DOI: 10.1098/rsta.2007.2092. The criticality hypothesis: how local cortical networks might optimize information processing

The criticality hypothesis: how local cortical networks might optimize information processing

10.1098/rsta.2007.2092

Crossref journal-article

The Royal Society

Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences (175)

Abstract

Early theoretical and simulation work independently undertaken by Packard, Langton and Kauffman suggested that adaptability and computational power would be optimized in systems at the ‘edge of chaos’, at a critical point in a phase transition between total randomness and boring order. This provocative hypothesis has received much attention, but biological experiments supporting it have been relatively few. Here, we review recent experiments on networks of cortical neurons, showing that they appear to be operating near the critical point. Simulation studies capture the main features of these data and suggest that criticality may allow cortical networks to optimize information processing. These simulations lead to predictions that could be tested in the near future, possibly providing further experimental evidence for the criticality hypothesis.

Bibliography

Beggs, J. M. (2007). The criticality hypothesis: how local cortical networks might optimize information processing. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, 366(1864), 329â343.

Authors 1

John M Beggs (first)

References 57 Referenced 361

10.1152/jn.1993.70.4.1629
Alessio R. Cozzi L. D'Angelo P. & Sanguinetti V. 2006 Cultures of dissociated neurons display a variety of avalanche behaviors. In ESANN'2006 Proc.—European Symp. on Artificial Neural Networks Bruges Belgium 26–28 April 2006 .
Bak P How nature works: the science of self-organized criticality. 1996 New York NY:Copernicus. (10.1007/978-1-4757-5426-1)
10.1103/PhysRevE.63.031912
10.1103/PhysRevLett.59.381
10.1523/JNEUROSCI.23-35-11167.2003
10.1523/JNEUROSCI.0540-04.2004
10.1162/089976604323057443
10.1103/PhysRevLett.84.6114
10.3233/THC-1996-4109
10.1016/S0956-5663(98)00015-3
10.1103/PhysRevE.75.051919
10.1016/S0306-4522(98)00472-2
10.1016/S0149-7634(01)00062-8
10.1103/PhysRevLett.78.1492
10.1126/science.290.5492.812
10.1103/PhysRevLett.96.028107
10.1103/PhysRevE.66.066137
10.1016/j.neuron.2005.02.001
10.1016/0165-0270(82)90046-2
10.1038/nature00974
10.1103/PhysRevLett.94.058101
Harris T.E The theory of branching processes. 1989 New York NY:Dover.
10.1103/PhysRevLett.75.1222
10.1016/j.neucom.2005.12.060
Jensen H.J Self-organized criticality: emergent complex behavior in physical and biological systems. 1998 Cambridge UK:Cambridge University Press. (10.1017/CBO9780511622717)
10.1016/S0302-4598(99)00083-5
Kauffman S.A The origins of order: self-organization and selection in evolution. 1993 New York NY:Oxford University Press. (10.1007/978-94-015-8054-0_8)
10.1016/S0022-5193(05)80094-3
10.1038/nphys289
10.1016/0167-2789(90)90064-V
10.1162/089976604323057434
10.1016/j.neunet.2007.04.017
Levina A. Hermann J. M. & Geisel T. 2005 Dynamical synapses give rise to a power-law distribution of neuronal avalanches. In 2005 NIPS Proc . See http://books.nips.cc/papers/files/nips18/NIPS2005_0646.pdf.
10.1103/PhysRevE.71.016133
10.1523/JNEUROSCI.21-04-01370.2001
10.1016/S0168-9002(98)00734-7
10.1523/JNEUROSCI.17-15-05666.1997
10.1162/089976602760407955
10.1523/JNEUROSCI.15-10-06834.1995
10.1371/journal.pone.0000439
{'key': 'e_1_3_2_43_1', 'first-page': '89', 'article-title': 'Revisiting the edge of chaos: evolving cellular automata to perform computations', 'volume': '7', 'author': 'Mitchell M', 'year': '1993', 'journal-title': 'Complex Syst'} / Complex Syst / Revisiting the edge of chaos: evolving cellular automata to perform computations by Mitchell M (1993)
{'key': 'e_1_3_2_44_1', 'first-page': '293', 'volume-title': 'Dynamic patterns in complex systems', 'author': 'Packard N', 'year': '1988'} / Dynamic patterns in complex systems by Packard N (1988)
10.1103/PhysRevE.53.414
{'key': 'e_1_3_2_46_1', 'first-page': '1', 'article-title': 'Neuronal avalanches in vivo', 'volume': '531', 'author': 'Petermann T', 'year': '2006', 'journal-title': 'Soc. Neurosci. Abstr'} / Soc. Neurosci. Abstr / Neuronal avalanches in vivo by Petermann T (2006)
10.1016/0165-0270(80)90042-4
10.1103/PhysRevLett.88.118102
Stanley H.E Introduction to phase transitions and critical phenomena. 1987 New York NY:Oxford University Press.
Stauffer D Introduction to percolation theory. 1994 London UK:Taylor and Francis.
10.1523/JNEUROSCI.0723-06.2006
10.1364/JOSAA.14.000529
10.1093/cercor/10.12.1185
10.1523/JNEUROSCI.18-05-01893.1998
10.1146/annurev.neuro.28.061604.135637
10.1186/1471-2202-7-11
10.1097/00001756-200211150-00005
Yeomans J.M Statistical mechanics of phase transitions. 1992 New York NY:Oxford University Press. (10.1093/oso/9780198517290.001.0001)

Dates

Type	When
Created	18 years ago (Aug. 16, 2007, 12:06 p.m.)
Deposited	1 year, 6 months ago (Feb. 17, 2024, 7:26 a.m.)
Indexed	19 minutes ago (Aug. 29, 2025, 8:37 a.m.)
Issued	18 years ago (Aug. 2, 2007)
Published	18 years ago (Aug. 2, 2007)
Published Online	18 years ago (Aug. 2, 2007)
Published Print	17 years, 6 months ago (Feb. 13, 2008)

Funders 0

None

BibTeX

@article{Beggs_2007, title={The criticality hypothesis: how local cortical networks might optimize information processing}, volume={366}, ISSN={1471-2962}, url={http://dx.doi.org/10.1098/rsta.2007.2092}, DOI={10.1098/rsta.2007.2092}, number={1864}, journal={Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences}, publisher={The Royal Society}, author={Beggs, John M}, year={2007}, month=aug, pages={329–343} }

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