Motor Cortex Microcircuit Simulation Based on Brain Activity Mapping

The deceptively simple laminar structure of neocortex belies the complexity of intra- and interlaminar connectivity. We developed a computational model based primarily on a unified set of brain activity mapping studies of mouse M1. The simulation consisted of 775 spiking neurons of 10 cell types with detailed population-to-population connectivity. Static analysis of connectivity with graph-theoretic tools revealed that the corticostriatal population showed strong centrality, suggesting that would provide a network hub. Subsequent dynamical analysis confirmed this observation, in addition to revealing network dynamics that cannot be readily predicted through analysis of the wiring diagram alone. Activation thresholds depended on the stimulated layer. Low stimulation produced transient activation, while stronger activation produced sustained oscillations where the threshold for sustained responses varied by layer: 13% in layer 2/3, 54% in layer 5A, 25% in layer 5B, and 17% in layer 6. The frequency and phase of the resulting oscillation also depended on stimulation layer. By demonstrating the effectiveness of combined static and dynamic analysis, our results show how static brain maps can be related to the results of brain activity mapping.

[1]  Bin He,et al.  Graph analysis of epileptogenic networks in human partial epilepsy , 2011, Epilepsia.

[2]  W. Lytton,et al.  Cortical Plasticity Induced by Spike-Triggered Microstimulation in Primate Somatosensory Cortex , 2013, PloS one.

[3]  S. Nelson,et al.  Region-Specific Spike-Frequency Acceleration in Layer 5 Pyramidal Neurons Mediated by Kv1 Subunits , 2008, The Journal of Neuroscience.

[4]  Jean Gotman,et al.  Are high frequency oscillations associated with altered network topology in partial epilepsy? , 2013, NeuroImage.

[5]  Ian R. Wickersham,et al.  Hierarchical Connectivity and Connection-Specific Dynamics in the Corticospinal–Corticostriatal Microcircuit in Mouse Motor Cortex , 2012, The Journal of Neuroscience.

[6]  W. Lytton,et al.  Reinforcement Learning of Targeted Movement in a Spiking Neuronal Model of Motor Cortex , 2012, PloS one.

[7]  E. Callaway,et al.  Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons , 2000, Nature Neuroscience.

[8]  R. Douglas,et al.  A Quantitative Map of the Circuit of Cat Primary Visual Cortex , 2004, The Journal of Neuroscience.

[9]  Nicholas T. Carnevale,et al.  The NEURON Book: Epilogue , 2006 .

[10]  R. Douglas,et al.  Neuronal circuits of the neocortex. , 2004, Annual review of neuroscience.

[11]  Takuma Tanaka,et al.  Parvalbumin‐producing cortical interneurons receive inhibitory inputs on proximal portions and cortical excitatory inputs on distal dendrites , 2012, The European journal of neuroscience.

[12]  Michael L. Hines,et al.  The virtual slice setup , 2008, Journal of Neuroscience Methods.

[13]  Taro Kiritani,et al.  Local-Circuit Phenotypes of Layer 5 Neurons in Motor-Frontal Cortex of YFP-H Mice , 2008, Frontiers in neural circuits.

[14]  William W. Lytton,et al.  Emergence of Physiological Oscillation Frequencies in a Computer Model of Neocortex , 2011, Front. Comput. Neurosci..

[15]  Karl J. Friston,et al.  Canonical Microcircuits for Predictive Coding , 2012, Neuron.

[16]  William W Lytton,et al.  Training oscillatory dynamics with spike-timing-dependent plasticity in a computer model of neocortex , 2011, 2011 IEEE Signal Processing in Medicine and Biology Symposium (SPMB).

[17]  Alex S. Ferecskó,et al.  Local Potential Connectivity in Cat Primary Visual Cortex , 2008 .

[18]  Valentin Dragoi,et al.  Mary visual cortex , 1997 .

[19]  Stefan Lang,et al.  Simulation of signal flow in 3D reconstructions of an anatomically realistic neural network in rat vibrissal cortex , 2011, Neural Networks.

[20]  L. Finkel,et al.  Ketamine Disrupts Theta Modulation of Gamma in a Computer Model of Hippocampus , 2011, The Journal of Neuroscience.

[21]  Neda Bernasconi,et al.  Graph-theoretical analysis reveals disrupted small-world organization of cortical thickness correlation networks in temporal lobe epilepsy. , 2011, Cerebral cortex.

[22]  William W. Lytton,et al.  Rule-based firing for network simulations , 2006, Neurocomputing.

[23]  Karel Svoboda,et al.  Precise Development of Functional and Anatomical Columns in the Neocortex , 2004, Neuron.

[24]  Jianing Yu,et al.  Top-down laminar organization of the excitatory network in motor cortex , 2008, Nature Neuroscience.

[25]  S. Nelson,et al.  Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. , 2007, Journal of neurophysiology.

[26]  Jessica A. Cardin,et al.  Driving fast-spiking cells induces gamma rhythm and controls sensory responses , 2009, Nature.

[27]  Ian R. Wickersham,et al.  Laminarly Orthogonal Excitation of Fast-Spiking and Low-Threshold-Spiking Interneurons in Mouse Motor Cortex , 2012, The Journal of Neuroscience.

[28]  Xiao-Jing Wang.  Neurophysiological and computational principles of cortical rhythms in cognition. , 2010, Physiological reviews.

[29]  Christopher I. Moore,et al.  Human Neuroscience , 2022 .

[30]  C. Petersen,et al.  The Excitatory Neuronal Network of the C2 Barrel Column in Mouse Primary Somatosensory Cortex , 2009, Neuron.

[31]  D. Chklovskii,et al.  Neurogeometry and potential synaptic connectivity , 2005, Trends in Neurosciences.

[32]  Y. Kawaguchi,et al.  Recurrent Connection Patterns of Corticostriatal Pyramidal Cells in Frontal Cortex , 2006, The Journal of Neuroscience.

[33]  Gerald E. Loeb,et al.  Major remaining gaps in models of sensorimotor systems , 2015, Front. Comput. Neurosci..

[34]  J. Cowan,et al.  Excitatory and inhibitory interactions in localized populations of model neurons. , 1972, Biophysical journal.

[35]  Jessica A. Cardin,et al.  Computational modeling of distinct neocortical oscillations driven by cell-type selective optogenetic drive: separable resonant circuits controlled by low-Citation , 2010 .

[36]  Roger D. Traub,et al.  Dual Gamma Rhythm Generators Control Interlaminar Synchrony in Auditory Cortex , 2011, The Journal of Neuroscience.

[37]  R. Morgan,et al.  Nonrandom connectivity of the epileptic dentate gyrus predicts a major role for neuronal hubs in seizures , 2008, Proceedings of the National Academy of Sciences.

[38]  Bryan M. Hooks,et al.  Laminar Analysis of Excitatory Local Circuits in Vibrissal Motor and Sensory Cortical Areas , 2011, PLoS biology.

[39]  William W Lytton,et al.  Tonic-Clonic Transitions in Computer Simulation , 2007, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[40]  田中 康代.  Local connections of layer 5 GABAergic interneurons to corticospinal neurons , 2012 .

[41]  Bryan M. Hooks,et al.  Organization of Cortical and Thalamic Input to Pyramidal Neurons in Mouse Motor Cortex , 2013, The Journal of Neuroscience.

[42]  R. Kötter,et al.  Layer-Specific Intracolumnar and Transcolumnar Functional Connectivity of Layer V Pyramidal Cells in Rat Barrel Cortex , 2001, The Journal of Neuroscience.

[43]  Michael L. Hines,et al.  Just-in-Time Connectivity for Large Spiking Networks , 2008, Neural Computation.

[44]  Valter Tucci,et al.  Layer-specific excitatory circuits differentially control recurrent network dynamics in the neocortex , 2013, Nature Neuroscience.

[45]  Lucy M. Carracedo,et al.  Period Concatenation Underlies Interactions between Gamma and Beta Rhythms in Neocortex , 2008, Frontiers in cellular neuroscience.

[46]  William W. Lytton,et al.  Synaptic information transfer in computer models of neocortical columns , 2011, Journal of Computational Neuroscience.

[47]  K. Harris,et al.  Laminar Structure of Spontaneous and Sensory-Evoked Population Activity in Auditory Cortex , 2009, Neuron.

[48]  Thomas K. Berger,et al.  Heterogeneity in the pyramidal network of the medial prefrontal cortex , 2006, Nature Neuroscience.

[49]  H. Markram.  The Blue Brain Project , 2006, Nature Reviews Neuroscience.

[50]  T. Sejnowski,et al.  Cortical Enlightenment: Are Attentional Gamma Oscillations Driven by ING or PING? , 2009, Neuron.

[51]  Taro Kiritani,et al.  Sublayer-specific microcircuits of corticospinal and corticostriatal neurons in motor cortex , 2010, Nature Neuroscience.

[52]  Wenjie Zhang,et al.  Towards real-time communication between in vivo neurophysiological data sources and simulator-based brain biomimetic models , 2014, Journal of computational surgery.

[53]  Michele Migliore,et al.  Intrinsic electrophysiology of mouse corticospinal neurons: a class-specific triad of spike-related properties. , 2013, Cerebral cortex.

[54]  Daniel Johnston,et al.  Projection-Specific Neuromodulation of Medial Prefrontal Cortex Neurons , 2010, The Journal of Neuroscience.

[55]  A. Thomson,et al.  Interlaminar connections in the neocortex. , 2003, Cerebral cortex.

[56]  R. Yuste,et al.  Dense, Unspecific Connectivity of Neocortical Parvalbumin-Positive Interneurons: A Canonical Microcircuit for Inhibition? , 2011, The Journal of Neuroscience.

[57]  Tomoki Fukai,et al.  Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements , 2009, Nature Neuroscience.

[58]  Hysell V. Oviedo,et al.  The functional asymmetry of auditory cortex is reflected in the organization of local cortical circuits , 2010, Nature Neuroscience.

[59]  J. T. Francis,et al.  Electrostimulation as a Prosthesis for Repair of Information Flow in a Computer Model of Neocortex , 2012, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[60]  B. Zemelman,et al.  The columnar and laminar organization of inhibitory connections to neocortical excitatory cells , 2010, Nature Neuroscience.

[61]  William W. Lytton,et al.  A rule-based firing model for neural networks , 2005 .

[62]  Eberhard E Fetz,et al.  Characteristic membrane potential trajectories in primate sensorimotor cortex neurons recorded in vivo. , 2005, Journal of neurophysiology.

[63]  Leonard M. Freeman,et al.  A set of measures of centrality based upon betweenness , 1977 .