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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Oct 11;91(21):10104–10108. doi: 10.1073/pnas.91.21.10104

Non-Hebbian properties of long-term potentiation enable high-capacity encoding of temporal sequences.

R Granger 1, J Whitson 1, J Larson 1, G Lynch 1
PMCID: PMC44966  PMID: 7937845

Abstract

A hypothesis commonly found in biological and computational studies of synaptic plasticity embodies a version of the 1949 postulate of Hebb that coactivity of pre- and postsynaptic elements results in increased efficacy of their synaptic contacts. This general proposal presaged the identification of the first and still only known long-lasting synaptic plasticity mechanism, long-term potentiation (LTP). Yet the detailed physiology of LTP induction and expression differs in many specifics from Hebb's rule. Incorporation of these physiological LTP constraints into a simple non-Hebbian network model enabled development of "sequence detectors" that respond preferentially to the sequences on which they were trained. The network was found to have unexpected capacity (e.g., 50 x 10(6) random sequences in a network of 10(5) cells), which scales linearly with network size, thereby addressing the question of memory capacity in brain circuitry of realistic size.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ambros-Ingerson J., Granger R., Lynch G. Simulation of paleocortex performs hierarchical clustering. Science. 1990 Mar 16;247(4948):1344–1348. doi: 10.1126/science.2315702. [DOI] [PubMed] [Google Scholar]
  2. Ballard D. H., Hinton G. E., Sejnowski T. J. Parallel visual computation. Nature. 1983 Nov 3;306(5938):21–26. doi: 10.1038/306021a0. [DOI] [PubMed] [Google Scholar]
  3. Bear M. F., Cooper L. N., Ebner F. F. A physiological basis for a theory of synapse modification. Science. 1987 Jul 3;237(4810):42–48. doi: 10.1126/science.3037696. [DOI] [PubMed] [Google Scholar]
  4. Collingridge G. L., Kehl S. J., McLennan H. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol. 1983 Jan;334:33–46. doi: 10.1113/jphysiol.1983.sp014478. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Diamond D. M., Dunwiddie T. V., Rose G. M. Characteristics of hippocampal primed burst potentiation in vitro and in the awake rat. J Neurosci. 1988 Nov;8(11):4079–4088. doi: 10.1523/JNEUROSCI.08-11-04079.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gabor D. Improved holographic model of temporal recall. Nature. 1968 Mar 30;217(5135):1288–1289. doi: 10.1038/2171288a0. [DOI] [PubMed] [Google Scholar]
  7. Grossberg S. Adaptive pattern classification and universal recoding: II. Feedback, expectation, olfaction, illusions. Biol Cybern. 1976 Aug 30;23(4):187–202. doi: 10.1007/BF00340335. [DOI] [PubMed] [Google Scholar]
  8. Kauer J. A., Malenka R. C., Nicoll R. A. A persistent postsynaptic modification mediates long-term potentiation in the hippocampus. Neuron. 1988 Dec;1(10):911–917. doi: 10.1016/0896-6273(88)90148-1. [DOI] [PubMed] [Google Scholar]
  9. Kelso S. R., Ganong A. H., Brown T. H. Hebbian synapses in hippocampus. Proc Natl Acad Sci U S A. 1986 Jul;83(14):5326–5330. doi: 10.1073/pnas.83.14.5326. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Larson J., Lynch G. Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events. Science. 1986 May 23;232(4753):985–988. doi: 10.1126/science.3704635. [DOI] [PubMed] [Google Scholar]
  11. Larson J., Lynch G. Theta pattern stimulation and the induction of LTP: the sequence in which synapses are stimulated determines the degree to which they potentiate. Brain Res. 1989 Jun 5;489(1):49–58. doi: 10.1016/0006-8993(89)90007-3. [DOI] [PubMed] [Google Scholar]
  12. Macrides F., Eichenbaum H. B., Forbes W. B. Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning. J Neurosci. 1982 Dec;2(12):1705–1717. doi: 10.1523/JNEUROSCI.02-12-01705.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. McNaughton B. L., Douglas R. M., Goddard G. V. Synaptic enhancement in fascia dentata: cooperativity among coactive afferents. Brain Res. 1978 Nov 24;157(2):277–293. doi: 10.1016/0006-8993(78)90030-6. [DOI] [PubMed] [Google Scholar]
  14. Muller D., Joly M., Lynch G. Contributions of quisqualate and NMDA receptors to the induction and expression of LTP. Science. 1988 Dec 23;242(4886):1694–1697. doi: 10.1126/science.2904701. [DOI] [PubMed] [Google Scholar]
  15. Muller D., Lynch G. Long-term potentiation differentially affects two components of synaptic responses in hippocampus. Proc Natl Acad Sci U S A. 1988 Dec;85(23):9346–9350. doi: 10.1073/pnas.85.23.9346. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Pavlides C., Greenstein Y. J., Grudman M., Winson J. Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res. 1988 Jan 26;439(1-2):383–387. doi: 10.1016/0006-8993(88)91499-0. [DOI] [PubMed] [Google Scholar]
  17. Staubli U., Lynch G. Stable hippocampal long-term potentiation elicited by 'theta' pattern stimulation. Brain Res. 1987 Dec 1;435(1-2):227–234. doi: 10.1016/0006-8993(87)91605-2. [DOI] [PubMed] [Google Scholar]
  18. Tank D. W., Hopfield J. J. Neural computation by concentrating information in time. Proc Natl Acad Sci U S A. 1987 Apr;84(7):1896–1900. doi: 10.1073/pnas.84.7.1896. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. von der Malsburg C. Self-organization of orientation sensitive cells in the striate cortex. Kybernetik. 1973 Dec 31;14(2):85–100. doi: 10.1007/BF00288907. [DOI] [PubMed] [Google Scholar]

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