Network Bursting Dynamics in Excitatory Cortical Neuron Cultures Results from the Combination of Different Adaptive Mechanism

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Masquelier, Timothée ^a,b   Deco, Gustavo ^a  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b Groupe Enzymologie Moléculaire et Fonctionnelle   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BICUCULLINE;

ADAPTATION; ANIMAL CELL; ARTICLE; BRAIN CELL CULTURE; EXCITATION; EXCITATORY POSTSYNAPTIC POTENTIAL; FACILITATION; FATIGUE; MEMBRANE POTENTIAL; NEWBORN; NONHUMAN; POISSON DISTRIBUTION; RAT; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANIMALS, NEWBORN; BICUCULLINE; CELLS, CULTURED; CEREBRAL CORTEX; GABA-A RECEPTOR ANTAGONISTS; MODELS, NEUROLOGICAL; NERVE NET; NEURAL INHIBITION; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84885391263     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075824     Document Type: Article

References (49)

1. Segev R, Benveniste M, Hulata E, Cohen N, Palevski A, et al. (2002) Long term behavior of lithographically prepared in vitro neuronal networks. Phys Rev Lett 88: 118102.
2. Giugliano M, Darbon P, Arsiero M, Lüscher H-R, Streit J (2004) Single-neuron discharge properties and network activity in dissociated cultures of neocortex. Journal of neurophysiology 92: 977-996. Available: http://dx.doi.org/10.1152/jn.00067.2004. Accessed 24 August 2013.
3. Van Pelt J, Vajda I, Wolters PS, Corner MA, Ramakers GJA (2005) Dynamics and plasticity in developing neuronal networks in vitro. Progress in brain research 147: 173-188. Available: http://dx.doi.org/10.1016/S0079-6123(04)47013-7. Accessed 7 August 2013.
4. Eytan D, Marom S (2006) Dynamics and effective topology underlying synchronization in networks of cortical neurons. The Journal of neuroscience: the official journal of the Society for Neuroscience 26: 8465-8476. Available: http://dx.doi.org/10.1523/JNEUROSCI.1627-06.2006. Accessed 9 August 2013.
5. Wagenaar DA, Pine J, Potter SM (2006) An extremely rich repertoire of bursting patterns during the development of cortical cultures. BMC neuroscience 7: 11. Available: http://dx.doi.org/10.1186/1471-2202-7-11. Accessed 13 August 2013.
6. DeMarse TB, Principe JC (2006) Modeling of Synchronized Burst in Dissociated Cortical Tissue: An Exploration of Parameter Space. The 2006 IEEE International Joint Conference on Neural Network Proceedings. IEEE. p. 581-586. Available: http://ieeexplore.ieee.org/lpdocs/epic03/wrapper.htm?arnumber=1716145. Accessed 24 August 2013.
7. Pasquale V, Massobrio P, Bologna LL, Chiappalone M, Martinoia S (2008) Self-organization and neuronal avalanches in networks of dissociated cortical neurons. Neuroscience 153: 1354-1369. Available: http://dx.doi.org/10.1016/j.neuroscience.2008.03.050. Accessed 15 August 2013.
8. Tetzlaff C, Okujeni S, Egert U, Wörgötter F, Butz M (2010) Self-organized criticality in developing neuronal networks. PLoS computational biology 6: e1001013. Available: http://dx.plos.org/10.1371/journal.pcbi.1001013. Accessed 14 August 2013.
9. Gritsun TA, Le Feber J, Stegenga J, Rutten WLC (2010) Network bursts in cortical cultures are best simulated using pacemaker neurons and adaptive synapses. Biological cybernetics 102: 293-310. Available: http://dx.doi.org/10.1007/s00422-010-0366-x. Accessed 16 August 2013.
10. Gritsun T, le Feber J, Stegenga J, Rutten WLC (2011) Experimental analysis and computational modeling of interburst intervals in spontaneous activity of cortical neuronal culture. Biological cybernetics 105: 197-210. Available: http://dx.doi.org/10.1007/s00422-011-0457-3. Accessed 16 August 2013.
11. Baltz T, Herzog A, Voigt T (2011) Slow oscillating population activity in developing cortical networks: models and experimental results. Journal of neurophysiology 106: 1500-1514. Available: http://dx.doi.org/10.1152/jn.00889.2010. Accessed 24 August 2013.
12. Thivierge J-P, Cisek P (2008) Nonperiodic synchronization in heterogeneous networks of spiking neurons. The Journal of neuroscience: the official journal of the Society for Neuroscience 28: 7968-7978. Available: http://dx.doi.org/10.1523/JNEUROSCI.0870-08.2008. Accessed 24 August 2013.
13. Tsodyks M, Uziel A, Markram H, (2000) Synchrony generation in recurrent networks with frequency-dependent synapses. J Neurosci 20: RC50.
14. Wiedemann UA, Lüthi A (2003) Timing of network synchronization by refractory mechanisms. Journal of neurophysiology 90: 3902-3911. Available: http://www.ncbi.nlm.nih.gov/pubmed/12930814. Accessed 24 August 2013.
15. Marom S, Shahaf G, (2002) Development, learning and memory in large random networks of cortical neurons: lessons beyond anatomy. Q Rev Biophys 35: 63-87.
16. Zrenner C, Eytan D, Wallach A, Thier P, Marom S (2010) A generic framework for real-time multi-channel neuronal signal analysis, telemetry control, and sub-millisecond latency feedback generation. Frontiers in neuroscience 4: 173. Available: http://dx.doi.org/10.3389/fnins.2010.00173. Accessed 24 August 2013.
17. Frere RC, Macdonald RL, Young AB (1982) GABA binding and bicuculline in spinal cord and cortical membranes from adult rat and from mouse neurons in cell culture. Brain research 244: 145-153. Available: http://www.ncbi.nlm.nih.gov/pubmed/6288176. Accessed 24 August 2013.
18. Markram H, Wang Y, Tsodyks M, (1998) Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci U S A 95: 5323-5328.
19. Brunel N, Wang XJ (2001) Effects of neuromodulation in a cortical network model of object working memory dominated by recurrent inhibition. Journal of computational neuroscience 11: 63-85. Available: http://dx.doi.org/10.1023/A:1011204814320. Accessed 24 August 2013.
20. Buehlmann A, Deco G (2008) The neuronal basis of attention: rate versus synchronization modulation. The Journal of neuroscience: the official journal of the Society for Neuroscience 28: 7679-7686. Available: http://dx.doi.org/10.1523/JNEUROSCI.5640-07.2008. Accessed 22 August 2013.
21. Albantakis L, Deco G (2011) Changes of mind in an attractor network of decision-making. PLoS computational biology 7: e1002086. Available: http://dx.doi.org/10.1371/journal.pcbi.1002086. Accessed 24 August 2013.
22. Nakanishi K, Kukita F, (1998) Functional synapses in synchronized bursting of neocortical neurons in culture. Brain Res 795: 137-146.
23. Gritsun TA, le Feber J, Rutten WLC (2012) Growth dynamics explain the development of spatiotemporal burst activity of young cultured neuronal networks in detail. PloS one 7: e43352. Available: http://dx.plos.org/10.1371/journal.pone.0043352. Accessed 26 March 2013.
24. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annual review of physiology 64: 355-405. Available: http://www.ncbi.nlm.nih.gov/pubmed/11826273. Accessed 24 May 2013.
25. Goodman D, Brette R (2008) Brian: a simulator for spiking neural networks in python. Frontiers in neuroinformatics 2: 5. Available: http://dx.doi.org/10.3389/neuro.11.005.2008. Accessed 14 August 2013.
26. Eytan D, Brenner N, Marom S, (2003) Selective adaptation in networks of cortical neurons. J Neurosci 23: 9349-9356.
27. Gigante G, Mattia M, Giudice P Del, (2007) Diverse population-bursting modes of adapting spiking neurons. Phys Rev Lett 98: 148101.
28. Gerstner W, Kistler W (2002) Spiking Neuron Models. Cambridge Univ. Press.
29. Beggs JM, Plenz D, (2003) Neuronal avalanches in neocortical circuits. J Neurosci 23: 11167-11177.
30. Shew WL, Yang H, Petermann T, Roy R, Plenz D (2009) Neuronal avalanches imply maximum dynamic range in cortical networks at criticality. The Journal of neuroscience: the official journal of the Society for Neuroscience 29: 15595-15600. Available: http://dx.doi.org/10.1523/JNEUROSCI.3864-09.2009. Accessed 12 August 2013.
31. Touboul J, Destexhe A (2010) Can power-law scaling and neuronal avalanches arise from stochastic dynamics? PloS one 5: e8982. Available: http://dx.doi.org/10.1371/journal.pone.0008982. Accessed 6 August 2013.
32. Benayoun M, Cowan JD, van Drongelen W, Wallace E (2010) Avalanches in a stochastic model of spiking neurons. PLoS computational biology 6: e1000846. Available: http://dx.doi.org/10.1371/journal.pcbi.1000846. Accessed 15 August 2013.
33. Shew WL, Yang H, Yu S, Roy R, Plenz D (2011) Information capacity and transmission are maximized in balanced cortical networks with neuronal avalanches. The Journal of neuroscience: the official journal of the Society for Neuroscience 31: 55-63. Available: http://dx.doi.org/10.1523/JNEUROSCI.4637-10.2011. Accessed 12 August 2013.
34. Rubinov M, Sporns O, Thivierge J-P, Breakspear M (2011) Neurobiologically realistic determinants of self-organized criticality in networks of spiking neurons. PLoS computational biology 7: e1002038. Available: http://dx.doi.org/10.1371/journal.pcbi.1002038. Accessed 13 August 2013.
35. Klaus A, Yu S, Plenz D (2011) Statistical analyses support power law distributions found in neuronal avalanches. PloS one 6: e19779. Available: http://dx.doi.org/10.1371/journal.pone.0019779. Accessed 13 August 2013.
36. Chiu C, Weliky M, (2001) Spontaneous activity in developing ferret visual cortex in vivo. J Neurosci 21: 8906-8914.
37. Petermann T, Thiagarajan TC, Lebedev MA, Nicolelis MAL, Chialvo DR, et al. (2009) Spontaneous cortical activity in awake monkeys composed of neuronal avalanches. Proceedings of the National Academy of Sciences of the United States of America 106: 15921-15926. Available: http://dx.doi.org/10.1073/pnas.0904089106. Accessed 24 August 2013.
38. Hahn G, Petermann T, Havenith MN, Yu S, Singer W, et al. (2010) Neuronal avalanches in spontaneous activity in vivo. Journal of neurophysiology 104: 3312-3322. Available: http://dx.doi.org/10.1152/jn.00953.2009. Accessed 18 August 2013.
39. Leinekugel X, Khazipov R, Cannon R, Hirase H, Ben-Ari Y, et al. (2002) Correlated bursts of activity in the neonatal hippocampus in vivo. Science (New York, NY) 296: 2049-2052. Available: http://dx.doi.org/10.1126/science.1071111. Accessed 24 August 2013.
40. Weliky M, Katz LC, (1999) Correlational structure of spontaneous neuronal activity in the developing lateral geniculate nucleus in vivo. Science 285: 599-604.
41. König P, Engel AK, Singer W, (1996) Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci 19: 130-7.
42. Brette R (2012) Computing with neural synchrony. PLoS computational biology 8: e1002561. Available: http://dx.doi.org/10.1371/journal.pcbi.1002561. Accessed 6 August 2013.
43. Gilson M, Masquelier T, Hugues E (2011) STDP allows fast rate-modulated coding with Poisson-like spike trains. PLoS computational biology 7: e1002231. Available: http://dx.doi.org/10.1371/journal.pcbi.1002231. Accessed 13 August 2013.
44. Singer W, (1999) Time as coding space? Curr Opin Neurobiol 9: 189-194.
45. Fries P (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends in cognitive sciences 9: 474-480. Available: http://dx.doi.org/10.1016/j.tics.2005.08.011. Accessed 6 August 2013.
46. Montemurro MA, Rasch MJ, Murayama Y, Logothetis NK, Panzeri S (2008) Phase-of-firing coding of natural visual stimuli in primary visual cortex. Current biology: CB 18: 375-380. Available: http://dx.doi.org/10.1016/j.cub.2008.02.023. Accessed 13 August 2013.
47. Masquelier T, Hugues E, Deco G, Thorpe SJ (2009) Oscillations, phase-of-firing coding, and spike timing-dependent plasticity: an efficient learning scheme. The Journal of neuroscience 29: 13484-13493. Available: http://dx.doi.org/10.1523/JNEUROSCI.2207-09.2009. Accessed 9 January 2013.
48. Corner MA, van Pelt J, Wolters PS, Baker RE, Nuytinck RH, (2002) Physiological effects of sustained blockade of excitatory synaptic transmission on spontaneously active developing neuronal networks--an inquiry into the reciprocal linkage between intrinsic biorhythms and neuroplasticity in early ontogeny. Neurosci Biobehav Rev 26: 127-185.
49. Hines ML, Morse T, Migliore M, Carnevale NT, Shepherd GM (2004) ModelDB: A Database to Support Computational Neuroscience. Journal of computational neuroscience 17: 7-11. Available: http://dx.doi.org/10.1023/B:JCNS.0000023869.22017.2e. Accessed 24 August 2013.