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Associative Memory Cells in Memory Trace

  • Jin-Hui Wang
Chapter
  • 334 Downloads

Abstract

Associative memory is characterized as the integrative storages and the reciprocal retrievals of associated signals after their joint acquisitions. Basic units in memory traces should be morphological and functional identities to work for memory-relevant processes. Beyond the concepts of memory traces, engrams, cell assemblies, and neural plasticity, associative memory cells have been functionally and structurally identified, which encode the integrative storage and reciprocal retrieval of associated signals as well as receive synapse innervation from coactivated brain areas. Associative memory cells are identified as primary associative memory cells in sensory cortices to memorize exogenous signals and secondary associative memory cells in sensory downstream brain areas, such as the prefrontal cortex, amygdala, and hippocampus, to memorize endogenous signals generated from cognitive events and emotional reactions. Based on experimental data, these associative memory cells have the following characters. They receive synapse innervations from the coactivated brain areas in a reciprocal manner. They are able to encode the associated signals acquired in associative learning and generated in integrative cognitions. Their encoded signals and received synapse innervations come from cross-modal and intramodal sources. Their axons innervate their downstream brain regions in convergent and divergent manners. Associative memory cells and their mediated memory formation are influenced by the chain reaction including neuronal activation, epigenetic process, and the expressions of genes and proteins in relevance to axon prolongation and synapse formation. Working principles of associative memory cells are based on their reception of synapse innervations from multiple sources and mutual synaptic innervations by the coactivations, as well as neuronal encoding capability and synaptic transmission efficacy. Moreover, their functional states are modulated by the arousal system that release monoamine and acetylcholine as well as by hormones. These associative memory cells constitute the foundations of memory-related physiological and psychological processes as well as memory deficits in pathology.

Keywords

Associative memory cells Synapse Neuron Cognition and emotion 

References

  1. 1.
    Kandel ER, Pittenger C. The past, the future and the biology of memory storage. Philos Trans R Soc Lond Ser B Biol Sci. 1999;354(1392):2027–52.CrossRefGoogle Scholar
  2. 2.
    Suzuki WA. Associative learning signals in the brain. Prog Brain Res. 2008;169:305–20.PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Wang D, et al. Neurons in the barrel cortex turn into processing whisker and odor signals: a cellular mechanism for the storage and retrieval of associative signals. Front Cell Neurosci. 2015;9:320.PubMedPubMedCentralGoogle Scholar
  4. 4.
    Wasserman EA, Miller RR. What’s elementary about associative learning? Annu Rev Psychol. 1997;48:573–607.PubMedCrossRefGoogle Scholar
  5. 5.
    Wang J-H. Searching basic units of memory traces: associative memory cells. F1000Research. 2019;8(457):1–28.Google Scholar
  6. 6.
    Wang JH, Cui S. Associative memory cells: formation, function and perspective. F1000Res. 2017;6:283.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Wang JH, Cui S. Associative memory cells and their working principle in the brain. F1000Res. 2018;7:108.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Liu Y, et al. Piriform cortical glutamatergic and GABAergic neurons express coordinated plasticity for whisker-induced odor recall. Oncotarget. 2017;8(56):95719–40.PubMedPubMedCentralGoogle Scholar
  9. 9.
    Yan F, et al. Coordinated plasticity between barrel cortical glutamatergic and GABAergic neurons during associative memory. Neural Plast. 2016;2016(ID5648390):1–20.Google Scholar
  10. 10.
    Wang JH, et al. Upregulation of glutamatergic receptor-channels is associated with cross-modal reflexes encoded in barrel cortex and piriform cortex. Biophys J. 2014;106(2):supplement 191a.CrossRefGoogle Scholar
  11. 11.
    Feng J, et al. Barrel cortical neuron integrates triple associated signals for their memory through receiving epigenetic-mediated new synapse innervations. Cereb Cortex. 2017;27(12):5858–71.PubMedCrossRefGoogle Scholar
  12. 12.
    Lei Z, et al. Synapse innervation and associative memory cell are recruited for integrative storage of whisker and odor signals in the barrel cortex through miRNA-mediated processes. Front Cell Neurosci. 2017;11(316):1–11.Google Scholar
  13. 13.
    Wang J-H, et al. Prefrontal cortical neurons are recruited as secondary associative memory cells for associative memory and cognition. Biophys J. 2018;114(3):155a.CrossRefGoogle Scholar
  14. 14.
    Wang JH, et al. Secondary associative memory cells and their plasticity in the prefrontal cortex. Biophys J. 2019;116(3):427a.CrossRefGoogle Scholar
  15. 15.
    Hebb DO. The organization of behavior, a neuropsychological theory. New York: Wiley; 1949.Google Scholar
  16. 16.
    Hebb DO. Animal and physiological psychology. Annu Rev Psychol. 1950;1:173–88.PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Poo MM, et al. What is memory? The present state of the engram. BMC Biol. 2016;14:40.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Kandel ER, Dudai Y, Mayford MR. The molecular and systems biology of memory. Cell. 2014;157(1):163–86.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Semon RW. In: Semon RW, editor. Mnemic psychology. London: Allen, Unwinis; 1923.Google Scholar
  20. 20.
    Tonegawa S, et al. Memory engram storage and retrieval. Curr Opin Neurobiol. 2015;35:101–9.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Black J, Greenough W. Developmental approaches to the memory process. In: Martinez J, Kesner R, editors. Learning and memory. San Diego: Academic; 1991. p. 61–91.CrossRefGoogle Scholar
  22. 22.
    Brown M, Keynes R, Lumsden A. Development of cerebral cortex and cerebellar cortex. In: Brown MEA, editor. The development of brain. New York: Oxford University Press Inc; 2001. p. 169–93.Google Scholar
  23. 23.
    Chang H, et al. The protocadherin 17 gene affects cognition, personality, amygdala structure and function, synapse development and risk of major mood disorders. Mol Psychiatry. 2017;231:1–13.Google Scholar
  24. 24.
    Dajani DR, Uddin LQ. Demystifying cognitive flexibility: implications for clinical and developmental neuroscience. Trends Neurosci. 2015;38(9):571–8.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Dumas TC. Developmental regulation of cognitive abilities: modified composition of a molecular switch turns on associative learning. Prog Neurobiol. 2005;76(3):189–211.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Cohen Kadosh R, Walsh V. Cognitive neuroscience: rewired or crosswired brains? Curr Biol. 2006;16(22):R962–3.PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Chen N, et al. The refractory periods and threshold potentials of sequential spikes measured by whole-cell recordings. Biochem Biophys Res Commun. 2006;340:151–7.PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    Chen N, et al. Sodium channel-mediated intrinsic mechanisms underlying the differences of spike programming among GABAergic neurons. Biochem Biophys Res Commun. 2006;346:281–7.PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Chen N, Chen X, Wang J-H. Homeostasis established by coordination of subcellular compartment plasticity improves spike encoding. J Cell Sci. 2008;121(17):2961–71.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Hodgkin AL, Huxley AF. Resting and action potentials in single nerve fibres. J Physiol. 1945;104(2):176–95.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Hodgkin AL, Huxley AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952;117(4):500–44.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Shepherd GM. Synaptic potentials and synaptic integration. In: Shepherd GM, editor. Neurobiology. New York: Oxford University Press; 1998. p. 97–117.Google Scholar
  33. 33.
    Stevens CF, Wang Y-Y. Facilitation and depression at single central synapses. Neuron. 1995;14:795–802.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Wang JH, et al. The gain and fidelity of transmission patterns at cortical excitatory unitary synapses improve spike encoding. J Cell Sci. 2008;121(17):2951–60.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Kandel ER. Nerve cells and behavior. In: Kandel ER, Schwartz JH, Jessell TM, editors. Principles of neural science. 4th ed. New York: McGraw-Hill; 2000. p. 19–35.Google Scholar
  36. 36.
    Thompson RF. In search of memory traces. Annu Rev Psychol. 2005;56:1–23.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Thompson RF. An essential memory trace found. Behav Neurosci. 2013;127(5):669–75.PubMedCrossRefGoogle Scholar
  38. 38.
    Reijmers LG, et al. Localization of a stable neural correlate of associative memory. Science. 2007;317(5842):1230–3.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Tayler KK, et al. Reactivation of neural ensembles during the retrieval of recent and remote memory. Curr Biol. 2013;23(2):99–106.PubMedCrossRefGoogle Scholar
  40. 40.
    Link W, et al. Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc Natl Acad Sci U S A. 1995;92(12):5734–8.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Morgan JI, Curran T. Stimulus-transcription coupling in neurons: role of cellular immediate-early genes. Trends Neurosci. 1989;12(11):459–62.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Kiessling M, Gass P. Immediate early gene expression in experimental epilepsy. Brain Pathol. 1993;3(4):381–93.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Meldrum BS. Concept of activity-induced cell death in epilepsy: historical and contemporary perspectives. Prog Brain Res. 2002;135:3–11.PubMedCrossRefGoogle Scholar
  44. 44.
    Wang X, et al. Persistent hyperactivity of hippocampal dentate interneurons after a silent period in the rat pilocarpine model of epilepsy. Front Cell Neurosci. 2016;10:94.PubMedPubMedCentralGoogle Scholar
  45. 45.
    Simonato M, et al. Differential expression of immediate early genes in the hippocampus in the kindling model of epilepsy. Brain Res Mol Brain Res. 1991;11(2):115–24.PubMedCrossRefGoogle Scholar
  46. 46.
    Abe H, Nowak TS Jr. Induced hippocampal neuron protection in an optimized gerbil ischemia model: insult thresholds for tolerance induction and altered gene expression defined by ischemic depolarization. J Cereb Blood Flow Metab. 2004;24(1):84–97.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Bokesch PM, et al. Dextromethorphan inhibits ischemia-induced c-fos expression and delayed neuronal death in hippocampal neurons. Anesthesiology. 1994;81(2):470–7.PubMedCrossRefGoogle Scholar
  48. 48.
    Kiessling M, et al. Differential transcription and translation of immediate early genes in the gerbil hippocampus after transient global ischemia. J Cereb Blood Flow Metab. 1993;13(6):914–24.PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Carr MF, Jadhav SP, Frank LM. Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat Neurosci. 2011;14(2):147–53.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Harris KD, et al. Organization of cell assemblies in the hippocampus. Nature. 2003;424(6948):552–6.PubMedCrossRefGoogle Scholar
  51. 51.
    Ji D, Wilson MA. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci. 2007;10(1):100–7.PubMedCrossRefGoogle Scholar
  52. 52.
    Jadhav SP, et al. Awake hippocampal sharp-wave ripples support spatial memory. Science. 2012;336(6087):1454–8.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Kay K, et al. A hippocampal network for spatial coding during immobility and sleep. Nature. 2016;531(7593):185–90.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Kudrimoti HS, Barnes CA, McNaughton BL. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci. 1999;19(10):4090–101.PubMedCrossRefPubMedCentralGoogle Scholar
  55. 55.
    McNaughton BL, Barnes CA, O’Keefe J. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res. 1983;52(1):41–9.PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Sirota A, et al. Communication between neocortex and hippocampus during sleep in rodents. Proc Natl Acad Sci U S A. 2003;100(4):2065–9.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Skaggs WE, McNaughton BL. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science. 1996;271(5257):1870–3.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Wilson MA, McNaughton BL. Dynamics of the hippocampal ensemble code for space. Science. 1993;261(5124):1055–8.CrossRefGoogle Scholar
  59. 59.
    Wilson MA, McNaughton BL. Reactivation of hippocampal ensemble memories during sleep. Science. 1994;265(5172):676–9.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Wirth S, et al. Single neurons in the monkey hippocampus and learning of new associations. Science. 2003;300(5625):1578–81.PubMedCrossRefGoogle Scholar
  61. 61.
    Yokose J, et al. Overlapping memory trace indispensable for linking, but not recalling, individual memories. Science. 2017;355(6323):398–403.PubMedCrossRefGoogle Scholar
  62. 62.
    Yu JY, et al. Specific hippocampal representations are linked to generalized cortical representations in memory. Nat Commun. 2018;9(1):2209.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Zhao J, Wang D, Wang J-H. Barrel cortical neurons and astrocytes coordinately respond to an increased whisker stimulus frequency. Mol Brain. 2012;5(12):1–10.Google Scholar
  64. 64.
    Nikolenko V, Poskanzer KE, Yuste R. Two-photon photostimulation and imaging of neural circuits. Nat Methods. 2007;4(11):943–50.PubMedCrossRefGoogle Scholar
  65. 65.
    Stosiek C, et al. In vivo two-photon calcium imaging of neural networks. Proc Natl Acad Sci U S A. 2003;100(12):7319–24.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Wang KH, et al. In vivo two-photon imaging reveals a role of arc in enhancing orientation specificity in visual cortex. Cell. 2006;126(2):389–402.PubMedCrossRefGoogle Scholar
  67. 67.
    Feng J, et al. Cell-specific plasticity associated with integrative memory of triple sensory signals in the barrel cortex. Oncotarget. 2018;9(57):30962–78.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Zhang G, et al. Upregulation of excitatory neurons and downregulation of inhibitory neurons in barrel cortex are associated with loss of whisker inputs. Mol Brain. 2013;6(1):2.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Gao Z, et al. Associations of unilateral whisker and olfactory signals induce synapse formation and memory cell recruitment in bilateral barrel cortices: cellular mechanism for unilateral training toward bilateral memory. Front Cell Neurosci. 2016;10(285):1–16.Google Scholar
  70. 70.
    Paxinos G, Watson C. The mouse brain: in stereotaxic coordinates. In: Paxinos G, Watson C, editors. The rat brain: in stereotaxic coordinates. London: Elsevier Academic Press; 2005.Google Scholar
  71. 71.
    Hama H, et al. Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain. Nat Neurosci. 2011;14(11):1481–8.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Yan F, et al. Coordinated plasticity between barrel cortical glutamatergic and GABAergic neurons during associative memory. Neural Plast. 2016;2016(ID 5648390):1–15.Google Scholar
  73. 73.
    Bliss T, Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol Lond. 1973;232:331–56.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Debanne D, Poo MM. Spike-timing dependent plasticity beyond synapse – pre- and post-synaptic plasticity of intrinsic neuronal excitability. Front Synaptic Neurosci. 2010;2:21.PubMedPubMedCentralGoogle Scholar
  75. 75.
    Stanton PK, Sejnowski TJ. Associative long-term depression in the hippocampus induced by hebbian covariance. Nature. 1989;339(6221):215–8.PubMedCrossRefGoogle Scholar
  76. 76.
    Aizenmann C, Linden DJ. Rapid, synaptically driven increases in the intrinsic excitability of cerebellar nuclear neurons. Nat Neurosci. 2000;3:109–11.CrossRefGoogle Scholar
  77. 77.
    Daoudal D, Debanne D. Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn Mem. 2003;10:456–65.PubMedCrossRefGoogle Scholar
  78. 78.
    Campanac E, Debanne D. Plasticity of neuronal excitability: Hebbian rules beyond the synapse. Arch Ital Biol. 2007;145(3–4):277–87.PubMedGoogle Scholar
  79. 79.
    Sourdet V, et al. Long-term enhancement of neuronal excitability and temporal fidelity mediated by metabotropic glutamate receptor subtype 5. J Neurosci. 2003;23(32):10238–48.PubMedCrossRefGoogle Scholar
  80. 80.
    Zhang M, et al. Calcium signal-dependent plasticity of neuronal excitability developed postnatally. J Neurobiol. 2004;61:277–87.PubMedCrossRefPubMedCentralGoogle Scholar
  81. 81.
    Banerjee SB, et al. Perineuronal nets in the adult sensory cortex are necessary for fear learning. Neuron. 2017;95(1):169–179 e3.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Doucette W, et al. Associative cortex features in the first olfactory brain relay station. Neuron. 2011;69(6):1176–87.PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Khodagholy D, Gelinas JN, Buzsaki G. Learning-enhanced coupling between ripple oscillations in association cortices and hippocampus. Science. 2017;358(6361):369–72.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Li H, et al. Experience-dependent modification of a central amygdala fear circuit. Nat Neurosci. 2013;16(3):332–9.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Liu X, et al. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature. 2012;484(7394):381–5.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Raymond JL, Lisberger SG, Mauk MD. The cerebellum: a neuronal learning mechacine? Science. 1996;272:1126–30.PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Otis JM, et al. Prefrontal cortex output circuits guide reward seeking through divergent cue encoding. Nature. 2017;543:103–7.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Pape HC, Pare D. Plastic synaptic networks of the amygdala for the acquisition, expression and extinction of conditioned fear. Physiol Rev. 2010;90(2):419–63.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Timmann D, et al. The human cerebellum contributes to motor, emotional and cognitive associative learning. A review. Cortex. 2010;46(7):845–57.PubMedCrossRefPubMedCentralGoogle Scholar
  90. 90.
    Weinberger NM. Specific long-term memory traces in primary auditory cortex. Nat Rev Neurosci. 2004;5:279–90.PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Xu W, Sudhof TC. A neural circuit for memory specificity and generalization. Science. 2013;339(6125):1290–5.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Reder LM, Park H, Kieffaber PD. Memory systems do not divide on consciousness: reinterpreting memory in terms of activation and binding. Psychol Bull. 2009;135(1):23–49.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    McGaugh JL. Time-dependent processes in memory storage. Science. 1966;153(3742):1351–8.PubMedCrossRefPubMedCentralGoogle Scholar
  94. 94.
    McLaughlin B. “Intentional” and “incidental” learning in human subjects: the role of instructions to learn and motivation. Psychol Bull. 1965;63:359–76.PubMedCrossRefPubMedCentralGoogle Scholar
  95. 95.
    Squire LR. Declarative and nondeclarative memory: multiple brain systems supporting learning and memory. J Cogn Neurosci. 1992;4(3):232–43.PubMedCrossRefPubMedCentralGoogle Scholar
  96. 96.
    Squire LR, Knowlton B, Musen G. The structure and organization of memory. Annu Rev Psychol. 1993;44:453–95.PubMedCrossRefPubMedCentralGoogle Scholar
  97. 97.
    Adler LL, Berkowitz PH. Influencing associative thinking and imagery in emotionally disturbed children. Psychol Rep. 1976;39(1):183–8.PubMedCrossRefPubMedCentralGoogle Scholar
  98. 98.
    Gordon R, Silverstein ML, Harrow M. Associative thinking in schizophrenia: a contextualist approach. J Clin Psychol. 1982;38(4):684–96.PubMedCrossRefPubMedCentralGoogle Scholar
  99. 99.
    Glassman RB. A working memory “theory of relativity”: elasticity in temporal, spatial, and modality dimensions conserves item capacity in radial maze, verbal tasks, and other cognition. Brain Res Bull. 1999;48(5):475–89.PubMedCrossRefPubMedCentralGoogle Scholar
  100. 100.
    Martins J, Mendes RV. Neural networks and logical reasoning systems: a translation table. Int J Neural Syst. 2001;11(2):179–86.PubMedPubMedCentralGoogle Scholar
  101. 101.
    Procyk E, Joseph JP. Problem solving and logical reasoning in the macaque monkey. Behav Brain Res. 1996;82(1):67–78.PubMedCrossRefPubMedCentralGoogle Scholar
  102. 102.
    Ramsey NF, et al. Excessive recruitment of neural systems subserving logical reasoning in schizophrenia. Brain. 2002;125(Pt 8):1793–807.PubMedCrossRefGoogle Scholar
  103. 103.
    Wang J-H, et al. Neurons in barrel cortex turn into processing whisker and odor signals: a novel form of associative learning. Soc Neurosci. 2013;653(14):WW11.Google Scholar
  104. 104.
    Wang J-H, et al. Both glutamatergic and Gabaergic neurons are recruited to be associative memory cells. Biophys J. 2016;110(3):supplement 481a.CrossRefGoogle Scholar
  105. 105.
    Zhang F, et al. mGluR1,5 activation improves network asynchrony and GABAergic synapse attenuation in the amygdala: implication for anxiety-like behavior in DBA/2 mice. Mol Brain. 2012;5(1):20.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Guo R, et al. Associative memory extinction is accompanied by decayed plasticity at motor cortical neurons and persistent plasticity at sensory cortical neurons. Front Cell Neurosci. 2017;11(168):1–12.Google Scholar
  107. 107.
    Liu Y, et al. Activity strengths of cortical glutamatergic and GABAergic neurons are correlated with transgenerational inheritance of learning ability. Oncotarget. 2017;8(68):112401–16.PubMedPubMedCentralGoogle Scholar
  108. 108.
    Zhao X, et al. Coordinated plasticity among glutamatergic and GABAergic neurons and synapses in the barrel cortex is correlated to learning efficiency. Front Cell Neurosci. 2017;11(221):1–12.Google Scholar
  109. 109.
    Saneyoshi T, Fortin DA, Soderling TR. Regulation of spine and synapse formation by activity-dependent intracellular signaling pathways. Curr Opin Neurobiol. 2009;20(1):108–15.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Spitzer NC. Activity-dependent neuronal differentiation prior to synapse formation: the functions of calcium transients. J Physiol Paris. 2002;96(1–2):73–80.PubMedCrossRefPubMedCentralGoogle Scholar
  111. 111.
    Ueda H, et al. Distinct roles of cytoskeletal components in immunological synapse formation and directed secretion. J Immunol. 2015;195(9):4117–25.PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Tagawa Y, Hirano T. Activity-dependent callosal axon projections in neonatal mouse cerebral cortex. Neural Plast. 2012;2012:797295.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Albright TD. On the perception of probable things: neural substrates of associative memory, imagery, and perception. Neuron. 2012;74(2):227–45.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Yang Z, et al. Functional compatibility between Purkinje cell axon branches and their target neurons in the cerebellum. Oncotarget. 2017;8(42):72424–37.PubMedPubMedCentralGoogle Scholar
  115. 115.
    Yu J, et al. Quantal glutamate release is essential for reliable neuronal encodings in cerebral networks. PLoS One. 2011;6(9):e25219.PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Yu J, Qian H, Wang JH. Upregulation of transmitter release probability improves a conversion of synaptic analogue signals into neuronal digital spikes. Mol Brain. 2012;5(1):26.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Cai DJ, et al. A shared neural ensemble links distinct contextual memories encoded close in time. Nature. 2016;534(7605):115–8.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Naya Y, Yoshida M, Miyashita Y. Forward processing of long-term associative memory in monkey inferotemporal cortex. J Neurosci. 2003;23(7):2861–71.PubMedCrossRefPubMedCentralGoogle Scholar
  119. 119.
    Takehara-Nishiuchi K, McNaughton BL. Spontaneous changes of neocortical code for associative memory during consolidation. Science. 2008;322(5903):960–3.PubMedCrossRefPubMedCentralGoogle Scholar
  120. 120.
    Viskontas IV. Advances in memory research: single-neuron recordings from the human medial temporal lobe aid our understanding of declarative memory. Curr Opin Neurol. 2008;21(6):662–8.PubMedCrossRefPubMedCentralGoogle Scholar
  121. 121.
    Wang J-H, Guo R, Wei Z. Associative memory extinction is accompanied by decays of associative memory cells and their plasticity at motor cortex but not sensory cortex. Soc Neurosci. 2017;81(09):10385.Google Scholar
  122. 122.
    Milo R. What is the total number of protein molecules per cell volume? A call to rethink some published values. BioEssays. 2013;35(12):1050–5.PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Grewe BF, et al. Neural ensemble dynamics underlying a long-term associative memory. Nature. 2017;543(7647):670–5.PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Xu C, et al. Distinct hippocampal pathways mediate dissociable roles of context in memory retrieval. Cell. 2016;167(4):961–972 e16.PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Baldi E, Bucherelli C. Brain sites involved in fear memory reconsolidation and extinction of rodents. Neurosci Biobehav Rev. 2015;53:160–90.PubMedCrossRefPubMedCentralGoogle Scholar
  126. 126.
    Okuyama T, et al. Ventral CA1 neurons store social memory. Science. 2016;353(6307):1536–41.PubMedPubMedCentralCrossRefGoogle Scholar
  127. 127.
    Kitamura T, et al. Engrams and circuits crucial for systems consolidation of a memory. Science. 2017;356(6333):73–8.PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Hubner C, et al. Ex vivo dissection of optogenetically activated mPFC and hippocampal inputs to neurons in the basolateral amygdala: implications for fear and emotional memory. Front Behav Neurosci. 2014;8:64.PubMedPubMedCentralGoogle Scholar
  129. 129.
    Zhao J, Wang D, Wang JH. Barrel cortical neurons and astrocytes coordinately respond to an increased whisker stimulus frequency. Mol Brain. 2012;5:12.PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Jin-Hui Wang
    • 1
  1. 1.University of Chinese Academy of SciencesBeijingChina

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