Crossref journal-article
Society for Neuroscience
The Journal of Neuroscience (393)
Abstract

Spontaneous neuronal activity is a ubiquitous feature of cortex. Its spatiotemporal organization reflects past input and modulates future network output. Here we study whether a particular type of spontaneous activity is generated by a network that is optimized for input processing. Neuronal avalanches are a type of spontaneous activity observed in superficial cortical layersin vitroandin vivowith statistical properties expected from a network operating at “criticality.” Theory predicts that criticality and, therefore, neuronal avalanches are optimal for input processing, but until now, this has not been tested in experiments. Here, we use cortex slice cultures grown on planar microelectrode arrays to demonstrate that cortical networks that generate neuronal avalanches benefit from a maximized dynamic range, i.e., the ability to respond to the greatest range of stimuli. By changing the ratio of excitation and inhibition in the cultures, we derive a network tuning curve for stimulus processing as a function of distance from criticality in agreement with predictions from our simulations. Our findings suggest that in the cortex, (1) balanced excitation and inhibition establishes criticality, which maximizes the range of inputs that can be processed, and (2) spontaneous activity and input processing are unified in the context of critical phenomena.

Bibliography

Shew, W. L., Yang, H., Petermann, T., Roy, R., & Plenz, D. (2009). Neuronal Avalanches Imply Maximum Dynamic Range in Cortical Networks at Criticality. The Journal of Neuroscience, 29(49), 15595–15600.

Authors 5
  1. Woodrow L. Shew (first)
  2. Hongdian Yang (additional)
  3. Thomas Petermann (additional)
  4. Rajarshi Roy (additional)
  5. Dietmar Plenz (additional)
References 30 Referenced 503
  1. 10.1126/science.273.5283.1868
  2. 10.1523/JNEUROSCI.19-06-02209.1999 / J Neurosci / Cellular mechanisms contributing to response variability of cortical neurons in vivo by Azouz (1999)
  3. 10.1073/pnas.92.15.6689
  4. 10.1523/JNEUROSCI.23-35-11167.2003 / J Neurosci / Neuronal avalanches in neocortical circuits by Beggs (2003)
  5. 10.1162/089976604323057443
  6. 10.1103/PhysRevLett.97.188102
  7. Buice MA Cowan JD (2007) Field-theoretic approach to fluctuation effects in neural networks. Phys Rev E Stat Nonlin Soft Matter Phys 75:051919. (10.1103/PhysRevE.75.051919)
  8. 10.1523/JNEUROSCI.1627-06.2006
  9. 10.1038/nature02907
  10. 10.1073/pnas.0800537105
  11. 10.1002/neu.480230702
  12. Harris TE (1989) The theory of branching processes (Dover, New York).
  13. 10.1038/nrn1787
  14. Jensen HJ (1998) Self-organized criticality (Cambridge UP, Cambridge, UK). (10.1017/CBO9780511622717)
  15. 10.1038/nature02078
  16. 10.1038/nphys289
  17. 10.1523/JNEUROSCI.19-23-10451.1999 / J Neurosci / Trial-to-trial variability and state-dependent modulation of auditory-evoked responses in cortex by Kisley (1999)
  18. 10.1016/j.neunet.2007.04.017
  19. 10.1016/j.neuron.2009.03.014
  20. 10.1038/35089076
  21. 10.1073/pnas.0904089106
  22. 10.1152/jn.1996.76.6.4180 / J Neurophysiol / Generation of high-frequency oscillations in local circuits of rat somatosensory cortex cultures by Plenz (1996)
  23. 10.1016/j.tins.2007.01.005
  24. Stanley HE (1971) Introduction to phase transitions and critical phenomena (Oxford UP, New York).
  25. 10.1523/JNEUROSCI.0723-06.2006
  26. 10.1016/j.jneumeth.2007.10.021
  27. 10.1162/neco.2008.03-08-727
  28. 10.1126/science.286.5446.1943
  29. 10.1038/nn1895
  30. 10.1103/PhysRevLett.75.4071
Dates
Type When
Created 15 years, 8 months ago (Dec. 9, 2009, 1:23 p.m.)
Deposited 2 years, 4 months ago (April 13, 2023, 3:40 p.m.)
Indexed 6 days, 19 hours ago (Aug. 22, 2025, 12:49 a.m.)
Issued 15 years, 8 months ago (Dec. 9, 2009)
Published 15 years, 8 months ago (Dec. 9, 2009)
Published Online 15 years, 8 months ago (Dec. 9, 2009)
Published Print 15 years, 8 months ago (Dec. 9, 2009)
Funders 0

None

@article{Shew_2009, title={Neuronal Avalanches Imply Maximum Dynamic Range in Cortical Networks at Criticality}, volume={29}, ISSN={1529-2401}, url={http://dx.doi.org/10.1523/jneurosci.3864-09.2009}, DOI={10.1523/jneurosci.3864-09.2009}, number={49}, journal={The Journal of Neuroscience}, publisher={Society for Neuroscience}, author={Shew, Woodrow L. and Yang, Hongdian and Petermann, Thomas and Roy, Rajarshi and Plenz, Dietmar}, year={2009}, month=dec, pages={15595–15600} }