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Chapter 10 - Epilepsy as a Complex Network Disorder

Insights from Functional MRI

Published online by Cambridge University Press:  06 January 2023

Rod C. Scott
Affiliation:
University of Vermont
J. Matthew Mahoney
Affiliation:
University of Vermont
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Summary

Functional magnetic resonance imaging (fMRI) was conceived in the early 1990s due to the coincidence of two advances: (1) MRI scanner technology able to support fast echo-planar imaging imaging techniques with the required temporal stability and (2) the scientific knowledge that differences in the magnetic susceptibility of blood may be associated with MRI signal changes based on alterations in blood oxygenation levels. These elements, together with the assumption that changes in blood oxygenation and volume would accompany changes in neural activity in the brain, motivated research groups around the world to develop fMRI.

Type
Chapter
Information
A Complex Systems Approach to Epilepsy
Concept, Practice, and Therapy
, pp. 135 - 152
Publisher: Cambridge University Press
Print publication year: 2023

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References

Belliveau, J. W., Kennedy, D. N., McKinstry, R. C., et al. Functional mapping of the human visual cortex by magnetic resonance imaging. Science, 254(5032), 716–9 (1991).Google Scholar
Kwong, K. K., Belliveau, J. W., Chesler, D. A., et al. Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc. Natl. Acad. Sci. USA, 89(12), 5675–9 (1992).Google Scholar
Ives, J. R., Warach, S., Schmitt, F., Edelman, R. R., and Schomer, D. L. Monitoring the patient’s EEG during echo planar MRI. Electroencephalogr. Clin. Neurophysiol., 87(6), 417–20 (1993).Google Scholar
Biswal, B., Yetkin, F. Z., Haughton, V. M., and Hyde, J. S. Functional connectivity in the motor cortex of resting human brain using echo‐planar mri. Magn. Reson. Med., 34(4), 537–41 (1995).Google Scholar
Centeno, M., and Carmichael, D. W. Network connectivity in epilepsy: Resting state fMRI and EEG-fMRI contributions. Front. Neurol., 5, 93 (2014).Google Scholar
McKeown, M. J., Jung, T. P., Makeig, S., et al. Spatially independent activity patterns in functional MRI data during the Stroop color-naming task. Proc. Natl. Acad. Sci. USA, 95(3), 803–10 (1998).Google Scholar
Seeley, W. W., Menon, V., Schatzberg, A. F., et al. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci., 27(9), 2349–56 (2007).Google Scholar
Xiong, J., Parsons, L. M., Gao, J. H., and Fox, P. T. Interregional connectivity to primary motor cortex revealed using MRI resting state images. Hum. Brain Mapp., 8(2–3), 151–6 (1999).Google Scholar
Smith, S. M., Fox, P. T., Miller, K. L., et al. Correspondence of the brain’s functional architecture during activation and rest. Proc. Natl. Acad. Sci. USA, 106(31), 130405 (2009).Google Scholar
Sporns, O. Graph theory methods: Applications in brain networks. Dialogues Clin. Neurosci., 20(2), 111–20 (2018).CrossRefGoogle ScholarPubMed
Murta, T., Leite, M., Carmichael, D. W., Figueiredo, P., and Lemieux, L. Electrophysiological correlates of the BOLD signal for EEG-informed fMRI. Hum. Brain Mapp., 36(1), 391414 (2015).Google Scholar
Jiang, W., Li, J., Chen, X., Ye, W., and Zheng, J.. Disrupted structural and functional networks and their correlation with alertness in right temporal lobe epilepsy: A graph theory study. Front. Neurol., 8, 179 (2017).CrossRefGoogle ScholarPubMed
Bettus, G., Guedj, E., Joyeux, F., et al. Decreased basal fMRI functional connectivity in epileptogenic networks and contralateral compensatory mechanisms. Hum. Brain Mapp., 30(5), 1580–91 (2009).Google Scholar
Morgan, V. L., Abou-Khalil, B., and Rogers, B. P. Evolution of functional connectivity of brain networks and their dynamic interaction in temporal lobe epilepsy. Brain Connect., 5(1), 3544 (2015).Google Scholar
Laufs, H., Hamandi, K., Salek-Haddadi, A., et al. Temporal lobe interictal epileptic discharges affect cerebral activity in “default mode” brain regions. Hum. Brain Mapp., 28(10), 1023–32 (2007).Google Scholar
Laufs, H., Rodionov, R., Thornton, R., et al. Altered fMRI connectivity dynamics in temporal lobe epilepsy might explain seizure semiology. Front. Neurol., 5, 175 (2014).Google Scholar
Stretton, J., Winston, G. P., Sidhu, M., et al. Disrupted segregation of working memory networks in temporal lobe epilepsy. Neuroimage Clin., 2, 273–81 (2013).Google Scholar
Deco, G., Kringelbach, M. L., Jirsa, V., and Ritter, P. The dynamics of resting fluctuations in the brain: Metastability and its dynamical cortical core. Sci. Rep., 7, 3095 (2017).Google Scholar
Voets, N. L., Beckmann, C. F., Cole, D. M., et al. Structural substrates for resting network disruption in temporal lobe epilepsy. Brain, 135(8), 2350–7 (2012).Google Scholar
He, X., Chaitanya, G., Asma, B., et al. Disrupted basal ganglia-thalamocortical loops in focal to bilateral tonic-clonic seizures. Brain, 143(1), 175–90 (2020).Google Scholar
Lui, S., Ouyang, L., Chen, Q., et al. Differential interictal activity of the precuneus/posterior cingulate cortex revealed by resting state functional MRI at 3T in generalized vs. Partial seizure. J. Magn. Reson. Imaging, 27(6), 1214–20 (2008).CrossRefGoogle ScholarPubMed
Mäkinen, V. T., May, P. J., and Tiitinen, H., The use of stationarity and nonstationarity in the detection and analysis of neural oscillations. Neuroimage, 28(2), 389–400 (2005).Google Scholar
Ibrahim, G. M., Sharma, P., Hyslop, A., et al. Presurgical thalamocortical connectivity is associated with response to vagus nerve stimulation in children with intractable epilepsy. Neuroimage Clin., 16, 634–42 (2017).Google Scholar
Sinha, N., Wang, Y., Moreira da Silva, N., et al. Structural brain network abnormalities and the probability of seizure recurrence after epilepsy surgery. Neurology, 96(5), e758–71 (2021).CrossRefGoogle ScholarPubMed
He, X., Doucet, G. E., Pustina, D., et al. Presurgical thalamic “hubness” predicts surgical outcome in temporal lobe epilepsy. Neurology, 88(24), 2285–93 (2017).Google Scholar
González, F. J., Chakravorti, S., Goodale, S. E., et al. Thalamic arousal network disturbances in temporal lobe epilepsy and improvement after surgery. J. Neurol. Neurosurg. Psychiatry, 90(10), 1109–16 (2019).CrossRefGoogle ScholarPubMed
Fisher, R., Salanova, V., Witt, T., et al. Electrical stimulation of the anterior nucleus of thalamus for treatment of refractory epilepsy. Epilepsia, 51(5), 899908 (2010).Google Scholar
Warren, A. E. L., Dalic, L. J., Thevathasan, W., et al. Targeting the centromedian thalamic nucleus for deep brain stimulation. J. Neurol. Neurosurg. Psychiatry, 91(4), 339–49 (2020).Google Scholar
Middlebrooks, E. H., Grewal, S. S., Stead, M., et al. Differences in functional connectivity profiles as a predictor of response to anterior thalamic nucleus deep brain stimulation for epilepsy: A hypothesis for the mechanism of action and a potential biomarker for outcomes. Neurosurg. Focus, 45(2), E7 (2018).CrossRefGoogle Scholar
Doucet, G. E., Pustina, D., Skidmore, C., et al. Resting-state functional connectivity predicts the strength of hemispheric lateralization for language processing in temporal lobe epilepsy and normals. Hum. Brain Mapp., 36(1), 288303 (2015).Google Scholar
Bonelli, S. B., Thompson, P. J., Yogarajah, M., et al. Imaging language networks before and after anterior temporal lobe resection: Results of a longitudinal fMRI study. Epilepsia, 53(4), 639–50 (2012).CrossRefGoogle ScholarPubMed
Foesleitner, O., Sigl, B., Schmidbauer, V., et al. Language network reorganization before and after temporal lobe epilepsy surgery. J. Neurosurg., 134(6), 16941702 (2020).CrossRefGoogle ScholarPubMed
Stufflebeam, S. M., Liu, H., Sepulcre, J., et al. Localization of focal epileptic discharges using functional connectivity magnetic resonance imaging: Clinical article. J. Neurosurg., 114(6), 1693–7 (2011).Google Scholar
Iannotti, G. R., Grouiller, F., Centeno, M., et al. Epileptic networks are strongly connected with and without the effects of interictal discharges. Epilepsia, 57(7), 1086–96 (2016).CrossRefGoogle ScholarPubMed
Vaessen, M. J., Braakman, H. M. H., Heerink, J. S., et al. Abnormal modular organization of functional networks in cognitively impaired children with frontal lobe epilepsy. Cereb. Cortex, 23(8), 19972006 (2012).Google Scholar
Ibrahim, G. M., Morgan, B. R., Lee, W., et al. Impaired development of intrinsic connectivity networks in children with medically intractable localization-related epilepsy. Hum. Brain Mapp., 35(11), 5686–700 (2014).Google Scholar
Hong, S.-J., Lee, H.-M., Gill, R., et al. A connectome-based mechanistic model of focal cortical dysplasia. Brain, 142(3), 688–99 (2019).Google Scholar
Lüttjohann, A., and van Luijtelaar, G. Dynamics of networks during absence seizure’s on- and offset in rodents and man. Front. Physiol., 6, 16 (2015).Google ScholarPubMed
Tangwiriyasakul, C., Perani, S., Centeno, M., et al. Dynamic brain network states in human generalized spike-wave discharges. Brain, 141(10), 2981–94 (2018).Google Scholar
Vulliemoz, S., Vollmar, C., Koepp, M. J., et al. Connectivity of the supplementary motor area in juvenile myoclonic epilepsy and frontal lobe epilepsy. Epilepsia, 52(3), 507–14 (2011).CrossRefGoogle ScholarPubMed
Tangwiriyasakul, C., Perani, S., Abela, E., Carmichael, D. W., and Richardson, M. P. Sensorimotor network hypersynchrony as an endophenotype in families with genetic generalized epilepsy: A resting‐state functional magnetic resonance imaging study. Epilepsia, 60(3), e14–9 (2019).Google Scholar
Routley, B., Shaw, A., Muthukumaraswamy, S. D., Singh, K. D., and Hamandi, K. Juvenile myoclonic epilepsy shows increased posterior theta, and reduced sensorimotor beta resting connectivity. Epilepsy Res., 163, 106324 (2020).Google Scholar
Chaudhary, U. J., Centeno, M., Carmichael, D. W., et al. Imaging the interaction: Epileptic discharges, working memory, and behavior. Hum Brain Mapp., 34(11), 2910–7 (2013).Google Scholar
Haag, A., and Bonelli, S.. Clinical application of language and memory fMRI in epilepsy. Epileptologie, 30, 101–8 (2013).Google Scholar
Tierney, T. M., Weiss-Croft, L. J., Centeno, M., et al. FIACH: A biophysical model for automatic retrospective noise control in fMRI. Neuroimage., 124, 1009–20 (2016).Google Scholar
Wandschneider, B., and Koepp, M. J. Pharmaco fMRI: Determining the functional anatomy of the effects of medication. Neuroimage Clin., 12, 691–7 (2016).Google Scholar
Vollmar, C., O’Muircheartaigh, J., Barker, G. J., et al. Motor system hyperconnectivity in juvenile myoclonic epilepsy: A cognitive functional magnetic resonance imaging study. Brain, 134(6), 1710–9 (2011).CrossRefGoogle ScholarPubMed
Wandschneider, B., Stretton, J., Sidhu, M., et al. Levetiracetam reduces abnormal network activations in temporal lobe epilepsy. Neurology., 83(17), 1508–12 (2014).Google Scholar
Joules, R., Doyle, O. M., Schwarz, A. J., et al. Ketamine induces a robust whole-brain connectivity pattern that can be differentially modulated by drugs of different mechanism and clinical profile. Psychopharmacology (Berl.), 232(21–22), 42054218 (2015).CrossRefGoogle ScholarPubMed
Haneef, Z., Levin, H. S., and Chiang, S. Brain graph topology changes associated with anti-epileptic drug use. Brain Connect., 5(5), 284–91 (2015).CrossRefGoogle ScholarPubMed
Eljamel, S.. Mechanism of action and overview of vagus nerve stimulation technology. In Neurostimulation: Principles and Practice. Oxford, UK: John Wiley & Sons, Ltd. 2013. p. 111–20.Google Scholar
Lomarev, M., Denslow, S., Nahas, Z., et al. Vagus nerve stimulation (VNS) synchronized BOLD fMRI suggests that VNS in depressed adults has frequency/dose dependent effects. J. Psychiatr. Res., 36(4), 219–27 (2002).CrossRefGoogle ScholarPubMed
Cortes, C., and Vapnik, V. Support-vector networks. Mach. Learn., 20(3), 273–97 (1995).CrossRefGoogle Scholar
Mithani, K., Mikhail, M., Morgan, B. R., et al. Connectomic profiling identifies responders to vagus nerve stimulation. Ann. Neurol., 86(5), 74353 (2019).Google Scholar
Li, L. M., Violante, I. R., Leech, R., et al. Brain state and polarity dependent modulation of brain networks by transcranial direct current stimulation. Hum. Brain Mapp., 40(3), 904–15 (2019).Google Scholar
Tzourio-Mazoyer, N, Landeau, B, Papathanassiou, D, Crivello, F, Etard, O, Delcroix, N, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. 15: 273–89 (2002). doi: 10.1006/nimg.2001.0978Google Scholar

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