Higher-Order Interactions Characterized in Cortical Activity

In the cortex, the interactions among neurons give rise to transient coherent activity patterns that underlie perception, cognition, and action. Recently, it was actively debated whether the most basic interactions, i.e., the pairwise correlations between neurons or groups of neurons, suffice to explain those observed activity patterns. So far, the evidence reported is controversial. Importantly, the overall organization of neuronal interactions and the mechanisms underlying their generation, especially those of high-order interactions, have remained elusive. Here we show that higher-order interactions are required to properly account for cortical dynamics such as ongoing neuronal avalanches in the alert monkey and evoked visual responses in the anesthetized cat. A Gaussian interaction model that utilizes the observed pairwise correlations and event rates and that applies intrinsic thresholding identifies those higher-order interactions correctly, both in cortical local field potentials and spiking activities. This allows for accurate prediction of large neuronal population activities as required, e.g., in brain–machine interface paradigms. Our results demonstrate that higher-order interactions are inherent properties of cortical dynamics and suggest a simple solution to overcome the apparent formidable complexity previously thought to be intrinsic to those interactions.

[1]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[2]  S. Bressler,et al.  Episodic multiregional cortical coherence at multiple frequencies during visual task performance , 1993, Nature.

[3]  E. Vaadia,et al.  Spatiotemporal firing patterns in the frontal cortex of behaving monkeys. , 1993, Journal of neurophysiology.

[4]  C. Koch,et al.  Recurrent excitation in neocortical circuits , 1995, Science.

[5]  A. Aertsen,et al.  Dynamics of neuronal interactions in monkey cortex in relation to behavioural events , 1995, Nature.

[6]  A. Aertsen,et al.  Spike synchronization and rate modulation differentially involved in motor cortical function. , 1997, Science.

[7]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[8]  F. Varela,et al.  Perception's shadow: long-distance synchronization of human brain activity , 1999, Nature.

[9]  Shun-ichi Amari,et al.  Information geometry on hierarchy of probability distributions , 2001, IEEE Trans. Inf. Theory.

[10]  Shun-ichi Amari,et al.  Information-Geometric Measure for Neural Spikes , 2002, Neural Computation.

[11]  Yutaka Sakai,et al.  Synchronous Firing and Higher-Order Interactions in Neuron Pool , 2003, Neural Computation.

[12]  Eric B. Baum,et al.  What is thought? , 2003 .

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

[14]  A. Destexhe,et al.  A method to estimate synaptic conductances from membrane potential fluctuations. , 2004, Journal of neurophysiology.

[15]  M. DeWeese,et al.  Non-Gaussian Membrane Potential Dynamics Imply Sparse, Synchronous Activity in Auditory Cortex , 2006, The Journal of Neuroscience.

[16]  Michael J. Berry,et al.  Weak pairwise correlations imply strongly correlated network states in a neural population , 2005, Nature.

[17]  D. Plenz,et al.  Inverted-U Profile of Dopamine–NMDA-Mediated Spontaneous Avalanche Recurrence in Superficial Layers of Rat Prefrontal Cortex , 2006, The Journal of Neuroscience.

[18]  Jonathon Shlens,et al.  The Structure of Multi-Neuron Firing Patterns in Primate Retina , 2006, The Journal of Neuroscience.

[19]  O. Kinouchi,et al.  Optimal dynamical range of excitable networks at criticality , 2006, q-bio/0601037.

[20]  D. Plenz,et al.  The organizing principles of neuronal avalanches: cell assemblies in the cortex? , 2007, Trends in Neurosciences.

[21]  S. Kauffman,et al.  Measures for information propagation in Boolean networks , 2007 .

[22]  Shan Yu,et al.  A Small World of Neuronal Synchrony , 2008, Cerebral cortex.

[23]  D. Plenz,et al.  Homeostasis of neuronal avalanches during postnatal cortex development in vitro , 2008, Journal of Neuroscience Methods.

[24]  John M. Beggs,et al.  A Maximum Entropy Model Applied to Spatial and Temporal Correlations from Cortical Networks In Vitro , 2008, The Journal of Neuroscience.

[25]  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.

[26]  Maik C. Stüttgen,et al.  Psychophysical and neurometric detection performance under stimulus uncertainty , 2008, Nature Neuroscience.

[27]  Jason Wolfe,et al.  Sparse temporal coding of elementary tactile features during active whisker sensation , 2009, Nature Neuroscience.

[28]  Haim Sompolinsky,et al.  Stimulus-Dependent Correlations in Threshold-Crossing Spiking Neurons , 2009, Neural Computation.

[29]  Takeshi Kaneko,et al.  Recurrent Infomax Generates Cell Assemblies, Neuronal Avalanches, and Simple Cell-Like Selectivity , 2009, Neural Computation.

[30]  Woodrow L. Shew,et al.  Neuronal Avalanches Imply Maximum Dynamic Range in Cortical Networks at Criticality , 2009, The Journal of Neuroscience.

[31]  Jonathon Shlens,et al.  The Structure of Large-Scale Synchronized Firing in Primate Retina , 2009, The Journal of Neuroscience.

[32]  Stefano Panzeri,et al.  The impact of high-order interactions on the rate of synchronous discharge and information transmission in somatosensory cortex , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[33]  Alexander S. Ecker,et al.  Generating Spike Trains with Specified Correlation Coefficients , 2009, Neural Computation.

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

[35]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[36]  Peter E. Latham,et al.  Pairwise Maximum Entropy Models for Studying Large Biological Systems: When They Can Work and When They Can't , 2008, PLoS Comput. Biol..

[37]  S. Leibler,et al.  Neuronal couplings between retinal ganglion cells inferred by efficient inverse statistical physics methods , 2009, Proceedings of the National Academy of Sciences.

[38]  Michael Okun,et al.  The Subthreshold Relation between Cortical Local Field Potential and Neuronal Firing Unveiled by Intracellular Recordings in Awake Rats , 2010, The Journal of Neuroscience.

[39]  Jonathan D. Victor,et al.  Information-geometric measure of 3-neuron firing patterns characterizes scale-dependence in cortical networks , 2011, Journal of Computational Neuroscience.

[40]  Ifije E. Ohiorhenuan,et al.  Sparse coding and high-order correlations in fine-scale cortical networks , 2010, Nature.

[41]  Dietmar Plenz,et al.  Hierarchical Interaction Structure of Neural Activities in Cortical Slice Cultures , 2010, The Journal of Neuroscience.

[42]  D. Plenz,et al.  Coherence Potentials: Loss-Less, All-or-None Network Events in the Cortex , 2010, PLoS biology.

[43]  M. Nicolelis,et al.  Spike Avalanches Exhibit Universal Dynamics across the Sleep-Wake Cycle , 2010, PloS one.

[44]  Fredric M. Wolf,et al.  Frontiers in Computational Neuroscience Materials and Methods Measures of Correlation , 2022 .

[45]  W. Singer,et al.  Neuronal avalanches in spontaneous activity in vivo. , 2010, Journal of neurophysiology.

[46]  R. Segev,et al.  Sparse low-order interaction network underlies a highly correlated and learnable neural population code , 2011, Proceedings of the National Academy of Sciences.

[47]  Randy M. Bruno,et al.  Effects and Mechanisms of Wakefulness on Local Cortical Networks , 2011, Neuron.

[48]  Woodrow L. Shew,et al.  Information Capacity and Transmission Are Maximized in Balanced Cortical Networks with Neuronal Avalanches , 2010, The Journal of Neuroscience.

[49]  M. Bethge,et al.  Common input explains higher-order correlations and entropy in a simple model of neural population activity. , 2011, Physical review letters.

[50]  R. Segev,et al.  The Architecture of Functional Interaction Networks in the Retina , 2011, The Journal of Neuroscience.

[51]  Andreas Klaus,et al.  Statistical Analyses Support Power Law Distributions Found in Neuronal Avalanches , 2011, PloS one.