Dataset Information

Human entorhinal cortex electrical stimulation evoked short-latency potentials in the broad neocortical regions: Evidence from cortico-cortical evoked potential recordings.

ABSTRACT:

Objective

We aimed at clarifying the clinical significance of the responses evoked by human entorhinal cortex (EC) electrical stimulation by means of cortico-cortical evoked potentials (CCEPs).

Methods

We enrolled nine patients with medically intractable medial temporal lobe epilepsy who underwent invasive presurgical evaluations with subdural or depth electrodes. Single-pulse electrical stimulation was delivered to the EC and fusiform gyrus (FG), and their evoked potentials were compared. The correlation between the evoked potentials and Wechsler Memory Scale-Revised (WMS-R) score was analyzed to investigate whether memory circuit was involved in the generation of the evoked potentials.

Results

In most electrodes placed on the neocortex, EC stimulation induced unique evoked potentials with positive polarity, termed as "widespread P1" (P1w). Compared with FG stimulation, P1w induced by EC stimulation were distinguished by their high occurrence rate, short peak latency (mean: 20.1 ms), small peak amplitude, and waveform uniformity among different recording sites. A stimulation of more posterior parts of the EC induced P1w with shorter latency and larger amplitude. P1w peak amplitude had a positive correlation (r = .69) with the visual memory score of the WMS-R. In one patient, with depth electrode implanted into the hippocampus, the giant evoked potentials were recorded in the electrodes of the anterior hippocampus and EC near the stimulus site.

Conclusions

The human EC electrical stimulation evoked the short-latency potentials in the broad neocortical regions. The origin of P1w remains unclear, although the limited evidence suggests that P1w is the far-field potential by the volume conduction of giant evoked potential from the EC itself and hippocampus. The significance of the present study is that those evoked potentials may be a potential biomarker of memory impairment in various neurological diseases, and we provided direct evidence for the functional subdivisions along the anterior-posterior axis in the human EC.

SUBMITTER: Takeyama H

PROVIDER: S-EPMC6749511 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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Publications

Human entorhinal cortex electrical stimulation evoked short-latency potentials in the broad neocortical regions: Evidence from cortico-cortical evoked potential recordings.

Takeyama Hirofumi H Matsumoto Riki R Usami Kiyohide K Nakae Takuro T Kobayashi Katsuya K Shimotake Akihiro A Kikuchi Takayuki T Yoshida Kazumichi K Kunieda Takeharu T Miyamoto Susumu S Takahashi Ryosuke R Ikeda Akio A

Brain and behavior 20190730 9

<h4>Objective</h4>We aimed at clarifying the clinical significance of the responses evoked by human entorhinal cortex (EC) electrical stimulation by means of cortico-cortical evoked potentials (CCEPs).<h4>Methods</h4>We enrolled nine patients with medically intractable medial temporal lobe epilepsy who underwent invasive presurgical evaluations with subdural or depth electrodes. Single-pulse electrical stimulation was delivered to the EC and fusiform gyrus (FG), and their evoked potentials were ...[more]

PMID: 31361093

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Project description:IntroductionCortico-cortical evoked potentials (CCEPs) are utilized to identify effective networks in the human brain. Following single-pulse electrical stimulation of cortical electrodes, evoked responses are recorded from distant cortical areas. A negative deflection (N1) which occurs 10-50 ms post-stimulus is considered to be a marker for direct cortico-cortical connectivity. However, with CCEPs alone it is not possible to observe the white matter pathways that conduct the signal or accurately predict N1 amplitude and latency at downstream recoding sites. Here, we develop a new approach, termed "dynamic tractography," which integrates CCEP data with diffusion-weighted imaging (DWI) data collected from the same patients. This innovative method allows greater insights into cortico-cortical networks than provided by each method alone and may improve the understanding of large-scale networks that support cognitive functions. The dynamic tractography model produces several fundamental hypotheses which we investigate: 1) DWI-based pathlength predicts N1 latency; 2) DWI-based pathlength negatively predicts N1 voltage; and 3) fractional anisotropy (FA) along the white matter path predicts N1 propagation velocity.MethodsTwenty-three neurosurgical patients with drug-resistant epilepsy underwent both extraoperative CCEP recordings and preoperative DWI scans. Subdural grids of 3 mm diameter electrodes were used for stimulation and recording, with 98-128 eligible electrodes per patient. CCEPs were elicited by trains of 1 Hz stimuli with an intensity of 5 mA and recorded at a sample rate of 1 kHz. N1 peak and latency were defined as the maximum of a negative deflection within 10-50 ms post-stimulus with a z-score > 5 relative to baseline. Electrodes and DWI were coregistered to construct electrode connectomes for white matter quantification.ResultsClinical variables (age, sex, number of anti-epileptic drugs, handedness, and stimulated hemisphere) did not correlate with the key outcome measures (N1 peak amplitude, latency, velocity, or DWI pathlength). All subjects and electrodes were therefore pooled into a group-level analysis to determine overall patterns. As hypothesized, DWI path length positively predicted N1 latency (R2 = 0.81, β = 1.51, p = 4.76e-16) and negatively predicted N1 voltage (R2 = 0.79, β = -0.094, p = 9.30e-15), while FA predicted N1 propagation velocity (R2 = 0.35, β = 48.0, p = 0.001).ConclusionWe have demonstrated that the strength and timing of the CCEP N1 is dependent on the properties of the underlying white matter network. Integrated CCEP and DWI visualization allows robust localization of intact axonal pathways which effectively interconnect eloquent cortex.

Project description:Recent studies have suggested that cortical gamma-oscillations are tightly linked with various forms of physiological activity. In the present study, the dynamic changes of intracranially recorded median-nerve somatosensory-evoked potentials (SEPs) and somatosensory-induced gamma-oscillations were animated on a three-dimensional MR image, and the temporal and spatial characteristics of these activities were analysed in 10 children being evaluated for epilepsy surgery. Visual and quantitative assessments revealed that short-latency SEPs and somatosensory-induced gamma-oscillations predominantly involved the post-central gyrus and less intensely involved the pre-central gyrus and the anterior parietal lobule. Formation of a dipole of N20 peak with opposite polarities across the central sulcus was well delineated in animation movies. High-frequency (100-250 Hz) somatosensory-induced gamma-oscillations emerged in the post-central gyrus at 13.6-17.5 ms after median-nerve stimulation, gradually slowed down in frequency around and below 100 Hz, and progressively involved the neighbouring areas. A substantial proportion of somatosensory-induced gamma-oscillations was initially phase-locked and the proportion of a non-phase-locked component gradually increased over time. The primary motor hand areas proven by cortical stimulation frequently coincided with the sites showing the largest N20 peak and the largest somatosensory-induced gamma oscillations. In vivo animation of SEPs and somatosensory-induced gamma oscillations both may be utilized to localize the primary sensory-motor hand area in pre-surgical evaluation. The dipole on SEPs is consistent with the previously accepted notion that the cortices along the central sulcus are activated. The high-frequency somatosensory-induced gamma-oscillations in the post-central gyrus may represent the initial neural processing for external somatosensory stimuli, whereas the subsequent lower-frequency oscillations might represent the reafferent cortical activity occurring in larger cortical networks.

Dataset Information

Human entorhinal cortex electrical stimulation evoked short-latency potentials in the broad neocortical regions: Evidence from cortico-cortical evoked potential recordings.

Objective

Methods

Results

Conclusions

Publications

Human entorhinal cortex electrical stimulation evoked short-latency potentials in the broad neocortical regions: Evidence from cortico-cortical evoked potential recordings.

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