Spontaneous modulations of high-frequency cortical activity

Abstract

Objective: We clarified the clinical and mechanistic significance of physiological modulations of high-frequency broadband cortical activity associated with spontaneous saccadic eye movements during a resting state.

Methods: We studied 30 patients who underwent epilepsy surgery following extraoperative electrocorticography and electrooculography recordings. We determined whether high-gamma activity at 70-110 Hz preceding saccade onset would predict upcoming ocular behaviors. We assessed how accurately the model incorporating saccade-related high-gamma modulations would localize the primary visual cortex defined by electrical stimulation.

Results: The dynamic atlas demonstrated transient high-gamma suppression in the striatal cortex before saccade onset and high-gamma augmentation subsequently involving the widespread posterior brain regions. More intense striatal high-gamma suppression predicted the upcoming saccade directed to the ipsilateral side and lasting longer in duration. The bagged-tree-ensemble model demonstrated that intense saccade-related high-gamma modulations localized the visual cortex with an accuracy of 95%.

Conclusions: We successfully animated the neural dynamics supporting saccadic suppression, a principal mechanism minimizing the perception of blurred vision during rapid eye movements. The primary visual cortex per se may prepare actively in advance for massive image motion expected during upcoming prolonged saccades.

Significance: Measuring saccade-related electrocorticographic signals may help localize the visual cortex and avoid misperceiving physiological high-frequency activity as epileptogenic.

Keywords: 4D brain mapping; Animation; Artificial intelligence; Eloquent area; High-frequency oscillation (HFO); Intracranial recording; Machine learning; Pediatric epilepsy surgery; Perception; Phosphine; Ripples; Saccadic eye movements; Video EEG monitoring.

Fig. 1.. The extent of non-epileptic electrode sites.

(A) The spatial distribution of the analyzed electrodes on each hemisphere is presented on a color-mapped 3D brain surface image. The color of each site indicates the number of patients available at a given spatial point. Of the total 2,290 non-epileptic artifact-free electrode sites, the number of electrode sites within each region of interest (ROI) is as follows. Striatal: 127 electrode sites. Lateral-occipital: 140. Fusiform: 104. Frontal-eye field (FEF): 77. (B) The number of electrode sites which were stimulated for cortical mapping is presented. Of the total 1,903 electrode sites, the number of electrode sites within each ROI is as follows. Striatal: 127. Lateral-occipital: 140. Fusiform: 104.

Fig. 2.. Regions of interest (ROIs).

All ROIs in the present study are presented (Nakai et al., 2019; Sugiura et al., 2020). Color-coded ROIs include striatal region (light blue), lateral-occipital gyrus (LOG; orange), fusiform gyrus (FG; green), and frontal-eye field (FEF; purple). The other ROIs are anterior cingulate gyrus (aCG), caudal middle frontal gyrus (cMFG), entorhinal gyrus (Ent), inferior parietal lobule (IPL), inferior-temporal gyrus (ITG), lateral orbitofrontal gyrus (LOrb), medial orbitofrontal gyrus (MOrb), middle-temporal gyrus (MTG), paracentral gyrus (PCL), parahippocampal gyrus (PHG), postcentral gyrus (PoCG), pars opercularis of the inferior-frontal gyrus (Pop), pars orbitalis of the inferior-frontal gyrus (POr), pars triangularis of the inferior-frontal gyrus (PTr), posterior cingulate gyrus (pCG), precentral gyrus (PreCG), precuneus (PCun), rostral middle-frontal gyrus (rMFG), superior frontal gyrus (SFG), supramarginal gyrus (SMG), superior parietal lobule (SPL), superior-temporal gyrus (STG), and temporal pole (TP).

Fig. 3.. Marking of saccade onset and offset in a 14-year-old girl with left temporal lobe epilepsy.

Upper trace: Intracranial EEG (iEEG) trace at a striatal site (High-cut filter: 300 Hz. Time constant: 0.003 s). Middle trace: Dynamics of striatal high-gamma amplitude modulations compared to that during the baseline period between 600 and 200 ms prior to the saccade onset. Lower trace: Electrooculography (EOG) trace determined the timing of the saccade onset and offset (High-cut filter: 300 Hz. Time constant: 10 s).

Fig. 4.. Saccade-related high-gamma modulations.

(A) Striatal region (light blue). (B) Lateral-occipital region (orange). (C) Fusiform region (green). (D) Frontal-eye field (FEF; purple). The plots demonstrate the temporal dynamics of high-gamma amplitude time-locked to saccade onset and offset. Red line: High-gamma dynamics during saccades directed to the side contralateral to the sampled hemisphere (standard error shades are provided). Blue line: High-gamma dynamics during ipsilateral saccades. Horizontal bars denote the timing when high-gamma augmentation (upper bar) or attenuation (lower bar) reached the significance at least for 40 ms.

Fig. 5.. The spatiotemporal dynamics of peri-saccadic high-gamma modulations.

The video snapshots demonstrate the group-level percent change of saccade-related high-gamma activity relative to the baseline period (200-600 ms prior to saccade onset) derived from all 30 patients. (A-B) Saccades directed to the side ipsilateral to the iEEG sampling hemisphere. (A) 0 ms: saccade onset. (B) 0 ms: saccade offset. (C-D) Contralateral saccades. (C) 0 ms: saccade onset. (D) 0 ms: saccade offset. High-gamma activity is displayed at sites where at least two patients’ data were available.

Fig. 5.. The spatiotemporal dynamics of peri-saccadic high-gamma modulations.

The video snapshots demonstrate the group-level percent change of saccade-related high-gamma activity relative to the baseline period (200-600 ms prior to saccade onset) derived from all 30 patients. (A-B) Saccades directed to the side ipsilateral to the iEEG sampling hemisphere. (A) 0 ms: saccade onset. (B) 0 ms: saccade offset. (C-D) Contralateral saccades. (C) 0 ms: saccade onset. (D) 0 ms: saccade offset. High-gamma activity is displayed at sites where at least two patients’ data were available.

Fig. 5.. The spatiotemporal dynamics of peri-saccadic high-gamma modulations.

The video snapshots demonstrate the group-level percent change of saccade-related high-gamma activity relative to the baseline period (200-600 ms prior to saccade onset) derived from all 30 patients. (A-B) Saccades directed to the side ipsilateral to the iEEG sampling hemisphere. (A) 0 ms: saccade onset. (B) 0 ms: saccade offset. (C-D) Contralateral saccades. (C) 0 ms: saccade onset. (D) 0 ms: saccade offset. High-gamma activity is displayed at sites where at least two patients’ data were available.

Fig. 5.. The spatiotemporal dynamics of peri-saccadic high-gamma modulations.

The video snapshots demonstrate the group-level percent change of saccade-related high-gamma activity relative to the baseline period (200-600 ms prior to saccade onset) derived from all 30 patients. (A-B) Saccades directed to the side ipsilateral to the iEEG sampling hemisphere. (A) 0 ms: saccade onset. (B) 0 ms: saccade offset. (C-D) Contralateral saccades. (C) 0 ms: saccade onset. (D) 0 ms: saccade offset. High-gamma activity is displayed at sites where at least two patients’ data were available.

Fig. 6.. Prediction of the stimulation-defined primary visual cortex.

(A) The spatial distribution of primary visual sites as suggested by the gold-standard electrical stimulation mapping. (B) The spatial distribution of primary visual sites as predicted by the bagged-tree-ensemble model. (C) The receiver-operating characteristics (ROC) analysis found the accuracy of bagged-tree-ensemble model to be 95%. Red filled circle: sensitivity of 52%, specificity of 98%, positive predictive value (PPV) of 57%, and negative predictive value (NPV) of 97%.