March  2015, 10(1): 223-232. doi: 10.3934/nhm.2015.10.223

EEG-based functional brain networks: Hemispheric differences in males and females

1. 

Department of Computer Engineering, Sharif University of Technology, Azadi Av., Tehran, Iran

Received  June 2014 Revised  December 2014 Published  February 2015

Functional connectivity in human brain can be represented as a network using electroencephalography (EEG) signals. Network representation of EEG time series can be an efficient vehicle to understand the underlying mechanisms of brain function. Brain functional networks whose nodes are brain regions and edges correspond to functional links between them are characterized by neurobiologically meaningful graph theory metrics. This study investigates the degree to which graph theory metrics are sex dependent. To this end, EEGs from 24 healthy female subjects and 21 healthy male subjects were recorded in eyes-closed resting state conditions. The connectivity matrices were extracted using correlation analysis and were further binarized to obtain binary functional networks. Global and local efficiency measures as graph theory metrics were computed for the extracted networks. We found that male brains have significantly greater global efficiency (i.e., global communicability of the network) across all frequency bands for a wide range of cost values in both hemispheres. Furthermore, for a range of cost values, female brains showed significantly greater right-hemispheric local efficiency (i.e., local connectivity) than male brains.
Citation: Mahdi Jalili. EEG-based functional brain networks: Hemispheric differences in males and females. Networks & Heterogeneous Media, 2015, 10 (1) : 223-232. doi: 10.3934/nhm.2015.10.223
References:
[1]

S. Achard and E. Bullmore, Efficiency and cost of economical brain functional networks,, PLoS Computational Biology, 3 (2007).

[2]

S. Achard, R. Salvador, B. Whitcher, J. Suckling and E. Bullmore, A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs,, The Journal of Neuroscience, 26 (2006), 63. doi: 10.1523/JNEUROSCI.3874-05.2006.

[3]

A. F. Alexander-Bloch, N. Gogtay, D. Meunier, R. Birn, L. Clasen, F. Lalonde, R. Lenroot, J. Giedd and E. T. Bullmore, Disrupted modularity and local connectivity of brain functional networks in childhood-onset schizophrenia,, Frontiers in Systems Neuroscience, 4 (2010).

[4]

A.-L. Barabási, Network science,, Philosophical Transactions of the Royal Society A: Mathematical, 371 (2013). doi: 10.1098/rsta.2012.0375.

[5]

A.-L. Barabási et al., Scale-free networks: A decade and beyond,, Science, 325 (2009), 412. doi: 10.1126/science.1173299.

[6]

E. Barzegaran, A. Joudaki, M. Jalili, A. O. Rossetti, R. S. Frackowiak and M. G. Knyazeva, Properties of functional brain networks correlate with frequency of psychogenic non-epileptic seizures,, Frontiers in Human Neuroscience, (2012). doi: 10.3389/fnhum.2012.00335.

[7]

D. S. Bassett, E. Bullmore, B. A. Verchinski, V. S. Mattay, D. R. Weinberger and A. Meyer-Lindenberg, Hierarchical organization of human cortical networks in health and schizophrenia,, The Journal of Neuroscience, 28 (2008), 9239. doi: 10.1523/JNEUROSCI.1929-08.2008.

[8]

D. S. Bassett and E. T. Bullmore, Human brain networks in health and disease,, Current Opinion in Neurology, 22 (2009), 340. doi: 10.1097/WCO.0b013e32832d93dd.

[9]

S. Boccaletti, V. Latora, Y. Moreno, M. Chavez and D.-U. Hwang, Complex networks: Structure and dynamics,, Physics Reports, 424 (2006), 175. doi: 10.1016/j.physrep.2005.10.009.

[10]

E. Bullmore and O. Sporns, Complex brain networks: Graph theoretical analysis of structural and functional systems,, Nature Reviews Neuroscience, 10 (2009), 186. doi: 10.1038/nrn2575.

[11]

E. Bullmore and O. Sporns, The economy of brain network organization,, Nature Reviews Neuroscience, 13 (2012), 336. doi: 10.1038/nrn3214.

[12]

R. J. Davidson, G. E. Schwartz, E. Pugash and E. Bromfield, Sex differences in patterns of eeg asymmetry,, Biological Psychology, 4 (1976), 119. doi: 10.1016/0301-0511(76)90012-0.

[13]

F. De Vico Fallani, L. Astolfi, F. Cincotti, D. Mattia, D. la Rocca, E. Maksuti, S. Salinari, F. Babiloni, B. Vegso and G. Kozmann, et al., Evaluation of the brain network organization from eeg signals: A preliminary evidence in stroke patient,, The Anatomical Record, 292 (2009), 2023.

[14]

V. M. Eguiluz, D. R. Chialvo, G. A. Cecchi, M. Baliki and A. V. Apkarian, Scale-free brain functional networks,, Physical Review Letters, 94 (2005). doi: 10.1103/PhysRevLett.94.018102.

[15]

R. Ferri, F. Rundo, O. Bruni, M. G. Terzano and C. J. Stam, Small-world network organization of functional connectivity of eeg slow-wave activity during sleep,, Clinical Neurophysiology, 118 (2007), 449. doi: 10.1016/j.clinph.2006.10.021.

[16]

E. Fornari, P. Maeder, R. Meuli, J. Ghika and M. G. Knyazeva, Demyelination of superficial white matter in early Alzheimer's disease: A magnetization transfer imaging study,, Neurobiology of Aging, 33 (2012), 7. doi: 10.1016/j.neurobiolaging.2010.11.014.

[17]

G. Gong, Y. He and A. C. Evans, Brain connectivity gender makes a difference,, The Neuroscientist, 17 (2011), 575. doi: 10.1177/1073858410386492.

[18]

G. Gong, P. Rosa-Neto, F. Carbonell, Z. J. Chen, Y. He and A. C. Evans, Age-and gender-related differences in the cortical anatomical network,, The Journal of Neuroscience, 29 (2009), 15684. doi: 10.1523/JNEUROSCI.2308-09.2009.

[19]

P. Hagmann, L. Cammoun, X. Gigandet, R. Meuli, C. J. Honey, V. J. Wedeen and O. Sporns, Mapping the structural core of human cerebral cortex,, PLoS Biology, 6 (2008).

[20]

M. Ingalhalikar, A. Smith, D. Parker, T. D. Satterthwaite, M. A. Elliott, K. Ruparel, H. Hakonarson, R. E. Gur, R. C. Gur and R. Verma, Sex differences in the structural connectome of the human brain,, Proceedings of the National Academy of Sciences, 111 (2014), 823. doi: 10.1073/pnas.1316909110.

[21]

M. Jalili and M. G. Knyazeva, Constructing brain functional networks from eeg: Partial and unpartial correlations,, Journal of Integrative Neuroscience, 10 (2011), 213. doi: 10.1142/S0219635211002725.

[22]

M. Jalili and M. G. Knyazeva, Eeg-based functional networks in schizophrenia,, Computers in Biology and Medicine, 41 (2011), 1178. doi: 10.1016/j.compbiomed.2011.05.004.

[23]

M. Jalili, S. Lavoie, P. Deppen, R. Meuli, K. Q. Do, M. Cu{\'e}nod, M. Hasler, O. De Feo and M. G. Knyazeva, Dysconnection topography in schizophrenia revealed with state-space analysis of eeg,, PLoS One, 2 (2007). doi: 10.1371/journal.pone.0001059.

[24]

A. Joudaki, N. Salehi, M. Jalili and M. G. Knyazeva, Eeg-based functional brain networks: Does the network size matter?,, PloS One, 7 (2012). doi: 10.1371/journal.pone.0035673.

[25]

D. Kimura, Sex differences in the brain,, Scientific American, 267 (1992), 118.

[26]

M. G. Knyazeva, M. Jalili, R. S. Frackowiak and A. O. Rossetti, Psychogenic seizures and frontal disconnection: Eeg synchronisation study,, Journal of Neurology, 82 (2011), 505. doi: 10.1136/jnnp.2010.224873.

[27]

V. Latora and M. Marchiori, Economic small-world behavior in weighted networks,, The European Physical Journal B-Condensed Matter and Complex Systems, 32 (2003), 249. doi: 10.1140/epjb/e2003-00095-5.

[28]

W. Liao, Z. Zhang, Z. Pan, D. Mantini, J. Ding, X. Duan, C. Luo, G. Lu and H. Chen, Altered functional connectivity and small-world in mesial temporal lobe epilepsy,, PloS One, 5 (2010). doi: 10.1371/journal.pone.0008525.

[29]

Y. Liu, C. Yu, M. Liang, J. Li, L. Tian, Y. Zhou, W. Qin, K. Li and T. Jiang, Whole brain functional connectivity in the early blind,, Brain, 130 (2007), 2085. doi: 10.1093/brain/awm121.

[30]

M. Matsuura, K. Yamamoto, H. Fukuzawa, Y. Okubo, H. Uesugi, M. Moriiwa, T. Kojima and Y. Shimazono, Age development and sex differences of various eeg elements in healthy children and adults-quantification by a computerized wave form recognition method,, Electroencephalography and Clinical Neurophysiology, 60 (1985), 394. doi: 10.1016/0013-4694(85)91013-2.

[31]

S. Micheloyannis, E. Pachou, C. J. Stam, M. Breakspear, P. Bitsios, M. Vourkas, S. Erimaki and M. Zervakis, Small-world networks and disturbed functional connectivity in schizophrenia,, Schizophrenia Research, 87 (2006), 60. doi: 10.1016/j.schres.2006.06.028.

[32]

P. L. Nunez and R. Srinivasan, Electric Fields of the Brain: The Neurophysics of EEG,, 2nd edition, (2006). doi: 10.1063/1.2915137.

[33]

O. Sporns, Small-world connectivity, motif composition, and complexity of fractal neuronal connections,, Biosystems, 85 (2006), 55. doi: 10.1016/j.biosystems.2006.02.008.

[34]

O. Sporns and J. D. Zwi, The small world of the cerebral cortex,, Neuroinformatics, 2 (2004), 145. doi: 10.1385/NI:2:2:145.

[35]

C. Stam, W. De Haan, A. Daffertshofer, B. Jones, I. Manshanden, A. V. C. Van Walsum, T. Montez, J. Verbunt, J. De Munck and B. Van Dijk, et al., Graph theoretical analysis of magnetoencephalographic functional connectivity in Alzheimer's disease,, Brain, 132 (2009), 213. doi: 10.1093/brain/awn262.

[36]

C. Stam, B. Jones, G. Nolte, M. Breakspear and P. Scheltens, Small-world networks and functional connectivity in Alzheimer's disease,, Cerebral Cortex, 17 (2007), 92. doi: 10.1093/cercor/bhj127.

[37]

M. S. Tahaei, M. Jalili and M. G. Knyazeva, Synchronizability of eeg-based functional networks in early alzheimer's disease,, IEEE Transactions on Neural Systems and Rehabilitation Engineering, 20 (2012), 636. doi: 10.1109/TNSRE.2012.2202127.

[38]

L. Tian, J. Wang, C. Yan and Y. He, Hemisphere-and gender-related differences in small-world brain networks: A resting-state functional mri study,, Neuroimage, 54 (2011), 191. doi: 10.1016/j.neuroimage.2010.07.066.

[39]

D. J. Watts and S. H. Strogatz, Collective dynamics of 'small-world' networks,, Nature, 393 (1998), 440.

[40]

C. Yan, G. Gong, J. Wang, D. Wang, D. Liu, C. Zhu, Z. J. Chen, A. Evans, Y. Zang and Y. He, Sex-and brain size-related small-world structural cortical networks in young adults: A dti tractography study,, Cerebral cortex, 21 (2011), 449. doi: 10.1093/cercor/bhq111.

[41]

A. Zalesky, A. Fornito, I. H. Harding, L. Cocchi, M. Yücel, C. Pantelis and E. T. Bullmore, Whole-brain anatomical networks: Does the choice of nodes matter?,, Neuroimage, 50 (2010), 970. doi: 10.1016/j.neuroimage.2009.12.027.

show all references

References:
[1]

S. Achard and E. Bullmore, Efficiency and cost of economical brain functional networks,, PLoS Computational Biology, 3 (2007).

[2]

S. Achard, R. Salvador, B. Whitcher, J. Suckling and E. Bullmore, A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs,, The Journal of Neuroscience, 26 (2006), 63. doi: 10.1523/JNEUROSCI.3874-05.2006.

[3]

A. F. Alexander-Bloch, N. Gogtay, D. Meunier, R. Birn, L. Clasen, F. Lalonde, R. Lenroot, J. Giedd and E. T. Bullmore, Disrupted modularity and local connectivity of brain functional networks in childhood-onset schizophrenia,, Frontiers in Systems Neuroscience, 4 (2010).

[4]

A.-L. Barabási, Network science,, Philosophical Transactions of the Royal Society A: Mathematical, 371 (2013). doi: 10.1098/rsta.2012.0375.

[5]

A.-L. Barabási et al., Scale-free networks: A decade and beyond,, Science, 325 (2009), 412. doi: 10.1126/science.1173299.

[6]

E. Barzegaran, A. Joudaki, M. Jalili, A. O. Rossetti, R. S. Frackowiak and M. G. Knyazeva, Properties of functional brain networks correlate with frequency of psychogenic non-epileptic seizures,, Frontiers in Human Neuroscience, (2012). doi: 10.3389/fnhum.2012.00335.

[7]

D. S. Bassett, E. Bullmore, B. A. Verchinski, V. S. Mattay, D. R. Weinberger and A. Meyer-Lindenberg, Hierarchical organization of human cortical networks in health and schizophrenia,, The Journal of Neuroscience, 28 (2008), 9239. doi: 10.1523/JNEUROSCI.1929-08.2008.

[8]

D. S. Bassett and E. T. Bullmore, Human brain networks in health and disease,, Current Opinion in Neurology, 22 (2009), 340. doi: 10.1097/WCO.0b013e32832d93dd.

[9]

S. Boccaletti, V. Latora, Y. Moreno, M. Chavez and D.-U. Hwang, Complex networks: Structure and dynamics,, Physics Reports, 424 (2006), 175. doi: 10.1016/j.physrep.2005.10.009.

[10]

E. Bullmore and O. Sporns, Complex brain networks: Graph theoretical analysis of structural and functional systems,, Nature Reviews Neuroscience, 10 (2009), 186. doi: 10.1038/nrn2575.

[11]

E. Bullmore and O. Sporns, The economy of brain network organization,, Nature Reviews Neuroscience, 13 (2012), 336. doi: 10.1038/nrn3214.

[12]

R. J. Davidson, G. E. Schwartz, E. Pugash and E. Bromfield, Sex differences in patterns of eeg asymmetry,, Biological Psychology, 4 (1976), 119. doi: 10.1016/0301-0511(76)90012-0.

[13]

F. De Vico Fallani, L. Astolfi, F. Cincotti, D. Mattia, D. la Rocca, E. Maksuti, S. Salinari, F. Babiloni, B. Vegso and G. Kozmann, et al., Evaluation of the brain network organization from eeg signals: A preliminary evidence in stroke patient,, The Anatomical Record, 292 (2009), 2023.

[14]

V. M. Eguiluz, D. R. Chialvo, G. A. Cecchi, M. Baliki and A. V. Apkarian, Scale-free brain functional networks,, Physical Review Letters, 94 (2005). doi: 10.1103/PhysRevLett.94.018102.

[15]

R. Ferri, F. Rundo, O. Bruni, M. G. Terzano and C. J. Stam, Small-world network organization of functional connectivity of eeg slow-wave activity during sleep,, Clinical Neurophysiology, 118 (2007), 449. doi: 10.1016/j.clinph.2006.10.021.

[16]

E. Fornari, P. Maeder, R. Meuli, J. Ghika and M. G. Knyazeva, Demyelination of superficial white matter in early Alzheimer's disease: A magnetization transfer imaging study,, Neurobiology of Aging, 33 (2012), 7. doi: 10.1016/j.neurobiolaging.2010.11.014.

[17]

G. Gong, Y. He and A. C. Evans, Brain connectivity gender makes a difference,, The Neuroscientist, 17 (2011), 575. doi: 10.1177/1073858410386492.

[18]

G. Gong, P. Rosa-Neto, F. Carbonell, Z. J. Chen, Y. He and A. C. Evans, Age-and gender-related differences in the cortical anatomical network,, The Journal of Neuroscience, 29 (2009), 15684. doi: 10.1523/JNEUROSCI.2308-09.2009.

[19]

P. Hagmann, L. Cammoun, X. Gigandet, R. Meuli, C. J. Honey, V. J. Wedeen and O. Sporns, Mapping the structural core of human cerebral cortex,, PLoS Biology, 6 (2008).

[20]

M. Ingalhalikar, A. Smith, D. Parker, T. D. Satterthwaite, M. A. Elliott, K. Ruparel, H. Hakonarson, R. E. Gur, R. C. Gur and R. Verma, Sex differences in the structural connectome of the human brain,, Proceedings of the National Academy of Sciences, 111 (2014), 823. doi: 10.1073/pnas.1316909110.

[21]

M. Jalili and M. G. Knyazeva, Constructing brain functional networks from eeg: Partial and unpartial correlations,, Journal of Integrative Neuroscience, 10 (2011), 213. doi: 10.1142/S0219635211002725.

[22]

M. Jalili and M. G. Knyazeva, Eeg-based functional networks in schizophrenia,, Computers in Biology and Medicine, 41 (2011), 1178. doi: 10.1016/j.compbiomed.2011.05.004.

[23]

M. Jalili, S. Lavoie, P. Deppen, R. Meuli, K. Q. Do, M. Cu{\'e}nod, M. Hasler, O. De Feo and M. G. Knyazeva, Dysconnection topography in schizophrenia revealed with state-space analysis of eeg,, PLoS One, 2 (2007). doi: 10.1371/journal.pone.0001059.

[24]

A. Joudaki, N. Salehi, M. Jalili and M. G. Knyazeva, Eeg-based functional brain networks: Does the network size matter?,, PloS One, 7 (2012). doi: 10.1371/journal.pone.0035673.

[25]

D. Kimura, Sex differences in the brain,, Scientific American, 267 (1992), 118.

[26]

M. G. Knyazeva, M. Jalili, R. S. Frackowiak and A. O. Rossetti, Psychogenic seizures and frontal disconnection: Eeg synchronisation study,, Journal of Neurology, 82 (2011), 505. doi: 10.1136/jnnp.2010.224873.

[27]

V. Latora and M. Marchiori, Economic small-world behavior in weighted networks,, The European Physical Journal B-Condensed Matter and Complex Systems, 32 (2003), 249. doi: 10.1140/epjb/e2003-00095-5.

[28]

W. Liao, Z. Zhang, Z. Pan, D. Mantini, J. Ding, X. Duan, C. Luo, G. Lu and H. Chen, Altered functional connectivity and small-world in mesial temporal lobe epilepsy,, PloS One, 5 (2010). doi: 10.1371/journal.pone.0008525.

[29]

Y. Liu, C. Yu, M. Liang, J. Li, L. Tian, Y. Zhou, W. Qin, K. Li and T. Jiang, Whole brain functional connectivity in the early blind,, Brain, 130 (2007), 2085. doi: 10.1093/brain/awm121.

[30]

M. Matsuura, K. Yamamoto, H. Fukuzawa, Y. Okubo, H. Uesugi, M. Moriiwa, T. Kojima and Y. Shimazono, Age development and sex differences of various eeg elements in healthy children and adults-quantification by a computerized wave form recognition method,, Electroencephalography and Clinical Neurophysiology, 60 (1985), 394. doi: 10.1016/0013-4694(85)91013-2.

[31]

S. Micheloyannis, E. Pachou, C. J. Stam, M. Breakspear, P. Bitsios, M. Vourkas, S. Erimaki and M. Zervakis, Small-world networks and disturbed functional connectivity in schizophrenia,, Schizophrenia Research, 87 (2006), 60. doi: 10.1016/j.schres.2006.06.028.

[32]

P. L. Nunez and R. Srinivasan, Electric Fields of the Brain: The Neurophysics of EEG,, 2nd edition, (2006). doi: 10.1063/1.2915137.

[33]

O. Sporns, Small-world connectivity, motif composition, and complexity of fractal neuronal connections,, Biosystems, 85 (2006), 55. doi: 10.1016/j.biosystems.2006.02.008.

[34]

O. Sporns and J. D. Zwi, The small world of the cerebral cortex,, Neuroinformatics, 2 (2004), 145. doi: 10.1385/NI:2:2:145.

[35]

C. Stam, W. De Haan, A. Daffertshofer, B. Jones, I. Manshanden, A. V. C. Van Walsum, T. Montez, J. Verbunt, J. De Munck and B. Van Dijk, et al., Graph theoretical analysis of magnetoencephalographic functional connectivity in Alzheimer's disease,, Brain, 132 (2009), 213. doi: 10.1093/brain/awn262.

[36]

C. Stam, B. Jones, G. Nolte, M. Breakspear and P. Scheltens, Small-world networks and functional connectivity in Alzheimer's disease,, Cerebral Cortex, 17 (2007), 92. doi: 10.1093/cercor/bhj127.

[37]

M. S. Tahaei, M. Jalili and M. G. Knyazeva, Synchronizability of eeg-based functional networks in early alzheimer's disease,, IEEE Transactions on Neural Systems and Rehabilitation Engineering, 20 (2012), 636. doi: 10.1109/TNSRE.2012.2202127.

[38]

L. Tian, J. Wang, C. Yan and Y. He, Hemisphere-and gender-related differences in small-world brain networks: A resting-state functional mri study,, Neuroimage, 54 (2011), 191. doi: 10.1016/j.neuroimage.2010.07.066.

[39]

D. J. Watts and S. H. Strogatz, Collective dynamics of 'small-world' networks,, Nature, 393 (1998), 440.

[40]

C. Yan, G. Gong, J. Wang, D. Wang, D. Liu, C. Zhu, Z. J. Chen, A. Evans, Y. Zang and Y. He, Sex-and brain size-related small-world structural cortical networks in young adults: A dti tractography study,, Cerebral cortex, 21 (2011), 449. doi: 10.1093/cercor/bhq111.

[41]

A. Zalesky, A. Fornito, I. H. Harding, L. Cocchi, M. Yücel, C. Pantelis and E. T. Bullmore, Whole-brain anatomical networks: Does the choice of nodes matter?,, Neuroimage, 50 (2010), 970. doi: 10.1016/j.neuroimage.2009.12.027.

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