Optimal dynamical range of excitable networks at criticality

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ABSTRACT A recurrent idea in the study of complex systems is that optimal information processing is to be found near phase transitions. However, this heuristic hypothesis has few (if any)


concrete realizations where a standard and biologically relevant quantity is optimized at criticality. Here we give a clear example of such a phenomenon: a network of excitable elements has


its sensitivity and dynamic range maximized at the critical point of a non-equilibrium phase transition. Our results are compatible with the essential role of gap junctions in olfactory


glomeruli and retinal ganglionar cell output. Synchronization and global oscillations also emerge from the network dynamics. We propose that the main functional role of electrical coupling


is to provide an enhancement of dynamic range, therefore allowing the coding of information spanning several orders of magnitude. The mechanism could provide a microscopic neural basis for


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COMPLEX NETWORK DYNAMICS THROUGH THE FORMATION OF QUASI-CRITICAL BRAIN STATES Article Open access 10 December 2020 REFERENCES * Stevens, S. S. _Psychophysics: Introduction to its


Perceptual, Neural and Social Prospects_ (Wiley, New York, 1975). Google Scholar  * Wachowiak, M. & Cohen, L. B. Representation of odorants by receptor neuron input to the mouse


olfactory bulb. _Neuron_ 32, 723–735 (2001). Article  Google Scholar  * Angioy, A. M., Desogus, A., Barbarossa, I. T., Anderson, P. & Hansson, B. S. Extreme sensitivity in an olfactory


system. _Chem. Senses_ 28, 279–284 (2003). Article  Google Scholar  * Fried, H. U., Fuss, S. H. & Korsching, S. I. Selective imaging of presynaptic activity in the mouse olfactory bulb


shows concentration and structure dependence of odor responses in identified glomeruli. _Proc. Natl Acad. Sci. USA_ 99, 3222–3227 (2002). Article  ADS  Google Scholar  * Cleland, T. A. &


Linster, C. Concentration tuning mediated by spare receptor capacity in olfactory sensory neurons: a theoretical study. _Neural Comput._ 11, 1673–1690 (1999). Article  Google Scholar  *


Copelli, M., Roque, A. C., Oliveira, R. F. & Kinouchi, O. Physics of psychophysics: Stevens and Weber-Fechner laws are transfer functions of excitable media. _Phys. Rev. E_ 65, 060901


(2002). Article  ADS  Google Scholar  * Copelli, M. & Kinouchi, O. Intensity coding in two-dimensional excitable neural networks. _Physica A_ 349, 431–442 (2005). Article  ADS  Google


Scholar  * Copelli, M., Oliveira, R. F., Roque, A. C. & Kinouchi, O. Signal compression in the sensory periphery. _Neurocomputing_ 65–66, 691–696 (2005). Article  Google Scholar  *


Reiser, J. & Matthews, H. Response properties of isolated mouse olfactory receptor cells. _J. Physiol._ 530, 113–122 (2001). Article  Google Scholar  * Tomaru, A. & Kurahashi, T.


Mechanisms determining the dynamic range of the bullfrog olfactory receptor cell. _J. Neurophysiol._ 93, 1880–1888 (2005). Article  Google Scholar  * Chater, N. & Brown, G. D.


Scale-invariance as a unifying psychological principle. _Cognition_ 69, B17–B24 (1999). Article  Google Scholar  * Furtado, L. S. & Copelli, M. Response of electrically coupled spiking


neurons: a cellular automaton approach. _Phys. Rev. E_ 73, 011907 (2006). Article  ADS  Google Scholar  * Beggs, J. M. & Plenz, D. Neuronal avalanches in neocortical circuits. _J.


Neurosci._ 23, 11167–11177 (2003). Article  Google Scholar  * Haldeman, C. & Beggs, J. M. Critical branching captures activity in living neural networks and maximizes the number of


metastable states. _Phys. Rev. Lett._ 94, 058101 (2005). Article  ADS  Google Scholar  * Langton, C. G. Computation at the edge of chaos: phase transitions and emergent computation. _Physica


D_ 42, 12–37 (1990). Article  ADS  MathSciNet  Google Scholar  * Bak, P. _How Nature Works: The Science of Self-Organized Criticality_ (Oxford Univ. Press, New York, 1997). MATH  Google


Scholar  * Chialvo, D. R. Critical brain networks. _Physica A_ 340, 756–765 (2004). Article  ADS  Google Scholar  * Kosaka, T., Deans, M. R., Paul, D. L. & Kosaka, K. Neuronal gap


junctions in the mouse main olfactory bulb: morphological analyses on transgenic mice. _Neuroscience_ 134, 757–769 (2005). Article  Google Scholar  * Migliore, M., Hines, M. L. &


Shepherd, G. M. The role of distal dendritic gap junctions in synchronization of mitral cell axonal output. _J. Comput. Neurosci._ 18, 151–161 (2005). Article  Google Scholar  * Christie, J.


M. et al. Connexin36 mediates spike synchrony in olfactory bulb glomeruli. _Neuron_ 46, 761–772 (2005). Article  Google Scholar  * Marro, J. & Dickman, R. _Nonequilibrium Phase


Transitions in Lattice Models_ (Cambridge Univ. Press, Cambridge, 1999). Book  Google Scholar  * Laurent, G. Olfactory network dynamics and the coding of multidimensional signals. _Nature


Rev. Neurosci._ 3, 884–895 (2002). Article  Google Scholar  * Lewis, T. J. & Rinzel, J. Topological target patterns and population oscillations in a network with random gap junctional


coupling. _Neurocomputing_ 38–40, 763–768 (2001). Article  Google Scholar  * Lewis, T. J. & Rinzel, J. Self-organized synchronous oscillations in a network of excitable cells coupled by


gap junctions. _Network Comput. Neural Syst._ 11, 299–320 (2000). Article  Google Scholar  * Schubert, T. et al. Connexin36 mediates gap junctional coupling of alpha-ganglion cells in mouse


retina. _J. Comp. Neurol._ 485, 191–201 (2005). Article  Google Scholar  * Hidaka, S., Akahori, Y. & Kurosawa, Y. Cellular/molecular dendrodendritic electrical synapses between mammalian


retinal ganglion cells. _J. Neurosci._ 24, 10553–10567 (2005). Article  Google Scholar  * Vogt, A., Hormuzdi, S. G. & Monyer, H. Pannexin1 and Pannexin2 expression in the developing and


mature rat brain. _Brain Res. Mol. Brain Res._ 141, 113–120 (2005). Article  Google Scholar  * Deans, M. R., Volgyi, B., Goodenough, D. A., Bloomfield, S. A. & Paul, D. L. Connexin36 is


essential for transmission of rod-mediated visual signals in the mammalian retina. _Neuron_ 36, 703–712 (2002). Article  Google Scholar  * Zhang, C. & Restrepo, D. Expression of


connexin 45 in the olfactory system. _Brain Res._ 929, 37–47 (2002). Article  Google Scholar  * Camalet, S., Duke, T., Jülicher, F. & Prost, J. Auditory sensitivity provided by


self-tuned critical oscillations of hair cells. _Proc. Natl Acad. Sci. USA_ 97, 3183–3188 (2000). Article  ADS  Google Scholar  * Sohl, G., Maxeiner, S. & Willecke, K. Expression and


functions of neuronal gap junctions. _Nature Rev. Neurosci._ 6, 191–200 (2005). Article  Google Scholar  Download references ACKNOWLEDGEMENTS This research is supported by CNPq, FACEPE,


CAPES and PRONEX. The authors are grateful for discussions with A. C. Roque, R. F. Oliveira, D. Restrepo, T. Cleland and V. R. Vitorino de Assis and for encouragement from N. Caticha. AUTHOR


INFORMATION Author notes * Osame Kinouchi and Mauro Copelli: These authors contributed equally to this work AUTHORS AND AFFILIATIONS * Departamento de Física e Matemática, Faculdade de


Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Av. dos Bandeirantes 3900, 14040-901 Ribeirão Preto, SP, Brazil Osame Kinouchi * Departamento de Física,


Laboratório de Física Teórica e Computacional, Universidade Federal de Pernambuco, 50670-901 Recife, PE, Brazil Mauro Copelli Authors * Osame Kinouchi View author publications You can also


search for this author inPubMed Google Scholar * Mauro Copelli View author publications You can also search for this author inPubMed Google Scholar CORRESPONDING AUTHOR Correspondence to


Osame Kinouchi. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing financial interests. RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS


ARTICLE Kinouchi, O., Copelli, M. Optimal dynamical range of excitable networks at criticality. _Nature Phys_ 2, 348–351 (2006). https://doi.org/10.1038/nphys289 Download citation *


Received: 06 February 2006 * Accepted: 27 March 2006 * Published: 23 April 2006 * Issue Date: May 2006 * DOI: https://doi.org/10.1038/nphys289 SHARE THIS ARTICLE Anyone you share the


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