Oscillatory and Intermittent Synchrony in the Hippocampus: Relevance to Memory Trace Formation

  • G. Buzsáki
  • A. Bragin
  • J. J. Chrobak
  • Z. Nádasdy
  • A. Sik
  • M. Hsu
  • A. Ylinen
Part of the Research and Perspectives in Neurosciences book series (NEUROSCIENCE)


The different cell populations of the hippocampus are involved in behaviorregulated intermittent population bursts (sharp-waves, (SPW) and dentate spikes) and oscillations (theta, gamma and 200 Hz). SPW occur during consummatory behaviors and slow wave sleep. This field potential reflects summated EPSPs in the apical dendrites of CA1 pyramidal neurons as a result of population synchrony in the CA3 recurrent network. During SPW bursts, CA1 pyramidal cells display highly coherent transient network oscillations (200 Hz). Participating pyramidal cells discharge at a significantly lower rate than the frequency of the population oscillation and their action potentials are phase-locked to the simultaneously recorded oscillatory field potentials. Antagonistic to these intermittent events are the theta (6–10 Hz) and associated gamma (40–100 Hz) oscillations during exploratory behavior and REM sleep. In the intact rat the gamma pattern has its largest amplitude in the hilus, is modulated by theta and is entrained by the entorhinal input. The theta pattern is generated by several spatially distinct but highly coherent dipoles and requires an external pacemaker (septum).

The cooperative neuronal discharges underlying the various oscillatory and intermittent synchronous patterns may support neuronal mechanisms underlying memory trace formation in the hippocampus. We hypothesize that such a process requires two stages. 1) During theta-associated exploration, activation vectors from the entorhinal cortex code mnemonic representations in subsets of CA 3 pyramidal cells, where information is temporarily held. 2) At the end of exploration, CA3 cells are disinhibited and discharge in bursts, the most recently and hence most strongly excited ones first (burst initiators). Excitation is spread to less excitable pyramidal cells by the extensive recurrent CA3 collateral system. In essence, the information gathered during the exploratory stage is “replayed” during the SPW bursts. The most important aspect of the model is that the sequential recruitment of individual cells into population bursts (dynamic hierarchy) is based on representations acquired during exploration. In this two-stage model both activation patterns (theta and gamma) and intermittent patterns (SPW) subserve to process specific information.


Granule Cell Dentate Gyrus Pyramidal Cell Entorhinal Cortex Mossy Fiber 
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  1. Alonso A, Llinas RR (1989) Subthreshold Na +-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342:175–177PubMedCrossRefGoogle Scholar
  2. Amaral DG (1978) A Golgi study of cell types in the hilar region of the hippocampus in the rat. J Comp Neurol 182:851–914PubMedCrossRefGoogle Scholar
  3. Amaral D, Witter M (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31:571–591PubMedCrossRefGoogle Scholar
  4. Azouz R, Jensen MS, Yaari Y (1992) Interictal activity induces long-term enhancement of excitatory postsynaptic potentials in the hippocampus. In: Engel J Jr, Wasterlain C, Cavalheiro EA, Heinemann U, Avanzini G (eds) Molecular neurobiology of epilepsy. Epilespy Res Suppl 9. Elsevier, Amsterdam, pp 313–316Google Scholar
  5. Bland BH (1990) Physiology and pharmacology of hippocampal formation theta rhythms. Prog Neurobiol 26:1–54CrossRefGoogle Scholar
  6. Bland B, Anderson P, Ganes T, Sveen O (1980) Automated analysis of rhythmicity of physiologically identified hippocampal formation neurons. Exp Brain Res 38:205–219PubMedCrossRefGoogle Scholar
  7. Bliss TVP, Lømo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 232:331–356Google Scholar
  8. Bliss TVP, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39Google Scholar
  9. Bragin A, Jandó G, Nádasdy Z, Horvath Z, Buzsáki G (1992) The dentate spike: a new network pattern reflecting interneuronal synchrony. Soc Neurosci Abst 141.11Google Scholar
  10. Bragin A, Jandó G, Nádasdy Z, Hetke J, Wise K, Buzsáki G (1993) Gamma frequency oscillation in the hippocampus: modulation by theta activity. Soc Neurosci Abst 148.3Google Scholar
  11. Brankack J, Stewart M, Fox SE (1993) Current source density analysis of the hippocampal theta rhythm: associated sustained potentials and candidate synaptic generators. Brain Res 615:310–327PubMedCrossRefGoogle Scholar
  12. Buzsáki G (1984) Feed-forward inhibition in the hippocampal formation. Prog Neurobiol 22:131–153PubMedCrossRefGoogle Scholar
  13. Buzsáki G (1986) Hippocampal sharp waves: their origin and significance. Brain Res 398:242–252PubMedCrossRefGoogle Scholar
  14. Buzsáki G (1989) A two-stage model of memory trace formation: a role for “noisy” brain states. Neuroscience 31:551–570PubMedCrossRefGoogle Scholar
  15. Buzsáki G (1991) The thalamic clock: emergent network properties. Neuroscience 41:351–364PubMedCrossRefGoogle Scholar
  16. Buzsáki G, Eideiberg E (1982) Direct afferent excitation and long-term potentiation of hippocampal interneurons. J Neurophysiol 48:597–607PubMedGoogle Scholar
  17. Buzsáki G, Leung L, Vanderwolf CH (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res Rev 6:139–171CrossRefGoogle Scholar
  18. Buzsáki G, Czopf J, Kondakor I, Kellenyi L (1986) Laminar distribution of hippocampal rhythmic slow activity (RSA) in the behaving rat: current source density analysis, effects of urethane and atropine. Brain Res 365:125–137PubMedCrossRefGoogle Scholar
  19. Buzsáki G, Haas HL, Anderson EG (1987) Long-term potentiation induced by physiologically relevant stimulus patterns. Brain Res 435:331–333PubMedCrossRefGoogle Scholar
  20. Buzsáki G, Horvath Z, Urioste R, Hetke J, Wise K (1992) High-frequency network oscillation in the hippocampus. Science 256:1025–1027PubMedCrossRefGoogle Scholar
  21. Charpak S, Pare D, Llinás RR (1992) Entorhinal cortex (EC) generates 40 Hz hippocampal oscillations. Soc Neurosci Abst 386.5Google Scholar
  22. Chattarji S, Stanton PK, Sejnowski TJ (1989) Commissural synapses, but not mossy fiber synapses, in hippocampal field CA3 exhibit associative long-term potention and depression. Brain Res 495:145–150PubMedCrossRefGoogle Scholar
  23. Christian EP, Dudek FE (1988) Electrophysiological evidence from glutamate microapplications for local excitatory circuits in the CA1 area of rat hippocampal slices. J Neurophysiol 59:110–123PubMedGoogle Scholar
  24. Chrobak JJ, Urioste R, Buzsáki G (1992) Hippocampal-retrohippocampal interactions during sharp waves. Soc Neurosci Abstr 141.13Google Scholar
  25. Chrobak JJ, Urioste R, Buzsáki G (1993) Selective activation of deep layer retrohippocampal neurons during hippocampal sharp waves. Soc Neurosci Abstr 19:148.2Google Scholar
  26. Churchland P, Sejnowski T (1992) The computational brain. MIT Press, Cambridge, MassGoogle Scholar
  27. Douglas RM (1977) Long-lasting synaptic potentiation in the dentate gyrus following brief high frequency stimulation. Brain Res 126:361–365PubMedCrossRefGoogle Scholar
  28. Eichenbaum H, Otto T (1992) The hippocampus — what does it do? Behav Neural Biol 57:2–36PubMedCrossRefGoogle Scholar
  29. Fox SE, Ranck JB Jr (1981) Electrophysiological characteristics of hippocampal complex-spike cells and theta cells. Exp Brain Res 41:299–313CrossRefGoogle Scholar
  30. Freund TF, Antal M (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336:170–173PubMedCrossRefGoogle Scholar
  31. Gray CM (1993) Rhythmic activity in neuronal systems: insights into integrative function. In: Nadel L, Stein D (eds) SFI Studies in the sciences of complexity. AddisonWesley, pp 89–161Google Scholar
  32. Hebb DO (1949) Organization of behavior. Wiley, New YorkGoogle Scholar
  33. Hsu M, Buzsáki G (1993) Vulnerability of mossy fiber targets in the rat hippocampus to forebrain ischemia. J Neurosci 13:3964–3979PubMedGoogle Scholar
  34. Ishizuka N, Weber J, Amaral D (1990) Organization of intrahippocampal projections originating from CA3 pyramical cells in the rat. J Comp Neurol 295:580–623PubMedCrossRefGoogle Scholar
  35. Jones RSG (1993) Entorhinal-hippocampal connections: a speculative view of their function. Trends Neurosci 16:58–64PubMedCrossRefGoogle Scholar
  36. Jung MW, McNaughton BL (1993) Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3:165–182PubMedCrossRefGoogle Scholar
  37. Kelso SR, Ganong AH, Brown TH (1983) Hebbian synapses in the hippocampus. Proc Natl Acad Sci USA 83:5326–5330CrossRefGoogle Scholar
  38. Kohonen T (1984) Self-organization and associative memory. Springer-Verlag, BerlinGoogle Scholar
  39. Konopacki J, Maclver MB, Bland BH, Roth SH (1987) Theta in hippocampal slices: relation to synaptic responses of dentate neurons. Brain Res Bull 18:25–27PubMedCrossRefGoogle Scholar
  40. Konorski J (1948) Conditioned reflexes and neuronal organization. Cambridge University Press, CambridgeGoogle Scholar
  41. Larson J, Lynch G (1986) Induction of synaptic potentiation in the hippocampus by patterned stimulation involves two events. Science 232:985–988PubMedCrossRefGoogle Scholar
  42. Lee MG, Chrobak JJ, Sik A, Wiley RG, Buzsáki G (1993) Hippocampal EEG changes with selective lesions of the septal cholinergic system. Annual Meeting of the American EEG Society, New OrleansGoogle Scholar
  43. Leung LS (1985) Model of gradual phase shift of the theta rhythm in the rat. J Neurophysiol 42:1051–1065Google Scholar
  44. Leung LS (1992) Fast (beta) rhythms in the hippocampus: a review. Hippocampus. 2:93–98PubMedCrossRefGoogle Scholar
  45. Leung LS, Yim CC (1991) Intrinsic membrane potential oscillations in hippocampal neurons in vitro. Brain Res 553:261–274PubMedCrossRefGoogle Scholar
  46. Li X-G, Somogyi P, Ylinen A, Buzsáki G (1993) The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol 338:1–29CrossRefGoogle Scholar
  47. Lopes da Silva FH, Witter M, Boeijinga PH, Lohman A (1990) Anatomie organization and physiology of the limbic cortex. Physiol Rev 70:453–511Google Scholar
  48. Lorente de Nó R (1934) Studies of the structure of the cerebral cortex: II. Continuation of the study of the ammonic system. J Psychol Neurol 46:113–177Google Scholar
  49. Lynch G (1986) Synapses, circuits, and the beginnings of memory. MIT Press, CambridgeGoogle Scholar
  50. Mac Vicar B, Tse FWY (1989) Local neuronal circuitry underlying cholinergic rhythmic slow activity in CA3 area of rat hippocampal slices. J Physiol (Lond.) 417:197–212Google Scholar
  51. McNaughton BL, Morris RGM (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408–415CrossRefGoogle Scholar
  52. Mitchell SJ, Ranck JB Jr (1980) Generation of theta rhythm in medial entorhinal cortex of freely moving rats. Brain Res 189:49–66PubMedCrossRefGoogle Scholar
  53. Mizumori SJY, McNaughton BL, Barnes CA, Fox KB (1989) Preserved spatial coding in hippocampal CA1 pyramidal cells during reversible suppression of CA3 output: evidence for pattern completion in hippocampus. J Neurosci 9:3915–3928PubMedGoogle Scholar
  54. O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Clarendon, OxfordGoogle Scholar
  55. Otto T, Eichenbaum H, Wiener SI, Wible CG (1991) Learning-related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long-term potentiation. Hippocampus 1:181–192PubMedCrossRefGoogle Scholar
  56. Pavlides C, Winson J (1989) Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J Neurosci 9:2907–2918PubMedGoogle Scholar
  57. Pavlides C, Greenstein YJ, Grudman M, Winson J (1988) Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta rhythm. Brain Res 439:383–387PubMedCrossRefGoogle Scholar
  58. Quirk GJ, Muller RU, Kubie JL, Ranck JB Jr (1992) The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells. J Neurosci 12:1945–1963PubMedGoogle Scholar
  59. Ranck JB Jr (1973) Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. Exp Neurol 42:461–531Google Scholar
  60. Ribak CE, Gall CM, Mody I (1992) The dentate gyrus and its role in seizures. Elsevier, AmsterdamGoogle Scholar
  61. Rose G, Dunviddie TV (1986) Induction of hippocampal long-term potentiation using physiologically patterned stimulation. Neurosci Lett 69:244–248PubMedCrossRefGoogle Scholar
  62. Sastry BR, Goh JW, Auyeung A (1986) Associative induction of posttetanic and longterm potentiation in CA1 neurons of rat hippocampus. Science 232:988–990PubMedCrossRefGoogle Scholar
  63. Schaffer K (1892) Beitrag zur Histologie der Ammonshorn Formation. Arch Microsk Anat 39:611–632CrossRefGoogle Scholar
  64. Scharfman HE (1991) Dentate hilar cells with dendrites in the molecular layer have lower thresholds for synaptic activation by perforant path than granule cells. J Neurosci 11:1660–1673PubMedGoogle Scholar
  65. Soltesz I, Mody I (1994) Patch-clamp recordings reveal powerful GABAergic inhibition in dentate hilar neurons. J Neurosci 14:2365–2376PubMedGoogle Scholar
  66. Squire LR (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys and humans. Psychol Rev 99:5–231Google Scholar
  67. Steriade M, Llinas RR (1988) The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 68:649–741PubMedGoogle Scholar
  68. Stewart M, Fox SE (1990) Do septal neurons pace the hippocampal theta rhythm? Trends Neurosci 13:163–168PubMedCrossRefGoogle Scholar
  69. Stumpf C (1965) The fast component in the electrical activity of rabbit’s hippocampus. Electroencephal Clin Neurophysiol 18:477–486CrossRefGoogle Scholar
  70. Suzuki SS, Smith GK (1987) Spontaneous EEG spikes in the normal hippocampus. I. Behavioral correlates, laminar profiles and bilateral synchrony. Electroencephal Clin Neurophysiol 67:438–459Google Scholar
  71. Swanson LW, Kohler C (1986) Anatomical evidence for direct projections from the entorhinal area to the entire cortical mantle in the rat. J Neurosci 6:3010–3023PubMedGoogle Scholar
  72. Tamamaki N, Nojyo Y (1991) Crossing fiber arrays in the rat hippocampus as demonstrated by three-dimensional reconstruction. J Comp Neurol 303:435–442PubMedCrossRefGoogle Scholar
  73. Thompson LT, Best PJ (1989) Place cell and silent cells in the hippocampus of freelybehaving rats. J Neurosci 9:2882–2890Google Scholar
  74. Thomson AM, Radpour S (1991) Excitatory connections between CA1 pyramidal cells revealed by spike-triggered averaging in slices of rat hippocampus are partially NMDA receptor mediated. Eur J Neurosci 3:587–601PubMedCrossRefGoogle Scholar
  75. Traub RD, Miles R (1991) Neuronal networks of the hippocampus. Cambridge University Press, CambridgeGoogle Scholar
  76. Traub RD, Miles R, Buzsáki G (1992) Computer simulation of carbachol-driven rhythmic population oscillations in the CA3 region of the in vitro rat hippocampus. J Physiol (Lond.) 451:653–672Google Scholar
  77. Treves A, Rolls ET (1991) What determines the capacity of autoassociative memories in the brain? Network 2:371–397CrossRefGoogle Scholar
  78. Vanderwolf CH (1969) Hippocampal electrical activity and voluntary movement in the rat. Electroencephal Gin Neurophysiol 26:407–418CrossRefGoogle Scholar
  79. Van Hoesen GW, Pandya DN (1975) Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections. Brain Res 95:39–59Google Scholar
  80. Wigstrom H, Gustafsson B (1985) On long-lasting potentiation in the hippocampus: a propposed mechanism for its dependence on coincident pre-and postsynaptic activity. Acta Physiol Scand 123:519–522PubMedCrossRefGoogle Scholar
  81. Winson J, Abzug C (1978) Neuronal transmission through hippocampal pathway dependent on behavior. J Neurophysiol 41:716–732PubMedGoogle Scholar
  82. Yeckel MF, Berger TW (1990) Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. Proc Natl Acad Sci USA 87:5832–5836PubMedCrossRefGoogle Scholar
  83. Ylinen A, Sik A, Bragin A, Jando G, Buzsáki G (1993) Intracellular correlates of hippocampal sharp wave bursts in vivo. Soc Neurosci Abstr 19:148.4Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1994

Authors and Affiliations

  • G. Buzsáki
  • A. Bragin
  • J. J. Chrobak
  • Z. Nádasdy
  • A. Sik
  • M. Hsu
  • A. Ylinen

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