Rich-club organization in effective connectivity among cortical neurons

Journal of Neuroscience

Volumn 36, Issue 3, 2016, Pages 655-669

  Nigam, Sunny ^a   Shimono, Masanori ^a   Ito, Shinya ^b   Yeh, Fang Chin ^c   Timme, Nicholas ^a   Myroshnychenko, Maxym ^a   Lapish, Christopher C ^d   Tosi, Zachary ^e   Hottowy, Pawel ^f   Smith, Wesley C ^g   Masmanidis, Sotiris C ^h   Litke, Alan M ^c   Sporns, Olaf ^a   Beggs, John M ^a  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA SANTA CRUZ   (United States)

^c DUKE NUS MEDICAL SCHOOL   (Singapore)

^d INDIANA UNIVERSITY   (United States)

^e Department of Geography   (United States)

^f AGH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Poland)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Effective connectivity; Information transfer; Microcircuits; Rich club; Transfer entropy

Indexed keywords

ALGORITHM; ARTICLE; BRAIN CELL; CRANIOTOMY; DYNAMICS; EFFECTIVE CONNECTIVITY; ENTROPY; FALSE POSITIVE RESULT; HUMAN; INFORMATION PROCESSING; INFORMATION TRANSFER; LEARNING; MATHEMATICAL MODEL; MEMORY; NERVE CELL NETWORK; NERVOUS SYSTEM FUNCTION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SOMATOSENSORY CORTEX; SPIKE; SYNAPSE; TASK PERFORMANCE; ANIMAL; C57BL MOUSE; CYTOLOGY; MOUSE; NERVE CELL; NEWBORN; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY;

ANIMALS; ANIMALS, NEWBORN; MICE; MICE, INBRED C57BL; NERVE NET; NEURONS; ORGAN CULTURE TECHNIQUES; SOMATOSENSORY CORTEX;

EID: 84955071899     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2177-15.2016     Document Type: Article

References (108)

1. Alivisatos AP, Chun M, Church GM, Deisseroth K, Donoghue JP, Greenspan RJ, McEuen PL, Roukes ML, Sejnowski TJ, Weiss PS, Yuste R (2013) The brain activity map. Science 339:1284-1285. CrossRef Medline
2. Alstott J, Panzarasa P, Rubinov M, Bullmore ET, Ve´rtes PE (2014) A unifying framework for measuring weighted rich clubs. Sci Rep 4:7258. CrossRef Medline
3. Baggio HC, Segura B, Junque C, de Reus MA, Sala-Llonch R, Van den Heuvel MP (2015) Rich club organization and cognitive performance in healthy older participants. J Cogn Neurosci 27:1801-1810. CrossRef Medline
4. Baker RE, Van Pelt J (1997) Cocultured, but not isolated, cortical explants display normal dendritic development: a long-term quantitative study. Brain Res Dev Brain Res 98:21-29. CrossRef Medline
5. Baker RE, Corner MA, van Pelt J (2006) Spontaneous neuronal discharge patterns in developing organotypic mega-co-cultures of neonatal rat cerebral cortex. Brain Res 1101:29-35. CrossRef Medline
6. Ball G, Aljabar P, Zebari S, Tusor N, Arichi T, Merchant N, Robinson EC, Ogundipe E, Rueckert D, Edwards AD, Counsell SJ (2014) Rich-club organization of the newborn human brain. Proc Natl Acad Sci U S A 111:7456-7461. CrossRef Medline
7. Barrat A, Barthelemy M, Vespignani A (2008) Dynamical processes on complex networks. Cambridge, UK: Cambridge UP.
8. Bartho´ P, Hirase H, Monconduit L, Zugaro M, Harris KD, Buzsáki G (2004) Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J Neurophysiol 92:600-608. CrossRef Medline
9. Batista CA, Lameu EL, Batista AM, Lopes SR, Pereira T, Zamora-López G, Kurths J, Viana RL (2012) Phase synchronization of bursting neurons in clustered small-world networks. Phys Rev E Stat Nonlin Soft Matter Phys 86:016211. CrossRef Medline
10. Beggs JM, Plenz D (2003) Neuronal avalanches in neocortical circuits. J Neurosci 23:11167-11177. Medline
11. Beggs JM, Plenz D (2004) Neuronal avalanches are diverse and precise activity patterns that are stable for many hours in cortical slice cultures. J Neurosci 24:5216-5229. CrossRef Medline
12. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 1165-1188.
13. Bock DD, Lee WC, Kerlin AM, Andermann ML, Hood G, Wetzel AW, Yurgenson S, Soucy ER, Kim HS, Reid RC (2011) Network anatomy and in vivo physiology of visual cortical neurons. Nature 471:177-182. CrossRef Medline
14. Bolz J, Novak N, Götz M, Bonhoeffer T (1990) Formation of target-specific neuronal projections in organotypic slice cultures from rat visual cortex. Nature 346:359-362. CrossRef Medline
15. Bonifazi P, Goldin M, Picardo MA, Jorquera I, Cattani A, Bianconi G, Represa A, Ben-Ari Y, Cossart R (2009) GABAergic hub neurons orchestrate synchrony in developing hippocampal networks. Science 326:1419-1424. CrossRef Medline
16. Brandes U (2001) A faster algorithm for betweenness centrality. J Math Sociol 25:163-177. CrossRef
17. Brovelli A, Ding M, Ledberg A, Chen Y, Nakamura R, Bressler SL (2004) Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. Proc Natl Acad Sci U S A 101:9849-9854. CrossRef Medline
18. Buonomano DV (2003) Timing of neural responses in cortical organotypic slices. Proc Natl Acad Sci U S A 100:4897-4902. CrossRef Medline
19. Buzsa´ki G, Mizuseki K (2014) The log-dynamic brain: how skewed distributions affect network operations. Nat Rev Neurosci 15:264-278. CrossRef Medline
20. Caeser M, Bonhoeffer T, Bolz J (1989) Cellular organization and development of slice cultures from rat visual cortex. Exp Brain Res 77:234-244. CrossRef Medline
21. Chiappalone M, Bove M, Vato A, Tedesco M, Martinoia S (2006) Dissociated cortical networks show spontaneously correlated activity patterns during in vitro development. Brain Res 1093:41-53. CrossRef Medline
22. Colizza V, Flammini A, Serrano MA, Vespignani A (2006) Detecting richclub ordering in complex networks. Nat Phys 2:110-115. CrossRef
23. Collin G, Sporns O, Mandl RC, van den Heuvel MP (2014) Structural and functional aspects relating to cost and benefit of rich club organization in the human cerebral cortex. Cereb Cortex 24:2258-2267. CrossRef Medline
24. Cossell L, Iacaruso MF, Muir DR, Houlton R, Sader EN, Ko H, Hofer SB, Mr ic-Flogel TD (2015) Functional organization of excitatory synaptic strength in primary visual cortex. Nature 518:399-403. CrossRef Medline
25. Crossley NA, Mechelli A, Vértes PE, Winton-Brown TT, Patel AX, Ginestet CE, McGuire P, Bullmore ET (2013) Cognitive relevance of the commu-nity structure of the human brain functional coactivation network. Proc Natl Acad Sci U S A 110:11583-11588. CrossRef Medline
26. de Reus MA, van den Heuvel MP (2013) Rich club organization and intermodule communication in the cat connectome. J Neurosci 33:12929-12939. CrossRef Medline
27. Eagle N, Macy M, Claxton R (2010) Network diversity and economic development. Science 328:1029-1031. CrossRef Medline
28. Field GD, Gauthier JL, Sher A, Greschner M, Machado TA, Jepson LH, Shlens J, Gunning DE, Mathieson K, Dabrowski W, Paninski L, Litke AM, Chichilnisky EJ (2010) Functional connectivity in the retina at the resolution of photoreceptors. Nature 467:673-677. CrossRef Medline
29. Freeman LC (1979) Centrality in social networks conceptual clarification. Soc Networks 1:215-239.
30. Friedman N, Ito S, Brinkman BA, Shimono M, DeVille RE, Dahmen KA, Beggs JM, Butler TC (2012) Universal critical dynamics in high resolution neuronal avalanche data. Phys Rev Lett 108:208102. CrossRef Medline
31. Garofalo M, Nieus T, Massobrio P, Martinoia S (2009) Evaluation of the performance of information theory-based methods and cross-correlation to estimate the functional connectivity in cortical networks. PLoS One 4:e6482. CrossRef Medline
32. Gerhard F, Pipa G, Lima B, Neuenschwander S, Gerstner W (2011) Extraction of network topology from multi-electrode recordings: is there a small-world effect? Front Comput Neurosci 5:4. CrossRef Medline
33. Gireesh ED, Plenz D (2008) Neuronal avalanches organize as nested thetaand beta/gamma-oscillations during development of cortical layer 2/3. Proc Natl Acad Sci U S A 105:7576-7581. CrossRef Medline
34. Goldman-Rakic PS (1995) Cellular basis of working memory. Neuron 14: 477-485. CrossRef Medline
35. Gómez-Gardeñes J, Zamora-Ló pez G, Moreno Y, Arenas A (2010) From modular to centralized organization of synchronization in functional areas of the cat cerebral cortex. PLoS One 5:e12313. CrossRef Medline
36. Götz M, Bolz J (1992) Formation and preservation of cortical layers in slice cultures. J Neurobiol 23:783-802. CrossRef Medline
37. Gourévitch B, Eggermont JJ (2007) Evaluating information transfer between auditory cortical neurons. J Neurophysiol 97:2533-2543. CrossRef Medline
38. Harriger L, van den Heuvel MP, Sporns O (2012) Rich club organization of macaque cerebral cortex and its role in network communication. PLoS One 7:e46497. CrossRef Medline
39. Harris-White ME, Zanotti SA, Frautschy SA, Charles AC (1998) Spiral intercellular calcium waves in hippocampal slice cultures. J Neurophysiol 79:1045-1052. Medline
40. Helmstaedter M, Briggman KL, Turaga SC, Jain V, Seung HS, Denk W (2013) Connectomic reconstruction of the inner plexiform layer in the mouse retina. Nature 500:168-174. CrossRef Medline
41. Hlaváčková-Schindler K, Palušm, Vejmelka M, Bhattacharya J (2007) Causality detection based on information-theoretic approaches in time series analysis. Phys Rep 441:1-46. CrossRef
42. Hromádka T, Deweese MR, Zador AM (2008) Sparse representation of sounds in the unanesthetized auditory cortex. PLoS Biol 6:e16. CrossRef Medline
43. Ikegaya Y, Aaron G, Cossart R, Aronov D, Lampl I, Ferster D, Yuste R (2004) Synfire chains and cortical songs: temporal modules of cortical activity. Science 304:559-564. CrossRef Medline
44. Ito S, Hansen ME, Heiland R, Lumsdaine A, Litke AM, Beggs JM (2011) Extending transfer entropy improves identification of effective connectivity in a spiking cortical network model. PLoS One 6:e27431. CrossRef Medline
45. Ito S, Yeh FC, Hiolski E, Rydygier P, Gunning DE, Hottowy P, Timme N, Litke AM, Beggs JM (2014) Large-scale, high-resolution multielectrodearray recording depicts functional network differences of cortical and hippocampal cultures. PLoS One 9:e105324. CrossRef Medline
46. Izhikevich EM (2003) Simple model of spiking neurons. IEEE Trans Neural Netw 14:1569-1572. CrossRef Medline
47. Izquierdo EJ, Beer RD (2013) Connecting a connectome to behavior: an ensemble of neuroanatomical models of C. elegans klinotaxis. PLoS Comput Biol 9:e1002890. CrossRef Medline
48. Jarrell TA, Wang Y, Bloniarz AE, Brittin CA, Xu M, Thomson JN, Albertson DG, Hall DH, Emmons SW (2012) The connectome of a decisionmaking neural network. Science 337:437-444. CrossRef Medline
49. Jimbo Y, Tateno T, Robinson HP (1999) Simultaneous induction of pathwayspecific potentiation and depression in networks of cortical neurons. Biophys J 76:670-678. CrossRef Medline
50. Johnson HA, Buonomano DV (2007) Development and plasticity of spontaneous activity and Up states in cortical organotypic slices. J Neurosci 27:5915-5925. CrossRef Medline
51. Johnson LA, Euston DR, Tatsuno M, McNaughton BL (2010) Stored-trace reactivation in rat prefrontal cortex is correlated with down-to-up state fluctuation density. J Neurosci 30:2650-2661. CrossRef Medline
52. Juergens E, Eckhorn R (1997) Parallel processing by a homogeneous group of coupled model neurons can enhance, reduce and generate signal correlations. Biol Cybern 76:217-227. CrossRef Medline
53. Klinshov VV, Teramae JN, Nekorkin VI, Fukai T (2014) Dense neuron clustering explains connectivity statistics in cortical microcircuits. PLoS One 9:e94292. CrossRef Medline
54. Klostermann O, Wahle P (1999) Patterns of spontaneous activity and morphology of interneuron types in organotypic cortex and thalamus—cortex cultures. Neuroscience 92:1243-1259. CrossRef Medline
55. Koulakov AA, Hromádka T, Zador AM (2009) Correlated connectivity and the distribution of firing rates in the neocortex. J Neurosci 29:3685-3694. CrossRef Medline
56. Larremore DB, Shew WL, Restrepo JG (2011) Predicting criticality and dynamic range in complex networks: effects of topology. Phys Rev Lett 106:58101. CrossRef
57. Larsch J, Ventimiglia D, Bargmann CI, Albrecht DR (2013) Highthroughput imaging of neuronal activity in Caenorhabditis elegans. Proc Natl Acad Sci U S A 110:E4266-E4273. CrossRef Medline
58. Leiman AL, Seil FJ (1986) Influence of subcortical neurons on the functional development of cerebral neocortex in tissue culture. Brain Res 365:205-210. CrossRef Medline
59. Lindner M, Vicente R, Priesemann V, Wibral M (2011) TRENTOOL: a Matlab open source toolbox to analyse information flow in time series data with transfer entropy. BMC Neurosci 12:119. CrossRef Medline
60. Litke A, Bezayiff N, Chichilnisky E, Cunningham W, Dabrowski W, Grillo A, Grivich M, Grybos P, Hottowy P, Kachiguine S (2004) What does the eye tell the brain? Development of a system for the large-scale recording of retinal output activity. IEEE Trans Nucl Sci 51:1434-1440. CrossRef
61. Lungarella M, Pitti A, Kuniyoshi Y (2007) Information transfer at multiple scales. Phys Rev E Stat Nonlin Soft Matter Phys 76:056117. CrossRef Medline
62. Maass W, Natschläger T, Markram H (2002) Real-time computing without stable states: a new framework for neural computation based on perturbations. Neural Comput 14:2531-2560. CrossRef Medline
63. Mason A, Nicoll A, Stratford K (1991) Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro. J Neurosci 11:72-84. Medline
64. Montalto A, Faes L, Marinazzo D (2014) MuTE: a MATLAB toolbox to compare established and novel estimators of the multivariate transfer entropy. PLoS One 9:e109462. CrossRef Medline
65. Nakhnikian A, Rebec GV, Grasse LM, Dwiel LL, Shimono M, Beggs JM (2014) Behavior modulates effective connectivity between cortex and striatum. PLoS One 9:e89443. CrossRef Medline
66. Okatan M, Wilson MA, Brown EN (2005) Analyzing functional connectivity using a network likelihood model of ensemble neural spiking activity. Neural Comput 17:1927-1961. CrossRef Medline
67. Opsahl T, Colizza V, Panzarasa P, Ramasco JJ (2008) Prominence and control: the weighted rich-club effect. Phys Rev Lett 101:168702. CrossRef Medline
68. Orlandi JG, Stetter O, Soriano J, Geisel T, Battaglia D (2014) Transfer Entropy reconstruction and labeling of neuronal connections from simulated calcium imaging. PLoS One 9:e98842. CrossRef Medline
69. Panzeri S, Petersen RS, Schultz SR, Lebedev M, Diamond ME (2001) The role of spike timing in the coding of stimulus location in rat somatosensory cortex. Neuron 29:769-777. CrossRef Medline
70. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. San Diego: Academic.
71. Perin R, Berger TK, Markram H (2011) A synaptic organizing principle for cortical neuronal groups. Proc Natl Acad Sci U S A 108:5419-5424. CrossRef Medline
72. Petrusca D, Grivich MI, Sher A, Field GD, Gauthier JL, Greschner M, Shlens J, Chichilnisky EJ, Litke AM (2007) Identification and characterization of a Y-like primate retinal ganglion cell type. J Neurosci 27:11019-11027. CrossRef Medline
73. Pillow JW, Shlens J, Paninski L, Sher A, Litke AM, Chichilnisky EJ, Simoncelli EP (2008) Spatio-temporal correlations and visual signalling in a complete neuronal population. Nature 454:995-999. CrossRef Medline
74. Plenz D, Aertsen A (1996) Neural dynamics in cortex-striatum co-cultures— II. Spatiotemporal characteristics of neuronal activity. Neuroscience 70:893-924. CrossRef Medline
75. Restrepo JG, Ott E, Hunt BR (2005) Onset of synchronization in large networks of coupled oscillators. Phys Rev E Stat Nonlin Soft Matter Phys 71:036151. CrossRef Medline
76. Restrepo JG, Ott E, Hunt BR (2006) Characterizing the dynamical importance of network nodes and links. Phys Rev Lett 97:094102. CrossRef Medline
77. Restrepo JG, Ott E, Hunt BR (2008) Weighted percolation on directed networks. Phys Rev Lett 100:58701. CrossRef
78. Roxin A, Brunel N, Hansel D, Mongillo G, van Vreeswijk C (2011) On the distribution of firing rates in networks of cortical neurons. J Neurosci 31:16217-16226. CrossRef Medline
79. Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52:1059-1069. CrossRef Medline
80. Schreiber T (2000) Measuring information transfer. Phys Rev Lett 85:461-464. CrossRef Medline
81. Schroeter MS, Charlesworth P, Kitzbichler MG, Paulsen O, Bullmore ET (2015) Emergence of rich-club topology and coordinated dynamics in development of hippocampal functional networks in vitro. J Neurosci 35:5459-5470. CrossRef Medline
82. Senden M, Deco G, de Reus MA, Goebel R, van den Heuvel MP (2014) Rich club organization supports a diverse set of functional network configurations. Neuroimage 96:174-182. CrossRef Medline
83. Shimono M, Beggs JM (2015) Functional clusters, hubs, and communities in the cortical microconnectome. Cereb Cortex 25:3743-3757. CrossRef Medline
84. Shlens J, Field GD, Gauthier JL, Grivich MI, Petrusca D, Sher A, Litke AM, Chichilnisky EJ (2006) The structure of multi-neuron firing patterns in primate retina. J Neurosci 26:8254-8266. CrossRef Medline
85. Shobe JL, Claar LD, Parhami S, Bakhurin KI, Masmanidis SC (2015) Brain activity mapping at multiple scales with silicon microprobes containing 1024 electrodes. J Neurophysiol 114:2043-2052. CrossRef Medline
86. Sirota A, Montgomery S, Fujisawa S, Isomura Y, Zugaro M, Buzsáki G (2008) Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60:683-697. CrossRef Medline
87. Song S, Sjo¨stro¨m PJ, Reigl M, Nelson S, Chklovskii DB (2005) Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol 3:e68. CrossRef Medline
88. Sporns O, Tononi G, Kötter R (2005) The human connectome: a structural description of the human brain. PLoS Comput Biol 1:e42. CrossRef Medline
89. Staal JA, Alexander SR, Liu Y, Dickson TD, Vickers JC (2011) Characterization of cortical neuronal and glial alterations during culture of organotypic whole brain slices from neonatal and mature mice. PLoS One 6:e22040. CrossRef Medline
90. Stetter O, Battaglia D, Soriano J, Geisel T (2012) Model-free reconstruction of excitatory neuronal connectivity from calcium imaging signals. PLoS Comput Biol 8:e1002653. CrossRef Medline
91. Swadlow HA (1994) Efferent neurons and suspected interneurons in motor cortex of the awake rabbit: axonal properties, sensory receptive fields, and subthreshold synaptic inputs. J Neurophysiol 71:437-453. Medline
92. Takemura SY, Bharioke A, Lu Z, Nern A, Vitaladevuni S, Rivlin PK, Katz WT, Olbris DJ, Plaza SM, Winston P, Zhao T, Horne JA, Fetter RD, Takemura S, Blazek K, Chang LA, Ogundeyi O, Saunders MA, Shapiro V, Sigmund C, et al. (2013) A visual motion detection circuit suggested by Drosophila connectomics. Nature 500:175-181. CrossRef Medline
93. Tang A, Jackson D, Hobbs J, Chen W, Smith JL, Patel H, Prieto A, Petrusca D, Grivich MI, Sher A, Hottowy P, Dabrowski W, Litke AM, Beggs JM (2008) A maximum entropy model applied to spatial and temporal correlations from cortical networks in vitro. J Neurosci 28:505-518. CrossRef Medline
94. Terrell GR, Scott DW (1985) Oversmoothed nonparametric density estimates. J Am Stat Assoc 80:209-214.
95. Teramae JN, Tsubo Y, Fukai T (2012) Optimal spike-based communication in excitable networks with strong-sparse and weak-dense links. Sci Rep 2:485. CrossRef Medline
96. Timme N, Ito S, Myroshnychenko M, Yeh FC, Hiolski E, Hottowy P, Beggs JM (2014) Multiplex networks of cortical and hippocampal neurons revealed at different timescales. PLoS One 9:e115764. CrossRef Medline
97. Towlson EK, Ve´rtes PE, Ahnert SE, Schafer WR, Bullmore ET (2013) The rich club of the C. elegans neuronal connectome. J Neurosci 33:6380-6387. CrossRef Medline
98. van den Heuvel MP, Sporns O (2011) Rich-club organization of the human connectome. J Neurosci 31:15775-15786. CrossRef Medline
99. van den Heuvel MP, Sporns O, Collin G, Scheewe T, Mandl RC, Cahn W, Goñi J, Hulshoff Pol HE, Kahn RS (2013) Abnormal rich club organization and functional brain dynamics in schizophrenia. JAMA Psychiatry 70:783-792. CrossRef Medline
100. Vicente R, Wibral M, Lindner M, Pipa G (2011) Transfer entropy—a model-free measure of effective connectivity for the neurosciences. J Comput Neurosci 30:45-67. CrossRef Medline
101. Watanabe T (2013) Rich-club network topology to minimize synchronization cost due to phase difference among frequency-synchronized oscillators. Physica A Stat Mech Appl 392:1246-1255. CrossRef
102. Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442-446. CrossRef Medline
103. White JG, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314:1-340. CrossRef Medline
104. Wibral M, Lizier JT, Priesemann V (2015) Bits from brains for biologicallyinspired computing. Front Robot AI 2:5. CrossRef
105. Wollstadt P, Martínez-Zarzuela M, Vicente R, Díaz-Pernas FJ, Wibral M (2014) Efficient transfer entropy analysis of non-stationary neural time series. PLoS One 9:e102833. CrossRef Medline
106. Yassin L, Benedetti BL, Jouhanneau JS, Wen JA, Poulet JF, Barth AL (2010) An embedded subnetwork of highly active neurons in the neocortex. Neuron 68:1043-1050. CrossRef Medline
107. Yatsenko D, Josic´ K, Ecker AS, Froudarakis E, Cotton RJ, Tolias AS, Pillow JW (2015) Improved estimation and interpretation of correlations in neural circuits. PLoS Comput Biol 11:e1004083-e1004083. CrossRef Medline
108. Zhou S, Mondragón RJ (2004) The rich-club phenomenon in the Internet topology. Commun Lett IEEE 8:180-182. CrossRef