Models of cortical networks with long-range patchy projections

The cortex exhibits an intricate vertical and horizontal architecture, the latter often featuring spatially clustered projection patterns, so-called patches. Many network studies of cortical dynamics ignore such spatial structures and assume purely random wiring. Here, we focus on non-random network structures provided by long-range horizontal (patchy) connections that remain inside the gray matter. We investigate how the spatial arrangement of patchy projections influences global network topology and predict its impact on the activity dynamics of the network. Since neuroanatomical data on horizontal projections is rather sparse, we suggest and compare four candidate scenarios of how patchy connections may be established. To identify a set of characteristic network properties that enables us to pin down the differences between the resulting network models, we employ the framework of stochastic graph theory. We find that patchy projections provide an exceptionally efficient way of wiring, as the resulting networks tend to exhibit small-world properties with significantly reduced wiring costs. Furthermore, the eigenvalue spectra, as well as the structure of common in- and output of the networks suggest that different spatial connectivity patterns support distinct types of activity propagation.

[1]  H. Lohmann,et al.  Long‐range horizontal connections between supragranular pyramidal cells in the extrastriate visual cortex of the rat , 1994, The Journal of comparative neurology.

[2]  S. Laughlin,et al.  An Energy Budget for Signaling in the Grey Matter of the Brain , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[3]  D. Fitzpatrick,et al.  Orientation Selectivity and the Arrangement of Horizontal Connections in Tree Shrew Striate Cortex , 1997, The Journal of Neuroscience.

[4]  German Barrionuevo,et al.  Synaptic targets of the intrinsic axon collaterals of supragranular pyramidal neurons in monkey prefrontal cortex , 2001, The Journal of comparative neurology.

[5]  H. Ojima,et al.  Cortical convergence from different frequency domains in the cat primary auditory cortex , 2004, Neuroscience.

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

[7]  T. Wiesel,et al.  Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  A. Burkhalter,et al.  Organization of local axon collaterals of efferent projection neurons in rat visual cortex , 1990, The Journal of comparative neurology.

[9]  L. M. Kitzes,et al.  Intrinsic inter- and intralaminar connections and their relationship to the tonotopic map in cat primary auditory cortex , 2004, Experimental Brain Research.

[10]  Stefan Rotter,et al.  Statistical analysis of spatially embedded networks: From grid to random node positions , 2007, Neurocomputing.

[11]  E. Batschelet Circular statistics in biology , 1981 .

[12]  Marcus Kaiser,et al.  Modelling the development of cortical systems networks , 2004, Neurocomputing.

[13]  R. Malach,et al.  Cortical hierarchy reflected in the organization of intrinsic connections in macaque monkey visual cortex , 1993, The Journal of comparative neurology.

[14]  Stefan Rotter,et al.  Correlations and Population Dynamics in Cortical Networks , 2008, Neural Computation.

[15]  A. Barabasi,et al.  Spectra of "real-world" graphs: beyond the semicircle law. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[16]  D. Chklovskii,et al.  Optimal sizes of dendritic and axonal arbors in a topographic projection. , 1999, Journal of neurophysiology.

[17]  J. B. Levitt,et al.  Patterns of intrinsic and associational circuitry in monkey prefrontal cortex , 1996, The Journal of comparative neurology.

[18]  U. Eysel,et al.  Cellular organization of reciprocal patchy networks in layer III of cat visual cortex (area 17) , 1992, Neuroscience.

[19]  Heather J. Chisum,et al.  The contribution of vertical and horizontal connections to the receptive field center and surround in V1 , 2004, Neural Networks.

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

[21]  Laurent Perrinet,et al.  Phase space analysis of networks based on biologically realistic parameters , 2010, Journal of Physiology-Paris.

[22]  T. Wiesel,et al.  Clustered intrinsic connections in cat visual cortex , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  Danielle Smith Bassett,et al.  Small-World Brain Networks , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[24]  R. Douglas,et al.  Stereotypical Bouton Clustering of Individual Neurons in Cat Primary Visual Cortex , 2007, The Journal of Neuroscience.

[25]  J. B. Levitt,et al.  Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. , 1993, Cerebral cortex.

[26]  Braitenberg,et al.  The Human Cortical White Matter: Quantitative Aspects of Cortico-Cortical Long-Range Connectivity , 2002 .

[27]  Kostadin Koroutchev,et al.  Improved Storage Capacity of Hebbian Learning Attractor Neural Network with Bump Formations , 2006, ICANN.

[28]  A. Schüz,et al.  Quantitative aspects of corticocortical connections: a tracer study in the mouse. , 2006, Cerebral cortex.

[29]  Moshe Abeles,et al.  Corticonics: Neural Circuits of Cerebral Cortex , 1991 .

[30]  Stephen D. Van Hooser,et al.  Lack of Patchy Horizontal Connectivity in Primary Visual Cortex of a Mammal without Orientation Maps , 2006, The Journal of Neuroscience.

[31]  Dmitri B Chklovskii,et al.  Synaptic Connectivity and Neuronal Morphology Two Sides of the Same Coin , 2004, Neuron.

[32]  L. Haberly,et al.  New Features of Connectivity in Piriform Cortex Visualized by Intracellular Injection of Pyramidal Cells Suggest that “Primary” Olfactory Cortex Functions Like “Association” Cortex in Other Sensory Systems , 2000, The Journal of Neuroscience.

[33]  Alex S. Ferecskó,et al.  Model‐based analysis of excitatory lateral connections in the visual cortex , 2006, The Journal of comparative neurology.

[34]  Markus Diesmann,et al.  Synchronization and rate dynamics in embedded synfire chains: effect of network heterogeneity and feedback , 2009, BMC Neuroscience.

[35]  G. Buzsáki,et al.  Interneuron Diversity series: Circuit complexity and axon wiring economy of cortical interneurons , 2004, Trends in Neurosciences.

[36]  Arvind Kumar,et al.  The High-Conductance State of Cortical Networks , 2008, Neural Computation.

[37]  Markus Diesmann,et al.  Activity dynamics and propagation of synchronous spiking in locally connected random networks , 2003, Biological Cybernetics.

[38]  Nicholas I. Fisher,et al.  Statistical Analysis of Circular Data , 1993 .

[39]  Olaf Sporns,et al.  The small world of the cerebral cortex , 2007, Neuroinformatics.

[40]  Mark E. J. Newman,et al.  The Structure and Function of Complex Networks , 2003, SIAM Rev..

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

[42]  E. G. Jones,et al.  Patterns of axon collateralization of identified supragranular pyramidal neurons in the cat auditory cortex. , 1991, Cerebral cortex.

[43]  Nicolas Brunel,et al.  Dynamics of Sparsely Connected Networks of Excitatory and Inhibitory Spiking Neurons , 2000, Journal of Computational Neuroscience.

[44]  Bernhard Hellwig,et al.  A quantitative analysis of the local connectivity between pyramidal neurons in layers 2/3 of the rat visual cortex , 2000, Biological Cybernetics.

[45]  Alessandro Treves,et al.  An associative network with spatially organized connectivity , 2004 .

[46]  Henry Markram,et al.  Deriving physical connectivity from neuronal morphology , 2003, Biological Cybernetics.

[47]  David A. Lewis,et al.  Specificity in the functional architecture of primate prefrontal cortex , 2002, Journal of neurocytology.

[48]  Marc Timme,et al.  Breaking synchrony by heterogeneity in complex networks. , 2003, Physical review letters.

[49]  Anders Lansner,et al.  Imposing Biological Constraints onto an Abstract Neocortical Attractor Network Model , 2007, Neural Computation.

[50]  A. Grinvald,et al.  The layout of iso-orientation domains in area 18 of cat visual cortex: optical imaging reveals a pinwheel-like organization , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  J. Lund,et al.  Intra- and inter-areal connections between the primary visual cortex V1 and the area immediately surrounding V1 in the rat , 2001, Neuroscience.

[52]  Alessandro Treves,et al.  Representing Where along with What Information in a Model of a Cortical Patch , 2008, PLoS Comput. Biol..

[53]  Amiram Grinvald,et al.  Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns , 1991, Nature.

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

[55]  Albert-László Barabási,et al.  Statistical mechanics of complex networks , 2001, ArXiv.

[56]  Ad Aertsen,et al.  Stable propagation of synchronous spiking in cortical neural networks , 1999, Nature.

[57]  J. B. Levitt,et al.  Intrinsic Connections in Mammalian Cerebral Cortex , 2002 .

[58]  P. De Los Rios,et al.  Existence, Cost and Robustness of Spatial Small-World Networks , 2007, Int. J. Bifurc. Chaos.

[59]  S. Strogatz Exploring complex networks , 2001, Nature.

[60]  E. Callaway,et al.  Emergence and refinement of clustered horizontal connections in cat striate cortex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[61]  Moritz Helias,et al.  Correlations in spiking neuronal networks with distance dependent connections , 2009, Journal of Computational Neuroscience.

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

[63]  A. Aertsen,et al.  Conditions for Propagating Synchronous Spiking and Asynchronous Firing Rates in a Cortical Network Model , 2008, The Journal of Neuroscience.