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Reverberatory Activity in Neuronal Networks

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Coherent Behavior in Neuronal Networks

Part of the book series: Springer Series in Computational Neuroscience ((NEUROSCI,volume 3))

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Abstract

Reverberatory activity in neuronal cell assemblies has been proposed to carry “online” memory traces in the brain. However, the dynamics and cellular mechanism of such reverberation have been difficult to study because of the enormous complexity of intact circuits. To overcome this difficulty, small networks of interconnected neurons have been grown in culture dishes to provide a model system for studies using patch-clamp recording and fluorescent imaging approaches. In such networks, brief stimulation could elicit rhythmic reverberation that consists of repeating motifs of specific patterns of population activation in the network. Experimental and modeling analysis suggested that the reverberation is driven by recurrent excitation, is sustained by the oft-overlooked asynchronous synaptic transmission modulated by intracellular calcium, and is terminated by a slow component of short-term synaptic depression. More recent data suggest that Hebbian synaptic plasticity could underlie activity-induced emergence of reverberation. Thus, these in vitro networks may serve as prototypic Hebbian cell assemblies for the study of potential mechanisms of information representation and storage in brain circuits.

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References

  1. Abbott LF and Nelson SB (2000) Synaptic plasticity: taming the beast. Nat Neurosci 3 Suppl: 1178–1183.

    Google Scholar 

  2. Amit DJ, Brunel N and Tsodyks MV (1994) Correlations of cortical Hebbian reverberations: theory versus experiment. J Neurosci 14: 6435–6445.

    PubMed  CAS  Google Scholar 

  3. Amit DJ, Gutfreund H and Sompolinsky H (1985) Spin-glass models of neural networks. Phys Rev A 32: 1007–1018.

    Article  PubMed  Google Scholar 

  4. Artola A and Singer W (1993) Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation. Trends Neurosci 16: 480–487.

    Article  PubMed  CAS  Google Scholar 

  5. Atluri PP and Regehr WG (1998) Delayed release of neurotransmitter from cerebellar granule cells. J Neurosci 18: 8214–8227.

    PubMed  CAS  Google Scholar 

  6. Banker G and Goslin K, eds. (1998) Culturing Nerve Cells, Second edn (Cambridge, MA: The MIT Press).

    Google Scholar 

  7. Barrett EF and Stevens CF (1972) The kinetics of transmitter release at the frog neuromuscular junction. J Physiol 227: 691–708.

    PubMed  CAS  Google Scholar 

  8. Beggs JM and Plenz D (2003) Neuronal avalanches in neocortical circuits. J Neurosci 23: 11167–11177.

    PubMed  CAS  Google Scholar 

  9. Beggs JM and Plenz D (2004) Neuronal avalanches are diverse and precise activity patterns that are stable for many hours in cortical slice cultures. J Neurosci 24: 5216–5229.

    Article  PubMed  CAS  Google Scholar 

  10. Bell CC, Han VZ, Sugawara Y and Grant K (1997) Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature 387: 278–281.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  12. Bi GQ and Poo MM (1999) Distributed synaptic modification in neural networks induced by patterned stimulation. Nature 401: 792–796.

    Article  PubMed  CAS  Google Scholar 

  13. Bi GQ and Poo MM (2001a) Synaptic modifications by correlated activity: Hebb’s postulate revisited. Annu Rev Neurosci 24: 139–166.

    Article  PubMed  CAS  Google Scholar 

  14. Bi GQ and Poo MM (2001b) Synaptic modification by correlated activity: Hebb’s postulate revisited. Annu Rev Neurosci 24: 139–166.

    Article  PubMed  CAS  Google Scholar 

  15. Bliss TV and Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31–39.

    Article  PubMed  CAS  Google Scholar 

  16. Brown TH, Kairiss EW and Keenan CL (1990) Hebbian synapses: biophysical mechanisms and algorithms. Annu Rev Neurosci 13: 475–511.

    Article  PubMed  CAS  Google Scholar 

  17. Caporale N and Dan Y (2008) Spike timing-dependent plasticity: a Hebbian learning rule. Annu Rev Neurosci 31: 25–46.

    Article  PubMed  CAS  Google Scholar 

  18. Cossart R, Aronov D and Yuste R (2003) Attractor dynamics of network UP states in the neocortex. Nature 423: 283–288.

    Article  PubMed  CAS  Google Scholar 

  19. Cummings DD, Wilcox KS and Dichter MA (1996) Calcium-dependent paired-pulse facilitation of miniature EPSC frequency accompanies depression of EPSCs at hippocampal synapses in culture. J Neurosci 16: 5312–5323.

    PubMed  CAS  Google Scholar 

  20. Dan Y and Poo MM (2006) Spike timing-dependent plasticity: from synapse to perception. Physiol Rev 86: 1033–1048.

    Article  PubMed  Google Scholar 

  21. Debanne D, Gahwiler BH and Thompson SM (1998) Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J Physiol (Lond) 507: 237–247.

    Article  CAS  Google Scholar 

  22. Del Castillo J and Katz B (1954) Statistical factors involved in neuromuscular facilitation and depression. J Physiol 124: 574–585.

    Google Scholar 

  23. Derkach VA, Oh MC, Guire ES and Soderling TR (2007) Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat Rev Neurosci 8: 101–113.

    Article  PubMed  CAS  Google Scholar 

  24. Durstewitz D, Seamans JK and Sejnowski TJ (2000) Neurocomputational models of working memory. Nat Neurosci 3 Suppl: 1184–1191.

    Google Scholar 

  25. Egorov AV, Hamam BN, Fransen E, Hasselmo ME and Alonso AA (2002) Graded persistent activity in entorhinal cortex neurons. Nature 420: 173–178.

    Article  PubMed  CAS  Google Scholar 

  26. Eytan D, Brenner N and Marom S (2003) Selective adaptation in networks of cortical neurons. J Neurosci 23: 9349–9356.

    PubMed  CAS  Google Scholar 

  27. Funahashi S, Bruce CJ and Goldman-Rakic PS (1989) Mnemonic coding of visual space in the monkey’s dorsolateral prefrontal cortex. J Neurophysiol 61: 331–349.

    PubMed  CAS  Google Scholar 

  28. Fuster JM and Alexander GE (1971) Neuron activity related to short-term memory. Science 173: 652–654.

    Article  PubMed  CAS  Google Scholar 

  29. Goda Y and Stevens CF (1994) Two components of transmitter release at a central synapse. Proc Natl Acad Sci U S A 91: 12942–12946.

    Article  PubMed  CAS  Google Scholar 

  30. Goda Y and Stevens CF (1996) Long-term depression properties in a simple system. Neuron 16: 103–111.

    Article  PubMed  CAS  Google Scholar 

  31. Gutkin BS, Laing CR, Colby CL, Chow CC and Ermentrout GB (2001) Turning on and off with excitation: the role of spike-timing asynchrony and synchrony in sustained neural activity. J comput neurosci 11: 121–134.

    Article  PubMed  CAS  Google Scholar 

  32. Hagler DJ, Jr. and Goda Y (2001) Properties of synchronous and asynchronous release during pulse train depression in cultured hippocampal neurons. J Neurophysiol 85: 2324–2334.

    PubMed  CAS  Google Scholar 

  33. Harris KD (2005) Neural signatures of cell assembly organization. Nat Rev Neurosci 6: 399–407.

    Article  PubMed  CAS  Google Scholar 

  34. Hebb DO (1949) The Organization of Behavior (New York: Wiley).

    Google Scholar 

  35. Hopfield JJ (1982) Neural networks and physical systems with emergent collective computational abilities. Proc Natl Acad Sci U S A 79: 2554–2558.

    Article  PubMed  CAS  Google Scholar 

  36. Ikegaya Y, Aaron G, Cossart R, Aronov D, Lampl I, Ferster D and Yuste R (2004) Synfire chains and cortical songs: temporal modules of cortical activity. Science 304: 559–564.

    Article  PubMed  CAS  Google Scholar 

  37. Kleinfeld D and Sompolinsky H (1988) Associative neural network model for the generation of temporal patterns. Theory and application to central pattern generators. Biophys J 54: 1039–1051.

    CAS  Google Scholar 

  38. Kubota K and Niki H (1971) Prefrontal cortical unit activity and delayed alternation performance in monkeys. J Neurophysiol 34: 337–347.

    PubMed  CAS  Google Scholar 

  39. Laing CR and Chow CC (2001) Stationary bumps in networks of spiking neurons. Neural Comput 13: 1473–1494.

    Article  PubMed  CAS  Google Scholar 

  40. Lau PM and Bi GQ (2005) Synaptic mechanisms of persistent reverberatory activity in neuronal networks. Proc Natl Acad Sci U S A 102: 10333–10338.

    Article  PubMed  CAS  Google Scholar 

  41. Lisman J, Lichtman JW and Sanes JR (2003) LTP: perils and progress. Nat Rev Neurosci 4: 926–929.

    Article  PubMed  CAS  Google Scholar 

  42. Llano I, Gonzalez J, Caputo C, Lai FA, Blayney LM, Tan YP and Marty A (2000) Presynaptic calcium stores underlie large-amplitude miniature IPSCs and spontaneous calcium transients. Nat Neurosci 3: 1256–1265.

    Article  PubMed  CAS  Google Scholar 

  43. Loewenstein Y, Mahon S, Chadderton P, Kitamura K, Sompolinsky H, Yarom Y and Hausser M (2005) Bistability of cerebellar Purkinje cells modulated by sensory stimulation. Nat Neurosci 8: 202–211.

    Article  PubMed  CAS  Google Scholar 

  44. Lorente de Nó R (1933) Vestibulo-ocular reflex arc. Arch Neurol Psychiatry 30: 245–291.

    Google Scholar 

  45. Lu T and Trussell LO (2000) Inhibitory transmission mediated by asynchronous transmitter release. Neuron 26: 683–694.

    Article  PubMed  CAS  Google Scholar 

  46. Maeda E, Robinson HP and Kawana A (1995) The mechanisms of generation and propagation of synchronized bursting in developing networks of cortical neurons. J Neurosci 15: 6834–6845.

    PubMed  CAS  Google Scholar 

  47. Magee JC and Johnston D (1997) A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275: 209–213.

    Article  PubMed  CAS  Google Scholar 

  48. Malenka RC (2003) The long-term potential of LTP. Nat Rev Neurosci 4: 923–926.

    Article  PubMed  CAS  Google Scholar 

  49. Malenka RC and Nicoll RA (1999) Long-term potentiation – a decade of progress. Science 285: 1870–1874.

    Article  PubMed  CAS  Google Scholar 

  50. Mann EO and Paulsen O (2007) Role of GABAergic inhibition in hippocampal network oscillations. Trends Neurosci 30: 343–349.

    Article  PubMed  CAS  Google Scholar 

  51. Markram H, Lubke J, Frotscher M and Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275: 213–215.

    Article  PubMed  CAS  Google Scholar 

  52. McCormick DA and Contreras D (2001) On the cellular and network bases of epileptic seizures. Annu Rev Physiol 63: 815–846.

    Article  PubMed  CAS  Google Scholar 

  53. McCulloch WS and Pitts W (1943) A logical calculus of the ideas immanent in nervous activity. Bull Math Biophys 5: 115–133.

    Article  Google Scholar 

  54. Mehta MR, Barnes CA and McNaughton BL (1997) Experience-dependent, asymmetric expansion of hippocampal place fields. Proc Natl Acad Sci U S A 94: 8918–8921.

    Article  PubMed  CAS  Google Scholar 

  55. Miledi R (1966) Strontium as a substitute for calcium in the process of transmitter release at the neuromuscular junction. Nature 212: 1233–1234.

    Article  PubMed  CAS  Google Scholar 

  56. Milner B, Squire LR and Kandel ER (1998) Cognitive neuroscience and the study of memory. Neuron 20: 445–468.

    Article  PubMed  CAS  Google Scholar 

  57. Molnar G, Olah S, Komlosi G, Fule M, Szabadics J, Varga C, Barzo P and Tamas G (2008) Complex events initiated by individual spikes in the human cerebral cortex. PLoS biology 6: e222.

    Article  PubMed  Google Scholar 

  58. Nelson S (2000) Timing isn’t everything. Neuron 26: 545–546.

    Article  PubMed  CAS  Google Scholar 

  59. Peng Y (1996) Ryanodine-sensitive component of calcium transients evoked by nerve firing at presynaptic nerve terminals. J Neurosci 16: 6703–6712.

    PubMed  CAS  Google Scholar 

  60. Segev R, Shapira Y, Benveniste M and Ben-Jacob E (2001) Observations and modeling of synchronized bursting in two-dimensional neural networks. Phys Rev E Stat Nonlin Soft Matter Phys 64: 011920.

    Article  PubMed  CAS  Google Scholar 

  61. Seung HS (2000) Half a century of Hebb. Nat Neurosci 3 Suppl: 1166.

    Google Scholar 

  62. Seung HS, Lee DD, Reis BY and Tank DW (2000) Stability of the memory of eye position in a recurrent network of conductance-based model neurons. Neuron 26: 259–271.

    Article  PubMed  CAS  Google Scholar 

  63. Shu Y, Hasenstaub A and McCormick DA (2003) Turning on and off recurrent balanced cortical activity. Nature 423: 288–293.

    Article  PubMed  CAS  Google Scholar 

  64. Simkus CR and Stricker C (2002) The contribution of intracellular calcium stores to mEPSCs recorded in layer II neurones of rat barrel cortex. J Physiol 545: 521–535.

    Article  PubMed  CAS  Google Scholar 

  65. Stent GS (1973) A physiological mechanism for Hebb’s postulate of learning. Proc Natl Acad Sci U S A 70: 997–1001.

    Article  PubMed  CAS  Google Scholar 

  66. Stevens CF (1996) Strengths and weaknesses in memory. Nature 381: 471–472.

    Article  PubMed  CAS  Google Scholar 

  67. Tegner J, Compte A and Wang XJ (2002) The dynamical stability of reverberatory neural circuits. Biol Cybern 87: 471–481.

    Article  PubMed  Google Scholar 

  68. Tsodyks M, Pawelzik K and Markram H (1998) Neural networks with dynamic synapses. Neural comput 10: 821–835.

    Article  PubMed  CAS  Google Scholar 

  69. Tsodyks M, Uziel A and Markram H (2000) Synchrony generation in recurrent networks with frequency-dependent synapses. J Neurosci 20: RC50.

    Google Scholar 

  70. Verkhratsky A (2002) The endoplasmic reticulum and neuronal calcium signalling. Cell Calcium 32: 393–404.

    Article  PubMed  CAS  Google Scholar 

  71. Volman V, Baruchi I and Ben-Jacob E (2005) Manifestation of function-follow-form in cultured neuronal networks. Phys Biol 2: 98–110.

    Article  PubMed  CAS  Google Scholar 

  72. Volman V, Gerkin RC, Lau PM, Ben-Jacob E and Bi GQ (2007) Calcium and synaptic dynamics underlying reverberatory activity in neuronal networks. Phys Biol 4: 91–103.

    Article  PubMed  CAS  Google Scholar 

  73. Wagenaar DA, Pine J and Potter SM (2006) An extremely rich repertoire of bursting patterns during the development of cortical cultures. BMC Neurosci 7: 11.

    Article  PubMed  Google Scholar 

  74. Wang XJ (1999) Synaptic basis of cortical persistent activity: the importance of NMDA receptors to working memory. J Neurosci 19: 9587–9603.

    PubMed  CAS  Google Scholar 

  75. Wang XJ (2001) Synaptic reverberation underlying mnemonic persistent activity. Trends Neurosci 24: 455–463.

    Article  PubMed  CAS  Google Scholar 

  76. Whittington MA and Traub RD (2003) Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci 26: 676–682.

    Article  PubMed  CAS  Google Scholar 

  77. Whittington MA, Traub RD, Kopell N, Ermentrout B and Buhl EH (2000) Inhibition-based rhythms: experimental and mathematical observations on network dynamics. Int J Psychophysiol 38: 315–336.

    Article  PubMed  CAS  Google Scholar 

  78. Xu-Friedman MA and Regehr WG (2000) Probing fundamental aspects of synaptic transmission with strontium. J Neurosci 20: 4414–4422.

    PubMed  CAS  Google Scholar 

  79. Zhang LI, Tao HW, Holt CE, Harris WA and Poo MM (1998) A critical window for cooperation and competition among developing retinotectal synapses. Nature 395: 37–44.

    Article  PubMed  CAS  Google Scholar 

  80. Zipser D, Kehoe B, Littlewort G and Fuster J (1993) A spiking network model of short-term active memory. J Neurosci 13: 3406–3420.

    PubMed  CAS  Google Scholar 

  81. Zucker RS and Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64: 355–405.

    Article  PubMed  CAS  Google Scholar 

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Lau, PM., Bi, GQ. (2009). Reverberatory Activity in Neuronal Networks. In: Josic, K., Rubin, J., Matias, M., Romo, R. (eds) Coherent Behavior in Neuronal Networks. Springer Series in Computational Neuroscience, vol 3. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-0389-1_4

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