Critical-state dynamics of avalanches and oscillations jointly emerge from balanced excitation/inhibition in neuronal networks

Journal of Neuroscience

Volumn 32, Issue 29, 2012, Pages 9817-9823

  Poil, Simon Shlomo ^a   Hardstone, Richard ^a   Mansvelder, Huibert D ^a   Linkenkaer Hansen, Klaus ^a,b  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; EXCITATION; FEMALE; HUMAN; HUMAN EXPERIMENT; MAGNETOENCEPHALOGRAPHY; MALE; MODEL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NORMAL HUMAN; PRIORITY JOURNAL; SYNAPTIC INHIBITION;

ACTION POTENTIALS; BRAIN; COMPUTER SIMULATION; HUMANS; MODELS, NEUROLOGICAL; NERVE NET; NEURAL INHIBITION; NEURONAL PLASTICITY; NEURONS;

EID: 84863899325     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5990-11.2012     Document Type: Article

References (53)

1. Atallah BV, Scanziani M (2009) Instantaneous modulation of gamma oscillation frequency by balancing excitation with inhibition. Neuron 62:566-577.
2. Bak P (1996) How nature works: the science of self-organized criticality. New York: Copernicus.
3. Bak P, Tang C, Wiesenfeld K (1987) Self-organized criticality: an explanation of the 1/f noise. Phys Rev Lett 59:381-384.
4. Beggs JM (2008) The criticality hypothesis: how local cortical networks might optimize information processing. Philos Transact A Math Phys Eng Sci 366:329-343.
5. Beggs JM, Plenz D (2003) Neuronal avalanches in neocortical circuits. J Neurosci 23:11167-11177.
6. Buzsáki G (2006) Rhythms of the brain. New York: Oxford UP.
7. Buzsáki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926-1929.
8. Carandini M (2012) From circuits to behavior: a bridge too far? Nat Neurosci 15:507-509.
9. Cassenaer S, Laurent G (2007) Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts. Nature 448:709-713.
10. Chen Z, Ivanov PCh, Hu K, Stanley HE (2002) Effect of nonstationarities on detrended fluctuation analysis. Phys Rev E Stat Nonlin Soft Matter Phys 65:041107.
11. Chialvo DR (2010) Emergent complex neural dynamics. Nat Phys 6:744-750.
12. Chialvo DR, Bak P (1999) Learning from mistakes. Neuroscience 90:1137-1148.
13. Christensen K, Moloney NR (2005) Complexity and criticality. London: Imperial College.
14. Clauset A, Shalizi CR, Newman ME (2009) Power-law distributions in empirical data. SIAM Rev 51:661-703.
15. Fries P (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 9:474-480.
16. Gao J, Hu J, Tung WW, Cao Y, Sarshar N, Roychowdhury VP (2006) Assessment of long-range correlation in time series: how to avoid pitfalls. Phys Rev E Stat Nonlin Soft Matter Phys 73:016117.
17. Gilden DL (2001) Cognitive emissions of 1/f noise. Psychol Rev 108:33-56.
18. Gireesh ED, Plenz D (2008) Neuronal avalanches organize as nested thetaand beta/gamma-oscillations during development of cortical layer 2/3. Proc Natl Acad Sci U S A 105:7576-7581.
19. Gong P, Nikolaev AR, van Leeuwen C (2003) Scale-invariant fluctuations of the dynamical synchronization in human brain electrical activity. Neurosci Lett 336:33-36.
20. Goutagny R, Jackson J, Williams S (2009) Self-generated theta oscillations in the hippocampus. Nat Neurosci 12:1491-1493.
21. Haldeman C, Beggs JM (2005) Critical branching captures activity in living neural networks and maximizes the number of metastable states. Phys Rev Lett 94:058101.
22. He BJ, Zempel JM, Snyder AZ, Raichle ME (2010) The temporal structures and functional significance of scale-free brain activity. Neuron 66:353-369.
23. Holmgren C, Harkany T, Svennenfors B, Zilberter Y (2003) Pyramidal cell communication within local networks in layer 2/3 of rat neocortex. J Physiol 551:139-153.
24. Jensen HJ (1998) Self-organized criticality: emergent complex behavior in physical and biological systems. Cambridge: Cambridge UP.
25. Kinouchi O, Copelli M (2006) Optimal dynamical range of excitable networks at criticality. Nat Phys 2:348-351.
26. Kitzbichler MG, Smith ML, Christensen SR, Bullmore E (2009) Broadband criticality of human brain network synchronization. PLoS Comput Biol 5:e1000314.
27. Levina A, Herrmann JM, Geisel T (2007) Dynamical synapses causing selforganized criticality in neural networks. Nat Phys 3:857-860.
28. Linkenkaer-Hansen K, Nikouline VV, Palva JM, Ilmoniemi RJ (2001) Long-range temporal correlations and scaling behavior in human brain oscillations. J Neurosci 21:1370-1377.
29. Linkenkaer-Hansen K, Nikulin VV, Palva JM, Kaila K, Ilmoniemi RJ (2004) Stimulus-induced change in long-range temporal correlations and scaling behaviour of sensorimotor oscillations. Eur J Neurosci 19:203-211.
30. Lisman J (2010) Working memory: the importance of theta and gamma oscillations. Curr Biol 20:R490-R492.
31. Mazzoni A, Broccard FD, Garcia-Perez E, Bonifazi P, Ruaro ME, Torre V (2007) On the dynamics of the spontaneous activity in neuronal networks. PloS One 2:e439.
32. Miller MN, Okaty BW, Nelson SB (2008) Region-specific spike-frequency acceleration in layer 5 pyramidal neurons mediated by Kv1 subunits. J Neurosci 28:13716-13726.
33. Millman D, Mihalas S, Kirkwood A, Niebur E (2010) Self-organized criticality occurs in non-conservative neuronal networks during Up states. Nat Phys 6:801-805.
34. Montez T, Poil SS, Jones BF, Manshanden I, Verbunt JP, van Dijk BW, Brussaard AB, van Ooyen A, Stam CJ, Scheltens P, Linkenkaer-Hansen K (2009) Altered temporal correlations in parietal alpha and prefrontal theta oscillations in early-stage Alzheimer disease. Proc Natl Acad Sci U S A 106:1614-1619.
35. Monto S, Vanhatalo S, Holmes MD, Palva JM (2007) Epileptogenic neocortical networks are revealed by abnormal temporal dynamics in seizurefree subdural EEG. Cereb Cortex 17:1386-1393.
36. Nikulin VV, Brismar T (2004) Long-range temporal correlations in alpha and beta oscillations: effect of arousal level and test-retest reliability. Clin Neurophysiol 115:1896-1908.
37. Nikulin VV, Jönsson EG, Brismar T (2012) Attenuation of long-range temporal correlations in the amplitude dynamics of alpha and beta neuronal oscillations in patients with schizophrenia. Neuroimage 61:162-169.
38. Pasquale V, Massobrio P, Bologna LL, Chiappalone M, Martinoia S (2009) Self-organization and neuronal avalanches in networks of dissociated cortical neurons. Neuroscience 153:1354-1369.
39. Petermann T, Thiagarajan TC, Lebedev MA, Nicolelis MA, Chialvo DR, Plenz D (2009) Spontaneous cortical activity in awake monkeys composed of neuronal avalanches. Proc Natl Acad Sci U S A 106:15921-15926.
40. Plenz D, Thiagarajan TC (2007) The organizing principles of neuronal avalanches: cell assemblies in the cortex? Trends Neurosci 30:101-110.
41. Poil SS, van Ooyen A, Linkenkaer-Hansen K (2008) Avalanche dynamics of human brain oscillations: relation to critical branching processes and temporal correlations. Hum Brain Mapp 29:770-777.
42. Poil SS, Jansen R, van Aerde K, Timmerman J, Brussaard AB, Mansvelder HD, Linkenkaer-Hansen K (2011) Fast network oscillations in vitro exhibit a slow decay of temporal auto-correlations. Eur J Neurosci 34:394-403.
43. Rubinov M, Sporns O, Thivierge JP, Breakspear M (2011) Neurobiologically realistic determinants of self-organized criticality in networks of spiking neurons. PLoS Comput Biol 7:e1002038.
44. Shew WL, Yang H, Petermann T, Roy R, Plenz D (2009) Neuronal avalanches imply maximum dynamic range in cortical networks at criticality. J Neurosci 29:15595-15600.
45. Shew WL, Yang H, Yu S, Roy R, Plenz D (2011) Information capacity and transmission are maximized in balanced cortical networks with neuronal avalanches. J Neurosci 31:55-63.
46. Sirota A, Montgomery S, Fujisawa S, Isomura Y, Zugaro M, Buzsáki G (2008) Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60:683-697.
47. Smit DJ, de Geus EJ, van de Nieuwenhuijzen ME, van Beijsterveldt CE, van Baal GC, Mansvelder HD, Boomsma DI, Linkenkaer-Hansen K (2011) Scale-free modulation of resting-state neuronal oscillations reflects prolonged brain maturation in humans. J Neurosci 31:13128-13136.
48. Sporns O, Zwi JD (2004) The small world of the cerebral cortex. Neuroinformatics 2:145-162.
49. Stewart CV, Plenz D (2006) Inverted-U profile of dopamine-NMD Amediated spontaneous avalanches recurrence in superficial layers of rat prefrontal cortex. J Neurosci 26:8148-8159.
50. Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5:97-107.
51. Wang SJ, Zhou C (2012) Hierarchical modular structure enhances the robustness of self-organized criticality in neural networks. New J Phys 14:023005.
52. Yang H, Shew WL, Roy R, Plenz D (2012) Maximal variability of phase synchrony in cortical networks with neuronal avalanches. J Neurosci 32:1061-1072.
53. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, O'Shea DJ, Sohal VS, Goshen I, Finkelstein J, Paz JT, Stehfest K, Fudim R, Ramakrishnan C, Huguenard JR, Hegemann P, Deisseroth K (2011) Neocortical excitation/ inhibition balance in information processing and social dysfunction. Nature 477:171-178.