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Synaptic consolidation: an approach to long-term learning

Abstract

Synaptic plasticity is thought to be the basis of learning and memory, but it is mostly studied on the timescale of mere minutes. This review discusses synaptic consolidation, a process that enables synapses to retain their strength for a much longer time (days to years), instead of returning to their original value. The process involves specific plasticity-related proteins, and depends on the dopamine D1/D5 receptors. Here, we review the research on synaptic consolidation, describing electrophysiology experiments, recent modeling work, as well as behavioral correlates.

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References

  1. Amit D, Fusi S (1994) Learning in neural networks with material synapses. Neural Comput 6:957–982

  2. Artola A, Bröcher S, Singer W (1990) Different voltage dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature 347:69–72

  3. Ballarini F, Moncada D, Martinez MC, Alen N, Viola H (2009) Behavioral tagging is a general mechanism of long-term memory formation. Proc Natl Acad Sci USA 106:14599–14604

  4. Barrett A, Billings G, Morris R, van Rossum M (2009) State based model of long-term potentiation and synaptic tagging and capture. PLoS Comp Biol 5(1):e1000259. doi:10.1371/journal.pcbi.1000259

  5. Bi G, Poo M (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18:10464–10472

  6. Bienenstock EL, Cooper LN, Munro PW (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2(1):32–48

  7. Bliss T, Lomo T (1973) Long-lasting potentation of synaptic transmission in the dendate area of anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:351–356

  8. Clopath C, Gerstner W (2010) Voltage and spike timing interact in stdp: a unified model. Frontiers in synaptic neuroscience doi:10.3389/fnsyn.2010.00025

  9. Clopath C, Vasilaki E, Buesing L, Gerstner W (2010) Connectivity reflects coding: a model of voltage-based spike-timing-dependent-plasticity with homeostasis. Nat Neurosci 13:344–352

  10. Clopath C, Ziegler L, Vasilaki E, Büsing L, Gerstner W (2008) Tag-trigger-consolidation: a model of early and late long-term-potentiation and depression. PLoS Comput Biol 4(12):e1000248. doi:10.1371/journal.pcbi.1000248

  11. Diba K, Buzsaki G (2007) Forward and reverse hippocampal place-cell sequences during ripples. Nat Neurosci 10:1241–1242

  12. Frey U, Morris R (1997) Synaptic tagging and long-term potentiation. Nature 385:533–536

  13. Frey U, Schroeder H, Matthies H (1990) Dopaminergic antagonists prevent long-term maintenance of posttetanic LTP in the ca1 region of rat hippocampal slices. Brain Res 522:69–75

  14. Froemke R, Dan Y (2002) Spike-timing dependent plasticity induced by natural spike trains. Nature 416:433–438

  15. Froemke RC, Tsay I, Raad M, Long J, Dan Y (2006) Contribution of individual spikes in burst-induced long-term synaptic modification. J Neurophysiol 95:1620–1629

  16. Fusi S, Drew P, Abbott L (2005) Cascade models of synaptically stored memories. Neuron 45:599–611

  17. Gerstner W, Abbott LF (1997) Learning navigational maps through potentiation and modulation of hippocampal place cells. J Comput Neurosci 4:79–94

  18. Gerstner W, Kempter R, van Hemmen J, Wagner H (1996) A neuronal learning rule for sub-millisecond temporal coding. Nature 383(6595):76–78

  19. Gerstner W, Kistler WK (2002) Spiking neuron models. Cambridge University Press, Cambridge

  20. Gütig R, Aharonov S, Rotter S, Sompolinsky H (2003) Learning input correlations through nonlinear temporally asymmetric Hebbian plasticity. J Neurosci 23(9):3697–3714

  21. Guyonneau R, VanRullen R, Thorpe S (2005) Neurons tune to the earliest spikes through stdp. Neural Comput 17(4):859–879

  22. Hebb DO (1949) The organization of behavior. Wiley, New York

  23. Kentros CG, Agnihotri NT, Streater S, Hawkins RD, Kandel ER (2004) Increased attention to spatial context increases both place field stability and spatial memory. Neuron 42:283–295

  24. Kirwan CB, Wixted JT, Squire LR (2008) Activity in the medial temporal lobe predicts memory strength, whereas activity in the prefrontal cortex predicts recollection. J Neurosci 28:10541–10548

  25. Legenstein R, Naeger C, Maass W (2005) What can a neuron learn with spike-timing dependent plasticity. Neural Comput 17:2337–2382

  26. Li S, Cullen WK, Anwyl R, Rowan MJ (2003) Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty. Nat Neurosci 6:526–531

  27. Lynch G, Dunwiddie T, Gribkoff V (1977) Heterosynaptic depression: a postsynaptic correlate of long-term potentiation. Nature 266:737–739

  28. Markram H, Lübke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postysnaptic AP and EPSP. Science 275:213–215

  29. Moncada D, Viola H (2007) Induction of long-term memory by exposure to novelty requires protein synthesis: evidence for a behavioral tagging. J Neurosci 27(28):7476–7481

  30. Nadal J-P, Toulouse G, Changeux J-P, Dehaene S (1986) Networks of formal neurons and memory palimpsests. Europhys Lett 1:349–381

  31. Navakkode S, Sajikumar S, Frey J (2007) Synergistic requirements for the induction of dopaminergic D1/D5-receptor-mediated LTP in hippocampal slices of rat CA1 in vitro. Neuropharmacology 52:1547–1554

  32. Ngezahayo A, Schachner M, Artola A (2000) Synaptic activation modulates the induction of bidirectional synaptic changes in adult mouse hippocamus. J Neurosci 20:2451–2458

  33. O’Connor D, Wittenberg G, Wang S-H (2005) Graded bidirectional synaptic plasticity is composed of switch-like unitary events. Proc Natl Acad Sci USA 102:9679–9684

  34. Oja E (1982) A simplified neuron as a principal component analyzer. J Math Biol 15:267–273

  35. Petersen C, Malenka R, Nicoll R, Hopfield J (1998) All-or-none potentiation of ca3-ca1 synapses. Proc Natl Acad Sci USA 95:4732–4737

  36. Pfister J-P, Gerstner W (2006) Triplets of spikes in a model of spike timing-dependent plasticity. J Neurosci 26:9673–9682

  37. Pfister J-P, Toyoizumi T, Barber D, Gerstner W (2006) Optimal spike-timing dependent plasticity for precise action potential firing in supervised learning. Neural Comput 18:1309–1339

  38. Redondo R, Morris R (2011) Making memories last: the synaptic tagging and capture hypothesis. Nat Rev Neurosci 12(1):17–30

  39. Reymann K, Frey J (2007) The late maintenance of hippocampal LTP: requirements, phases,synaptic tagging, late associativity and implications. Neuropharmacology 52:24–40

  40. Roberts P, Bell C (2000) Computational consequences of temporally asymmetric learning rules: II. Sensory image cancellation. Comput Neurosci 9:67–83

  41. Sajikumar S, Frey J (2004) Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD. Neurobiol Learn Mem 82:12–25

  42. Sajikumar S, Frey J (2004) Resetting of synaptic tags is time- and activity dependent in rat hippocampal ca1 in vitro. Neuroscience 129:503–507

  43. Sajikumar S, Navakkode S, Sacktor T, Frey J (2005) Synaptic tagging and cross-tagging: the role of protein kinase Mζ in maintaining long-term potentiation but not long-term depression. J Neurosci 25:5750–5756

  44. Schultz W, Dayan P, Montague R (1997) A neural substrate for prediction and reward. Science 275:1593–1599

  45. Sjöström P, Turrigiano G, Nelson S (2001) Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32:1149–1164

  46. Smith CN, Squire LR (2009) Medial temporal lobe activity during retrieval of semantic memory is related to the age of the memory. J Neurosci 29:930–938

  47. Song S, Miller K, Abbott L (2000) Competitive Hebbian learning through spike-time-dependent synaptic plasticity. Nat Neurosci 3:919–926

  48. Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatr 20:11–21

  49. Sutton R, Barto A (1998) Reinforcement learning: an introduction. MIT Press, Cambridge

  50. Wang S, Redondo R, Morris R (2010) Relevance of synaptic tagging and capture to the persistence of long-term potentiation and everyday spatial memory. Proc Natl Acad Sci USA 107(45):19537–19542

  51. Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265:676–679

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Acknowledgments

This work was funded in part by the Agence Nationale de la Recherche grant ANR-08-SYSC-005. We thank Tom Schaul for helpful input.

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Correspondence to Claudia Clopath.

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Clopath, C. Synaptic consolidation: an approach to long-term learning. Cogn Neurodyn 6, 251–257 (2012) doi:10.1007/s11571-011-9177-6

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Keywords

  • Synaptic tagging
  • Synaptic consolidation
  • Synaptic plasticity
  • Model
  • Behavior
  • Electrophysiology
  • Review