aSection on Critical Brain Dynamics, National Institute of Mental Health, Bethesda, MD 20892;
bDepartment of Neurobiology, Center for Neuroengineering, Duke University, Durham, NC 27710; and
cDepartment of Physiology, Northwestern University, Chicago, IL 60611
Edited by Eve Marder, Brandeis University, Waltham, MA, and approved July 16, 2009 (received for review April 16, 2009)
Spontaneous neuronal activity is an important property of the cerebral cortex but its spatiotemporal organization and dynamical framework remain poorly understood. Studies in reduced systems—tissue cultures, acute slices, and anesthetized rats—show that spontaneous activity forms characteristic clusters in space and time, called neuronal avalanches. Modeling studies suggest that networks with this property are poised at a critical state that optimizes input processing, information storage, and transfer, but the relevance of avalanches for fully functional cerebral systems has been controversial. Here we show that ongoing cortical synchronization in awake rhesus monkeys carries the signature of neuronal avalanches. Negative LFP deflections (nLFPs) correlate with neuronal spiking and increase in amplitude with increases in local population spike rate and synchrony. These nLFPs form neuronal avalanches that are scale-invariant in space and time and with respect to the threshold of nLFP detection. This dimension, threshold invariance, describes a fractal organization: smaller nLFPs are embedded in clusters of larger ones without destroying the spatial and temporal scale-invariance of the dynamics. These findings suggest an organization of ongoing cortical synchronization that is scale-invariant in its three fundamental dimensions—time, space, and local neuronal group size. Such scale-invariance has ontogenetic and phylogenetic implications because it allows large increases in network capacity without a fundamental reorganization of the system.
Woodrow L. Shew,1Hongdian Yang,1,2Thomas Petermann,1Rajarshi Roy,2 and Dietmar Plenz1
1Section on Critical Brain Dynamics, Laboratory of Systems Neuroscience, National Institute of Mental Health, Bethesda, Maryland 20892, and 2Institute for Physical Science and Technology, University of Maryland, College Park, Maryland 20742
Correspondence should be addressed to Dr. Dietmar Plenz, Section on Critical Brain Dynamics, Laboratory of Systems Neuroscience, Porter Neuroscience Research Center, National Institute of Mental Health, Room 3A-100, 35 Convent Drive, Bethesda, MD 20892. Email: email@example.com
Spontaneous neuronal activity is a ubiquitous feature of cortex.Its spatiotemporal organization reflects past input and modulatesfuture network output. Here we study whether a particular typeof spontaneous activity is generated by a network that is optimizedfor input processing. Neuronal avalanches are a type of spontaneousactivity observed in superficial cortical layers in vitro andin vivo with statistical properties expected from a networkoperating at "criticality." Theory predicts that criticalityand, 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 microelectrodearrays to demonstrate that cortical networks that generate neuronalavalanches benefit from a maximized dynamic range, i.e., theability to respond to the greatest range of stimuli. By changingthe ratio of excitation and inhibition in the cultures, we derivea network tuning curve for stimulus processing as a functionof distance from criticality in agreement with predictions fromour 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 inthe context of critical phenomena.
Received Aug. 6, 2009; revised Sept. 28, 2009; accepted Oct. 30, 2009.