Functional brain network efficiency predicts intelligence

Human Brain Mapping

Volumn 33, Issue 6, 2012, Pages 1393-1406

  Langer, Nicolas ^a   Pedroni, Andreas ^a,b   Gianotti, Lorena R R ^b   Hänggi, Jürgen ^a   Knoch, Daria ^b   Jäncke, Lutz ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

EEG; Intelligence; Neuroscience; Small world network

Indexed keywords

ADULT; ARTICLE; ELECTROENCEPHALOGRAPHY; FUNCTIONAL BRAIN NETWORK; HUMAN; HUMAN EXPERIMENT; INTELLECT; INTELLIGENCE; MALE; NERVE CELL NETWORK; NORMAL HUMAN; PARIETAL CORTEX; PRIORITY JOURNAL; PSYCHOMETRY;

ADULT; BRAIN; BRAIN MAPPING; ELECTROENCEPHALOGRAPHY; HUMANS; INTELLIGENCE; INTELLIGENCE TESTS; MALE; MODELS, NEUROLOGICAL; NERVE NET; PREDICTIVE VALUE OF TESTS;

EID: 84860840927     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.21297     Document Type: Article

References (99)

1. Achard S, Bullmore E (2007): Efficiency and cost of economical brain functional networks. PLoS Comput Biol 3: e17.
2. Ambrosius U, Lietzenmaier S, Wehrle R, Wichniak A, Kalus S, Winkelmann J, Bettecken T, Holsboer F, Yassouridis A, Friess E (2008): Heritability of sleep electroencephalogram. Biol Psychiatry 64: 344-348.
3. Andersen RA, Cui H (2009): Intention, action planning, and decision making in parietal-frontal circuits. Neuron 63: 568-583.
4. Angelakis E, Lubar JF, Stathopoulou S (2004): Electroencephalographic peak alpha frequency correlates of cognitive traits. Neurosci Lett 371: 60-63.
5. Annett M (1970): A classification of hand preference by association analysis. Br J Psychol 61: 303-321.
6. Anokhin AP, Müller V, Lindenberger U, Heath AC, Myers E (2006): Genetic influences on dynamic complexity of brain oscillations. Neurosci Lett 397: 93-98.
7. Babiloni C, Binetti G, Cassetta E, Cerboneschi D, Dal Forno G, Del Percio C, Ferreri F, Ferri R, Lanuzza B, Miniussi C, Moretti DV, Nobili F, Pascual-Marqui RD, Rodriguez G, Romani GL, Salinari S, Tecchio F, Vitali P, Zanetti O, Zappasodi F, Rossini PM (2004): Mapping distributed sources of cortical rhythms in mild Alzheimer's disease. A multicentric EEG study. Neuroimage 22: 57-67.
8. Barrat A, Barthelemy M, Pastor-Satorras R, Vespignani A (2004): The architecture of complex weighted networks. Proc Natl Acad Sci USA 101: 3747-3752.
9. Bartolomei F, Bosma I, Klein M, Baayen JC, Reijneveld JC, Postma TJ, Heimans JJ, van Dijk BW, de Munck JC, de Jongh A, Cover KS, Stam CJ (2006): Disturbed functional connectivity in brain tumour patients: Evaluation by graph analysis of synchronization matrices. Clin Neurophysiol 117: 2039-2049.
10. Birbaumer N, Elbert T, Canavan AG, Rockstroh B (1990): Slow potentials of the cerebral cortex and behavior. Physiol Rev 70: 1-41.
11. Brett M, Johnsrude IS, Owen AM (2002): The problem of functional localization in the human brain. Nat Rev Neurosci 3: 243-249.
12. Brodmann K. (1909). Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Leipzig: Barth.
13. Bullmore E, Sporns O (2009): Complex brain networks: Graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10: 186-198.
14. de Haan W, Pijnenburg YA, Strijers RL, van der Made Y, van der Flier WM, Scheltens P, Stam CJ (2009): Functional neural network analysis in frontotemporal dementia and Alzheimer's disease using EEG and graph theory. BMC Neurosci 10: 101.
15. De Vico Fallani F, Maglione A, Babiloni F, Mattia D, Astolfi L, Vecchiato G, De Rinaldis A, Salinari S, Pachou E, Micheloyannis S (2010): Cortical network analysis in patients affected by schizophrenia. Brain Topogr 23: 214-220.
16. Deary IJ, Penke L, Johnson W (2010): The neuroscience of human intelligence differences. Nat Rev Neurosci 11: 201-211.
17. Doppelmayr M, Klimesch W, Stadler W, Pöllhuber D, Heine C (2002): EEG alpha power and intelligence. Intelligence 30: 289-302.
18. Eguíluz VM, Chialvo DR, Cecchi GA, Baliki M (2005): Apkarian AVScale-free brain functional networks. Phys Rev Lett 94: 018102.
19. Evans AC, Collins DL, Mills SR, Brwon ED, Kelly RL, Peters TM (1993): 3d statistical neuroanatomical models from 305 MRI volumes. In: Processings IEEE Nuclear Science Symposium and Medical Imaging Conference. San Francisco, CA. pp 1813-1817.
20. Fisher RA (1935). The Design of Experiment. New York: Hafner.
21. Freeman LC (1978): Centrality in social networks: Conceptual clarification. Soc Netw 1: 215-239.
22. Fuchs M, Kastner J, Wagner M, Hawes S, Ebersole JS (2002): A standardized boundary element method volume conductor model. Clin Neurophysiol 113: 702-712.
23. Geweke J (1982): Measurement of linear-dependence and feedback between multiple time-series. J Am Stat Assoc 77: 304-313.
24. Golubeva EA (1980): Individual Characteristics of Human Memory: A Psychophysiological Study. Pedagogika, Moscow.
25. Gray JR, Thompson PM (2004): Neurobiology of intelligence: Science and ethics. Nat Rev Neurosci 5: 471-482.
26. Gray JR, Chabris CF, Braver TS (2003): Neural mechanisms of general fluid intelligence. Nat Neurosci 6: 316-322.
27. Haier RJ, White NS, Alkire MT (2003): Individual differences in general intelligence correlate with brain function during nonreasoning tasks. Intelligence 31: 429-441.
28. Herculano-Houzel S (2009): The human brain in numbers: A linearly scaled-up primate brain. Front Hum Neurosci 3: 31.
29. Holm S (1979): A simple sequentially rejective multiple test procedure. Scand J Stat 6: 65-70.
30. Humphries MD, Gurney K (2008): Network 'small-world-ness': A quantitative method for determining canonical network equivalence. PLoS One 3: e0002051.
31. Humphries MD, Gurney K, Prescott TJ (2006): The brainstem reticular formation is a small-world, not scale-free, network. Proc Biol Sci 273: 503-511.
32. Ishai A, Ungerleider LG, Haxby JV (2000): Distributed neural systems for the generation of visual images. Neuron 28: 979-990.
33. Ivonin AA, Tsitseroshin MN, Pogosyan AA, Shuvaev VT (2004): Genetic determination of neurophysiological mechanisms of cortical-subcortical integration of bioelectrical brain activity. Neurosci Behav Physiol 34: 369-378.
34. Jann K, Koenig T, Dierks T, Boesch C, Federspiel A (2010): Association of individual resting state EEG alpha frequency and cerebral blood flow. Neuroimage 51: 365-372.
35. Jausovec N, Jausovec K (2000): Differences in resting EEG related to ability. Brain Topogr 12: 229-240.
36. Jung RE, Haier RJ (2007): The Parieto-Frontal Integration Theory (P-FIT) of intelligence: Converging neuroimaging evidence. Behav Brain Sci 30: 135-154; discussion 154-187.
37. Jurcak V, Tsuzuki D, Dan I (2007): 10/20, 10/10, and 10/5 systems revisited: Their validity as relative head-surface-based positioning systems. Neuroimage 34: 1600-1611.
38. Kaiser M, Hilgetag CC (2006): Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput Biol 2: e95.
39. Klimesch W (1999): EEG alpha and theta oscillations reflect cognitive and memory performance: A review and analysis. Brain Res Brain Res Rev 29: 169-195.
40. Kondacs A, Szabó M (1999): Long-term intra-individual variability of the background EEG in normals. Clin Neurophysiol 110: 1708-1716.
41. Kubicki S, Herrmann WM, Fichte K, Freund G (1979): Reflections on the topics: EEG frequency bands and regulation of vigilance. Pharmakopsychiatr Neuropsychopharmakol 12: 237-245.
42. Lancaster JL, Woldorff MG, Parsons LM, Liotti M, Freitas ES, Rainey L, Kochunov PV, Nickerson D, Mikiten SA, Fox PT (2000): Automated Talairach Atlas labels for functional brain mapping. Hum Brain Mapp 10: 120-131.
43. Langer N, Beeli G, Jancke L (2010): When the sun prickles your nose: An EEG study identifying neural bases of photic sneezing. PLoS One 5: e9208.
44. Laufs H (2008): Endogenous brain oscillations and related networks detected by surface EEG-combined fMRI. Hum Brain Mapp 29: 762-769.
45. Lehmann D, Faber PL, Gianotti LR, Kochi K, Pascual-Marqui RD (2006): Coherence and phase locking in the scalp EEG and between LORETA model sources, and microstates as putative mechanisms of brain temporo-spatial functional organization. J Physiol Paris 99: 29-36.
46. Li Y, Liu Y, Li J, Qin W, Li K, Yu C, Jiang T (2009): Brain anatomical network and intelligence. PLoS Comput Biol 5: e1000395.
47. Linkenkaer-Hansen K, Smit DJ, Barkil A, van Beijsterveldt TE, Brussaard AB, Boomsma DI, van Ooyen A, de Geus EJ (2007): Genetic contributions to long-range temporal correlations in ongoing oscillations. J Neurosci 27: 13882-13889.
48. Lisman JE, Idiart MA (1995): Storage of 7 +/- 2 short-term memories in oscillatory subcycles. Science 267: 1512-1515.
49. Martin A, Wiggs CL, Ungerleider LG, Haxby JV (1996): Neural correlates of category-specific knowledge. Nature 379: 649-652.
50. Mazziotta J, Toga A, Evans A, Fox P, Lancaster J, Zilles K, Woods R, Paus T, Simpson G, Pike B, Holmes C, Collins L, Thompson P, MacDonald D, Iacoboni M, Schormann T, Amunts K, Palomero-Gallagher N, Geyer S, Parsons L, Narr K, Kabani N, Le Goualher G, Boomsma D, Cannon T, Kawashima R, Mazoyer B (2001): A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos Trans R Soc B Biol Sci 356: 1293-1322.
51. Michel CM, Koenig T, Brandeis D, Gianotti LR, Wackermann J (2009). Electrical Neuroimaging. Cambridge: Cambridge University Press.
52. Micheloyannis S, Pachou E, Stam CJ, Vourkas M, Erimaki S, Tsirka V (2006): Using graph theoretical analysis of multi channel EEG to evaluate the neural efficiency hypothesis. Neurosci Lett 402: 273-277.
53. Micheloyannis S, Vourkas M, Tsirka V, Karakonstantaki E, Kanatsouli K, Stam CJ (2009): The influence of ageing on complex brain networks: A graph theoretical analysis. Hum Brain Mapp 30: 200-208.
54. Miller EK, Cohen JD (2001): An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24: 167-202.
55. Mulert C, Jager L, Schmitt R, Bussfeld P, Pogarell O, Moller HJ, Juckel G, Hegerl U (2004): Integration of fMRI and simultaneous EEG: Towards a comprehensive understanding of localization and time-course of brain activity in target detection. Neuroimage 22: 83-94.
56. Näpflin M, Wildi M, Sarnthein J (2007): Test-retest reliability of resting EEG spectra validates a statistical signature of persons. Clin Neurophysiol 118: 2519-2524.
57. Neubauer AC, Fink A (2009): Intelligence and neural efficiency. Neurosci Biobehav Rev 33: 1004-1023.
58. Neuper C, Grabner RH, Fink A, Neubauer AC (2005): Long-term stability and consistency of EEG event-related (de-)synchronization across different cognitive tasks. Clin Neurophysiol 116: 1681-1694.
59. Newman ME (2004): Analysis of weighted networks. Phys Rev E Stat Nonlin Soft Matter Phys 70(5 Part 2): 056131.
60. Nichols TE, Holmes AP (2002): Nonparametric permutation tests for functional neuroimaging: A primer with examples. Hum Brain Mapp 15: 1-25.
61. Oostenveld R, Praamstra P (2001): The five percent electrode system for high-resolution EEG and ERP measurements. Clin Neurophysiol 112: 713-719.
62. Opsahl T (2009): Structure and Evolution of Weighted Networks. London: University of London (Queen Mary College).
63. Opsahl T, Panzarasa P (2009): Clustering in weighted networks. Soc Netw 31: 155-163.
64. Opsahl T, Colizza V, Panzarasa P, Ramasco JJ (2008): Prominence and control: The weighted rich-club effect. Phys Rev Lett 101:168702.
65. Orekhova EV, Stroganova TA, Posikera IN, Malykh SB (2003): Heritability and "environmentability" of electroencephalogram in infants: The twin study. Psychophysiology 40: 727-741.
66. Pascual-Marqui RD (2002): Standardized low-resolution brain electromagnetic tomography (sLORETA): Technical details. Methods Find Exp Clin Pharmacol 24 (Suppl D): 5-12.
67. Pascual-Marqui RD (2007a): Discrete, 3D distributed, linear imaging methods of electrical neuronal activity. Part 1: Exact, zero error localization. arXiv:0710.3341 [math-ph].
68. Pascual-Marqui RD (2007b): Instantaneous and lagged measurements of linear and nonlinear dependence between groups of multivariate times series: Frequency decomposition. arXiv: 0711.1455[stat.ME].
69. Perrin F, Pernier J, Bertrand O, Giard MH, Echallier JF (1987): Mapping of scalp potentials by surface spline interpolation. Electroencephalogr Clin Neurophysiol 66: 75-81.
70. Posthuma D, Neale MC, Boomsma DI, de Geus EJ (2001): Are smarter brains running faster? Heritability of alpha peak frequency, IQ, and their interrelation. Behav Genet 31: 567-579.
71. Raven J, Raven JC, Court JH (2003): Manual for Raven's Progressive Matrices and Vocabulary Scales. Section 1: General Overview. San Antonia: Harcourt Assessment.
72. Reijneveld JC, Ponten SC, Berendse HW, Stam CJ (2007): The application of graph theoretical analysis to complex networks in the brain. Clin Neurophysiol 118: 2317-2331.
73. Rubinov M, Knock SA, Stam CJ, Micheloyannis S, Harris AW, Williams LM, Breakspear M (2009): Small-world properties of nonlinear brain activity in schizophrenia. Hum Brain Mapp 30: 403-416.
74. Rykhlevskaia E, Uddin LQ, Kondos L, Menon V (2009): Neuroanatomical correlates of developmental dyscalculia: Combined evidence from morphometry and tractography. Front Hum Neurosci 3: 51.
75. Shaffer JP (1995): Mutiple hypothesis testing. Annu Rev Psychol 46: 561-584.
76. Sinai A, Pratt H (2003): High-resolution time course of hemispheric dominance revealed by low-resolution electromagnetic tomography. Clin Neurophysiol 114: 1181-1188.
77. Singer W, Gray CM (1995): Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18: 555-586.
78. Smit CM, Wright MJ, Hansell NK, Geffen GM, Martin NG (2006): Genetic variation of individual alpha frequency (IAF) and alpha power in a large adolescent twin sample. Int J Psychophysiol 61: 235-243.
79. Sporns O, Kötter R (2004): Motifs in brain networks. PLoS Biol 2: e369.
80. Sporns O, Zwi JD (2004): The small world of the cerebral cortex. Neuroinformatics 2: 145-162.
81. Sporns O, Chialvo DR, Kaiser M, Hilgetag CC (2004): Organization, development and function of complex brain networks. Trends Cogn Sci 8: 418-425.
82. Stam CJ (2004): Functional connectivity patterns of human magnetoencephalographic recordings: A 'small-world' network? Neurosci Lett 355: 25-28.
83. Stam CJ, Reijneveld JC (2007): Graph theoretical analysis of complex networks in the brain. Nonlinear Biomed Phys 1: 3.
84. Stam CJ, Jones BF, Nolte G, Breakspear M, Scheltens P (2007): Small-world networks and functional connectivity in Alzheimer's disease. Cereb Cortex 17: 92-99.
85. Strogatz SH (2001): Exploring complex networks. Nature 410: 268-276.
86. Tachibana K, Suzuki K, Mori E, Miura N, Kawashima R, Horie K, Sato S, Tanji J, Mushiake H (2009): Neural activity in the human brain signals logical rule identification. J Neurophysiol 102: 1526-1537.
87. Tang Y, Chorlian DB, Rangaswamy M, Porjesz B, Bauer L, Kuperman S, O'Connor S, Rohrbaugh J, Schuckit M, Stimus A, Begleiter H (2007): Genetic influences on bipolar EEG power spectra. Int J Psychophysiol 65: 2-9.
88. Thatcher RW, North D, Biver C (2007): Intelligence and EEG current density using low-resolution electromagnetic tomography (LORETA). Hum Brain Mapp 28: 118-33.
89. Thatcher RW, North DM, Biver CJ (2008): Intelligence and EEG phase reset: A two compartmental model of phase shift and lock. Neuroimage 42: 1639-1653.
90. Tsapkini K, Rapp B (2009): The orthography-specific functions of the left fusiform gyrus: Evidence of modality and category specificity. Cortex 46:185-205.
91. van den Heuvel MP, Stam CJ, Kahn RS, Hulshoff Pol HE (2009): Efficiency of functional brain networks and intellectual performance. J Neurosci 29: 7619-7624.
92. Varela F, Lachaux JP, Rodriguez E, Martinerie J (2001): The brainweb: Phase synchronization and large-scale integration. Nat Rev Neurosci 2: 229-239.
93. Vogel F (2000): Genetics and the Electroencephalogram. Berlin: Springer.
94. Wasserman S, Faust K (1994). Social Network Analysis. Cambridge, MA: Cambridge University Press.
95. Watts DJ, Strogatz SH (1998): Collective dynamics of 'small-world' networks. Nature 393: 440-442.
96. Womelsdorf T, Schoffelen JM, Oostenveld R, Singer W, Desimone R, Engel AK, Fries P (2007): Modulation of neuronal interactions through neuronal synchronization. Science 316: 1609-1612.
97. Wong ACN, Palmeri TJ, Rogers BP, Gore JC, Gauthier I (2009): Beyond shape: How you learn about objects affects how they are represented in visual cortex. PLoS One 4: e8405.
98. Yu S, Huang D, Singer W, Nikolic D (2008): A small world of neuronal synchrony. Cereb Cortex 18: 2891-2901.
99. Zaehle T, Frund I, Schadow J, Tharig S, Schoenfeld MA, Herrmann CS (2009): Inter- and intra-individual covariations of hemodynamic and oscillatory gamma responses in the human cortex. Front Hum Neurosci 3: 8.