Disruption of Rolandic Gamma-Band Functional Connectivity by Seizures is Associated with Motor Impairments in Children with Epilepsy

Although children with epilepsy exhibit numerous neurological and cognitive deficits, the mechanisms underlying these impairments remain unclear. Synchronization of oscillatory neural activity in the gamma frequency range (>30 Hz) is purported to be a mechanism mediating functional integration within neuronal networks supporting cognition, perception and action. Here, we tested the hypothesis that seizure-induced alterations in gamma synchronization are associated with functional deficits. By calculating synchrony among electrodes and performing graph theoretical analysis, we assessed functional connectivity and local network structure of the hand motor area of children with focal epilepsy from intracranial electroencephalographic recordings. A local decrease in inter-electrode phase synchrony in the gamma bands during ictal periods, relative to interictal periods, within the motor cortex was strongly associated with clinical motor weakness. Gamma-band ictal desychronization was a stronger predictor of deficits than the presence of the seizure-onset zone or lesion within the motor cortex. There was a positive correlation between the magnitude of ictal desychronization and impairment of motor dexterity in the contralateral, but not ipsilateral hand. There was no association between ictal desynchronization within the hand motor area and non-motor deficits. This study uniquely demonstrates that seizure-induced disturbances in cortical functional connectivity are associated with network-specific neurological deficits.

[1]  Bin He,et al.  Graph analysis of epileptogenic networks in human partial epilepsy , 2011, Epilepsia.

[2]  Shan Yu,et al.  A Small World of Neuronal Synchrony , 2008, Cerebral cortex.

[3]  K. Kaski,et al.  Intensity and coherence of motifs in weighted complex networks. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[4]  J. Drake,et al.  Neurosurgical management of intractable rolandic epilepsy in children: role of resection in eloquent cortex. Clinical article. , 2009, Journal of neurosurgery. Pediatrics.

[5]  Kenneth D. Harris,et al.  Early cognitive and language skills are linked to resting frontal gamma power across the first 3 years , 2008, Behavioural Brain Research.

[6]  Ayako Ochi,et al.  Dynamic Changes of Ictal High‐Frequency Oscillations in Neocortical Epilepsy: Using Multiple Band Frequency Analysis , 2007, Epilepsia.

[7]  K. Lehnertz,et al.  State dependent properties of epileptic brain networks: Comparative graph–theoretical analyses of simultaneously recorded EEG and MEG , 2010, Clinical Neurophysiology.

[8]  M. Vinck,et al.  Source (or Part of the following Source): Type Article Title Learning-associated Gamma-band Phase-locking of Action-outcome Selective Neurons in Orbitofrontal Cortex Author(s) Learning-associated Gamma-band Phase-locking of Action–outcome Selective Neurons in Orbitofrontal Cortex Gamma Oscillations , 2022 .

[9]  J. Régis,et al.  Acute alteration of emotional behaviour in epileptic seizures is related to transient desynchrony in emotion-regulation networks , 2005, Clinical Neurophysiology.

[10]  Fabrice Wendling,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[11]  Nikolai Axmacher,et al.  Rhinal–hippocampal coupling during declarative memory formation: Dependence on item characteristics , 2006, Neuroscience Letters.

[12]  J. I.  The Design of Experiments , 1936, Nature.

[13]  W. Liao,et al.  Impaired perceptual networks in temporal lobe epilepsy revealed by resting fMRI , 2009, Journal of Neurology.

[14]  Gustavo Deco,et al.  Oscillations, Phase-of-Firing Coding, and Spike Timing-Dependent Plasticity: An Efficient Learning Scheme , 2009, The Journal of Neuroscience.

[15]  C. Elger,et al.  Chronic temporal lobe epilepsy: a neurodevelopmental or progressively dementing disease? , 2009, Brain : a journal of neurology.

[16]  C. Elger,et al.  Human memory formation is accompanied by rhinal–hippocampal coupling and decoupling , 2001, Nature Neuroscience.

[17]  Bob Kemp,et al.  European data format ‘plus’ (EDF+), an EDF alike standard format for the exchange of physiological data , 2003, Clinical Neurophysiology.

[18]  A. Burgess,et al.  Functional connectivity of gamma EEG activity is modulated at low frequency during conscious recollection. , 2002, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[19]  Mark Newman,et al.  Networks: An Introduction , 2010 .

[20]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[21]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[22]  J. Pastor,et al.  Synchronization Clusters of Interictal Activity in the Lateral Temporal Cortex of Epileptic Patients: Intraoperative Electrocorticographic Analysis , 2008, Epilepsia.

[23]  G. Mangun,et al.  Functional Disconnection of Frontal Cortex and Visual Cortex in Attention-Deficit/Hyperactivity Disorder , 2010, Biological Psychiatry.

[24]  A. Kleinschmidt,et al.  Temporal lobe interictal epileptic discharges affect cerebral activity in “default mode” brain regions , 2006, Human brain mapping.

[25]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[26]  Mark R. Bower,et al.  Synchrony in normal and focal epileptic brain: the seizure onset zone is functionally disconnected. , 2010, Journal of neurophysiology.

[27]  K. Meador.  Cognitive outcomes and predictive factors in epilepsy , 2002, Neurology.

[28]  Matthias M. Müller,et al.  Directed Cortical Information Flow during Human Object Recognition: Analyzing Induced EEG Gamma-Band Responses in Brain's Source Space , 2007, PloS one.

[29]  Q. Gong,et al.  Altered functional connectivity in default mode network in absence epilepsy: A resting‐state fMRI study , 2011, Human brain mapping.

[30]  Ayako Ochi,et al.  Focal resection of fast ripples on extraoperative intracranial EEG improves seizure outcome in pediatric epilepsy , 2011, Epilepsia.

[31]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[32]  W. Liao,et al.  Impaired attention network in temporal lobe epilepsy: A resting FMRI study , 2009, Neuroscience Letters.

[33]  F. Varela,et al.  Perception's shadow: long-distance synchronization of human brain activity , 1999, Nature.

[34]  R M Ruff,et al.  Gender- and Age-Specific Changes in Motor Speed and Eye-Hand Coordination in Adults: Normative Values for the Finger Tapping and Grooved Pegboard Tests , 1993, Perceptual and motor skills.

[35]  G. Holmes,et al.  Seizures in the Developing Brain Perhaps Not So Benign after All , 1998, Neuron.

[36]  Valentin Dragoi,et al.  Adaptive Changes in Neuronal Synchronization in Macaque V4 , 2011, The Journal of Neuroscience.

[37]  Maria Thom,et al.  The clinicopathologic spectrum of focal cortical dysplasias: A consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission 1 , 2011, Epilepsia.

[38]  K. Koepsell,et al.  Oscillatory phase coupling coordinates anatomically dispersed functional cell assemblies , 2010, Proceedings of the National Academy of Sciences.

[39]  Christoph Braun,et al.  Coherence of gamma-band EEG activity as a basis for associative learning , 1999, Nature.

[40]  G. Holmes,et al.  Power spectral analysis in infants with seizures: Relationship to development , 2011, Epilepsy & Behavior.

[41]  Christian Büchel,et al.  Integration of local features to a global percept by neural coupling. , 2006, Cerebral cortex.

[42]  W. Singer,et al.  Temporal binding and the neural correlates of sensory awareness , 2001, Trends in Cognitive Sciences.

[43]  Kaspar Anton Schindler,et al.  Assessing seizure dynamics by analysing the correlation structure of multichannel intracranial EEG. , 2006, Brain : a journal of neurology.

[44]  A. Schnitzler,et al.  Normal and pathological oscillatory communication in the brain , 2005, Nature Reviews Neuroscience.

[45]  R. Asarnow,et al.  Cerebral hemispherectomy , 2004, Neurology.

[46]  Eugenio Rodriguez,et al.  The development of neural synchrony reflects late maturation and restructuring of functional networks in humans , 2009, Proceedings of the National Academy of Sciences.

[47]  Eishi Asano,et al.  Statistical mapping of ictal high‐frequency oscillations in epileptic spasms , 2011, Epilepsia.

[48]  G. Dawson,et al.  Resting State Cortical Connectivity Reflected in EEG Coherence in Individuals With Autism , 2007, Biological Psychiatry.