BMB Reports

생화학분자생물학회 (Korean Society for Biochemistry and Molecular Biology)
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Memory allocation at the neuronal and synaptic levels

  • HyoJin Park (Center for Cognition and Sociality, Life Science Institute, Institute for Basic Science (IBS)) ;
  • Bong-Kiun Kaang (Center for Cognition and Sociality, Life Science Institute, Institute for Basic Science (IBS))
  • 투고 : 2023.09.15
  • 심사 : 2023.11.10
  • 발행 : 2024.04.30
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초록

Memory allocation, which determines where memories are stored in specific neurons or synapses, has consistently been demonstrated to occur via specific mechanisms. Neuronal allocation studies have focused on the activated population of neurons and have shown that increased excitability via cAMP response element-binding protein (CREB) induces a bias toward memory-encoding neurons. Synaptic allocation suggests that synaptic tagging enables memory to be mediated through different synaptic strengthening mechanisms, even within a single neuron. In this review, we summarize the fundamental concepts of memory allocation at the neuronal and synaptic levels and discuss their potential interrelationships.

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과제정보

This work was supported by the Institute for Basic Science (IBS-R001-D3).

참고문헌

  1. Josselyn SA and Tonegawa S (2020) Memory engrams: recalling the past and imagining the future. Science 367, eaaw4325 
  2. Davis M (1992) The role of the amygdala in fear and anxiety. Annu Rev Neurosci 15, 353-375 
  3. Fanselow MS and Gale GD (2003) The amygdala, fear, and memory. Ann N Y Acad Sci 985, 125-134 
  4. Han JH, Kushner SA, Yiu AP et al (2007) Neuronal competition and selection during memory formation. Science 316, 457-460 
  5. Han JH, Kushner SA, Yiu AP et al (2009) Selective erasure of a fear memory. Science 323, 1492-1496 
  6. Zhou Y, Won J, Karlsson MG et al (2009) CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala. Nat Neurosci 12, 1438-1443 
  7. Maren S and Fanselow MS (1996) The amygdala and fear conditioning: has the nut been cracked? Neuron 16, 237-240 
  8. Repa JC, Muller J, Apergis J, Desrochers TM, Zhou Y and LeDoux JE (2001) Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat Neurosci 4, 724-731 
  9. Reijmers LG, Perkins BL, Matsuo N and Mayford M (2007) Localization of a stable neural correlate of associative memory. Science 317, 1230-1233 
  10. Hebb DO (1949) Organization of behavior: a neurophysiological theory, Wiley, New York 
  11. Han DH, Park P, Choi DI, Bliss TVP and Kaang BK (2022) The essence of the engram: cellular or synaptic? Semin Cell Dev Biol 125, 122-135 
  12. Yiu AP, Mercaldo V, Yan C et al (2014) Neurons are recruited to a memory trace based on relative neuronal excitability immediately before training. Neuron 83, 722-735 
  13. Gouty-Colomer LA, Hosseini B, Marcelo IM et al (2016) Arc expression identifies the lateral amygdala fear memory trace. Mol Psychiatry 21, 364-375 
  14. Zhao B, Rassendren F, Kaang BK, Furukawa Y, Kubo T and Kandel ER (1994) A new class of noninactivating K+ channels from Aplysia capable of contributing to the resting potential and firing patterns of neurons. Neuron 13, 1205-1213 
  15. Sargin D, Mercaldo V, Yiu AP et al (2013) CREB regulates spine density of lateral amygdala neurons: implications for memory allocation. Front Behav Neurosci 7, 209 
  16. Park S, Kramer EE, Mercaldo V et al (2016) Neuronal allocation to a hippocampal engram. Neuropsychopharmacology 41, 2987-2993 
  17. Sano Y, Shobe JL, Zhou M et al (2014) CREB regulates memory allocation in the insular cortex. Curr Biol 24, 2833-2837 
  18. Choi GB, Stettler DD, Kallman BR, Bhaskar ST, Fleischmann A and Axel R (2011) Driving opposing behaviors with ensembles of piriform neurons. Cell 146, 1004-1015 
  19. Lonze BE and Ginty DD (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35, 605-623 
  20. Kaang BK, Kandel ER and Grant SG (1993) Activation of cAMP-responsive genes by stimuli that produce long-term facilitation in Aplysia sensory neurons. Neuron 10, 427-435 
  21. Lee SH, Lim CS, Park H et al (2007) Nuclear translocation of CAM-associated protein activates transcription for long-term facilitation in Aplysia. Cell 129, 801-812 
  22. Chrivia JC, Kwok RP, Lamb N, Hagiwara M, Montminy MR and Goodman RH (1993) Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365, 855-859 
  23. Montminy M (1997) Transcriptional regulation by cyclic AMP. Annu Rev Biochem 66, 807-822 
  24. Leung CCY and Wong YH (2017) Role of G protein-coupled receptors in the regulation of structural plasticity and cognitive function. Molecules 22, 1239 
  25. Deisseroth K, Bito H and Tsien RW (1996) Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron 16, 89-101 
  26. Swulius MT and Waxham MN (2008) Ca(2+)/calmodulin-dependent protein kinases. Cell Mol Life Sci 65, 2637-2657 
  27. Ma H, Groth RD, Cohen SM et al (2014) GammaCaMKII shuttles Ca(2)(+)/CaM to the nucleus to trigger CREB phosphorylation and gene expression. Cell 159, 281-294 
  28. Dieterich DC, Karpova A, Mikhaylova M et al (2008) Caldendrin-Jacob: a protein liaison that couples NMDA receptor signalling to the nucleus. PLoS Biol 6, e34 
  29. Karpova A, Mikhaylova M, Bera S et al (2013) Encoding and transducing the synaptic or extrasynaptic origin of NMDA receptor signals to the nucleus. Cell 152, 1119-1133 
  30. Grochowska KM, Bar J, Gomes GM, Kreutz MR and Karpova A (2021) Jacob, a synapto-nuclear protein messenger linking N-methyl-D-aspartate receptor activation to nuclear gene expression. Front Synaptic Neurosci 13, 787494 
  31. Lakhina V, Arey RN, Kaletsky R et al (2015) Genome-wide functional analysis of CREB/long-term memory-dependent transcription reveals distinct basal and memory gene expression programs. Neuron 85, 330-345 
  32. Bliss TV and Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39 
  33. Matsuzaki M, Honkura N, Ellis-Davies GC and Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429, 761-766 
  34. Choi JH, Sim SE, Kim JI et al (2018) Interregional synaptic maps among engram cells underlie memory formation. Science 360, 430-435 
  35. Frey U and Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385, 533-536 
  36. Sajikumar S and Frey JU (2004) Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD. Neurobiol Learn Mem 82, 12-25 
  37. Redondo RL and Morris RG (2011) Making memories last: the synaptic tagging and capture hypothesis. Nat Rev Neurosci 12, 17-30 
  38. Redondo RL, Okuno H, Spooner PA, Frenguelli BG, Bito H and Morris RG (2010) Synaptic tagging and capture: differential role of distinct calcium/calmodulin kinases in protein synthesis-dependent long-term potentiation. J Neurosci 30, 4981-4989 
  39. Lamprecht R and LeDoux J (2004) Structural plasticity and memory. Nat Rev Neurosci 5, 45-54 
  40. Ramachandran B and Frey JU (2009) Interfering with the actin network and its effect on long-term potentiation and synaptic tagging in hippocampal CA1 neurons in slices in vitro. J Neurosci 29, 12167-12173 
  41. Pinho J, Marcut C and Fonseca R (2020) Actin remodeling, the synaptic tag and the maintenance of synaptic plasticity. IUBMB Life 72, 577-589 
  42. Lu W, Man H, Ju W, Trimble WS, MacDonald JF and Wang YT (2001) Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 29, 243-254 
  43. Anggono V and Huganir RL (2012) Regulation of AMPA receptor trafficking and synaptic plasticity. Curr Opin Neurobiol 22, 461-469 
  44. Yao Y, Kelly MT, Sajikumar S et al (2008) PKM zeta maintains late long-term potentiation by N-ethylmaleimide-sensitive factor/GluR2-dependent trafficking of postsynaptic AMPA receptors. J Neurosci 28, 7820-7827 
  45. Muslimov IA, Nimmrich V, Hernandez AI, Tcherepanov A, Sacktor TC and Tiedge H (2004) Dendritic transport and localization of protein kinase Mzeta mRNA: implications for molecular memory consolidation. J Biol Chem 279, 52613-52622 
  46. Kelly MT, Crary JF and Sacktor TC (2007) Regulation of protein kinase Mzeta synthesis by multiple kinases in long-term potentiation. J Neurosci 27, 3439-3444 
  47. Sacktor TC (2011) How does PKMzeta maintain long-term memory? Nat Rev Neurosci 12, 9-15 
  48. Park P, Kang H, Sanderson TM et al (2019) On the role of calcium-permeable AMPARs in long-term potentiation and synaptic tagging in the rodent hippocampus. Front Synaptic Neurosci 11, 4 
  49. Park P, Kang H, Georgiou J, Zhuo M, Kaang BK and Collingridge GL (2021) Further evidence that CP-AMPARs are critically involved in synaptic tag and capture at hippocampal CA1 synapses. Mol Brain 14, 26 
  50. Hirokawa N (1998) Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279, 519-526 
  51. Soykan T, Haucke V and Kuijpers M (2021) Mechanism of synaptic protein turnover and its regulation by neuronal activity. Curr Opin Neurobiol 69, 76-83 
  52. Okuno H, Akashi K, Ishii Y et al (2012) Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3.1 with CaMKIIbeta. Cell 149, 886-898 
  53. Guzowski JF, McNaughton BL, Barnes CA and Worley PF (1999) Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 2, 1120-1124 
  54. Benito E, Valor LM, Jimenez-Minchan M, Huber W and Barco A (2011) cAMP response element-binding protein is a primary hub of activity-driven neuronal gene expression. J Neurosci 31, 18237-18250 
  55. Sajikumar S, Morris RG and Korte M (2014) Competition between recently potentiated synaptic inputs reveals a winner-take-all phase of synaptic tagging and capture. Proc Natl Acad Sci U S A 111, 12217-12221 
  56. Silva AJ, Zhou Y, Rogerson T, Shobe J and Balaji J (2009) Molecular and cellular approaches to memory allocation in neural circuits. Science 326, 391-395 
  57. Cai DJ, Aharoni D, Shuman T et al (2016) A shared neural ensemble links distinct contextual memories encoded close in time. Nature 534, 115-118 
  58. Rogerson T, Cai DJ, Frank A et al (2014) Synaptic tagging during memory allocation. Nat Rev Neurosci 15, 157-169 
  59. Rashid AJ, Yan C, Mercaldo V et al (2016) Competition between engrams influences fear memory formation and recall. Science 353, 383-387 
  60. Yokose J, Okubo-Suzuki R, Nomoto M et al (2017) Overlapping memory trace indispensable for linking, but not recalling, individual memories. Science 355, 398-403 
  61. Josselyn SA and Frankland PW (2018) Memory allocation: mechanisms and function. Annu Rev Neurosci 41, 389-413 
  62. Lisman J, Cooper K, Sehgal M and Silva AJ (2018) Memory formation depends on both synapse-specific modifications of synaptic strength and cell-specific increases in excitability. Nat Neurosci 21, 309-314 
  63. Abdou K, Shehata M, Choko K et al (2018) Synapse-specific representation of the identity of overlapping memory engrams. Science 360, 1227-1231 
  64. Shires KL, Da Silva BM, Hawthorne JP, Morris RG and Martin SJ (2012) Synaptic tagging and capture in the living rat. Nat Commun 3, 1246