Promises and limitations of human intracranial electroencephalography

Abstract

Intracranial electroencephalography (iEEG), also known as electrocorticography when using subdural grid electrodes or stereotactic EEG when using depth electrodes, is blossoming in various fields of human neuroscience. In this article, we highlight the potentials of iEEG in exploring functions of the human brain while also considering its limitations. The iEEG signal provides anatomically precise information about the selective engagement of neuronal populations at the millimeter scale and the temporal dynamics of their engagement at the millisecond scale. If several nodes of a given network are monitored simultaneously with implanted electrodes, the iEEG signals can also reveal information about functional interactions within and across networks during different stages of neural computation. As such, human iEEG can complement other methods of neuroscience beyond simply replicating what is already known, or can be known, from noninvasive lines of research in humans or from invasive recordings in nonhuman mammalian brains.

Figure 1:. Two Methods of Intracranial EEG: Electrocorticography (ECoG) and Stereo-EEG (sEEG)

While grids and strips of subdural electrodes (left) provide a large coverage over the bare surface of the cerebral cortex, they are often implanted in one hemisphere and do not reach deeper brain structures (e.g., hippocampus or insula). By comparison, depth electrodes (right) can enable bilateral monitoring of superficial and deep cortical structures but only the most superficial and deep contacts will be within the cortical gray matter while the rest of the contacts are placed in the white matter. ECoG electrodes have a circular plate shape while depth electrode contacts have a cylinder shape. The diameter of subdural plate electrodes is often 1.2 to 3mm while the diameter of depth electrodes is 0.86–1.1mm with 2.29 or 2.41mm height. The distance between the centers of two adjacent electrodes (subdural or depth) is often in the range of 4 to 10mm. The total area of the brain covered with electrodes can be in the range of 1mm² to 15mm². Lastly, it should be noted that the number of electrodes and the coverage areas are defined according to the patient’s clinical needs. Because majority of patients have seizures originating from medial temporal and frontal lobes, it is exceedingly rare to find coverage outside these regions of the brain. This often explains the relatively small number of subjects in iEEG publications reporting data from non-temporal and non-frontal sites.

Figure 2:. Recent Surge in the Number of iEEG Publications

Number of publications in PubMed using the search terms “sEEG”, “depth electrodes”, “iEEG”, “iEEG”, “ECoG”, or electrocorticography.

Figure 3:. Simultaneous recording with a broad coverage for tracking the spatiotemporal profiles of activity of populations of neurons during a particular cognitive task.

In a group of subjects simultaneous recordings in the lateral parietal and inferior temporal regions tracked HFB responses in each electrode site while the subjects were making true/false judgments on an arithmetic task in which operands (numerals 1–9) and operators (+. =) were visually presented one symbol at a time (e.g. “2”, “+”, “2”, “=”, “4”). Non-selective HFB responses in lateral occipital gyrus (LOG) and medial fusiform gyrus (mFG) contrasted the selective HFB responses to numerals in the posterior inferior temporal gyrus (pITG, red) and anterior intraparietal sulcus region (aIPS, upper left panel). Note the stronger responses in the pITG and aIPS after the presentation of the second numeral following the “+” sign and the opposite profile of HFB responses in the LOG and mFG sites. Also, of interest was the finding of HFB response selectivity across the three adjacent pITG sites (left lower panel). Neuronal populations that are ~5mm apart show clearly different profiles of responses. Note the most selective responses to numbers in the number form area (NFA) that has previously been reported in a different set of subjects. Adapted from Daitch et al 2016.

Figure 4:. Ratio of electrodes in epileptic and non- epileptic tissue.

In 100 patients implanted with ECoG or sEEG electrodes at Stanford Medical Center, we reviewed the iEEGs in each patient and labeled pathological electrodes that contained epileptic activity (i.e., recorded seizures or epileptiform spikes). We used the total number of electrodes implanted in these patients to calculate the ratio of pathological (gray) to non-pathological (green) sites. In patients with focal epilepsy, sites with pathological activity are clustered to few electrode contacts. The extent of non-pathological electrodes will depend on the density, form, and size of implanted intracranial electrodes. In a patient with wide coverage and focal epileptic zone, non-pathological sites will be covered across a large region of the brain.