High-frequency population oscillations are predicted to occur in hippocampal pyramidal neuronal networks interconnected by axoaxonal gap junctions

Neuroscience

Volumn 92, Issue 2, 1999, Pages 407-426

  Traub, R D ^a   Schmitz, D ^b   Jefferys, J G R ^a   Draguhn, A ^b  

^a UNIVERSITY DEPARTMENT OF MEDICINE   (United Kingdom)

^b HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Electrotonic coupling; Epilepsy; Graph theory; Oscillations; Ripples

Indexed keywords

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; EPILEPSY; GAP JUNCTION; HIGH FREQUENCY OSCILLATION; HIPPOCAMPUS; MODEL; NERVE CONDUCTION; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SIMULATION; SPIKE; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; GAP JUNCTIONS; HIPPOCAMPUS; HUMANS; MODELS, NEUROLOGICAL; NERVE NET; PRESYNAPTIC TERMINALS; PYRAMIDAL CELLS;

EID: 0033063207     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(98)00755-6     Document Type: Article

References (52)

1. Bennett M. V. L. (1977) Electrical transmission: a functional analysis and comparison to chemical transmission. In Handbook of Physiology, Section 1: The Nervous System, Vol. 1: Cellular Biology of Neurons, Part 1 (ed. Kandel E. R.), pp. 357-416. American Physiological Society, Bethesda, MD.
2. Buhl E.H., Han Z.-S., Lörinczi Z., Stezhka V.V., Karnup S.V., Somogyi P. Physiological properties of anatomically identified axo-axonic cells in the rat hippocampus. J. Neurophysiol. 71:1994;1289-1307.
3. Buzsáki G., Horváth Z., Urioste R., Hetke J., Wise K. High-frequency network oscillation in the hippocampus. Science. 256:1992;1025-1027.
4. Chrobak J.J., Buzsáki G. High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J. Neurosci. 16:1996;3056-3066.
5. + conductance in hippocampus. Nature. 389:1997;286-289.
6. Deuchars J., Thomson A.M. CA1 pyramid-pyramid connections in rat hippocampus in vitro: dual intracellular recordings with biocytin filling. Neuroscience. 74:1996;1009-1018.
7. Draguhn A., Traub R.D., Schmitz D., Jefferys J.G.R. Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature. 394:1998;189-192.
8. Dye J., Heiligenberg W. Intracellular recording in the medullary pacemaker nucleus of the weakly electric fish, Apteronotus, during modulatory behaviors. J. comp. Physiol. A. 161:1987;187-200.
9. Elekes K., Szabo T. Synaptology of the medullary command (pacemaker) nucleus of the weakly electric fish (Apteronotus leptorhynchus) with particular reference to comparative aspects. Expl Brain Res. 60:1985;509-520.
10. Erdös P., Rényi A. On the evolution of random graphs. Publ. Math. Inst. Hung. Acad. Sci. 5:1960;17-61.
11. Fisher R.S., Webber W.R.S., Lesser R.P., Arroyo S., Uematsu S. High-frequency EEG activity at the start of seizures. J. clin. Neurophysiol. 9:1992;441-448.
12. Haas H.L., Jefferys J.G.R. Low-calcium field burst discharges of CA1 pyramidal neurones in rat hippocampal slices. J. Physiol. 354:1984;185-201.
13. Jefferys J.G.R. Influence of electric fields on the excitability of granule cells in guinea-pig hippocampal slices. J. Physiol. 319:1981;143-152.
14. Jefferys J.G.R., Haas H.L. Synchronized bursting of CA1 hippocampal pyramidal cells in the absence of synaptic transmission. Nature. 300:1982;448-450.
15. Johnston D., Brown T.H. Giant synaptic potential hypothesis for epileptiform activity. Science. 211:1981;294-297.
16. MacVicar B.A., Dudek F.E. Electrotonic coupling between pyramidal cells: a direct demonstration in rat hippocampal slices. Science. 213:1981;782-785.
17. MacVicar B.A., Dudek F.E. Electrotonic coupling between granule cells of the rat dentate gyrus: physiological and anatomical evidence. J. Neurophysiol. 47:1982;579-592.
18. Miles R., Wong R.K.S. Excitatory synaptic interactions between CA3 neurones in the guinea-pig hippocampus. J. Physiol. 373:1986;397-418.
19. Moortgat K.T., Bullock T.H., Sejnowski T.J. Blocking gap junctions in the electric fish pacemaker nucleus alters the frequency and synchrony of oscillations. Soc. Neurosci. Abstr. 24:1998;186.
20. Moortgat K.T., Keller C.H., Bullock T.H., Sejnowski T.J. Submicrosecond pacemaker precision is behaviorally modulated: the gymnotiform electromotor pathway. Proc. natn. Acad. Sci. U.S.A. 95:1998;4684-4689.
21. o solutions in rat hippocampal and cortical slices. Neuroscience. 74:1996;107-118.
22. Perez Velazquez J.L., Han D., Carlen P.L. Neurotransmitter modulation of gap junctional communication in the rat hippocampus. Eur. J. Neurosci. 9:1997;2522-2531.
23. Perez Velazquez J.L., Valiante T.A., Carlen P.L. Modulation of gap junctional mechanisms during calcium-free induced field burst activity: a possible role for electrotonic coupling in epileptogenesis. J. Neurosci. 14:1994;4308-4317.
24. Rash J., Duffy H.S., Dudek F.E., Bilhartz H.L., Whalen L.R., Yasumura T. Grid-mapped freeze-fracture analysis of gap juncitons in gray and white matter of adult rat central nervous system, with evidence for a "pan-glial syncytium" that is not coupled to neurons. J. comp. Neurol. 388:1977;265-292.
25. Schwartzkroin P.A., Prince D.A. Penicillin-induced epileptiform activity in the hippocampal in vitro preparation. Ann. Neurol. 1:1977;463-469.
26. Schwartzkroin P.A., Prince D.A. Cellular and field potential properties of epileptogenic hippocampal slices. Brain Res. 147:1978;117-130.
27. Snow R.W., Dudek F.E. Electrical fields directly contribute to action potential synchronization during convulsant-induced epileptiform bursts. Brain Res. 323:1984;114-118.
28. Somogyi P., Freund T.F., Cowey A. The axo-axonic interneuron in the cerebral cortex of the rat, cat and monkey. Neuroscience. 7:1982;2577-2607.
29. Spencer W.A., Kandel E.R. Electrophysiology of hippocampal neurons. IV. Fast prepotentials. J. Neurophysiol. 24:1961;272-285.
30. Stasheff S.F., Hines M., Wilson W.A. Axon terminal hyperexcitability associated with epileptogenesis in vitro. I. Origin of ectopic spikes. J. Neurophysiol. 70:1993;960-975.
31. A receptors. J. Neurophysiol. 70:1993;976-984.
32. Swann J.W., Brady R.J., Friedman R.J., Smith E.J. The dendritic origins of penicillin-induced epileptogenesis in CA3 hippocampal pyramidal cells. J. Neurophysiol. 56:1986;1718-1738.
33. Taylor C.P., Dudek F.E. Synchronous neural afterdischarges in rat hippocampal slices without active chemical synapses. Science. 218:1982;810-812.
34. Taylor C.P., Dudek F.E. Excitation of hippocampal pyramidal cells by an electrical field effect. J. Neurophysiol. 52:1984;126-142.
35. Taylor C.P., Dudek F.E. Synchronization without active chemical synapses during hippocampal afterdischarges. J. Neurophysiol. 52:1984;143-155.
36. Tokunaga A., Akert K., Sandri C., Bennett M.V.L. Cell types and synaptic organization of the medullary electromotor nucleus in a constant frequency weakly electric fish, Sternarchus albifrons. J. comp. Neurol. 192:1980;407-426.
37. Traub R.D., Colling S.B., Jefferys J.G.R.J. Cellular mechanisms of 4-aminopyridine-induced synchronized after-discharges in the rat hippocampal slice. J. Physiol. 489:1995;127-140.
38. Traub R.D., Dingledine R. Model of synchronized epileptiform bursts induced by high potassium in CA3 region of rat hippocampal slice. Role of spontaneous EPSPs in initiation. J. Neurophysiol. 64:1990;1009-1018.
39. Traub R.D., Dudek F.E., Snow R.W., Knowles W.D. Computer simulations indicate that electrical field effects contribute to the shape of the epileptiform field potential. Neuroscience. 15:1985;947-958.
40. Traub R.D., Dudek F.E., Taylor C.P., Knowles W.D. Simulation of hippocampal afterdischarges synchronized by electrical interactions. Neuroscience. 14:1985;1033-1038.
41. Traub R.D., Jefferys J.G.R., Miles R., Whittington M.A., Tóth K. A branching dendritic model of a rodent CA3 pyramidal neurone. J. Physiol. 481:1994;79-95.
42. 2+ in the rat hippocampal slice. J. Physiol. 478:1994;379-393.
43. Traub R.D., Miles R., Jefferys J.G.R. Synaptic and intrinsic conductances shape picrotoxin-induced synchronized after-discharges in the guinea-pig hippocampal slice. J. Physiol. 461:1993;525-547.
44. Traub R.D., Whittington M.A., Colling S.B., Buzsáki G., Jefferys J.G.R. Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J. Physiol. 493:1996;471-484.
45. Traub R.D., Wong R.K.S. Cellular mechanism of neuronal synchronization in epilepsy. Science. 216:1982;745-747.
46. Traub R.D., Wong R.K.S. Synaptic mechanisms underlying interictal spike initiation in a hippocampal network. Neurology. 33:1983;257-266.
47. Valiante T.A., Perez Velazquez J.L., Jahromi S.S., Carlen P.L. Coupling potentials in CA1 neurons during calcium-free-induced field burst activity. J. Neurosci. 15:1995;6946-6956.
48. Vaney D.I. The coupling pattern of axon-bearing horizontal cells in the mammalian retina. Proc. R. Soc. Lond. B. 252:1993;93-101.
49. Wong R.K.S., Traub R.D. Synchronized burst discharge in disinhibited hippocampal slice. I. Initiation in CA2-CA3 region. J. Neurophysiol. 49:1983;442-458.
50. Yang X.-D., Korn H., Faber D.S. Long-term potentiation of electrotonic coupling at mixed synapses. Nature. 348:1990;542-545.
51. Yasargil G.M., Sandri C. Topography and ultrastructure of commissural interneurons that may establish reciprocal inhibitory connections of the Mauthner axons in the spinal cord of the tench, Tinca tinca L. J. Neurocytol. 19:1990;111-126.
52. Ylinen A., Bragin A., Nádasdy Z., Jandó G., Szabó I., Sik A., Buzsáki G. Sharp wave-associated high-frequency oscillaiton (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J. Neurosci. 15:1995;30-46.