681-9692

  Aradi, Ildiko ^a   Maccaferri, Gianmaria ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Burst; Epilepsy; GABA; Hippocampus; Interneurons; Network

Indexed keywords

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SYNCHRONIZATION; CELL TYPE; CLAMP; DYNAMICS; EXPERIMENT; GABAERGIC SYSTEM; HIPPOCAMPUS; INTERNEURON; KINETICS; NERVE CELL NETWORK; NERVE CONDUCTION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPSE;

ACTION POTENTIALS; ANIMALS; CHLORIDES; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; INTERNEURONS; MODELS, NEUROLOGICAL; NERVE NET; NEURAL INHIBITION; PYRAMIDAL CELLS; PYRIDAZINES; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; RECEPTORS, GABA-A; SYNAPSES; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 7444266725     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2800-04.2004     Document Type: Article

References (58)

1. Acsady L, Katona I, Martinez-Guijarro FJ, Buzsaki G, Freund TF (2000) Unusual target selectivity of perisomatic inhibitory cells in the hilar region of the rat hippocampus. J Neurosci 20:6907-6919.
2. Alger BE, Nicoll RA (1980) Epileptiform burst afterhyperpolarization: calcium-dependent potassium potential in hippocampal CA1 pyramidal cells. Science 210:1122-1124.
3. Aradi I, Santhakumar V, Soltesz I (2004) Impact of perisomatic IPSC populations on pyramidal cell firing rates. J Neurophysiol 91:2849-2858.
4. Bains JS, Longacher JM, Staley KJ (1999) Reciprocal interactions between CA3 network activity and strength of recurrent collateral synapses. Nat Neurosci 2:720-726.
5. Bi GQ, Poo MM (1998) Synaptic modifications in culture hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18:10464-10472.
6. Bormann JH, Hamill OP, Sakmann B (1987) Mechanism of anion permeation through channels gated by glycine and gamma-aminobutyric acid in mouse cultured spinal neurones. J Physiol (Lond) 385:243-286.
7. Buhl EH, Halasy K, Somogyi P (1994) Diverse source of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368:823-828.
8. Buzsaki G (1986) Hippocampal sharp waves: their origin and significance. Brain Res 398:242-252.
9. Buzsaki G (1989) Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience 31:551-570.
10. Buzsaki G, Leung LM, Vanderwolf CH (1983) Cellular bases of hippocampal EGG in behaving rat. Brain Res 287:139-171.
11. Chamberlin NL, Dingledine R (1989) Control of epileptiform burst rate by CA3 hippocampal cell afterhyperpolarizations in vitro. Brain Res 492:337-346.
12. Chevaleyre V, Castillo PE (2003) Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38:461-472.
13. Csicsvari J, Hirase H, Mamiya A, Buzsaki G (2000) Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 28:585-594.
14. Dzhala VI, Staley KJ (2003) Excitatory actions of endogenously released GABA contribute to initiation of ictal epileptiform activity in the developing hippocampus. J Neurosci 23:1840-1846.
15. Freund T, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
16. Fricker D, Miles R (2001) EPSP amplification and the precision of spike timing in the hippocampus. Neuron 28:559-569.
17. Hajos N, Mody I (1997) Synaptic communication among hippocampal interneurons: properties of spontaneous IPSCs in morphologically identified cells. J Neurosci 17:8427-8442.
18. A channel subtypes. Mol Neurobiol 18:35-86.
19. A receptor site. Brain Res 384:224-231.
20. Hestrin S, Nicoll RA, Perkel DJ, Sah P (1990) Analysis of excitatory synaptic action in pyramidal cells using whole-cell recording from rat hippocampal slices. J Physiol (Lond) 422:203-225.
21. Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9:1179-1209.
22. Kamondi A, Acsady L, Buzsaki G (1998) Dendritic spikes are enhanced by cooperative network activity in the intact hippocampus. J Neurosci 18:3919-3928.
23. Khazipov R, Khalilov RT, Morozova E, Ben-Ari Y, Holmes GL (2004) Developmental changes in GABAergic actions and seizure susceptibility in the rat hippocampus. Eur J Neurosci 19:590-600.
24. 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.
25. Kogo N, Dalezios Y, Capogna M, Ferraguti F, Shigemoto R, Somogyi P (2004) Depression of GABAergic input to identified hippocampal neurons by group III metabotropic glutamate receptors in the rat. Eur J Neurosci 19:2727-2740.
26. Korn SJ, Giacchino JL, Chamberlin NL, Dingledine R (1987) Epileptiform burst activity induced by potassium in the hippocampus and its regulation by GABA-mediated inhibition. J Neurophysiol 57:325-340.
27. A receptors. Prog Neurobiol 71:67-80.
28. 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.
29. B-mediated IPSPs in hippocampal pyramidal cells. J Neurophysiol 82:1218-1223.
30. B-mediated IPSPs in hippocampal pyramidal cells. J Neurophysiol 85:2381-2387.
31. Maccaferri G, Dingledine R (2002) Control of feedforward dendritic inhibition by NMDA receptor-dependent spike timing in hippocampal interneurons. J Neurosci 22:5462-5472.
32. Maccaferri G, Roberts JD, Szucs P, Cottingham CA, Somogyi P (2000) Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurons in rat hippocampus in vitro. J Physiol (Lond) 524:91-116.
33. MacVicar BA, Dudek FE (1982) Local circuit interactions in rat hippocampus: interactions between pyramidal cells. Brain Res 242:341-344.
34. Matsumoto H, Ajmone-Marsan C (1964) Cortical cellular phenomena in experimental epilepsy: interictal manifestations. Exp Neurol 9:286-304.
35. McBain CJ (1995) Hippocampal inhibitory neuron activity in the elevated potassium model of epilepsy. J Neurophysiol 73:2853-2863.
36. McBain CJ, Traynelis SF, Dingledine R (1993) High potassium-induced synchronous bursts and electrographic seizures. In: Epilepsy: models, mechanisms and concepts (Schwartzkroin PA, ed), pp 437-461. Cambridge, UK: Cambridge UP.
37. Migliore M, Cook EP, Jaffe DB, Turner DA, Johnston D (1995) Computer simulations of morphologically reconstructed CA3 hippocampal neurons. J Neurophysiol 73:1157-1168.
38. Miles R, Wong RKS (1983) Single neurons can initiate synchronized population discharges in the hippocampus. Nature 306:371-373.
39. Miles R, Wong RKS (1984) Unitary inhibitory synaptic potentials in the guina-pig hippocampus in vitro. J Physiol (Lond) 356:97-113.
40. Nusser Z, Sieghart W, Benke D, Fritschy JM, Somogyi P (1996) Differential synaptic localization of two major gamma-aminobutyric acid type A receptor alpha subuinits on hippocampal pyramidal cells. Proc Natl Acad Sci USA 93:11939-11944.
41. B responses using patch-clamp recordings in rat hippocampal slices. J Physiol (Lond) 463:391-407.
42. A receptors in acutely isolated pyramidal neurons of rat hippocampus. Neuropharmacology 35:1279-1288.
43. A receptor function by PKA and PKC in adult hippocampal neurons. J Neurosci 19:674-683.
44. Robinson HP, Kawai N (2000) Injection of digitally synthesized synaptic conductance transients to measure the integrative properties of neurons. J Neurosci Methods 49:157-165.
45. Rutecki PA, Lebeda FJ, Johnston D (1985) Epileptiform activity induced by changes in extracellular potassium in hippocampus. J Neurophysiol 54:1363-1374.
46. Sah P, Hestrin S, Nicoll RA (1990) Properties of excitatory postsynaptic currents recorded in vitro from rat hippocampal interneurons. J Physiol (Lond) 430:605-616.
47. Salin PA, Scanziani M, Malenka RC, Nicoll RA (1996) Distinct short-term plasticity at two excitatory synapses in the hippocampus. Proc Natl Acad Sci USA 93:13304-13309.
48. Scanziani M (2000) GABA spillover activates postsynaptic GABA(B) receptors to control rhythmic hippocampal activity. Neuron 25:673-681.
49. Schwartzkroin PA, Haglund MM (1986) Spontaneous rhythmic synchronous activity in epileptic human and normal monkey temporal lobe. Epilepsia 27:523-533.
50. Somogyi P, Nunzi MG, Gorio A, Smith AD (1983) A new type of specific interneuron in the monkey hippocampus forming synapses exclusevely with the axon initial segments of pyramidal cells. Brain Res 259:137-142.
51. Staley KJ, Longacher M, Bains JS, Yee A (1998) Presynaptic modulation of CA3 network activity. Nat Neurosci 1:201-209.
52. Suzuki SS, Smith GK (1985) Single-cell activity and synchronous bursting in the rat hippocampus during waking behavior and sleep. Exp Neurol 89:71-89.
53. Suzuki SS, Smith GK (1988) Spontaneous EEG spikes in the normal hippocampus. II. Relations to synchronous burst discharges. Electroencephalogr Clin Neurophysiol 69:532-540.
54. Traub RD, Miles R (1991) Neuronal networks of the hippocampus. New York: Cambridge UP.
55. Traub RD, Wong RK, Miles R, Michelson H (1991) A model of a CA3 hippocampal pyramidal neuron incorporating coltage-clamp data on intrinsic conductances. J Neurophysiol 66:635-650.
56. Traynelis SF, Dingledine R (1988) Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice. J Neurophysiol 59:259-276.
57. Wilson WA, Bragdon A (1993) Brain slice models for the study of seizures and interictal spikes. In: Epilepsy: models, mechanisms and concepts (Schwartzkroin PA, ed), pp 371-387. Cambridge, UK: Cambridge UP.
58. Wong RKS, Prince DA (1981) Afterpotential generation in hippocampal pyramidal cells. J Neurophysiol 45:86-97.