Artigo Revisado por pares

Neuronal branching patterns and the economy of cortical wiring

1991; Royal Society; Volume: 245; Issue: 1313 Linguagem: Inglês

10.1098/rspb.1991.0102

ISSN

1471-2954

Autores

Graeme Mitchison,

Tópico(s)

Neural Networks and Applications

Resumo

Restricted accessMoreSectionsView PDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmail Cite this article Mitchison Graeme 1991Neuronal branching patterns and the economy of cortical wiringProc. R. Soc. Lond. B.245151–158http://doi.org/10.1098/rspb.1991.0102SectionRestricted accessArticleNeuronal branching patterns and the economy of cortical wiring Graeme Mitchison Google Scholar Find this author on PubMed Search for more papers by this author Graeme Mitchison Google Scholar Find this author on PubMed Published:22 August 1991https://doi.org/10.1098/rspb.1991.0102AbstractKeeping the volume of connections in the cortex as low as possible may be an important evolutionary constraint on the design of the brain. Much as an engineer tries to arrange the components of a computer in such a way as to give efficient wiring, so the brain may have evolved a layout of neuronal types which gives an economical use of axonal 'wiring'. One key difference between computer and brain is that connections in the brain take the form of elaborate branching structures. It is argued here that certain features of cortical mapping, such as the stripes and patches seen within cortical areas, may be adaptations which allow efficient wiring by such structures. Some simple calculations are given to support this, using as models for axonal arbors certain branching patterns which give a low volume of wiring. In particular, it is shown that a pattern of stripes can give economical wiring when axon diameters follow a law dp = dp + dwith p >4, where d1 and d2 are the diameters of the daughter bFootnotesThis text was harvested from a scanned image of the original document using optical character recognition (OCR) software. As such, it may contain errors. Please contact the Royal Society if you find an error you would like to see corrected. Mathematical notations produced through Infty OCR. Previous Article VIEW FULL TEXT DOWNLOAD PDF FiguresRelatedReferencesDetailsCited by Tobore T (2021) On the theory of mental representation block. a novel perspective on learning and behavior, Communicative & Integrative Biology, 10.1080/19420889.2021.1898752, 14:1, (41-50), Online publication date: 1-Jan-2021. Ma J, Zhang J, Lin Y and Dai Z (2021) Cost-efficiency trade-offs of the human brain network revealed by a multiobjective evolutionary algorithm, NeuroImage, 10.1016/j.neuroimage.2021.118040, 236, (118040), Online publication date: 1-Aug-2021. Smith J, Rowland C, Harland B, Moslehi S, Montgomery R, Schobert K, Watterson W, Dalrymple-Alford J and Taylor R (2021) How neurons exploit fractal geometry to optimize their network connectivity, Scientific Reports, 10.1038/s41598-021-81421-2, 11:1, Online publication date: 1-Dec-2021. Barton B and A. Brewer A (2020) Attention and Working Memory in Human Auditory Cortex The Human Auditory System - Basic Features and Updates on Audiological Diagnosis and Therapy, 10.5772/intechopen.85537 Lesciotto K and Richtsmeier J (2019) Craniofacial skeletal response to encephalization: How do we know what we think we know?, American Journal of Physical Anthropology, 10.1002/ajpa.23766, 168:S67, (27-46), Online publication date: 1-Jan-2019. Kremkow J and Alonso J (2018) Thalamocortical Circuits and Functional Architecture, Annual Review of Vision Science, 10.1146/annurev-vision-091517-034122, 4:1, (263-285), Online publication date: 15-Sep-2018. Brewer A and Barton B (2018) Cloverleaf Clusters: A Common Macrostructural Organization across Human Visual and Auditory Cortex Sensory Nervous System, 10.5772/intechopen.77964 Puppo F, George V and Silva G (2018) An Optimized Structure-Function Design Principle Underlies Efficient Signaling Dynamics in Neurons, Scientific Reports, 10.1038/s41598-018-28527-2, 8:1, Online publication date: 1-Dec-2018. MAZADE R and ALONSO J (2017) Thalamocortical processing in vision, Visual Neuroscience, 10.1017/S0952523817000049, 34, . Yu L and Yu Y (2017) Energy-efficient neural information processing in individual neurons and neuronal networks, Journal of Neuroscience Research, 10.1002/jnr.24131, 95:11, (2253-2266), Online publication date: 1-Nov-2017. Pehlevan C and Sengupta A (2017) Resource-efficient perceptron has sparse synaptic weight distribution 2017 25th Signal Processing and Communications Applications Conference (SIU), 10.1109/SIU.2017.7960683, 978-1-5090-6494-6, (1-4) Fornito A, Bullmore E and Zalesky A (2017) Opportunities and Challenges for Psychiatry in the Connectomic Era, Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 10.1016/j.bpsc.2016.08.003, 2:1, (9-19), Online publication date: 1-Jan-2017. Schröter M, Paulsen O and Bullmore E (2017) Micro-connectomics: probing the organization of neuronal networks at the cellular scale, Nature Reviews Neuroscience, 10.1038/nrn.2016.182, 18:3, (131-146), Online publication date: 1-Mar-2017. Barton B and Brewer A (2016) Human Auditory Cortex Neurobiology of Language, 10.1016/B978-0-12-407794-2.00005-5, (49-58), . Niven J (2016) Neuronal energy consumption: biophysics, efficiency and evolution, Current Opinion in Neurobiology, 10.1016/j.conb.2016.09.004, 41, (129-135), Online publication date: 1-Dec-2016. (2016) References Fundamentals of Brain Network Analysis, 10.1016/B978-0-12-407908-3.10000-7, (433-472), . Betzel R, Avena-Koenigsberger A, Goñi J, He Y, de Reus M, Griffa A, Vértes P, Mišic B, Thiran J, Hagmann P, van den Heuvel M, Zuo X, Bullmore E and Sporns O (2016) Generative models of the human connectome, NeuroImage, 10.1016/j.neuroimage.2015.09.041, 124, (1054-1064), Online publication date: 1-Jan-2016. Wang I and Clandinin T (2016) The Influence of Wiring Economy on Nervous System Evolution, Current Biology, 10.1016/j.cub.2016.08.053, 26:20, (R1101-R1108), Online publication date: 1-Oct-2016. Galinsky V and Frank L (2016) The Lamellar Structure of the Brain Fiber Pathways, Neural Computation, 10.1162/NECO_a_00896, 28:11, (2533-2556), Online publication date: 1-Nov-2016. (2016) Motifs, Small Worlds, and Network Economy Fundamentals of Brain Network Analysis, 10.1016/B978-0-12-407908-3.00008-X, (257-301), . Brewer A and Barton B (2016) Maps of the Auditory Cortex, Annual Review of Neuroscience, 10.1146/annurev-neuro-070815-014045, 39:1, (385-407), Online publication date: 8-Jul-2016. Semendeferi K and Horton C (2015) Evolution of the Cerebral Cortex Brain Mapping, 10.1016/B978-0-12-397025-1.00192-5, (3-10), . Niven J (2015) Neural Evolution: Marginal Gains through Soma Location, Current Biology, 10.1016/j.cub.2015.02.059, 25:8, (R330-R332), Online publication date: 1-Apr-2015. Xing J, Berger T, Sungkar M and Levy W Energy Efficient Neurons With Generalized Inverse Gaussian Conditional and Marginal Hitting Times, IEEE Transactions on Information Theory, 10.1109/TIT.2015.2444401, 61:8, (4390-4398) Wilson S and Bednar J (2015) What, if anything, are topological maps for?, Developmental Neurobiology, 10.1002/dneu.22281, 75:6, (667-681), Online publication date: 1-Jun-2015. Avena-Koenigsberger A, Goñi J, Betzel R, van den Heuvel M, Griffa A, Hagmann P, Thiran J and Sporns O (2014) Using Pareto optimality to explore the topology and dynamics of the human connectome, Philosophical Transactions of the Royal Society B: Biological Sciences, 369:1653, Online publication date: 5-Oct-2014. Patel G, Kaplan D and Snyder L (2014) Topographic organization in the brain: searching for general principles, Trends in Cognitive Sciences, 10.1016/j.tics.2014.03.008, 18:7, (351-363), Online publication date: 1-Jul-2014. Yaeger L (2014) Evolution of Complexity and Neural Topologies Guided Self-Organization: Inception, 10.1007/978-3-642-53734-9_15, (415-454), . Nauhaus I and Nielsen K (2014) Building maps from maps in primary visual cortex, Current Opinion in Neurobiology, 10.1016/j.conb.2013.08.007, 24, (1-6), Online publication date: 1-Feb-2014. Xing J and Berger T (2013) Energy efficient neurons with generalized inverse Gaussian conditional and marginal hitting times 2013 IEEE International Symposium on Information Theory (ISIT), 10.1109/ISIT.2013.6620542, 978-1-4799-0446-4, (1824-1828) Varshney L The Wiring Economy Principle for Designing Inference Networks, IEEE Journal on Selected Areas in Communications, 10.1109/JSAC.2013.130611, 31:6, (1095-1104) YAEGER L (2013) IDENTIFYING NEURAL NETWORK TOPOLOGIES THAT FOSTER DYNAMICAL COMPLEXITY, Advances in Complex Systems, 10.1142/S021952591350032X, 16:02n03, (1350032), Online publication date: 1-May-2013. Ercsey-Ravasz M, Markov N, Lamy C, Van Essen D, Knoblauch K, Toroczkai Z and Kennedy H (2013) A Predictive Network Model of Cerebral Cortical Connectivity Based on a Distance Rule, Neuron, 10.1016/j.neuron.2013.07.036, 80:1, (184-197), Online publication date: 1-Oct-2013. Just M, Keller T, Malave V, Kana R and Varma S (2012) Autism as a neural systems disorder: A theory of frontal-posterior underconnectivity, Neuroscience & Biobehavioral Reviews, 10.1016/j.neubiorev.2012.02.007, 36:4, (1292-1313), Online publication date: 1-Apr-2012. Stevens C (2012) Brain Organization: Wiring Economy Works for the Large and Small, Current Biology, 10.1016/j.cub.2011.11.036, 22:1, (R24-R25), Online publication date: 1-Jan-2012. Xing J, Berger T and Sejnowski T (2012) A Berger-Levy energy efficient neuron model with unequal synaptic weights 2012 IEEE International Symposium on Information Theory - ISIT, 10.1109/ISIT.2012.6284081, 978-1-4673-2579-0, (2964-2968) Gallos L, Makse H and Sigman M (2012) A small world of weak ties provides optimal global integration of self-similar modules in functional brain networks, Proceedings of the National Academy of Sciences, 10.1073/pnas.1106612109, 109:8, (2825-2830), Online publication date: 21-Feb-2012. Zucker S (2012) Local field potentials and border ownership: A conjecture about computation in visual cortex, Journal of Physiology-Paris, 10.1016/j.jphysparis.2012.08.001, 106:5-6, (297-315), Online publication date: 1-Sep-2012. Rivera-Alba M, Vitaladevuni S, Mishchenko Y, Lu Z, Takemura S, Scheffer L, Meinertzhagen I, Chklovskii D and de Polavieja G (2011) Wiring Economy and Volume Exclusion Determine Neuronal Placement in the Drosophila Brain, Current Biology, 10.1016/j.cub.2011.10.022, 21:23, (2000-2005), Online publication date: 1-Dec-2011. Murthy V (2011) Olfactory Maps in the Brain, Annual Review of Neuroscience, 10.1146/annurev-neuro-061010-113738, 34:1, (233-258), Online publication date: 21-Jul-2011. Wen Q and Chklovskii D (2010) To Myelinate or Not to Myelinate? New Aspects of Axonal Structure and Function, 10.1007/978-1-4419-1676-1_6, (103-113), . Itzhack R and Louzoun Y (2010) Random distance dependent attachment as a model for neural network generation in the Caenorhabditis elegans, Bioinformatics, 10.1093/bioinformatics/btq015, 26:5, (647-652), Online publication date: 1-Mar-2010., Online publication date: 1-Mar-2010. Hasenstaub A, Otte S, Callaway E and Sejnowski T (2010) Metabolic cost as a unifying principle governing neuronal biophysics, Proceedings of the National Academy of Sciences, 10.1073/pnas.0914886107, 107:27, (12329-12334), Online publication date: 6-Jul-2010. Wen Q, Stepanyants A, Elston G, Grosberg A and Chklovskii D (2009) Maximization of the connectivity repertoire as a statistical principle governing the shapes of dendritic arbors, Proceedings of the National Academy of Sciences, 10.1073/pnas.0901530106, 106:30, (12536-12541), Online publication date: 28-Jul-2009. Chittka L and Niven J (2009) Are Bigger Brains Better?, Current Biology, 10.1016/j.cub.2009.08.023, 19:21, (R995-R1008), Online publication date: 1-Nov-2009. Graham D and Field D (2009) Natural Images: Coding Efficiency Encyclopedia of Neuroscience, 10.1016/B978-008045046-9.00212-6, (19-27), . Vasalou C, Herzog E and Henson M (2009) Small-World Network Models of Intercellular Coupling Predict Enhanced Synchronization in the Suprachiasmatic Nucleus, Journal of Biological Rhythms, 10.1177/0748730409333220, 24:3, (243-254), Online publication date: 1-Jun-2009. Zalesky A and Fornito A A DTI-Derived Measure of Cortico-Cortical Connectivity, IEEE Transactions on Medical Imaging, 10.1109/TMI.2008.2012113, 28:7, (1023-1036) Calcraft L, Adams R and Davey N (2008) Efficient connection strategies in 1D and 2D associative memory models with and without displaced connectivity, Biosystems, 10.1016/j.biosystems.2008.05.014, 94:1-2, (87-94), Online publication date: 1-Oct-2008. Niven J, Graham C and Burrows M (2008) Diversity and Evolution of the Insect Ventral Nerve Cord, Annual Review of Entomology, 10.1146/annurev.ento.52.110405.091322, 53:1, (253-271), Online publication date: 1-Jan-2008. Jehee J and Murre J (2008) The scalable mammalian brain: emergent distributions of glia and neurons, Biological Cybernetics, 10.1007/s00422-008-0228-y, 98:5, (439-445), Online publication date: 1-May-2008. Sakata S (2007) , The Brain & Neural Networks, 10.3902/jnns.14.205, 14:3, (205-217), . Changizi M (2007) Scaling the Brain and Its Connections Evolution of Nervous Systems, 10.1016/B0-12-370878-8/00061-6, (167-180), . Perez-Escudero A and de Polavieja G (2007) Optimally wired subnetwork determines neuroanatomy of Caenorhabditis elegans, Proceedings of the National Academy of Sciences, 10.1073/pnas.0703183104, 104:43, (17180-17185), Online publication date: 23-Oct-2007. Kaas J (2007) Reconstructing the Organization of Neocortex of the First Mammals and Subsequent Modifications Evolution of Nervous Systems, 10.1016/B0-12-370878-8/00057-4, (27-48), . Tereshko V (2007) Lateral and Elastic Interactions: Deriving One Form from Another Artificial Neural Networks – ICANN 2007, 10.1007/978-3-540-74695-9_7, (59-68), . Lyon D (2007) The Evolution of Visual Cortex and Visual Systems Evolution of Nervous Systems, 10.1016/B0-12-370878-8/00075-6, (267-306), . Changizi M (2006) The Optimal Human Ventral Stream from Estimates of the Complexity of Visual Objects, Biological Cybernetics, 10.1007/s00422-006-0056-x, 94:5, (415-426), Online publication date: 1-May-2006. Varshney L, Sjöström P and Chklovskii D (2006) Optimal Information Storage in Noisy Synapses under Resource Constraints, Neuron, 10.1016/j.neuron.2006.10.017, 52:3, (409-423), Online publication date: 1-Nov-2006. Graham D, Chandler D and Field D (2006) Can the theory of "whitening" explain the center-surround properties of retinal ganglion cell receptive fields?, Vision Research, 10.1016/j.visres.2006.03.008, 46:18, (2901-2913), Online publication date: 1-Sep-2006. Schmitt O, Eggers R and Modersitzki J (2005) Videomicroscopy, image processing, and analysis of whole histologic sections of the human brain, Microscopy Research and Technique, 10.1002/jemt.20163, 66:4, (203-218), Online publication date: 1-Mar-2005. Changizi M and He D (2005) Four correlates of complex behavioral networks: Differentiation, behavior, connectivity, and compartmentalization: Carving networks at their joints, Complexity, 10.1002/cplx.20085, 10:6, (13-40), Online publication date: 1-Jul-2005. Shefi O, Golebowicz S, Ben-Jacob E and Ayali A (2005) A two-phase growth strategy in cultured neuronal networks as reflected by the distribution of neurite branching angles, Journal of Neurobiology, 10.1002/neu.20108, 62:3, (361-368), Online publication date: 15-Feb-2005. da Fontoura Costa L and Diambra L (2005) Topographical maps as complex networks, Physical Review E, 10.1103/PhysRevE.71.021901, 71:2 Changizi M and Shimojo S (2005) Parcellation and Area-Area Connectivity as a Function of Neocortex Size, Brain, Behavior and Evolution, 10.1159/000085942, 66:2, (88-98), . Tereshko V (2005) Deriving Cortical Maps and Elastic Nets from Topology-Preserving Maps Computational Intelligence and Bioinspired Systems, 10.1007/11494669_40, (326-332), . Ross C, Henneberg M, Ravosa M and Richard S (2004) Curvilinear, geometric and phylogenetic modeling of basicranial flexion: is it adaptive, is it constrained?, Journal of Human Evolution, 10.1016/j.jhevol.2003.11.001, 46:2, (185-213), Online publication date: 1-Feb-2004. Chklovskii D (2004) Exact Solution for the Optimal Neuronal Layout Problem, Neural Computation, 10.1162/0899766041732422, 16:10, (2067-2078), Online publication date: 1-Oct-2004. Chklovskii D and Koulakov A (2004) MAPS IN THE BRAIN: What Can We Learn from Them?, Annual Review of Neuroscience, 10.1146/annurev.neuro.27.070203.144226, 27:1, (369-392), Online publication date: 21-Jul-2004. Chklovskii D (2004) Synaptic Connectivity and Neuronal Morphology, Neuron, 10.1016/j.neuron.2004.08.012, 43:5, (609-617), Online publication date: 1-Sep-2004. Douglas R and Martin K (2004) NEURONAL CIRCUITS OF THE NEOCORTEX, Annual Review of Neuroscience, 10.1146/annurev.neuro.27.070203.144152, 27:1, (419-451), Online publication date: 21-Jul-2004. Shefi O, Harel A, B. Chklovskii D, Ben-Jacob E and Ayali A (2004) Biophysical constraints on neuronal branching, Neurocomputing, 10.1016/j.neucom.2004.01.085, 58-60, (487-495), Online publication date: 1-Jun-2004. Schmitt O, Pakura M, Aach T, Hömke L, Böhme M, Bock S and Preuße S (2004) Analysis of nerve fibers and their distribution in histologic sections of the human brain, Microscopy Research and Technique, 10.1002/jemt.20033, 63:4, (220-243), Online publication date: 1-Mar-2004. Klyachko V and Stevens C (2003) Connectivity optimization and the positioning of cortical areas, Proceedings of the National Academy of Sciences, 10.1073/pnas.0932745100, 100:13, (7937-7941), Online publication date: 24-Jun-2003. Chklovskii D, Schikorski T and Stevens C (2002) Wiring Optimization in Cortical Circuits, Neuron, 10.1016/S0896-6273(02)00679-7, 34:3, (341-347), Online publication date: 1-Apr-2002. Koulakov A and Chklovskii D (2002) Direction of motion maps in the visual cortex: a wire length minimization approach, Neurocomputing, 10.1016/S0925-2312(02)00406-X, 44-46, (489-494), Online publication date: 1-Jun-2002. Karbowski J (2002) Optimal wiring in the cortex and neuronal degree of separation, Neurocomputing, 10.1016/S0925-2312(02)00486-1, 44-46, (875-879), Online publication date: 1-Jun-2002. Karbowski J (2001) Optimal Wiring Principle and Plateaus in the Degree of Separation for Cortical Neurons, Physical Review Letters, 10.1103/PhysRevLett.86.3674, 86:16, (3674-3677) Tereshko V Topological ordering in neural nets with weak nearest neighbour interactions International Joint Conference on Neural Networks (IJCNN'01), 10.1109/IJCNN.2001.939035, 0-7803-7044-9, (296-301) Koulakov A and Chklovskii D (2001) Orientation Preference Patterns in Mammalian Visual Cortex, Neuron, 10.1016/S0896-6273(01)00223-9, 29:2, (519-527), Online publication date: 1-Feb-2001. Tereshko V (2001) Topology-Preserving Elastic Nets Connectionist Models of Neurons, Learning Processes, and Artificial Intelligence, 10.1007/3-540-45720-8_66, (554-560), . Eriksson S, Rugg-Gunn F, Symms M, Barker G and Duncan J (2001) Diffusion tensor imaging in patients with epilepsy and malformations of cortical development, Brain, 10.1093/brain/124.3.617, 124:3, (617-626), Online publication date: 1-Mar-2001., Online publication date: 1-Mar-2001. McCarthy R (2001) Anthropoid cranial base architecture and scaling relationships, Journal of Human Evolution, 10.1006/jhev.2000.0446, 40:1, (41-66), Online publication date: 1-Jan-2001. Strogatz S (2001) Exploring complex networks, Nature, 10.1038/35065725, 410:6825, (268-276), Online publication date: 1-Mar-2001. Swindale N (2001) Keeping the Wires Short, Neuron, 10.1016/S0896-6273(01)00206-9, 29:2, (316-317), Online publication date: 1-Feb-2001. Chklovskii D (2000) Optimal Sizes of Dendritic and Axonal Arbors in a Topographic Projection, Journal of Neurophysiology, 10.1152/jn.2000.83.4.2113, 83:4, (2113-2119), Online publication date: 1-Apr-2000. Sporns O, Tononi G and Edelman G (2000) Connectivity and complexity: the relationship between neuroanatomy and brain dynamics, Neural Networks, 10.1016/S0893-6080(00)00053-8, 13:8-9, (909-922), Online publication date: 1-Nov-2000. Chklovskii D (2000) Binocular disparity can explain the orientation of ocular dominance stripes in primate primary visual area (V1), Vision Research, 10.1016/S0042-6989(00)00023-7, 40:13, (1765-1773), Online publication date: 1-Jun-2000. Lieberman D, Ross C and Ravosa M (2001) The primate cranial base: Ontogeny, function, and integration, American Journal of Physical Anthropology, 10.1002/1096-8644(2000)43:31+ 3.0.CO;2-I, 113:S31, (117-169), . Chklovskii D and Koulakov A (2000) A wire length minimization approach to ocular dominance patterns in mammalian visual cortex, Physica A: Statistical Mechanics and its Applications, 10.1016/S0378-4371(00)00219-3, 284:1-4, (318-334), Online publication date: 1-Sep-2000. Rapoport S (1999) How did the human brain evolve? a proposal based on new evidence from in vivo brain imaging during attention and ideation, Brain Research Bulletin, 10.1016/S0361-9230(99)00095-7, 50:3, (149-165), Online publication date: 1-Oct-1999. Ascoli G (1999) Progress and perspectives in computational neuroanatomy, The Anatomical Record, 10.1002/(SICI)1097-0185(19991215)257:6 3.0.CO;2-H, 257:6, (195-207), Online publication date: 15-Dec-1999. Cherniak C, Changizi M and Won Kang D (1999) Large-scale optimization of neuron arbors, Physical Review E, 10.1103/PhysRevE.59.6001, 59:5, (6001-6009) Goodhill G and Sejnowski T (1998) Objective Functions for Topography: A Comparison of Optimal Maps 4th Neural Computation and Psychology Workshop, London, 9–11 April 1997, 10.1007/978-1-4471-1546-5_7, (73-83), . Lennie P (2016) Single Units and Visual Cortical Organization, Perception, 10.1068/p270889, 27:8, (889-935), Online publication date: 1-Aug-1998. Goodhill G (1998) The influence of neural activity and intracortical connectivity on the periodicity of ocular dominance stripes, Network: Computation in Neural Systems, 10.1088/0954-898X/9/3/009, 9:3, (419-432), Online publication date: 1-Aug-1998. Manger P, Sum M, Szymanski M, Ridgway S and Krubitzer L (1998) Modular Subdivisions of Dolphin Insular Cortex: Does Evolutionary History Repeat Itself?, Journal of Cognitive Neuroscience, 10.1162/089892998562627, 10:2, (153-166), Online publication date: 1-Mar-1998. Goodhill G (2009) The influence of neural activity and intracortical connectivity on the periodicity of ocular dominance stripes, Network: Computation in Neural Systems, 10.1088/0954-898X_9_3_009, 9:3, (419-432), Online publication date: 1-Jan-1998. Tovée M (1998) The Visual System The Speed of Thought, 10.1007/978-3-662-10408-8_1, (1-26), . Weinberg R (1997) Are Topographic Maps Fundamental to Sensory Processing?, Brain Research Bulletin, 10.1016/S0361-9230(97)00095-6, 44:2, (113-116), . Essen D (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system, Nature, 10.1038/385313a0, 385:6614, (313-318), Online publication date: 1-Jan-1997. Windhorst U (1996) Specific Networks of the Cerebral Cortex: Functional Organization and Plasticity Comprehensive Human Physiology, 10.1007/978-3-642-60946-6_55, (1105-1136), . Swindale N (2009) The development of topography in the visual cortex: a review of models, Network: Computation in Neural Systems, 10.1088/0954-898X_7_2_002, 7:2, (161-247), Online publication date: 1-Jan-1996. Young M, Scannell J, O'Neill M, Hilgetag C, Burns G and Blakemore C (1997) Non-metric multidimensional scaling in the analysis of neuroanatomical connection data and the organization of the primate cortical visual system, Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 348:1325, (281-308), Online publication date: 30-May-1995. Murre J and Sturdy D (1995) The connectivity of the brain: multi-level quantitative analysis, Biological Cybernetics, 10.1007/BF00199545, 73:6, (529-545), Online publication date: 1-Nov-1995. Young M (1994) Visual Attention: Turn on, tune in and drop out, Current Biology, 10.1016/S0960-9822(00)00011-7, 4:1, (51-53), Online publication date: 1-Jan-1994. Mogi K On the schematic representation of binding in perception 1993 International Conference on Neural Networks (IJCNN-93-Nagoya, Japan), 10.1109/IJCNN.1993.716742, 0-7803-1421-2, (1151-1154) Tamori Y (1993) Theory of dendritic morphology, Physical Review E, 10.1103/PhysRevE.48.3124, 48:4, (3124-3129) Ruppin E, Schwartz E and Yeshurun Y (1993) Examining the volume efficiency of the cortical architecture in a multi-processor network model, Biological Cybernetics, 10.1007/BF00202570, 70:1, (89-94), Online publication date: 1-Nov-1993. Young M (1992) Objective analysis of the topological organization of the primate cortical visual system, Nature, 10.1038/358152a0, 358:6382, (152-155), Online publication date: 1-Jul-1992. Budd J, Kovács K, Ferecskó A, Buzás P, Eysel U, Kisvárday Z and Morrison A (2010) Neocortical Axon Arbors Trade-off Material and Conduction Delay Conservation, PLoS Computational Biology, 10.1371/journal.pcbi.1000711, 6:3, (e1000711) Rajtmajer S, Roy A, Albert R, Molenaar P and Hillary F (2015) A voxelwise approach to determine consensus regions-of-interest for the study of brain network plasticity, Frontiers in Neuroanatomy, 10.3389/fnana.2015.00097, 9 Barberis S (2018) Cajal's Law of Dynamic Polarization: Mechanism and Design, Philosophies, 10.3390/philosophies3020011, 3:2, (11) Chen Y, Wang S, Hilgetag C, Zhou C and Sporns O (2013) Trade-off between Multiple Constraints Enables Simultaneous Formation of Modules and Hubs in Neural Systems, PLoS Computational Biology, 10.1371/journal.pcbi.1002937, 9:3, (e1002937) Leibo J, Liao Q, Anselmi F, Poggio T and Kriegeskorte N (2015) The Invariance Hypothesis Implies Domain-Specific Regions in Visual Cortex, PLOS Computational Biology, 10.1371/journal.pcbi.1004390, 11:10, (e1004390) Wen Q, Chklovskii D and Friston K (2005) Segregation of the Brain into Gray and White Matter: A Design Minimizing Conduction Delays, PLoS Computational Biology, 10.1371/journal.pcbi.0010078, 1:7, (e78) Barton B and Brewer A (2017) Visual Field Map Clusters in High-Order Visual Processing: Organization of V3A/V3B and a New Cloverleaf Cluster in the Posterior Superior Temporal Sulcus, Frontiers in Integrative Neuroscience, 10.3389/fnint.2017.00004, 11 Laramée M and Boire D (2015) Visual cortical areas of the mouse: comparison of parcellation and network structure with primates, Frontiers in Neural Circuits, 10.3389/fncir.2014.00149, 8 Yu L, Shen Z, Wang C and Yu Y (2018) Efficient Coding and Energy Efficiency Are Promoted by Balanced Excitatory and Inhibitory Synaptic Currents in Neuronal Network, Frontiers in Cellular Neuroscience, 10.3389/fncel.2018.00123, 12 Wagener R, Witte M, Guy J, Mingo-Moreno N, Kügler S and Staiger J (2015) Thalamocortical Connections Drive Intracortical Activation of Functional Columns in the Mislaminated Reeler Somatosensory Cortex , Cerebral Cortex, 10.1093/cercor/bhv257, (bhv257) This Issue22 August 1991Volume 245Issue 1313 Article InformationDOI:https://doi.org/10.1098/rspb.1991.0102PubMed:1682939Published by:Royal SocietyPrint ISSN:0962-8452Online ISSN:1471-2954History: Manuscript received22/05/1991Manuscript accepted29/05/1991Published online01/01/1997Published in print22/08/1991 License:Scanned images copyright © 2017, Royal Society Citations and impact Large datasets are available through Proceedings B's partnership with Dryad

Referência(s)