Characteristics of very high frequency oscillations of somatosensory evoked potentials in humans with epilepsy

We previously firstly reported very high frequency oscillations (VHFOs, over 1,000 Hz) in somatosensory evoked potentials (SEP) recorded by subdural electrodes following median nerve stimulation on 6 patients. In this study, we fatherly studied the characteristics and the clinical significance of VHFOs) in SEP elicited by stimulating not only the median, but also the ulnar nerves. Conventional somatosensory evoked potentials, including higher frequency components, were recorded by subdural electrodes in 25 patients with intractable epilepsy who underwent intracranial electroencephalographic monitoring for epilepsy surgery. The location, latency, frequency, amplitude and duration of very high frequency components were analyzed. The location of VHFOs was compared with N20 for median and ulnar nerves in each patient. VHFOs were recorded in a very limited region around the central sulcus, mainly on the postcentral gyrus. All VHFOs preceded the earliest peaks of conventional SEP, with the following characteristics: frequencies ranging from 1,000 to 5,000 Hz (mostly from 1,000 to 2,500 Hz), mean amplitude 1.5 μV, and mean duration 1.67 ms. There were no significant differences in amplitude and frequency of VHFOs among median and ulnar nerve stimulations. We hypothesize that VHFOs may be generated in the representative zone for each nerve within the primary somatosensory cortex, and hence can be utilized for more precise localization of the central sulcus. Neurology Asia 2014; 19(2) : 137 – 148 Address correspondence to: Kiyohito TERADA, M.D., Department of Neurology, National Epilepsy Center, Shizuoka Institute of Epilepsy and Neurological Disorders, 886 Urushiyama, Aoi-ku, Shizuoka, 420-8688 JAPAN. Tel: +81-54-245-5446, Fax: +81-54-247-9781, Email: [email protected], [email protected] INTRODUCTION Confirmation of the primary somatosensory area (SI) and the primary motor area (MI) is clinically important in epilepsy surgery. Currently, cortical stimulation is generally used as the golden standard, and somatosensory evoked potentials (SEP) are recorded in the clinical situation. However, cortical stimulation is well known to give false negative and false positive results. Furthermore, although SEP in response to median nerve stimulation (Med-SEP) can be used for this purpose by analyzing N20/P22, the specificity is also limited. Therefore, it is clinically important to develop a new technique to identify these eloquent areas more precisely. The first cortical component of Med-SEP is termed N20, and has been reported to be generated from area 3b in SI. Recent studies on human SEP have identified the existence of a high frequency component around 600 Hz, which can be isolated from the underlying parietal N20 component by expanding the high-pass filter (to above 300 Hz). This component is termed high frequency oscillations (HFOs). HFOs reportedly show phase reversal across the central sulcus, and are therefore speculated to be generated within SI, probably in area 3b. Magnetoencephalographic studies also suggest that HFOs are generated in SI. In contrast, dipole source analysis of multichannel scalp SEP recordings showed that the early oscillations originate from the subcortical structures near the thalamus, whereas the subsequent components originate from SI. Our previous study also demonstrated that HFOs do not show clear phase reversal between MI and SI in some patients, which indicates that the generator is not likely to be on the bank of the central sulcus. Furthermore, the amplitude of Neurology Asia June 2014 138 HFOs decreases in sleep and the waves gradually disappear, which suggests that HFOs may be generated by mechanisms different from that of N20. Only a few studies have reported SEP (UlnSEP) and HFOs in response to ulnar nerve stimulation. On scalp EEG, Med-SEP and Uln-SEP show no significant difference. To the best of our knowledge, the present study is the first to record and characterize HFOs in response to ulnar nerve stimulation, recorded directly from the surface of human cortex by subdural electrodes. In a previous animal study, very high frequency components of SEP (greater than 1,000 Hz) were reported in pigs. We also recorded high frequency SEP components greater than 1,000 Hz from the human brain, and named these components “very high frequency oscillations (VHFOs)”. Compared with N20/P22 and HFOs, VHFOs were recorded in a more restricted area around SI. Therefore, we speculated that VHFOs might be clinically useful to delineate the eloquent areas. However, in the previous study, we studied only four patients showing VHFOs in response to median nerve stimulation. In the present study, we increased the number of patients, and studied VHFOs not only from the median nerve but also from the ulnar and tibial nerves. Furthermore, we investigated the characteristics of VHFOs more precisely, and examined their clinical significance.