fMRI activation during spike and wave discharges evoked by photic stimulation
Introduction
Photosensitivity or photoparoxysmal response (PPR) is an abnormal, highly hereditary electroencephalographic (EEG) trait characterized by the occurrence of spikes or spike-wave discharges in response to visual stimulation (Fisher et al., 2005). Although PPR has been found in 0.5 to 7.6% subjects without epilepsy (Doose and Gerken, 1973, Trojaborg, 1992, Nagarajan et al., 2003), it is a more common feature of idiopathic generalised epilepsies (IGE), in which a PPR may be observed in 40–90% of the patients (Wolf and Goosses, 1986; Appleton et al., 2000; Lu et al., 2008). Sustained exposure to photic stimulation can induce epileptic seizures in photosensitive patients (Ferlazzo et al., 2005). Because of this close relationship between photosensitivity and epilepsy, studying mechanisms underlying PPR may shed light onto the pathophysiology of epilepsy in general. Several studies have shown that photosensitivity is characterized by an increased excitability of the occipital cortex (Porciatti et al., 2000, Siniatchkin et al., 2007). It has been demonstrated that a PPR occurs if normal physiological excitation in the occipital cortex exceeds a critical level (Wilkins et al., 2004) and if synchronization of gamma oscillations increases (Parra et al., 2003). However, these studies are only part of an incomplete puzzle and the pathophysiological mechanisms of the PPR are still insufficiently understood.
Simultaneous recording of EEG and blood oxygenation level-dependent (BOLD) functional MRI (EEG–fMRI) is a non-invasive imaging technique that allows to measure haemodynamic changes in the brain associated with GSW (Gotman et al., 2006, Laufs and Duncan, 2007). EEG–fMRI studies on spontaneous GSW have revealed a significant BOLD signal increase in the thalamus in the majority of patients, demonstrating an important role of this structure in the generation of this hypersynchronized activity (Aghakhani et al., 2004, Gotman et al., 2005, Hamandi et al., 2006, Moeller et al., 2008a, Moeller et al., 2008b). Moreover, these studies have shown a significant BOLD signal decrease in frontoparietal areas associated with GSW. These BOLD signal changes were interpreted in terms of the default mode theory which states that the parietal cortex, precuneus and frontal cortical areas are active at rest and support the state of consciousness in awake subjects (Raichle and Mintun, 2006). GSW-related BOLD signal decreases in those areas may indicate a disturbance of this physiological activity due to GSW (Gotman et al., 2005). A previous EEG–fMRI study on photosensitive patients failed to detect any PPR-related BOLD signal changes. It only showed an increased activation of the visual cortex during intermittent photic stimulation (IPS) when compared to controls, irrespectively of whether a PPR was elicited or not (Hill et al., 1999). The aim of this EEG–fMRI study was to investigate the pathophysiological mechanisms of PPRs by characterizing brain areas involved in their generation.
Section snippets
Subjects
From April 2006 to January 2008, 30 subjects with PPR were recruited from the Department of Neuropediatrics at the University Hospital Schleswig Holstein, Campus Kiel and the Northern German Epilepsy Centre for Children and Adolescents in Raisdorf, Germany. The mean age of subjects was 14 years (range: 8–22 years) at the time of the study. Neurological examination and structural MRI were normal. Visual acuity was normal or corrected-to-normal as assessed by the Snellen-chart. The study was
Results
Eight subjects had to be excluded from the study due to one of the following reasons: a) excessive movements, b) stopping of the investigation due to discomfort during IPS, c) technical problems, or d) frequent interictal generalised discharges. One other subject developed a photic induced seizure during the investigation and was reported elsewhere (Moeller et al., 2009). Six of the remaining 21 subjects showed reproducible PPR during the experiment and were included into the fMRI analysis. All
Discussion
This EEG–fMRI study describes BOLD signal changes associated with PPRs. All 6 subjects showed PPR-related increases in BOLD signal 3 s before the onset of the PPR (early regressor). In five subjects these early BOLD signal changes involved the parietal cortex in the in the vicinity of the intraparietal sulcus and the premotor cortex; in one subject, only bilateral frontal activation was found. In the analysis corresponding to the onset of PPR (standard regressor) deactivation in areas that had
Acknowledgments
We thank the subjects and their parents for participating in our study. This work was supported by grants from the BMBF (Bundesministerium für Bildung und Forschung) to H.R. Siebner (01GO 0511) and M. Siniatchkin and an intramural grant from the Medical Faculty of the University of Kiel to F. Moeller.
References (51)
- et al.
Identification of EEG events in the MR scanner: the problem of pulse artifact and a method for its subtraction
Neuroimage
(1998) - et al.
A method for removing imaging artifact from continuous EEG recorded during functional MRI
Neuroimage
(2000) - et al.
Photosensitivity in juvenile myoclonic epilepsy
Seizure
(2000) - et al.
Interaction of cortex and thalamus in spike and wave discharges of feline generalized penicillin epilepsy
Exp. Neurol.
(1982) - et al.
EEG–fMRI of idiopathic and secondarily generalized epilepsies
Neuroimage
(2006) - et al.
Hemodynamic changes preceding the interictal EEG spike in patients with focal epilepsy investigated using simultaneous EEG–fMRI
NeuroImage
(2009) - et al.
Medical technology assessment: photic stimulation—standardization of screening methods
Neurophysiol. Clin.
(1999) - et al.
Changes in activity of striato-thalamo-cortical network precede generalized spike wave discharges
NeuroImage
(2008) - et al.
Photoparoxysmal responses in children: their characteristics and clinical correlates
Pediatr. Neurol.
(2003) - et al.
Coupling between neuronal firing rate, gamma LFP, and BOLF fMRI is related to interneuronal correlations
Curr. Biol.
(2007)
Role of afferent input of subcortical origin in the genesis of bilaterally synchronous epileptic discharges of feline generalized penicillin epilepsy
Exp. Neurol.
ICA-based procedures for removing ballistocardiogram artifacts from EEG data acquired in the MRI scanner
NeuroImage
Neocortical seizures: initiation, development and cessation
Neuroscience
The different patterns of the photoparoxysmal response—a genetic study
Electroencephalogr. Clin. Neurophysiol.
fMRI activation during spike and wave discharges in idiopathic generalized epilepsy
Brain
The effects of transient functional depression of the thalamus on spindles and on bilateral synchronous epileptic discharges of feline generalized penicillin epilepsy
Epilepsia
Cellular and network mechanisms of spike-wave seizures. [Review]
Epilepsia
On the genetics of EEG-anomalies in childhood. IV. Photoconvulsive reaction
Neuropadiatrie
Cortical triggers in generalized reflex seizures and epilepsies
Brain
Epilepsy Foundation of America Working Group. Photic- and pattern-induced seizures: a review for the Epilepsy Foundation of America Working Group
Epilepsia
Statistical parametric maps in functional imaging: a general linear approach
Hum. Brain Map.
Generalized epileptic discharges show thalamocortical activation and suspension of the default state of the brain
Proc. Natl. Acad. Sci. U. S. A.
Combining EEG and fMRI: a multimodal tool for epilepsy research
J. Magn. Reson. Imaging
Two visual mechanisms of photosensitivity
Epilepsia
Hemodynamic and metabolic aspects of photosensitive epilepsy revealed by functional magnetic resonance imaging and magnetic resonance spectroscopy
Epilepsia
Cited by (63)
Drug-resistant juvenile myoclonic epilepsy: A literature review
2024, Revue NeurologiqueThe baboon in epilepsy research: Revelations and challenges
2021, Epilepsy and BehaviorCitation Excerpt :Functional neuroimaging data acquired in baboons with epilepsy further corroborated these findings [28,29]. Functional neuroimaging, including BOLD fMRI and magnetoencephalography (MEG), is the only feasible approach to studying GGE networks in humans [31–34]. Phase clustering in the high-frequency gamma range is enhanced by ILS prior to photoepileptic responses; this is most dramatic in parieto-occipital cortices during photoparoxysmal responses, and in the frontocentral cortices and parietal lobes before myoclonic and parietal lobes before absence seizures [31].
Clinical advances in photosensitive epilepsy
2019, Brain ResearchMultifocal epilepsy in children is associated with increased long-distance functional connectivity: An explorative EEG-fMRI study
2018, European Journal of Paediatric NeurologyCitation Excerpt :Therefore, abnormal connectivity in the DMN may be suggested as a functional substrate for the epileptic encephalopathy in these patients. Finally, syndrome-specific alterations in functional connectivity may also be assumed, since different epileptic syndromes are characterized by activation of specific neuronal networks during epileptic activity.36–39 Thus, in one patient suffering from Lennox-Gastaut syndrome a FC analysis has been performed pre- and postoperatively showing an increase of connectivity in the DMN when multifical IEDs were present at the clinical routine EEG.40
Photosensitivity and epilepsy: Current concepts and perspectives—A narrative review
2017, SeizureCitation Excerpt :“The maximum of BOLD signal increase related to PPR was found in the parietal cortex adjacent to intraparietal sulcus in 4 and in the frontal cortex in two subjects. The standard analysis revealed a deactivation of areas activated by using the early regressor and also deactivation of the caudate nucleus in two subject and changes in thalamus in one” [49]. Comparative MRI studies revealed an increased bilateral thickness in the occipital, frontal and parietal cortices in PPR-positive-subjects in comparison to healthy controls and a significant decrease in the temporal cortex.