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Reverberatory activity in neuronal networks in vitro

  • Review/Neuroscience
  • Published:
Chinese Science Bulletin

Abstract

It has been proposed that during cognitive processes, “online” memory traces in the brain are carried by reverberatory activity in neuronal circuits. However, the nature of such reverberation has remained elusive from experimental studies, largely due to the enormous complexity of intact circuits. Recent works have attempted to address this issue using cultured neuronal network and have revealed new dynamic properties of network reverberation as well as the underlying cellular mechanisms. These results demonstrate the effectiveness of in vitro networks as a useful tool for mechanistic dissection of neuronal circuit dynamics.

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Reberences

  1. Hebb D O. The Organization of Behavior. New York: Wiley, 1949

    Google Scholar 

  2. Stent G S. A physiological mechanism for Hebb’s postulate of learning. Proc Natl Acad Sci USA, 1973, 70: 997–1001

    Article  Google Scholar 

  3. Brown T H, Kairiss E W, Keenan C L. Hebbian synapses: Biophysical mechanisms and algorithms. Annu Rev Neurosci, 1990, 13: 475–511

    Article  Google Scholar 

  4. Bliss T V, Collingridge G L. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature, 1993, 361: 31–39

    Article  Google Scholar 

  5. Milner B, Squire L R, Kandel E R. Cognitive neuroscience and the study of memory. Neuron, 1998, 20: 445–468

    Article  Google Scholar 

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

    Article  Google Scholar 

  7. Stevens C F. Strengths and weaknesses in memory. Nature, 1996, 381: 471–472

    Article  Google Scholar 

  8. Malenka R C, Nicoll R A. Long-term potentiation—a decade of progress. Science, 1999, 285: 1870–1874

    Article  Google Scholar 

  9. Lisman J, Lichtman J W, Sanes J R. LTP: Perils and progress. Nat Rev Neurosci, 2003, 4: 926–929

    Article  Google Scholar 

  10. Malenka R C. The long-term potential of LTP. Nat Rev Neurosci, 2003, 4: 923–926

    Article  Google Scholar 

  11. Derkach V A, Oh M C, Guire E S, et al. Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat Rev Neurosci, 2007, 8: 101–113

    Article  Google Scholar 

  12. Bell C C, Han V Z, Sugawara Y, et al. Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature, 1997, 387: 278–281

    Article  Google Scholar 

  13. Magee J C, Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science, 1997, 275: 209–213

    Article  Google Scholar 

  14. Markram H, Lubke J, Frotscher M, et al. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science, 1997, 275: 213–215

    Article  Google Scholar 

  15. Mehta M R, Barnes C A, McNaughton B L. Experience-dependent, asymmetric expansion of hippocampal place fields. Proc Natl Acad Sci USA, 1997, 94: 8918–8921

    Article  Google Scholar 

  16. Bi G Q, Poo M M. Synaptic modifications in cultured hippocampal neurons: Dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci, 1998, 18: 10464–10472

    Google Scholar 

  17. Debanne D, Gahwiler B H, Thompson S M. Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J Physiol (Lond), 1998, 507: 237–247

    Article  Google Scholar 

  18. Zhang L I, Tao H W, Holt C E, et al. A critical window for cooperation and competition among developing retinotectal synapses. Nature, 1998, 395: 37–44

    Article  Google Scholar 

  19. Abbott L F, Nelson S B. Synaptic plasticity: Taming the beast. Nat Neurosci, 2000, 3(Suppl): 1178–1183

    Article  Google Scholar 

  20. Bi G Q, Poo M M. Synaptic modification by correlated activity: Hebb’s postulate revisited. Annu Rev Neurosci, 2001, 24: 139–166

    Article  Google Scholar 

  21. Dan Y, Poo M M. Spike timing-dependent plasticity: From synapse to perception. Physiol Rev, 2006, 86: 1033–1048

    Article  Google Scholar 

  22. Fuster J M, Alexander G E. Neuron activity related to short-term memory. Science, 1971, 173: 652–654

    Article  Google Scholar 

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

    Google Scholar 

  24. Funahashi S, Bruce C J, Goldman-Rakic P S. Mnemonic coding of visual space in the monkey’s dorsolateral prefrontal cortex. J Neurophysiol, 1989, 61: 331–349

    Google Scholar 

  25. Durstewitz D, Seamans J K, Sejnowski T J. Neurocomputational models of working memory. Nat Neurosci, 2000, 3(Suppl): 1184–1191

    Article  Google Scholar 

  26. Wang X J. Synaptic reverberation underlying mnemonic persistent activity. Trends Neurosci, 2001, 24: 455–463

    Article  Google Scholar 

  27. Harris K D. Neural signatures of cell assembly organization. Nat Rev Neurosci, 2005, 6: 399–407

    Article  Google Scholar 

  28. Seung H S. Half a century of Hebb. Nat Neurosci, 2000, 3(Suppl): 1166

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  31. Shu Y, Hasenstaub A, McCormick D A. Turning on and off recurrent balanced cortical activity. Nature, 2003, 423: 288–293

    Article  Google Scholar 

  32. Ikegaya Y, Aaron G, Cossart R, et al. Synfire chains and cortical songs: Temporal modules of cortical activity. Science, 2004, 304: 559–564

    Article  Google Scholar 

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

    Google Scholar 

  34. Beggs J M, Plenz D. Neuronal avalanches in neocortical circuits. J Neurosci, 2003, 23: 11167–11177

    Google Scholar 

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

    Article  Google Scholar 

  36. Segev R, Shapira Y, Benveniste M, et al. Observations and modeling of synchronized bursting in two-dimensional neural networks. Phys Rev E Stat Nonlin Soft Matter Phys, 2001, 64: 011920

    Google Scholar 

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

    Article  Google Scholar 

  38. Wagenaar D A, Pine J, Potter S M. An extremely rich repertoire of bursting patterns during the development of cortical cultures. BMC Neuroscience, 2006, 7: 11

    Article  Google Scholar 

  39. Lau P M, Bi G Q. Synaptic mechanisms of persistent reverberatory activity in neuronal networks. Proc Natl Acad Sci USA, 2005, 102: 10333–10338

    Article  Google Scholar 

  40. Banker G, Goslin K, eds. Culturing Nerve Cells. Cambridge, Massachusetts: The MIT Press, 1998

    Google Scholar 

  41. Bi G Q, Poo M M. Distributed synaptic modification in neural networks induced by patterned stimulation. Nature, 1999, 401: 792–796

    Article  Google Scholar 

  42. Egorov A V, Hamam B N, Fransen E, et al. Graded persistent activity in entorhinal cortex neurons. Nature, 2002, 420: 173–178

    Article  Google Scholar 

  43. Loewenstein Y, Mahon S, Chadderton P, et al. Bistability of cerebellar Purkinje cells modulated by sensory stimulation. Nat Neurosci, 2005, 8: 202–211

    Article  Google Scholar 

  44. McCormick D A, Contreras D. On the cellular and network bases of epileptic seizures. Annu Rev Physiol, 2001, 63: 815–846

    Article  Google Scholar 

  45. Wang X J. Synaptic basis of cortical persistent activity: The importance of NMDA receptors to working memory. J Neurosci, 1999, 19: 9587–9603

    Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  48. Barrett E F, Stevens C F. The kinetics of transmitter release at the frog neuromuscular junction. J Physiol, 1972, 227: 691–708

    Google Scholar 

  49. Goda Y, Stevens C F. Two components of transmitter release at a central synapse. Proc Natl Acad Sci USA, 1994, 91: 12942–12946

    Article  Google Scholar 

  50. Cummings D D, Wilcox K S, Dichter M A. Calcium-dependent paired-pulse facilitation of miniature EPSC frequency accompanies depression of EPSCs at hippocampal synapses in culture. J Neurosci, 1996, 16: 5312–5323

    Google Scholar 

  51. Atluri P P, Regehr W G. Delayed release of neurotransmitter from cerebellar granule cells. J Neurosci, 1998, 18: 8214–8227

    Google Scholar 

  52. Lu T, Trussell L O. Inhibitory transmission mediated by asynchronous transmitter release. Neuron, 2000, 26: 683–694

    Article  Google Scholar 

  53. Nelson S. Timing isn’t everything. Neuron, 2000, 26: 545–546

    Article  Google Scholar 

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

    Google Scholar 

  55. Xu-Friedman M A, Regehr W G. Probing fundamental aspects of synaptic transmission with strontium. J Neurosci, 2000, 20: 4414–4422

    Google Scholar 

  56. Seung H S, Lee D D, Reis B Y, et al. Stability of the memory of eye position in a recurrent network of conductance-based model neurons. Neuron, 2000, 26: 259–271

    Article  Google Scholar 

  57. Tegner J, Compte A, Wang X J. The dynamical stability of reverberatory neural circuits. Biol Cybern, 2002, 87: 471–481

    Article  Google Scholar 

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

    Google Scholar 

  59. Llano I, González J, Caputo C, et al. Presynaptic calcium stores underlie large-amplitude miniature IPSCs and spontaneous calcium transients. Nat Neurosci, 2000, 3: 1256–1265

    Article  Google Scholar 

  60. Simkus C R & Stricker C. The contribution of intracellular calcium stores to mEPSCs recorded in layer II neurones of rat barrel cortex. J Physiol, 2002, 545: 521–535.

    Article  Google Scholar 

  61. Verkhratsky A. The endoplasmic reticulum and neuronal calcium signalling. Cell Calcium, 2002, 32: 393–404

    Article  Google Scholar 

  62. Zucker R S, Regehr W G. Short-term synaptic plasticity. Annu Rev Physiol, 2002, 64: 355–405

    Article  Google Scholar 

  63. Tsodyks M, Pawelzik K, Markram H. Neural networks with dynamic synapses. Neural Comput, 1998, 10: 821–835

    Article  Google Scholar 

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

    Google Scholar 

  65. Goda Y, Stevens C F. Long-term depression properties in a simple system. Neuron, 1996, 16: 103–111

    Article  Google Scholar 

  66. Volman V, Gerkin R C, Lau P M, et al. Calcium and synaptic dynamics underlying reverberatory activity in neuronal networks. Phys Biol, 2007, 4: 91–103

    Article  Google Scholar 

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Authors and Affiliations

  1. School of Life Science, University of Science and Technology of China, Hefei, 230026, China

    PakMing Lau & GuoQiang Bi

  2. Department of Neurobiology, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15261, USA

    PakMing Lau & GuoQiang Bi

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  1. PakMing Lau
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  2. GuoQiang Bi
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Correspondence to GuoQiang Bi.

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Lau, P., Bi, G. Reverberatory activity in neuronal networks in vitro . Chin. Sci. Bull. 54, 1828–1835 (2009). https://doi.org/10.1007/s11434-009-0135-1

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  • DOI: https://doi.org/10.1007/s11434-009-0135-1

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