How Local Excitation–Inhibition Ratio Impacts the Whole Brain Dynamics

The spontaneous activity of the brain shows different features at different scales. On one hand, neuroimaging studies show that long-range correlations are highly structured in spatiotemporal patterns, known as resting-state networks, on the other hand, neurophysiological reports show that short-range correlations between neighboring neurons are low, despite a large amount of shared presynaptic inputs. Different dynamical mechanisms of local decorrelation have been proposed, among which is feedback inhibition. Here, we investigated the effect of locally regulating the feedback inhibition on the global dynamics of a large-scale brain model, in which the long-range connections are given by diffusion imaging data of human subjects. We used simulations and analytical methods to show that locally constraining the feedback inhibition to compensate for the excess of long-range excitatory connectivity, to preserve the asynchronous state, crucially changes the characteristics of the emergent resting and evoked activity. First, it significantly improves the model's prediction of the empirical human functional connectivity. Second, relaxing this constraint leads to an unrealistic network evoked activity, with systematic coactivation of cortical areas which are components of the default-mode network, whereas regulation of feedback inhibition prevents this. Finally, information theoretic analysis shows that regulation of the local feedback inhibition increases both the entropy and the Fisher information of the network evoked responses. Hence, it enhances the information capacity and the discrimination accuracy of the global network. In conclusion, the local excitation–inhibition ratio impacts the structure of the spontaneous activity and the information transmission at the large-scale brain level.

[1]  A. C. Webb,et al.  The spontaneous activity of neurones in the cat’s cerebral cortex , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[2]  William R. Softky,et al.  The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  P S Goldman-Rakic,et al.  Functional synergism between putative gamma-aminobutyrate-containing neurons and pyramidal neurons in prefrontal cortex. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[4]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[5]  Stefano Panzeri,et al.  The Upward Bias in Measures of Information Derived from Limited Data Samples , 1995, Neural Computation.

[6]  H. Sompolinsky,et al.  Chaos in Neuronal Networks with Balanced Excitatory and Inhibitory Activity , 1996, Science.

[7]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[8]  Peter Dayan,et al.  The Effect of Correlated Variability on the Accuracy of a Population Code , 1999, Neural Computation.

[9]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[10]  P. Robinson,et al.  Prediction of electroencephalographic spectra from neurophysiology. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[11]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[12]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[14]  Martial Van der Linden,et al.  Self-referential reflective activity and its relationship with rest: a PET study , 2005, NeuroImage.

[15]  P. Fransson Spontaneous low‐frequency BOLD signal fluctuations: An fMRI investigation of the resting‐state default mode of brain function hypothesis , 2005, Human brain mapping.

[16]  D. Hansel,et al.  Role of delays in shaping spatiotemporal dynamics of neuronal activity in large networks. , 2005, Physical review letters.

[17]  Peter A. Robinson,et al.  BOLD responses to stimuli: Dependence on frequency, stimulus form, amplitude, and repetition rate , 2006, NeuroImage.

[18]  Xiao-Jing Wang,et al.  A Recurrent Network Mechanism of Time Integration in Perceptual Decisions , 2006, The Journal of Neuroscience.

[19]  E. Bullmore,et al.  A Resilient, Low-Frequency, Small-World Human Brain Functional Network with Highly Connected Association Cortical Hubs , 2006, The Journal of Neuroscience.

[20]  E. Bullmore,et al.  Adaptive reconfiguration of fractal small-world human brain functional networks , 2006, Proceedings of the National Academy of Sciences.

[21]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[22]  M. Corbetta,et al.  Electrophysiological signatures of resting state networks in the human brain , 2007, Proceedings of the National Academy of Sciences.

[23]  Olaf Sporns,et al.  Network structure of cerebral cortex shapes functional connectivity on multiple time scales , 2007, Proceedings of the National Academy of Sciences.

[24]  Scott T. Grafton,et al.  Wandering Minds: The Default Network and Stimulus-Independent Thought , 2007, Science.

[25]  Viktor K. Jirsa,et al.  Noise during Rest Enables the Exploration of the Brain's Dynamic Repertoire , 2008, PLoS Comput. Biol..

[26]  Derek K. Jones Studying connections in the living human brain with diffusion MRI , 2008, Cortex.

[27]  Gary H. Glover,et al.  Default-mode function and task-induced deactivation have overlapping brain substrates in children , 2008, NeuroImage.

[28]  Andreas Draguhn,et al.  Fast Homeostatic Plasticity of Inhibition via Activity-Dependent Vesicular Filling , 2008, PloS one.

[29]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[30]  G. Edelman,et al.  Large-scale model of mammalian thalamocortical systems , 2008, Proceedings of the National Academy of Sciences.

[31]  K. Christoff,et al.  Experience sampling during fMRI reveals default network and executive system contributions to mind wandering , 2009, Proceedings of the National Academy of Sciences.

[32]  Moshe Bar,et al.  The proactive brain: memory for predictions , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[33]  O Sporns,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009, Proceedings of the National Academy of Sciences.

[34]  Vince D. Calhoun,et al.  An ICA-based method for the identification of optimal FMRI features and components using combined group-discriminative techniques , 2009, NeuroImage.

[35]  O. Sporns,et al.  Key role of coupling, delay, and noise in resting brain fluctuations , 2009, Proceedings of the National Academy of Sciences.

[36]  Catie Chang,et al.  Time–frequency dynamics of resting-state brain connectivity measured with fMRI , 2010, NeuroImage.

[37]  Jeff H. Duyn,et al.  Large-scale spontaneous fluctuations and correlations in brain electrical activity observed with magnetoencephalography , 2010, NeuroImage.

[38]  Alexander S. Ecker,et al.  Decorrelated Neuronal Firing in Cortical Microcircuits , 2010, Science.

[39]  P. Dayan,et al.  Supporting Online Material Materials and Methods Som Text Figs. S1 to S9 References the Asynchronous State in Cortical Circuits , 2022 .

[40]  Darren Price,et al.  Investigating the electrophysiological basis of resting state networks using magnetoencephalography , 2011, Proceedings of the National Academy of Sciences.

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

[42]  James A. Roberts,et al.  Biophysical Mechanisms of Multistability in Resting-State Cortical Rhythms , 2011, The Journal of Neuroscience.

[43]  M. Corbetta,et al.  Episodic Memory Retrieval, Parietal Cortex, and the Default Mode Network: Functional and Topographic Analyses , 2011, The Journal of Neuroscience.

[44]  Timothy O. Laumann,et al.  Functional Network Organization of the Human Brain , 2011, Neuron.

[45]  Vesa Kiviniemi,et al.  A Sliding Time-Window ICA Reveals Spatial Variability of the Default Mode Network in Time , 2011, Brain Connect..

[46]  Marc Joliot,et al.  Brain activity at rest: a multiscale hierarchical functional organization. , 2011, Journal of neurophysiology.

[47]  Tomoki Fukai,et al.  Power-Law Inter-Spike Interval Distributions Infer a Conditional Maximization of Entropy in Cortical Neurons , 2012, PLoS Comput. Biol..

[48]  Moritz Helias,et al.  Decorrelation of Neural-Network Activity by Inhibitory Feedback , 2012, PLoS Comput. Biol..

[49]  Gustavo Deco,et al.  Balanced Input Allows Optimal Encoding in a Stochastic Binary Neural Network Model: An Analytical Study , 2012, PloS one.

[50]  Mark W. Woolrich,et al.  Inferring task-related networks using independent component analysis in magnetoencephalography , 2012, NeuroImage.

[51]  Alison L. Barth,et al.  Experimental evidence for sparse firing in the neocortex , 2012, Trends in Neurosciences.

[52]  G. Deco,et al.  Ongoing Cortical Activity at Rest: Criticality, Multistability, and Ghost Attractors , 2012, The Journal of Neuroscience.

[53]  Stanislas Dehaene,et al.  An accumulator model for spontaneous neural activity prior to self-initiated movement , 2012, Proceedings of the National Academy of Sciences.

[54]  Kenneth D. Harris,et al.  Laminar-dependent effects of cortical state on auditory cortical spontaneous activity , 2012, Front. Neural Circuits.

[55]  M. Corbetta,et al.  A Cortical Core for Dynamic Integration of Functional Networks in the Resting Human Brain , 2012, Neuron.

[56]  Gustavo Deco,et al.  Resting brains never rest: computational insights into potential cognitive architectures , 2013, Trends in Neurosciences.

[57]  Correction: Mantini et al., Evolutionarily Novel Functional Networks in the Human Brain? , 2013, The Journal of Neuroscience.

[58]  Ravi S. Menon,et al.  Resting‐state networks show dynamic functional connectivity in awake humans and anesthetized macaques , 2013, Human brain mapping.

[59]  Abraham Z. Snyder,et al.  Frequency specific interactions of MEG resting state activity within and across brain networks as revealed by the multivariate interaction measure , 2013, NeuroImage.

[60]  Maurizio Corbetta,et al.  Resting-State Functional Connectivity Emerges from Structurally and Dynamically Shaped Slow Linear Fluctuations , 2013, The Journal of Neuroscience.

[61]  Carl D. Hacker,et al.  Resting state network estimation in individual subjects , 2013, NeuroImage.

[62]  Eswar Damaraju,et al.  Tracking whole-brain connectivity dynamics in the resting state. , 2014, Cerebral cortex.

[63]  Habib Benali,et al.  Relating Structure and Function in the Human Brain: Relative Contributions of Anatomy, Stationary Dynamics, and Non-stationarities , 2014, PLoS Comput. Biol..