Do scalp-recorded slow potentials during neuro-feedback training reflect the cortical activity?
Introduction
Neuro-feedback (NFB) is a therapy for treating various neurological diseases such as epilepsy, attention-deficit hyperactivity disorder, and migraine (Wyckoff and Strehl, 2011). The regulation of slow potentials (SPs) can be applied for alleviating the symptoms of brain disorders. The SPs recorded by the scalp electrodes area are generated in the cerebral cortex and are therefore called as slow cortical potentials (SCPs).
The proposed mechanism of SCP includes the direct current potential shifts of the large neuronal assemblies of the cortex. Negative SCP shifts increase the firing probabilities of a cell assembly, whereas positive SCP shifts inhibit this activity (Birbaumer et al., 1990). In epilepsy patients, negative SCPs are recorded at the time of seizure onset as ictal electrocortico-corticogram (ECoG) with subdural electrode changes (Ikeda et al., 1996). Thus, NFB training was attempted to reduce the seizure frequency by the reinforcement of positive SCP (positivation or positive shift). In fact, several studies have demonstrated considerable the clinical efficacy of this approach (Rockstrohet al., 1993, Kotchoubeyet al., 1999, Strehlet al., 2005).
However, a previous report revealed no direct relationship between the number of spikes at the seizure onset zone (SOZ) and the shifts of SCPs in the scalp vertex EEG (Fritz et al., 2011). Furthermore, SP is highly susceptible to artifact contamination from various sources such as eye blinks, body movement, and galvanic skin response (GSR). Therefore, there is considerable doubt on whether patients who learned NFB were actually trained with SCPs derived from the brain itself. Despite the considerable clinical value on the NFB of SPs for seizure control in epilepsy, the underlying mechanism remains unclear.
Thus, we aimed to investigate the consistency of SPs between the subdural ECoG and scalp electroencephalogram (EEG) by using simultaneous recordings in patients with refractory epilepsy who underwent chronic implantation of intracranial electrodes for presurgical evaluation. We hypothesized that SPs recorded from the scalp were well-correlated with the SCPs recorded from intracranial electrodes. In other words, SPs recorded from the scalp are SCPs. We also hypothesized that electrode pairs that are closer to each other produces SCPs with higher consistency irrespective of the anatomy. To prove this hypothesis, we first grouped the intracranial electrodes on the basis of their embedded anatomical regions and then analyzed the coherence of SPs between a scalp-recorded EEG and intracranial-recorded ECoG with respect to each anatomical region.
Section snippets
Subjects
The inclusion criteria consisted of patients with drug-resistant focal epilepsy who underwent extraoperative subdural electrocorticography recording for presurgical evaluation between 2011 and 2014. A total of 10 patients (4 women; age: 24–45 years), who provided their informed consent, were enrolled in our research (Table 1). Intracranial electrodes were placed over the cortical surfaces or within the cortices, including the lateral convexity and lateral and basal temporal areas (left
Results
After excluding a bad electrode, the number of analyzed ECoG channels ranged from 18 to 25 among the patients (Table 1). In Pt. 6, a defective electrode was found in an HEOG electrode. This fault caused several ECoG channels to develop considerable AC contamination. Hence, we excluded all data belonging to Pt. 6 from further analysis.
As shown in Table 1, most recorded intracranial electrodes in this study were subdural grid/strip, which attached over the cortical surface. On the other hand, no
Discussion
The results of this study suggest that SP coherence has a negative correlation with the distance between the subdural and scalp electrodes. In this study, electrodes in high lateral convexity, such as dPrCG, dPoCG, and middle frontal gyrus, which had the closest proximity to the scalp electrodes, revealed high coherence values. By contrast, the distantly positioned electrodes, such as those in the basal temporal and basal frontal regions, revealed comparatively lower coherence values (
Conclusions
This study proved that SPs recorded in the scalp vertex electrodes were primarily derived from high lateral convexity. We also confirmed that NFB participants regulate SPs derived from the cortices.
Acknowledgments
This work was supported by the Japan Ministry of Education, Culture, Sports, Science and Technology (MEXT) KAKENHI Grant Numbers 15H05874, 17H05907, Japan Society for the Promotion of Science (JSPS) KAKENHI Grant Numbers 26293209, 26282218, and the Research Grants from the Japan Epilepsy Research Foundation. The authors would like to thank Enago (www.enago.jp) for the English language review.
Conflict of interest
Department of Epilepsy, Movement Disorders and Physiology is an endowment department, supported with a grant from GlaxoSmithKline K.K., Nihon Kohden Corporation, Otsuka Pharmaceuticals Co., and UCB Japan Co., Ltd. K. Other authors have no conflict of interest to disclose.
References (24)
- et al.
Comparison of subcortical, cortical and scalp activity using chronically indwelling electrodes in man
Electroencephalogr Clin Neurophysiol
(1965) - et al.
Coherence between fMRI time-series distinguishes two spatial working memory networks
NeuroImage
(2005) - et al.
Do surface DC-shifts affect epileptic hippocampal EEG activity?
Epilepsy Res
(2011) - et al.
Bereitschaftspotential augmentation by neuro-feedback training in Parkinson's disease
Clin Neurophysiol
(2013) - et al.
Correlation between scalp-recorded electroencephalographic and electrocorticographic activities during ictal period
Seizure
(2007) - et al.
Virtual 10–20 measurement on MR images for inter-modal linking of transcranial and tomographic neuroimaging methods
NeuroImage
(2005) - et al.
Negative potential shifts and the prediction of the outcome of neurofeedback therapy in epilepsy
Clin Neurophysiol
(1999) - et al.
Cephalic skin potentials in electroencephalography
Electroencephalogr Clin Neurophysiol
(1972) - et al.
Cortical self-regulation in patients with epilepsies
Epilepsy Res
(1993) - et al.
Predictors of seizure reduction after self-regulation of slow cortical potentials as a treatment of drug-resistant epilepsy
Epilepsy Behav
(2005)
Electrode and brain modeling in stereo-EEG
Clin Neurophysiol
Extent of cortical generators visible on the scalp: effect of a subdural grid
NeuroImage
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2019, Clinical NeurophysiologyCitation Excerpt :However, epileptiform activity can be modified in at least some patients with generalized seizures (Beniczky et al., 2012; Lunardi et al., 2016). Operant conditioning, biofeedback, relaxation therapies, and other behavioral methods can reduce seizures and can alter EEG or evoked potential activity (Efron, 1957; Sterman et al., 1974; Sterman and Shouse, 1980; Kotchoubey et al., 2001; Nagai et al., 2004; Fumuro et al., 2013; Kotwas et al., 2016, Fumuro et al., 2018). These take time to learn, and often several training sessions, whereas our patients’ ADs were terminated quickly, and without prior training.