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Neuroscience and Behavioral Physiology

, Volume 48, Issue 6, pp 734–740 | Cite as

Molecular Mechanism of Memory Modification

  • P. M. Balaban
Article
  • 10 Downloads

The present review of our own and published data proposes a hypothesis for the molecular mechanisms regulating synaptic efficiency which may underlie long-term changes in behavior and modification of memory on the reactivation. The hypotheses is based on data on role of the atypical protein kinase molecule Mζ in long-term changes in synaptic efficiency by controlling the delivery of AMPA receptors, and on data on the possible nitrosylation of these molecules by nitric oxide, which is produced in synapses when nerve cells are activated.

Keywords

neurons invertebrates learning Mζ protein kinase 

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References

  1. 1.
    Anokhin, K. V., Tiunova, A. A., and S. P. R. Rose, “Reminder effects – reconsolidation or retrieval deficit? Pharmacological dissection with protein synthesis inhibitors following reminder for a passive-avoidance task in young chicks,” Eur. J. Neurosci., 15, No. 11, 1759–65 (2002).CrossRefPubMedGoogle Scholar
  2. 2.
    Antonov, I., Ha, T., Antonova, I., Moroz, L. L., and Hawkins, R. D., “Role of nitric oxide in classical conditioning of siphon withdrawal in Aplysia,” J. Neurosci., 27, 10,993–11,002 (2007).Google Scholar
  3. 3.
    Artinian, J., McGauran A.-M. T., De Jaeger, X., et al., “Protein degradation, as with protein synthesis, is required during not only long-term spatial memory consolidation but also reconsolidation,” Eur. J. Neurosci., 27, 3009–3019 (2008).CrossRefPubMedGoogle Scholar
  4. 4.
    Bal, N. V. and Balaban, P. M., “Ubiquitin-dependent protein degradation is required for long-term plasticity and memory,” Neirokhimiya, 32, No. 4, 275–284 (2015).Google Scholar
  5. 5.
    Bal, N., Roshchin, M., Salozhin, S., and Balaban, P., “Nitric oxide upregulates proteasomal protein degradation in neurons,” Cell. Mol. Neurobiol. (2016), doi:  https://doi.org/10.1007/s10571-016-0413-9.
  6. 6.
    Balaban, P. M., Roshchin, M., Timoshenko, A. K., et al., “Nitric oxide is necessary for labilization of a consolidated context memory during reconsolidation in terrestrial snails,” Eur. J. Neurosci., 40, 2963–2970 (2014).CrossRefPubMedGoogle Scholar
  7. 7.
    Balaban, P. M., Roshchin, M., Timoshenko, A. K., et al., “Homolog of protein kinase Mζ maintains context aversive memory and underlying long-term facilitation in terrestrial snail Helix,” Front. Cell. Neurosci., 9, 222 (2015).CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Bredt, D. S., “Nitric oxide signaling specificity – the heart of the problem,” J. Cell Sci., 116, 9–15 (2003).CrossRefPubMedGoogle Scholar
  9. 9.
    Cai, D., Chen, S., and Glanzman, D. L., “Postsynaptic regulation of longterm facilitation in Aplysia,” Curr. Biol., 18, 920–925 (2008).CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Calabrese, V., Cornelius, C., Rizzarelli, E., et al., “Nitric oxide in cell survival: a Janus molecule,” Antioxid. Redox. Signal., 11, 2717–2739 (2009).CrossRefPubMedGoogle Scholar
  11. 11.
    Christopherson, K. S. and Bredt, D. S., “Nitric oxide in excitable tissues: physiological roles and disease,” J. Clin. Invest., 100, 2424–2429 (1997).CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Debiec, J., LeDoux, J. E., and Nader K., “Cellular and systems reconsolidation in the hippocampus,” Neuron, 36, 527–538 (2002).CrossRefPubMedGoogle Scholar
  13. 13.
    Duvarci, S. and Nader, K., “Characterization of fear memory reconsolidation,” J. Neurosci., 24, 9269–9275 (2004).CrossRefPubMedGoogle Scholar
  14. 14.
    Duvarci, S., C. B. Mamou, and Nader, K., “Extinction is not a sufficient condition to prevent fear memories from undergoing reconsolidation in the basolateral amygdala,” Eur. J. Neurosci., 24, 249–260 (2006).CrossRefPubMedGoogle Scholar
  15. 15.
    Duvarci, S., Nader, K., and LeDoux, J. E., “De novo mRNA synthesis is required for both consolidation and re-consolidation of fear memories in the amygdala,” Learn. Mem., 15, 747–755 (2008).CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Eisenberg, M., Kobilo, T., Berman, D. E., and Dudai, Y., “Stability of retrieved memory: inverse correlation with trace dominance,” Science, 301, 1102–1104 (2003).CrossRefPubMedGoogle Scholar
  17. 17.
    Evuarherhe, O., Barker, G. R. I., Savalli, G., et al., “Early memory formation disrupted by atypical PKC inhibitor ZIP in the medial prefrontal cortex but not hippocampus,” Hippocampus, 24, 934–942 (2014).CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Fedele, E. and Raiteri, M., “In vivo studies of the cerebral glutamate receptor/NO/cGMP pathway,” Prog. Neurobiol., 58, 89–120 (1999).CrossRefPubMedGoogle Scholar
  19. 19.
    Gainutdinova, T. H., Tagirova, R. R., Ismailova, A. I., et al., “Reconsolidation of a context long-term memory in the terrestrial snail requires protein synthesis,” Learn. Mem., 12, 620–625 (2005).CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Gelbard-Sagiv, H., Mukamel, R., Harel, M., et al., “Internally generated reactivation of single neurons in human hippocampus during free recall,” Science, 322, 96–101 (2008).CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Hawkins, R. D., Son, H., and Arancio, O., “Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus,” Prog. Brain Res., 118, 155–172 (1998).CrossRefPubMedGoogle Scholar
  22. 22.
    Hegde, A. N., Haynes, K. A., Bach, S. V., and Beckelman, B. C., “Local ubiquitin-proteasome-mediated proteolysis and long-term synaptic plasticity,” Front. Mol. Neuroscience, 7, 95 (2014), doi: 10:3389/fnmol.2014.00096.Google Scholar
  23. 23.
    Hernandez, A. I., Blace, N., Crary, J. F., et al., “Protein kinase M synthesis from a brain mRNA encoding an independent protein kinase C catalytic domain: implications for the molecular mechanism of memory,” J. Biol. Chem., 278, 40,305–40,316 (2003).CrossRefGoogle Scholar
  24. 24.
    Inda, M. C., Muravieva, E. V., and Alberini, C. M., “Memory retrieval and the passage of time: From reconsolidation and strengthening to extinction,” J. Neurosci., 31, 1635–1643 (2011).CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Jacklet, J. W., “Nitric oxide signaling in invertebrates,” Invert. Neurosc., 3, 1–14 (1997).CrossRefGoogle Scholar
  26. 26.
    Jarome, T. J., Werner, C. T., Kwapis, J. L., and Helmstetter, F. J., “Activity dependent protein degradation is critical for the formation and stability of fear memory in the amygdala,” PLoS One, 6, (2011), doi:  https://doi.org/10.1371/journal.pone.0024349.
  27. 27.
    Katzoff, A., Ben-Gedalya, T., and Susswein, A. J., “Nitric oxide is necessary for multiple memory processes after learning that a food is inedible in Aplysia,” J. Neurosci., 22, 9581–9594 (2002).CrossRefPubMedGoogle Scholar
  28. 28.
    Kelly, M. T., Crary, J. F., and Sacktor, T. C., “Regulation of protein kinase M synthesis by multiple kinases in long-term potentiation,” J. Neurosci., 27, 3439–3444 (2007).CrossRefPubMedGoogle Scholar
  29. 29.
    Kwapis, J. L., Jarome, T. J., Gilmartin, M. R., and Helmstetter, F. J., “Intra-amygdala infusion of the protein kinase Mzeta inhibitor ZIP disrupts foreground context fear memory,” Neurobiol. Learn. Mem, 98, 148–153 (2012).CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Lee, A. M., Kanter, B. R., Wang, D., et al., “Prkcz null mice show normal learning and memory,” Nature, 493, 416–419 (2013).CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Lee, S.-H., Choi, J.-H., Lee, N., et al., “Synaptic protein degradation underlies destabilization of retrieved fear memory,” Science, 319, 1253–1256 (2008).CrossRefPubMedGoogle Scholar
  32. 32.
    Ling, D. S. F., Benardo, L. S., Serrano, P. A., et al., “Protein kinase Mζ is necessary and sufficient for LTP maintenance,” Nat. Neurosci., 5, 295–296 (2002).CrossRefPubMedGoogle Scholar
  33. 33.
    Litvin, O. O. and Anokhin, K. V., “The mechanisms of memory reorganization during the retrieval of acquired behavioral experience in chicks: the effects of protein synthesis blockade in the brain,” Zh. Vyssh. Nerv. Deyat., 49, No. 4, 554–65 (1999).Google Scholar
  34. 34.
    Mactutus, C. F., Riccio, D. C., and Ferek, J. M., “Retrograde amnesia for old (reactivated) memory: some anomalous characteristics,” Science, 204, 1319–1320 (1979).CrossRefPubMedGoogle Scholar
  35. 35.
    Migues, P. V., Hardt, O., Wu, D. C., et al., “PKMζ maintains memories by regulating GluR2-dependent AMPA receptor trafficking,” Nat. Neurosci., 13, 630–634 (2010).CrossRefPubMedGoogle Scholar
  36. 36.
    Misanin, J. R., Miller, R. R., and Lewis, D. J., “Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace,” Science, 160, No. 3827, 554–555 (1968).CrossRefPubMedGoogle Scholar
  37. 37.
    Muller, U., “The nitric oxide system in insects,” Prog. Neurobiol., 51, 363–381 (1997).CrossRefPubMedGoogle Scholar
  38. 38.
    Nader, K., Schafe, G. E., and Le Doux, J. E., “Fear memories require protein synthesis in the amygdala for re-consolidation after retrieval,” Nature, 406, 722–726 (2000).CrossRefPubMedGoogle Scholar
  39. 39.
    Nikitin, E. S., Balaban, P. M., and Kemenes, G., “Nonsynaptic plasticity underlies a compartmentalized increase in synaptic efficacy after classical conditioning,” Curr. Biol., 23, No. 7, 614–619 (2013).CrossRefPubMedGoogle Scholar
  40. 40.
    Nishizuka, Y., “Protein kinase C and lipid signaling for sustained cellular responses,” FASEB J., 9, 484–496 (1995).CrossRefPubMedGoogle Scholar
  41. 41.
    Pastalkova, E., Serrano, P., Pinkhasova, D., et al., “Storage of spatial information by the maintenance mechanism of LTP,” Science, 313, 1141–1144 (2006).CrossRefPubMedGoogle Scholar
  42. 42.
    Pedreira, M. E. and Maldonado, H., “Protein synthesis subserves reconsolidation or extinction depending on reminder duration,” Neuron, 38, 863–869 (2003).CrossRefPubMedGoogle Scholar
  43. 43.
    Ren, S.-Q., Yan, J.-Z., Zhang, X.-Y., et al., “PKCλ is critical in AMPA receptor phosphorylation and synaptic incorporation during LTP,” EMBO J., 32, 1365–1380 (2013).CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Roberts, A. C. and Glanzman, D. L., “Learning in Aplysia: looking at synaptic plasticity from both sides,” Trends Neurosci., 26, 662–670 (2003).CrossRefPubMedGoogle Scholar
  45. 45.
    Rose, S. P., “God’s organism? The chick as a model system for memory studies,” Learn. Mem., 7, 1–17 (2000).CrossRefPubMedGoogle Scholar
  46. 46.
    Sacktor, T. C., “How does PKMzeta maintain long-term memory?” Nat. Rev. Neuroscience, 12, 9–15 (2011).CrossRefPubMedGoogle Scholar
  47. 47.
    Sacktor, T. C., “Memory maintenance by PKMzeta – an evolutionary perspective,” Mol. Brain, 5, 31 (2012).CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Sacktor, T. C., Osten, P., Valsamis, H., et al., “Persistent activation of the zeta isoform of protein kinase C in the maintenance of long-term potentiation,” Proc. Natl. Acad. Sci. USA, 90, 8342–8346 (1993).CrossRefPubMedGoogle Scholar
  49. 49.
    Sara, S. J., “Strengthening the shaky trace through retrieval,” Nat. Rev. Neurosci., 1, 212–213 (2000).CrossRefPubMedGoogle Scholar
  50. 50.
    Schweighofer, N. and Ferriol, G., “Diffusion of nitric oxide can facilitate cerebellar learning: A simulation study,” Proc. Natl. Acad. Sci. USA, 97, 10661–10665 (2000).CrossRefPubMedGoogle Scholar
  51. 51.
    Shema, R., Hazvi, S., Sacktor, T. C., and Dudai, Y., “Boundary conditions for the maintenance of memory by PKM in neocortex,” Learn. Mem., 16, 122–128 (2009).CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Shema, R., Sacktor, T. C., and Dudai, Y., “Rapid erasure of long-term memory associations in the cortex by an inhibitor of PKM,” Science, 317, 951–953 (2007).CrossRefPubMedGoogle Scholar
  53. 53.
    Si, K., Lindquist, S., and Kandel, E. R., “A neuronal isoform of the Aplysia CPEB has prion-like properties,” Cell, 115, 879–891 (2003).CrossRefPubMedGoogle Scholar
  54. 54.
    Suzuki, A., “Memory reconsolidation and extinction have distinct temporal and biochemical signatures,” J. Neurosci., 24, 4787–4795 (2004).CrossRefPubMedGoogle Scholar
  55. 55.
    Tsokas, P., Hsieh, C., Yao, Y., et al., “Compensation for PKMζ in long-term potentiation and spatial long-term memory in mutant mice,” eLife, 5 (2016), doi:  https://doi.org/10.7554/Elife.14846.
  56. 56.
    Volk, L. J., Bachman, J. L., Johnson, R., et al., “PKM-ζ is not required for hippocampal synaptic plasticity, learning and memory,” Nature, 493, 420–423 (2013).CrossRefPubMedGoogle Scholar
  57. 57.
    Wass, C., Archer, T., Palsson, E., et al., “Phencyclidine affects memory in a nitric oxide-dependent manner: working and reference memory,” Behav. Brain Res., 174, 49–55 (2006).CrossRefPubMedGoogle Scholar
  58. 58.
    Zyuzina, A. B. and Balaban, P. M., “Extinction and reconsolidation of memory,” Zh. Vyssh. Nerv. Deyat., 5, No. 5, 564–576 (2015).Google Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Higher Nervous Activity and NeurophysiologyRussian Academy of SciencesMoscowRussia

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