Criticality in the brain

Spontaneous brain activity has been recently characterized by avalanche dynamics with critical features for systems in vitro and in vivo. In this contribution we present a review of experimental results on neuronal avalanches in cortex slices, together with numerical results from a neuronal model implementing several physiological properties of living neurons. Numerical data reproduce experimental results for avalanche statistics. The temporal organization of avalanches can be characterized by the distribution of waiting times between successive avalanches. Experimental measurements exhibit a non-monotonic behaviour, not usually found in other natural processes. Numerical simulations provide evidence that this behaviour is a consequence of the alternation between states of high and low activity, leading to a balance between excitation and inhibition controlled by a single parameter. During these periods both the single neuron state and the network excitability level, keeping memory of past activity, are tuned by homoeostatic mechanisms. Interestingly, the same homoeostatic balance is detected for neuronal activity at the scale of the whole brain. We finally review the learning abilities of this neuronal network. Learning occurs via plastic adaptation of synaptic strengths by a non-uniform negative feedback mechanism. The system is able to learn all the tested rules and the learning dynamics exhibits universal features as a function of the strength of plastic adaptation. Any rule could be learned provided that the plastic adaptation is sufficiently slow.

[1]  a.R.V.,et al.  Clinical neurophysiology , 1961, Neurology.

[2]  J. M. Herrmann,et al.  Dynamical synapses causing self-organized criticality in neural networks , 2007, 0712.1003.

[3]  H. Robinson,et al.  The mechanisms of generation and propagation of synchronized bursting in developing networks of cortical neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  D. Plenz,et al.  Neural dynamics in cortex-striatum co-cultures—II. Spatiotemporal characteristics of neuronal activity , 1996, Neuroscience.

[5]  Peter J Hellyer,et al.  Human brain mapping , 2012, Nature Methods.

[6]  Kevin J. Staley,et al.  Presynaptic modulation of CA3 network activity , 1998, Nature Neuroscience.

[7]  David Holcman,et al.  Time scale of diffusion in molecular and cellular biology , 2014 .

[8]  Dmitri D. Pervouchine,et al.  Neuronal metabolism governs cortical network response state. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[9]  B. Roerig,et al.  Relationships of local inhibitory and excitatory circuits to orientation preference maps in ferret visual cortex. , 2002, Cerebral cortex.

[10]  A. Grinvald,et al.  Dynamics of Ongoing Activity: Explanation of the Large Variability in Evoked Cortical Responses , 1996, Science.

[11]  V. Torre,et al.  On the Dynamics of the Spontaneous Activity in Neuronal Networks , 2007, PloS one.

[12]  M Steriade,et al.  Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[13]  M. Corbetta,et al.  Learning sculpts the spontaneous activity of the resting human brain , 2009, Proceedings of the National Academy of Sciences.

[14]  D. Plenz,et al.  Neuronal avalanches organize as nested theta- and beta/gamma-oscillations during development of cortical layer 2/3 , 2008, Proceedings of the National Academy of Sciences.

[15]  Charles J. Wilson,et al.  Membrane potential synchrony of simultaneously recorded striatal spiny neurons in vivo , 1998, Nature.

[16]  Hans J. Herrmann,et al.  Activity-Dependent Neuronal Model on Complex Networks , 2012, Front. Physio..

[17]  Mariano Sigman,et al.  A small world of weak ties provides optimal global integration of self-similar modules in functional brain networks , 2011, Proceedings of the National Academy of Sciences.

[18]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[19]  J. M. Oshorn Proc. Nat. Acad. Sei , 1978 .

[20]  L. de Arcangelis,et al.  Learning as a phenomenon occurring in a critical state , 2010, Proceedings of the National Academy of Sciences.

[21]  R. Rosenfeld Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[22]  Andrea Hasenstaub,et al.  State Changes Rapidly Modulate Cortical Neuronal Responsiveness , 2007, The Journal of Neuroscience.

[23]  Danny Eytan,et al.  Dynamics and Effective Topology Underlying Synchronization in Networks of Cortical Neurons , 2006, The Journal of Neuroscience.

[24]  Dante R. Chialvo,et al.  Strobing brain thunders: Functional correlation of extreme activity events , 2013 .

[25]  D. Plenz,et al.  Balance between excitation and inhibition controls the temporal organization of neuronal avalanches. , 2012, Physical review letters.

[26]  C. Stam,et al.  Small‐world properties of nonlinear brain activity in schizophrenia , 2009, Human brain mapping.

[27]  B. Sakmann,et al.  Phase-locking of hippocampal interneurons' membrane potential to neocortical up-down states , 2006, Nature Neuroscience.

[28]  C. Stam,et al.  Disturbed functional connectivity in brain tumour patients: Evaluation by graph analysis of synchronization matrices , 2006, Clinical Neurophysiology.

[29]  Dante R. Chialvo,et al.  What kind of noise is brain noise: anomalous scaling behavior of the resting brain activity fluctuations , 2010, Front. Physio..

[30]  John M. Beggs,et al.  Behavioral / Systems / Cognitive Neuronal Avalanches Are Diverse and Precise Activity Patterns That Are Stable for Many Hours in Cortical Slice Cultures , 2004 .

[31]  C. Stam,et al.  Small-world networks and epilepsy: Graph theoretical analysis of intracerebrally recorded mesial temporal lobe seizures , 2007, Clinical Neurophysiology.

[32]  C. Gray,et al.  Cellular Mechanisms Contributing to Response Variability of Cortical Neurons In Vivo , 1999, The Journal of Neuroscience.

[33]  C. Stam,et al.  Small-world networks and functional connectivity in Alzheimer's disease. , 2006, Cerebral cortex.

[34]  John M. Beggs,et al.  Neuronal Avalanches in Neocortical Circuits , 2003, The Journal of Neuroscience.

[35]  L. L. Bologna,et al.  Self-organization and neuronal avalanches in networks of dissociated cortical neurons , 2008, Neuroscience.

[36]  L de Arcangelis,et al.  Influence of time and space correlations on earthquake magnitude. , 2007, Physical review letters.

[37]  L de Arcangelis,et al.  Universality in solar flare and earthquake occurrence. , 2006, Physical review letters.

[38]  L. de Arcangelis,et al.  Self-organized criticality model for brain plasticity. , 2006, Physical review letters.

[39]  Amir Ayali,et al.  Morphological characterization of in vitro neuronal networks. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[40]  C. Stevens,et al.  Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill the pool. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[41]  D. Plenz,et al.  Neuronal Avalanches in the Resting MEG of the Human Brain , 2012, The Journal of Neuroscience.

[42]  R. Yuste,et al.  Attractor dynamics of network UP states in the neocortex , 2003, Nature.

[43]  D. Plenz,et al.  Spontaneous cortical activity in awake monkeys composed of neuronal avalanches , 2009, Proceedings of the National Academy of Sciences.

[44]  廣瀬雄一,et al.  Neuroscience , 2019, Workplace Attachments.

[45]  T. Sejnowski,et al.  Origin of slow cortical oscillations in deafferented cortical slabs. , 2000, Cerebral cortex.

[46]  Carla Perrone-Capano,et al.  Activity-dependent neural network model on scale-free networks. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[47]  G. Cecchi,et al.  Scale-free brain functional networks. , 2003, Physical review letters.

[48]  E. G. Jones Cerebral Cortex , 1987, Cerebral Cortex.

[49]  D. Plenz,et al.  Up and Down States in Striatal Medium Spiny Neurons Simultaneously Recorded with Spontaneous Activity in Fast-Spiking Interneurons Studied in Cortex–Striatum–Substantia Nigra Organotypic Cultures , 1998, The Journal of Neuroscience.

[50]  Stefan Mihalas,et al.  Self-organized criticality occurs in non-conservative neuronal networks during Up states , 2010, Nature physics.