Cellular and Molecular Changes in Associative Memory

  • Jin-Hui Wang


Basic units in the brain include neurons, glia cells, and their synaptic connections. Neuronal codes for the execution of various brain functions, such as memory, cognition, and emotion, are programmed by these neurons and synapses. While acquiring exogenous signals and processing endogenous signals, these signals are memorized in the brain essentially for guiding cognitions and behaviors. Memory formation and memory-relevant behavior emergence may be based on the recruitment and/or refinement of these neurons and synapses. The recruitment of neurons to be the basic units in memory traces will be discussed in Chap.  5. Here, author intends to summarize the plasticity of neurons and synapses, which is presumably relevant to memory formation. The featured function of neurons is to produce action potentials, or spikes, once excitatory synaptic signals drive their membrane potentials to a threshold potential for firing spikes or their membrane potentials fluctuate to this threshold potential. The patterns of neuronal spikes constitute the digital signals to program various signals and manager neuronal functions. In this regard, the plasticity at neurons is mainly characterized by changes in their spike patterns and/or threshold potentials that may move closely or away from the resting membrane potential. In terms of chemical synapses, their signal transmission includes transmitter release from presynaptic boutons as well as interactions between transmitters and their receptors in postsynaptic density. The plasticity at chemical synapses includes the changes in the capacity and release efficacy of presynaptic transmitters as well as in the number and responsiveness of postsynaptic receptors, which may control the conversions between inactive synapses and active synapses or between silent synapses and functional synapses. Long-term plasticity at synapses and neurons is believed to be cellular mechanisms underlying memory formation, which leads to long-term changes in memory-relevant behaviors.


Synaptic plasticity Neuronal plasticity Neuronal homeostasis and neuronal compatibility 


  1. 1.
    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
  2. 2.
    Stanton PK, Sejnowski TJ. Associative long-term depression in the hippocampus induced by hebbian covariance. Nature. 1989;339(6221):215–8.CrossRefGoogle Scholar
  3. 3.
    Wang JH, Ko G, Kelly PT. Cellular and molecular bases of memory: synaptic and neuronal plasticity. J Clin Neurophysiol. 1997;14:264–93.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Zhang M, et al. Calcium signal-dependent plasticity of neuronal excitability developed postnatally. J Neurobiol. 2004;61:277–87.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Bliss TVP, Lynch MA. Long-term potentiation of synaptic transmission in the hippocampus: properties and mechanisms. In: Landfield PW, Deadwyler SA, editors. Long-term potentiation: from biophysics to behavior. New York: Alan R. Liss; 1988. p. 3–72.Google Scholar
  6. 6.
    Nicoll RA, Malenka RC. Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature. 1995;377:115–8.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Poo MM, et al. What is memory? The present state of the engram. BMC Biol. 2016;14:40.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Zucker RS. Short-term synaptic plasticity. Ann Rev Neurosci. 1989;12:13–31.PubMedCrossRefGoogle Scholar
  9. 9.
    Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol. 2002;25:355–405.CrossRefGoogle Scholar
  10. 10.
    Liao D-Z, Hessler NA, Malinow R. Activation of postsynaptic silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature. 1995;375:400–4.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Wang J-H, Kelly PT. Ca2+/CaM signalling pathway up-regulates glutamatergic synaptic function in non-pyramidal fast-spiking neurons of hippocampal CA1. J Physiol Lond. 2001;533(2):407–22.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Daoudal D, Debanne D. Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn Mem. 2003;10:456–65.CrossRefGoogle Scholar
  14. 14.
    Wang JH, Cui S. Associative memory cells: formation, function and perspective. F1000Res. 2017;6:283.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Wang J-H, Kelly PT. Balance between postsynaptic Ca2+−dependent protein kinase and phosphatase activities controlling synaptic strength. Learn Mem. 1996;3:170–81.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Epsztein J, et al. Impact of spikelets on hippocampal CA1 pyramidal cell activity during spatial exploration. Science. 2010;327:474–7.PubMedCrossRefGoogle Scholar
  18. 18.
    Chen N, et al. Axons amplify somatic incomplete spikes into uniform amplitudes in mouse cortical pyramidal neurons. PLoS One. 2010;5(7):e11868.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Bucher D, Goaillard JM. Beyond faithful conduction: short-term dynamics, neuromodulation, and long-term regulation of spike propagation in the axon. Prog Neurobiol. 2011;94(4):307–46.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Debanne D, et al. Axon physiology. Physiol Rev. 2011;91(2):555–602.PubMedCrossRefGoogle Scholar
  21. 21.
    Yang Z, et al. Essential role of axonal VGSC inactivation in time-dependent deceleration and unreliability of spike propagation at cerebellar Purkinje cells. Mol Brain. 2014;7:1.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Yang Z, Wang JH. Frequency-dependent reliability of spike propagation is function of axonal voltage-gated sodium channels in cerebellar Purkinje cells. Cerebellum. 2013;12(6):862–9.PubMedCrossRefGoogle Scholar
  23. 23.
    Wang JH, et al. Functional compatibility between Purkinje cell axon branches and their target neurons in the cerebellum. Biophys J. 2013;104(2):330a.CrossRefGoogle Scholar
  24. 24.
    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
  25. 25.
    Dubnau J, Chiang AS, Tully T. Neural substrates of memory: from synapse to system. J Neurobiol. 2003;54(1):238–53.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Kelso SR, Ganong AH, Brown TH. Hebbian synapses in hippocampus. Proc Natl Acad Sci U S A. 1986;83:5326–30.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Lee SH, Sheng M. Development of neuron-neuron synapses. Curr Opin Neurobiol. 2000;10(1):125–31.PubMedCrossRefGoogle Scholar
  28. 28.
    Lichtman JW, Colman H. Synapse elimination and indelible memory. Neuron. 2000;25(2):269–78.PubMedCrossRefGoogle Scholar
  29. 29.
    London M, et al. The information efficacy of a synapse. Nat Neurosci. 2002;5(4):332–40.PubMedCrossRefGoogle Scholar
  30. 30.
    Mayford M, Siegelbaum SA, Kandel ER. Synapses and memory storage. Cold Spring Harb Perspect Biol. 2012;4(6):a005710.CrossRefGoogle Scholar
  31. 31.
    Stevens CF, Wang Y-Y. Facilitation and depression at single central synapses. Neuron. 1995;14:795–802.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Borst A, Theunissen FE. Information theory and neural coding. Nat Neurosci. 1999;2(11):947–57.PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    Shepherd GM. Synaptic potentials and synaptic integration. In: Shepherd GM, editor. Neurobiology. New York: Oxford University Press; 1998. p. 97–117.Google Scholar
  34. 34.
    Borst JG, Sakmann B. Calcium influx and transmitter release in a fast CNS synapse. Nature. 1996;383(6599):431–4.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Borst JG. The low synaptic release probability in vivo. Trends Neurosci. 2010;33(6):259–66.PubMedCrossRefGoogle Scholar
  36. 36.
    Sudhof T. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature. 1995;375:645–53.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Sudhof TC. The synaptic vesicle cycle revisited. Neuron. 2000;28:317–20.PubMedCrossRefGoogle Scholar
  38. 38.
    Bito H, Deisseroth K, Tsien RW. CREB phosphorylation and dephosphorylation: a Ca2+− and stimulus duration-dependent switch for hippocampal gene expression. Cell. 1996;87:1203–14.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Kandel ER, Siegelbaum SA, Schwartz JH. Elementary interactions between neurons: synaptic transmission. In: Kandel ER, Schwartz JH, Jessell TM, editors. Principles of neural science. New York: McGraw-Hill; 2000. p. 175–308.Google Scholar
  40. 40.
    Kandel ER. The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2, and CPEB. Mol Brain. 2012;5(1):14.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Josselyn SA, Nguyen PV. CREB, synapses and memory disorders: past progress and future challenges. Curr Drug Targets CNS Neurol Disord. 2005;4(5):481–97.PubMedCrossRefGoogle Scholar
  42. 42.
    Sheng M, Thompson MA, Greenberg ME. CREB: a calcium-regulated transcription factor phosphorylated by calmodulin-dependent kinase. Science. 1991;252:1427–30.PubMedCrossRefGoogle Scholar
  43. 43.
    Wang JH, Feng DP. Postsynaptic protein kinase C essential to induction and maintenance of long-term potentiation in the hippocampal CA1 region. Proc Natl Acad Sci U S A. 1992;89(7):2576–80.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Wang JH, W J. The regulation of unitary synaptic responses to multipulse inputs. Soc Neurosci Abstr. 2001. 501.1.Google Scholar
  45. 45.
    Wang J-H. Searching basic units of memory traces: associative memory cells. F1000Res. 2019;8(457):1–28.Google Scholar
  46. 46.
    Sakmann B, Neher E. Single-channel recording. New York: Plenum Publishing Corp; 1983. p. 503.Google Scholar
  47. 47.
    Hodgkin AL, Huxley AF. The dual effect of membrane potential on sodium conductance in the giant axon of Loligo. J Physiol. 1952;116(4):497–506.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    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
  49. 49.
    Hodgkin A. The optimum density of sodium channels in an unmyelinated nerve. Philos Trans R Soc Lond Ser B Biol Sci. 1975;270(908):297–300.CrossRefGoogle Scholar
  50. 50.
    Huxley AF, Stampfli R. Evidence for saltatory conduction in peripheral myelinated nerve fibres. J Physiol. 1949;108(3):315–39.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Johnston D, Wu SM-S. Functional diversity of voltage-gated conductances. In: Johnston D, Wu SM-S, editors. Foundations of cellular neurophysiology. Cambridge, MA/London: MIT Press; 1995. p. 183–214.Google Scholar
  52. 52.
    Linden DJ. The return of the spike: postsynaptic action potentials and the induction of LTP and LTD. Neuron. 1999;22(4):661–6.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Trussell LO, Fischbach GD. Glutamate receptor desensitization and its role in synaptic transmission. Neuron. 1989;3(2):209–18.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Feng TP. Looking back, looking forward. Annu Rev Neurosci. 1988;11:1–12.PubMedCrossRefGoogle Scholar
  55. 55.
    Zucker RS. The calcium hypothesis and modulation of transmitter release by hyperpolarizing pulses. Biophys J. 1987;52:347–50.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Wang J-H, Kelly PT. Regulation of synaptic facilitation by postsynaptic Ca2+/CaM pathways in hippocampal CA1 neurons. J Neurophysiol. 1996;76(1):276–86.PubMedCrossRefGoogle Scholar
  57. 57.
    Wang J-H, Kelly PT. Attenuation of paired-pulse facilitation associated with synaptic potentiation mediated by postsynaptic mechanisms. J Neurophysiol. 1997;78:2707–16.PubMedCrossRefGoogle Scholar
  58. 58.
    Reyes A, et al. Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci. 1998;1:279–85.PubMedCrossRefGoogle Scholar
  59. 59.
    Reyes A, Sakmann B. Developmental switch in the short-term modification of unitary EPSPs evoked in layer 2/3 and layer 5 pyramidal neurons of rat neocortex. J Neurosci. 1999;15:3827–35.CrossRefGoogle Scholar
  60. 60.
    Charlton MP, Smith SJ, Zucker RS. Role of presynaptic calcium ions and channels in synaptic facilitation and depression at the squid giant synapse. J Physiol Lond. 1982;323:173–93.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Katz B, Miledi R. The timing of calcium action during neuromuscular transmission. J Physiol Lond. 1967;189:535–44.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Muller D, et al. Phorbol ester-induced synaptic facilitation is different than long-term potentiation. Proc Natl Acad Sci U S A. 1988;85(18):6997–7000.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Wang JH, et al. Secondary associative memory cells and their plasticity in the prefrontal cortex. Biophys J. 2019;116(3):427a.CrossRefGoogle Scholar
  64. 64.
    Bliss TVP, Collingridge GL. A synaptic model of memory: LTP in the hippocampus. Nature. 1993;361:31–9.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Malenka RC, Nicoll RA. Long-term potentiation – a decade of progress? Nat Neurosci. 1999;285:1870–4.Google Scholar
  66. 66.
    Bliss T, Gardner-Medwin A, Lømo T. Synaptic plasticity in the hippocampal formation. In: Ansell G, Bradley P, editors. Macromolecules and behaviour. London: Macmillan; 1973. p. 193–203.Google Scholar
  67. 67.
    Lynch G, Dunwiddie T, Gribkoff V. Heterosynaptic depression: a postsynaptic correlate of long-term potentiation. Nature. 1977;266:737–9.PubMedCrossRefGoogle Scholar
  68. 68.
    Lynch G, et al. Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature. 1983;305:719–21.PubMedCrossRefGoogle Scholar
  69. 69.
    Hebb DO. The organization of behavior, a neuropsychological theory. New York: Wiley; 1949.Google Scholar
  70. 70.
    Hebb DO. Animal and physiological psychology. Annu Rev Psychol. 1950;1:173–88.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Chavez NLE, Halliwell JV, Bliss TV. A decrease in firing threshold observed after induction of the EPSP-spike (E-S) component of long-term potentiation in rat hippocampal slices. Exp Brain Res. 1990;79(3):633–41.Google Scholar
  72. 72.
    Collingridge GL, et al. Involvement of excitatory amino acid receptors in long-term potentiation in the Schaffer collateral-commissural pathway of rat hippocampal slices. Can J Physiol Pharmacol. 1991;69(7):1084–90.PubMedCrossRefGoogle Scholar
  73. 73.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    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
  75. 75.
    Silva AJ, et al. Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice. Science. 1992;257:206–11.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Silva AJ, et al. Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice. Science. 1992;257:201–6.PubMedCrossRefGoogle Scholar
  77. 77.
    Wang JH, Cui S. Associative memory cells and their working principle in the brain. F1000Res. 2018;7:108.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Reymann KG, et al. Calcium-induced long-term potentiation in the hippocampal slice: characterization of the time course and conditions. Brain Res Bull. 1986;17(3):291–6.PubMedCrossRefGoogle Scholar
  79. 79.
    Wang JH, Kelly PT. Postsynaptic injection of Ca2+/CaM induces synaptic potentiation requiring CaM-KII and PKC activity. Neuron. 1995;15(2):443–52.PubMedCrossRefGoogle Scholar
  80. 80.
    Malenka RC, et al. An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation. Nature. 1989;340(6234):554–7.PubMedCrossRefGoogle Scholar
  81. 81.
    Nayak AS, Morre CI, Browning MD. Ca2+/calmodulin-dependent protein kinase II phosphorylation of the presynaptic protein synapsin I is persistently increased during long-term potentiation. Proc Natl Acad Sci U S A. 1996;93:15451–6.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Popov NS, et al. Alterations in calmodulin content in fractions of rat hippocampal slices during tetanic- and calcium-induced long-term potentiation. Brain Res Bull. 1988;21(2):201–6.PubMedCrossRefGoogle Scholar
  83. 83.
    Reymann KG, et al. Inhibitors of calmodulin and protein kinase C block different phases of hippocampal long-term potentiation. Brain Res. 1988;461(2):388–92.PubMedCrossRefGoogle Scholar
  84. 84.
    Wang J-H, Kelly PT. Postsynaptic calcineurin activity down-regulates synaptic transmission by weakening intracellular Ca2+ signaling mechanisms in hippocampal CA1 neurons. J Neurosci. 1997;17:4600–11.PubMedCrossRefGoogle Scholar
  85. 85.
    Hu GY, et al. PKC injection into hippocampal pyramidal cells elicits features of long term potentiation. Nature. 1987;328(6129):426–9.PubMedCrossRefGoogle Scholar
  86. 86.
    Chen HX, Wang JH. Potentiation of synaptic transmission induced by daicylglycerol/phosphatidylserine and its mutual occlusion with long-term potentiation in rat hippocampal slice. Chin J Physiol Sci. 1995;11:97–102.Google Scholar
  87. 87.
    Malinow R, Madison DV, Tsien RW. Persistent protein kinase activity underlying long-term potentiation. Nature. 1988;335(6193):820–4.PubMedCrossRefGoogle Scholar
  88. 88.
    Malinow R, Schulman H, Tsien RW. Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science. 1989;245:862–6.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Malinow R, Tsien RW. Long-term potentiation: postsynaptic activation of Ca(2+)-dependent protein kinases with subsequent presynaptic enhancement. Prog Brain Res. 1991;89:271–89.PubMedCrossRefGoogle Scholar
  90. 90.
    Nicoll RA, Kauer JA, Malenka RC. The current excitement in long-term potentiation. Neuron. 1988;1:93–103.CrossRefGoogle Scholar
  91. 91.
    Clements MP, Bliss TV, Lynch MA. Increase in arachidonic acid concentration in a postsynaptic membrane fraction following the induction of long-term potentiation in the dentate gyrus. Neuroscience. 1991;45(2):379–89.PubMedCrossRefGoogle Scholar
  92. 92.
    Errington ML, et al. The nitric oxide synthase inhibitor N𝜔–nitro-L-arginine reduces the magnitude of long-term potentiation in the dentate gyrus but not in area CA1 of the hippocampus in vitro. Soc Neurosci. 1991;76:387–95.Google Scholar
  93. 93.
    Lynch MA, et al. Is arachidonic acid a retrograde messenger in long-term potentiation? Biochem Soc Trans. 1991;19(2):391–6.PubMedCrossRefGoogle Scholar
  94. 94.
    Liao D, et al. Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons. Nat Neurosci. 1999;2:37–43.CrossRefGoogle Scholar
  95. 95.
    Petralia RS, et al. Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nat Neurosci. 1999;2:31–6.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Takumi Y, et al. Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat Neurosci. 1999;2:618–24.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Blank T, Nijholt I, Spiess J. Treatment strategies of age-related memory dysfunction by modulation of neuronal plasticity. Mini Rev Med Chem. 2007;7(1):55–64.CrossRefGoogle Scholar
  98. 98.
    Byrne JH, et al. Roles of second messenger pathways in neuronal plasticity and in learning and memory. Adv Second Messenger Phosphoprotein Res. 1993;27:47–108.PubMedGoogle Scholar
  99. 99.
    Kemenes I, et al. Role of delayed nonsynaptic neuronal plasticity in long-term associative memory. Curr Biol. 2006;16(13):1269–79.PubMedCrossRefGoogle Scholar
  100. 100.
    Teyler TJ, Fountain SB. Neuronal plasticity in the mammalian brain: relevance to behavioral learning and memory. Child Dev. 1987;58(3):698–712.PubMedCrossRefGoogle Scholar
  101. 101.
    Turrigiano GG, Nelson SB. Hebb and homeostasis in neuronal plasticity. Curr Opin Neurobiol. 2000;10(3):358–64.PubMedCrossRefGoogle Scholar
  102. 102.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Chen N, et al. After-hyperpolarization improves spike programming through lowering threshold potentials and refractory periods mediated by voltage-gated sodium channels. Biochem Biophys Res Commun. 2006;346:938–45.PubMedCrossRefGoogle Scholar
  105. 105.
    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
  106. 106.
    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
  107. 107.
    Ganguly K, Kiss L, Poo M-M. Enhancement of presynaptic neuronal excitability by correlated presynaptic and postsynaptic spiking. Nat Neurosci. 2000;3(10):1018–26.PubMedCrossRefGoogle Scholar
  108. 108.
    Nick TA, Ribera AB. Synaptic activity modulates presynaptic excitability. Nat Neurosci. 2000;3(2):142–9.PubMedCrossRefGoogle Scholar
  109. 109.
    Aizenmann C, Linden DJ. Rapid, synaptically driven increases in the intrinsic excitability of cerebellar nuclear neurons. Nat Neurosci. 2000;3:109–11.CrossRefGoogle Scholar
  110. 110.
    Campanac E, Debanne D. Plasticity of neuronal excitability: Hebbian rules beyond the synapse. Arch Ital Biol. 2007;145(3–4):277–87.Google Scholar
  111. 111.
    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.CrossRefGoogle Scholar
  112. 112.
    Desai NS, Rutherford L, Turrigiano GG. Plasticity in the intrinsic excitability of cortical pyramidal neurons. Nat Neurosci. 1999;2(6):515–20.PubMedCrossRefGoogle Scholar
  113. 113.
    Burrone J, O’Byrne M, Murthy VN. Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature. 2002;420:414–8.PubMedCrossRefGoogle Scholar
  114. 114.
    Ramakers GJ, Corner MA, Habers AM. Development in the absence of spontaneous bioelectric activity results in increased stereotyped burst firing in cultures of associated cerebral cortex. Exp Brain Res. 1990;79:157–66.PubMedCrossRefGoogle Scholar
  115. 115.
    Van Den Pol AN, Obrietan K, Belousov A. Glutamate hyperexcitability and seizure-like activity throughout the brain and spinal cord upon relief from chronic glutamate receptor blockade in culture. Neuroscience. 1996;74:653–74.CrossRefGoogle Scholar
  116. 116.
    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
  117. 117.
    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
  118. 118.
    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
  119. 119.
    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
  120. 120.
    Ashby MC, Isaac JT. Maturation of a recurrent excitatory neocortical circuit by experience-dependent unsilencing of newly formed dendritic spines. Neuron. 2011;70(3):510–21.PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Bourne J, Harris KM. Do thin spines learn to be mushroom spines that remember? Curr Opin Neurobiol. 2007;17(3):381–6.PubMedCrossRefGoogle Scholar
  122. 122.
    Fifkova E, Van Harreveld A. Long-lasting morphological changes in dendritic spines of dentate granular cells following stimulation of the entorhinal area. J Neurocytol. 1977;6:211–30.PubMedCrossRefGoogle Scholar
  123. 123.
    Fortin DA, Srivastava T, Soderling TR. Structural modulation of dendritic spines during synaptic plasticity. Neuroscientist. 2011;18(4):326–41.PubMedCrossRefGoogle Scholar
  124. 124.
    Hongpaisan J, Alkon DL. A structural basis for enhancement of long-term associative memory in single dendritic spines regulated by PKC. Proc Natl Acad Sci U S A. 2007;104(49):19571–6.PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Kasai H, et al. Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci. 2010;33(3):121–9.PubMedCrossRefGoogle Scholar
  126. 126.
    Kitanishi T, et al. Experience-dependent, rapid structural changes in hippocampal pyramidal cell spines. Cereb Cortex. 2009;19(11):2572–8.PubMedPubMedCentralCrossRefGoogle Scholar
  127. 127.
    Lendvai B, et al. Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature. 2000;404:876–81.PubMedCrossRefGoogle Scholar
  128. 128.
    Leuner B, Falduto J, Shors TJ. Associative memory formation increases the observation of dendritic spines in the hippocampus. J Neurosci. 2003;23(2):659–65.PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Matsuzaki M, et al. Structural basis of long-term potentiation in single dendritic spines. Nature. 2004;429(6993):761–6.PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Moczulska KE, et al. Dynamics of dendritic spines in the mouse auditory cortex during memory formation and memory recall. Proc Natl Acad Sci U S A. 2013;110(45):18315–20.PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Murakoshi H, Yasuda R. Postsynaptic signaling during plasticity of dendritic spines. Trends Neurosci. 2012;35(2):135–43.PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Zuo Y, Perkon I, Diamond ME. Whisking and whisker kinematics during a texture classification task. Philos Trans R Soc Lond Ser B Biol Sci. 2011;366(1581):3058–69.CrossRefGoogle Scholar
  133. 133.
    Yuste R, Denk W. Dendritic spines as basic functional units of neuronal integration. Nature. 1995;375:682–4.PubMedCrossRefGoogle Scholar
  134. 134.
    Patterson M, Yasuda R. Signalling pathways underlying structural plasticity of dendritic spines. Br J Pharmacol. 2011;163(8):1626–38.PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Tanaka J, et al. Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science. 2008;319(5870):1683–7.PubMedPubMedCentralCrossRefGoogle Scholar
  136. 136.
    Harnett MT, et al. Synaptic amplification by dendritic spines enhances input cooperativity. Nature. 2012;491(7425):599–602.PubMedPubMedCentralCrossRefGoogle Scholar
  137. 137.
    Jung CK, Herms J. Structural dynamics of dendritic spines are influenced by an environmental enrichment: an in vivo imaging study. Cereb Cortex. 2014;24(2):377–84.PubMedCrossRefGoogle Scholar
  138. 138.
    Schiegg A, Gerstner W, Ritz R, Leo van Hemmen J. Intracellular Ca2+ stores can account for the time course of LTP induction: a model of Ca2+ dynamics in dendritic spines. J Neurophysiol. 1995;74(3):1046–55.PubMedCrossRefGoogle Scholar
  139. 139.
    Garin-Aguilar ME, et al. Extinction procedure induces pruning of dendritic spines in CA1 hippocampal field depending on strength of training in rats. Front Behav Neurosci. 2012;6:12.PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Leuner B, Shors TJ. New spines, new memories. Mol Neurobiol. 2004;29(2):117–30.PubMedPubMedCentralCrossRefGoogle Scholar
  141. 141.
    Sanders J, et al. Elimination of dendritic spines with long-term memory is specific to active circuits. J Neurosci. 2012;32(36):12570–8.PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Vees AM, et al. Increased number and size of dendritic spines in ipsilateral barrel field cortex following unilateral whisker trimming in postnatal rat. J Comp Neurol. 1998;400(1):110–24.PubMedCrossRefGoogle Scholar
  143. 143.
    Ni H, et al. Upregulation of barrel GABAergic neurons is associated with cross-modal plasticity in olfactory deficit. PLoS One. 2010;5(10):e13736.PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    Wang GY, et al. Glucocorticoid induces incoordination between glutamatergic and GABAergic neurons in the amygdala. PLoS One. 2016;11(11):e0166535.PubMedPubMedCentralCrossRefGoogle Scholar
  145. 145.
    Ye B, et al. The functional upregulation of piriform cortex is associated with cross-modal plasticity in loss of whisker tactile inputs. PLoS One. 2012;7(8):e41986.PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Zhu Z, et al. GABAergic neurons in nucleus accumbens are correlated to resilience and vulnerability to chronic stress for major depression. Oncotarget. 2017;8(22):35933–45.PubMedPubMedCentralGoogle Scholar
  147. 147.
    Liu B, Feng J, Wang J-H. Protein kinase C is essential for kainate-induced anxiety-related behavior and glutamatergic synapse upregulation in prelimbic cortex. CNS Neurosci Ther. 2014;20:982–90.PubMedPubMedCentralCrossRefGoogle Scholar
  148. 148.
    Ma K, et al. Impaired GABA synthesis, uptake and release are associated with depression-like behaviors induced by chronic mild stress. Transl Psychiatry. 2016;6(e910):1–10.Google Scholar
  149. 149.
    Wen B, et al. A portion of inhibitory neurons in human temporal lobe epilepsy are functionally upregulated: an endogenous mechanism for seizure termination. CNS Neurosci Ther. 2015;21(2):204–14.PubMedPubMedCentralCrossRefGoogle Scholar
  150. 150.
    Xu A, Cui S, Wang J. Incoordination among subcellular compartments is associated to depression-like behavior induced by chronic mild stress. Int J Neuropsychopharmacol. 2015;19(5):pyv122.CrossRefPubMedPubMedCentralGoogle Scholar
  151. 151.
    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

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

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

Personalised recommendations