Natural patterns of activity and long-term synaptic plasticity

Current Opinion in Neurobiology

Volumn 10, Issue 2, 2000, Pages 172-180

  Paulsen, Ole ^a   Sejnowski, Terrence J ^b,c  

^a OX1 3QT   (United Kingdom)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; REVIEW;

EID: 0034088617     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(00)00076-3     Document Type: Review

References (73)

1. Hebb D.O. The Organization of Behavior. 1949;John Wiley & Sons, New York.
2. Bliss T.V.P., Lømo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol. 232:1973;331-356.
3. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 361:1993;31-39.
4. Stuart G.J., Sakmann B. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature. 367:1994;69-72.
5. Markram H., Lubke J., Frotscher M., Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science. 275:1997;213-215.
6. Magee J.C., Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science. 275:1997;209-213.
7. Squire L.R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev. 99:1992;195-231.
8. O'Keefe J.A., Nadel L. The Hippocampus as a Cognitive Map. 1978;Clarendon, Oxford.
9. Wood E.R., Dudchenko P.A., Eichenbaum H. The global record of memory in hippocampal neuronal activity. Nature. 397:1999;613-616. The authors provide compelling evidence for specific hippocampal neuronal activity that is unrelated to particular spatial locations, indicating that the hippocampus has a broader role in memory processing than in spatial navigation.
10. Hampson R.E., Simeral J.D., Deadwyler S.A. Distribution of spatial and nonspatial information in dorsal hippocampus. Nature. 402:1999;610-614. The authors describe a multielectrode recording experiment showing anatomical segregation of spatial information with interleaved representation of nonspatial information in the rat hippocampus.
11. Riedel G., Micheau J., Lam A.G.M., Roloff E.V.L., Martin S.J., Bridge H., de Hoz L., Poeschel B., McCulloch J., Morris R.G.M. Reversible neural inactivation reveals hippocampal participation in several memory processes. Nat Neurosci. 2:1999;898-905. By reversible inactivation of synaptic transmission by intrahippocampal infusion of an antagonist at AMPA/kainate-receptors, the authors show that hippocampal neuronal activity is necessary for both encoding and retrieval of spatial memory in the rat.
12. Moser M.B., Moser E.I. Distributed encoding and retrieval of spatial memory in the hippocampus. J Neurosci. 18:1998;7535-7542. To determine whether memory is processed in a localized or distributed manner by the hippocampus, the authors made a number of small discrete lesions in the hippocampus in a rat pretrained in a spatial memory task. These lesions disrupted the retrieval of pre-established memories while sparing the encoding of new memories, suggesting that spatial memory is normally both encoded and retrieved by a widely distributed hippocampal network.
13. Moser E.I., Krobert K.A., Moser M.B., Morris R.G.M. Impaired spatial learning after saturation of long-term potentiation. Science. 281:1998;2038-2042. Tetanization-induced saturation of LTP correlates with impairment of spatial learning in a Morris water maze task. This result strengthens results of previous studies using antagonists at NMDA receptors to suggest that LTP is necessary for certain aspects of spatial learning in a Morris water maze task.
14. Buzsáki G., Leung L., Vanderwolf C.H. Cellular bases of hippocampal EEG in the behaving rat. Brain Res Rev. 6:1983;139-171.
15. Kahana M.J., Sekuler R., Caplan J.B., Kirschen M., Madsen J.R. Human theta oscillations exhibit task dependence during virtual maze navigation. Nature. 399:1999;781-784. Subdural recordings were made from epileptic patients learning to navigate computer-generated mazes. Theta activity similar to that seen during spatial learning and navigation in rodents was seen during this task, suggesting that theta oscillations may have a role in spatial navigation also in humans.
16. Penttonen M., Kamondi A., Acsady L., Buzsaki G. Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo. Eur J Neurosci. 10:1998;718-728. The authors describe intracellular recordings made from morphologically identified neurons during gamma oscillations in anesthetized rats.
17. Fellous J-M., Sejnowski T.J. Cholinergic induction of spontaneous oscillations in the hippocampal slice in the slow (.5-2 Hz), theta (5-12 Hz) and gamma (35-70 Hz) bands. Hippocampus. 10:2000;. in press.
18. Fisahn A., Pike F.G., Buhl E.H., Paulsen O. Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature. 394:1998;186-189.
19. Csicsvari J., Hirase H., Czurko A., Mamiya A., Buzsaki G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci. 19:1999;274-287. The authors studied firing relations of pyramidal neurons and interneurons to theta oscillations and sharp waves recorded in behaving rats. They found that the average firing rate was similar for both types of neurons during theta and non-theta states. Pyramidal neurons were silent, or fired one or more action potentials during each theta cycle, and the participation during sharp-wave bursts was variable. Interneurons fired 20-60° before the population discharge of pyramidal cells during theta oscillations, whereas the activity of interneurons lagged behind the maximum discharge probability of pyramidal neurons by 90° corresponding to 1-2 ms during sharp-wave-associated field ripples.
20. Otto T., Eichenbaum H., Wiener S.I., Wible C.G. Learning-related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long-term potentiation. Hippocampus. 1:1991;181-192.
21. O'Keefe J., Recce M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus. 3:1993;317-330.
22. Ylinen A., Soltesz I., Bragin A., Penttonen M., Sik A., Buzsáki G. Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells. Hippocampus. 5:1995;78-90.
23. Tsodyks M.V., Skaggs W.E., Sejnowski T.J., McNaughton B.L. Paradoxical effects of external modulation of inhibitory interneurons. J Neurosci. 17:1997;4382-4388.
24. Lisman J.E. Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron. 22:1999;233-242. The author describes a new model for storage and retrieval of memory sequences in the hippocampus by reciprocal connections between two recurrent networks, the dentate and the CA3. This model represents a step towards trying to link cellular, network and behavioural phenomena.
25. Buzsaki G., Penttonen M., Nadasdy Z., Bragin A. Pattern and inhibition-dependent invasion of pyramidal cell dendrites by fast spikes in the hippocampus in vivo. Proc Natl Acad Sci USA. 93:1996;9921-9925.
26. 2+ spikes were always preceded by large-amplitude fast spikes.
27. Debanne D., Gahwiler B.H., Thompson S.M. Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J Physiol. 507:1998;237-247. The authors describe LTP and LTD of excitatory connections between pairs of CA3 pyramidal cells induced by single pre- and postsynaptic action potentials in hippocampal slice cultures.
28. Bi G.Q., Poo M.M. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci. 18:1998;10464-10472. This is a compelling demonstration of an asymmetric Hebbian rule for NMDA-receptor-dependent synaptic modification of excitatory synapses between cultured glutamatergic (but not GABAergic) hippocampal neurons. Repeated pairing of postsynaptic spiking within 20 ms after presynaptic activation resulted in LTP, whereas postsynaptic spiking within 20 ms before presynaptic activation led to LTD.
29. Zhang L.I., Tao H.W., Holt C.E., Harris W.A., Poo M.M. A critical window for cooperation and competition among developing retinotectal synapses. Nature. 395:1998;37-44. The authors demonstrate that excitatory synapses in the developing frog visual system can undergo activity-dependent potentiation or depression depending on the temporal order of activation of pre- and postsynaptic neurons.
30. ••] for polysynaptic pathways in cultured hippocampal neurons.
31. Abbott L.F., Blum K.I. Functional significance of long-term potentiation for sequence learning and prediction. Cereb Cortex. 6:1996;406-416.
32. Blum K.I., Abbott L.F. A model of spatial map formation in the hippocampus of the rat. Neural Comp. 8:1996;85-93.
33. Lisman J. What makes the brain's tickers tock. Nature. 394:1998;132-133.
34. Rao R.P.N., Sejnowski T.J. Predictive learning of temporal sequences in recurrent neocortical circuits. Solla S.A., Leen T.K., Müller K-R. Advances in Neural Information Processing Systems 12. 2000;MIT Press, Cambridge, MA. A network with recurrently connected neurons displaying asymmetric Hebbian plasticity can learn sequences and, in particular, can develop direction selectivity similar to that observed in complex cells in visual cortex.
35. Linden D.J. The return of the spike: postsynaptic action potentials and the induction of LTP and LTD. Neuron. 22:1999;661-666. The author provides an insightful review of the experimental evidence for a role of postsynaptic action potentials in the induction of long-term depression and long-term potentiation, and the importance of the temporal order of pre- and postsynaptic activity for the sign of synaptic change.
36. + channels involved in regulating back-propagation of action potentials in hippocampal neurons. The authors emphasise a role for protein kinases in this regulation.
37. 2+ transient was larger if the AP followed the EPSP than if it preceded it.
38. 2+ channels. However, when glutamate was paired with postsynaptic action potentials, the NMDA-receptor-dependent component was selectively amplified.
39. 2+ release in individual spines.
40. 2+ transients.
41. Markram H., Helm P.J., Sakmann B. Dendritic calcium transients evoked by single backpropagating action potentials in rat neocortical pyramidal neurons. J Physiol. 485:1995;1-20.
42. Stiles J.S., Bartol R.M., Salpeter M.M., Salpeter E.E., Sejnowski T.J. Synaptic variability: new insights from reconstructions and Monte Carlo simulations with MCell. Cowan M., Davies K. Synapses. 2000;Johns Hopkins University Press, Baltimore. A general overview of MCell, a computer program that uses Monte Carlo techniques to simulate subcellular signaling in cells.
43. Franks K.M., Bartol T.M., Egelman D.M., Poo M.M., Sejnowski T.J. Simulated dendritic influx of calcium ions through voltage- and ligand-gated channels using Mcell. Soc Neurosci Abstr 1999. 25:1989.
44. Thomas M.J., Watabe A.M., Moody T.D., Makhinson M., O'Dell T.J. Postsynaptic complex spike bursting enables the induction of LTP by theta frequency synaptic stimulation. J Neurosci. 18:1998;7118-7126. Using 5 Hz afferent stimulation in the CA1 area of hippocampal slices prepared from 4-7 week old mice, the authors describe a correlation between postsynaptic complex spike bursting and the induction of LTP. This finding indicates that postsynaptic bursting might have an important role in synaptic plasticity induced by physiologically relevant synaptic activity.
45. ••] that postsynaptic burst firing is important for the induction of LTP by physiologically relevant synaptic activity in the adult hippocampus.
46. Mayford M., Wang J., Kandel E.R., O'Dell T.J. CaMKII regulates the frequency-response function of hippocampal synapses for the production of both LTD and LTP. Cell. 81:1995;891-904.
47. Mayford M., Bach M.E., Huang Y.Y., Wang L., Hawkins R.D., Kandel E.R. Control of memory formation through regulated expression of a CaMKII transgene. Science. 274:1996;1678-1683.
48. Migaud M., Charlesworth P., Dempster M., Webster L.C., Watabe A.M., Makhinson M., He Y., Ramsay M.F., Morris R.G.M., Morrison J.H., O'Dell T.J., Grant S.G. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature. 396:1998;433-439. The frequency threshold for induction of LTP was shifted towards lower frequencies in mice with mutant PSD-95. Surprisingly, this enhancement of LTP was associated with impaired learning in a water maze task.
49. Bienenstock E.L., Cooper L.N., Munro P.W. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci. 2:1982;32-48.
50. Wang H., Wagner J.J. Priming-induced shift in synaptic plasticity in the rat hippocampus. J Neurophysiol. 82:1999;2024-2028. Using field recordings from the CA1 area of hippocampal slices, the authors induced synaptic plasticity by a train of 600 pulses at a frequency between 3 and 100 Hz. They observed a >5-fold rightward shift in the frequency threshold between long-term depression and long-term potentiation after priming of the Schaffer collateral input with two sets of three high-frequency trains (100 Hz, 1 s). Since the effect of priming was expressed heterosynaptically as well as homosynaptically, this result suggests that the history of the neuron is important for the plastic properties of the synapses onto that neuron (metaplasticity).
51. 2+ spikes was seen when the EPSP occurred 5 ms after the backpropagating action potential.
52. Golding N.L., Jung Hy, Mickus T., Spruston N. Dendritic calcium spike initiation and repolarization are controlled by distinct potassium channel subtypes in CA1 pyramidal neurons. J Neurosci. 19:1999;8789-8798.
53. 2+ channels in the proximal versus distal dendrites to synaptic integration in prefrontal cortical neurons. J Neurosci. 17:1997;5936-5948.
54. 2+ channels correlates with the induction of LTP by a theta-burst stimulation paradigm.
55. Kudrimoti H.S., Barnes C.A., McNaughton B.L. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci. 19:1999;4090-4101. In this paper, reactivation of experience-specific firing rate correlations between pairs of pyramidal neurons was seen during sharp waves that occurred during subsequent slow-wave sleep and quiet wakefulness.
56. Nadasdy Z., Hirase H., Czurko A., Csicsvari J., Buzsaki G. Replay and time compression of recurring spike sequences in the hippocampus. J Neurosci. 19:1999;9497-9507. In this paper, experience-specific spike sequences observed in the behaving rat were 'replayed' at a faster time-scale during sharp waves seen during subsequent slow-wave sleep.
57. King C., Henze D.A., Leinekugel X., Buzsaki G. Hebbian modification of a hippocampal population pattern in the rat. J Physiol. 521:1999;159-167. The authors demonstrate that strong depolarisation of individual CA1 pyramidal neurons during sharp waves can increase the cellular responsiveness to subsequent sharp waves.
58. 2+, cAMP-responsive element binding proteins, and mitogen-activated protein kinase signalling. J Neurosci. 17:1997;7252-7266.
59. Frey U., Morris R.G.M. Synaptic tagging and long-term potentiation. Nature. 385:1997;533-536.
60. Frey U., Morris R.G.M. Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci. 21:1998;181-188. A review by the discoverers of the phenomenon which led to the synaptic tagging concept.
61. Dudek S.M., Fields R.D. Somatic action potentials are sufficient for rescue of tagged synapses. Soc Neurosci Abstr. 24:1998;1074.
62. Steriade M., McCormick D.A., Sejnowski T.J. Thalamocortical oscillations in the sleeping and aroused brain. Science. 262:1993;679-685.
63. Sejnowski T.J. Sleep and memory. Curr Biol. 5:1995;832-834.
64. Deisseroth K., Bito H., Tsien R.W. Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron. 16:1996;89-101.
65. Mainen Z.F., Joerges J., Huguenard J.R., Sejnowski T.J. A model of spike initiation in neocortical pyramidal neurons. Neuron. 15:1995;1427-1443.
66. Montague P.R., Sejnowski T.J. The predictive brain: temporal coincidence and temporal order in synaptic learning mechanisms. Learn Memory. 1:1994;1-33.
67. Schultz W., Dayan P., Montague P.R. A neural substrate of prediction and reward. Science. 275:1997;1593-1599.
68. Sejnowski T.J. Statistical constraints on synaptic plasticity. J Theor Biol. 69:1977;385-389.
69. Abbott L.F., Song S. Temporally asymmetric Hebbian learning, spike timing and neuronal response variability. Kearns M.S., Solla S.A., Cohn D.A. Advances in Neural Information Processing Systems 11. 1999;69-75 MIT Press, Cambridge, MA. The authors show that a recurrent network of spiking neurons with time-dependent plasticity achieves a balanced condition where the interspike intervals are irregular, similar to that observed in cortex.
70. Seung H.S. Learning continuous attractors in recurrent networks. Kearns M., Jordan M., Solla S. Advances in Neural Information Processing Systems 10. MIT Press;Cambridge-MA. Uses the anti-Hebbian form of the temporally asymmetric learning rule in a recurrent network to form a stable neural integrator.
71. Bell C.C., Han V.Z., Sugawara Y., Grant K. Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature. 387:1997;278-281.
72. Abbott LF, Munro P: Neural Information Processing Systems (NIPS). Workshop on spike timing and synaptic plasticity. December 4, 1999; Breckenridge, CO. http://www.pitt.edu/~pwm/LTP_LTD_99/.
73. Sejnowski T.J. The book of Hebb. Neuron. 24:1999;773-776. The author reviews the motivation for the Hebb synapse and shows how it is related to recent theoretical ideas about cell assemblies.