Altered Rolandic Gamma-Band Activation Associated with Motor Impairment and Ictal Network Desynchronization in Childhood Epilepsy

Abstract

Epilepsy is associated with an abnormal expression of neural oscillations and their synchronization across brain regions. Oscillatory brain activation and synchronization also play an important role in cognition, perception and motor control. Childhood epilepsy is associated with a variety of cognitive and motor deficits, but the relationship between altered functional brain responses in various frequency ranges and functional impairment in these children remains poorly understood. We investigated functional magnetoencephalographic (MEG) responses from motor cortex in multiple functionally relevant frequency bands following median nerve stimulation in twelve children with epilepsy, including four children with motor impairments. We demonstrated that children with motor impairments exhibit an excessive gamma-band response from Rolandic cortex, and that the magnitude of this Rolandic gamma response is negatively associated with motor function. Abnormal responses from motor cortex were also associated with ictal desynchronization of oscillations within Rolandic cortex measured using intracranial EEG (iEEG). These results provide the evidence that ictal disruption of motor networks is associated with an altered functional response from motor cortex, which is in turn associated with motor impairment.

Coupling between gamma-band power and cerebral blood volume during recurrent acute neocortical seizures

“…Our observation of increased gamma power during seizures in close proximity to the 4-AP infusion site is consistent with previous reports suggesting that increases in gamma activity are highly localized to the seizure onset zone ( Andrade-Valenca et al, 2011; Fisher et al, 1992; Medvedev et al, 2011; Worrell et al, 2004 ). There is considerable evidence for abnormal gamma-band activity in clinical epilepsy syndromes ( Doesburg et al, 2013; Fisher et al, 1992; Herrmann and Demiralp, 2005; Wu et al, 2008 ) and in experimental epilepsy ( Köhling et al, 2000; Medvedev, 2002; Traub et al, 2005 ). Under normal conditions, gamma oscillations are thought to be dependent on fast-spiking parvalbumin-expressing inhibitory interneurons ( Cardin et al, 2009 ).…”

“…These reports underscore the potential value for non-invasive perfusion-based neuroimaging studies to probe cognitive processes. However, while there are considerable reports of pathological gamma activity in clinical ( Doesburg et al, 2013; Fisher et al, 1992; Herrmann and Demiralp, 2005; Wu et al, 2008 ) and experimental ( Köhling et al, 2000; Medvedev, 2002; Traub et al, 2005 ) epilepsy, whether pathological gamma activity is preferentially coupled with hemodynamic signals in the epileptic state is untested. Confirmation of this relationship would suggest a common neural driver of perfusion-related signals in health and epilepsy and, since gamma-band neural measures are strongly co-localized to the EZ, highlight the potential for EEG-neuroimaging paradigms to further delineate the EZ through localization of hemodynamic correlates of pathological gamma activity.…”

Do cortical gamma oscillations promote or suppress perception? An under-asked question with an over-assumed answer

“…There is also evidence that the magnitude of narrowband gamma oscillations correlates with the degree to which visual stimuli are consciously perceived even when all other stimulus features remain unchanged (Schurger et al, 2006; Wyart and Tallon-Baudry, 2008), suggesting a positive role in conscious sensory representation. Narrowband gamma seems to be related to epileptogenesis (Parra et al, 2003; Adjamian et al, 2004; Visani et al, 2010; Doesburg et al, 2013) but, while a role in suppressing epileptiform activity is plausible, there is a lack of direct evidence in this context to favor either an inhibitory or excitatory role. Broadband gamma seems to occur in various cortical areas, and unlike narrowband visual gamma it is positively coupled to other measures of mass neural activity (Mukamel et al, 2005; Canolty et al, 2006).…”

“…While this immediately raises the possibility that these gamma oscillations therefore have a role in epilepsy, it does not help to establish whether the gamma oscillations are a precursor to epileptogenesis, or whether they are triggered by epileptogenic stimuli and act to prevent a transition to epileptiform activity. Further evidence of a link between gamma and ictal activity comes from the study of children with Rolandic epilepsy (Doesburg et al, 2013). This found that children with the highest motor cortex gamma induced by median nerve stimulation, measured with MEG, showed the strongest gamma synchrony in motor cortex ictally, recorded with intracranial EEG.…”

Functional Connectivity Hubs and Thalamic Hemodynamics in Rolandic Epilepsy

“…Seizures can be infrequent and usually occur at night during sleep. Despite seizure remission during adolescence, recent studies have shown a series of comorbidities in attention [2], language [3], motor performance [4] , memory [5]. The risk of cognitive impairments has been linked to interictal epileptic discharges (IED) [2,6,7] that are abnormal waveforms not associated with seizure symptoms.…”