Direct brain recordings fuel advances in cognitive electrophysiology

Abstract

Electrocorticographic brain recordings in patients with surgically implanted electrodes have recently emerged as a powerful tool for examining the neural basis of human cognition. These recordings measure the electrical activity of the brain directly, and thus provide data with higher temporal and spatial resolution than other human neuroimaging techniques. Here we review recent research in this area and in particular we explain how electrocorticographic recordings have provided insight into the neural basis of human working memory, episodic memory, language, and spatial cognition. In some cases this research has identified patterns of human brain activity that were unexpected on the basis of studies in animals.

Figure 1. Performing electrocorticographic recordings in humans

A. An MRI image of one patient's brain with the locations of implanted ECoG electrodes indicated with white dots. Modified, with permission, from Ref. [56]. B. An illustration of an 8×8 electrode grid; gray shading indicates electrodes' conductive surfaces. (Illustrations not to scale). C. A illustration of an 8-electrode strip. D. A depth electrode with eight contacts. E. A depth electrode with microwires extending from the tip to record action potentials (marked by the arrow). F. A recording of ECoG activity from the right temporal gyrus. G. The power spectrum of the recording from Panel F, which shows that this trace exhibits a robust theta oscillation.

Figure 2. Oscillatory brain activity in human working memory

A. Schematic of a working-memory task. B. Phase-reset analysis of ECoG activity from an electrode in one patient's right subcallosal gyrus during this task. The color at each frequency and timepoint indicates the z score from a Raleigh test evaluating the uniformity of the ECoG phase distribution (computed across trials). Warm colors indicate significant phase resetting. Modified, with permission, from Ref. [27]. C. Gamma power from a Broca's Area electrode in a different patient performing a variant of this task where each stimulus is preceded by an indication of whether the item should be attended (green dot) or ignored (red dot). This electrode's gamma power is correlated with memory load, as this activity increases following stimuli that are remembered. Modified, with permission, from Ref. [62]. D. Normalized oscillatory power at a site from one patient's in the parahippocampal gyrus that exhibited elevated theta activity during memory retention. Red coloring indicates elevated oscillatory power relative to baseline. Modified, with permission, from Ref. [97]. E. An electrode from a right frontal cortex that resetted to different phases between viewing study items (left) and viewing cues (right). Each plot is a circular histogram that indicates the number of trials where different theta phases were observed 100 ms after stimulus onset (0°indicates the peak phase of theta, and 180°is the trough). Black arrow indicates the mean theta phase. Modified, with permission, from [66].

Figure 3. The relation between oscillatory brain activity and neuronal spiking

A. The activity of a neuron from the right superior temporal gyrus that spiked just before the peak of the theta oscillation. Left panel, average local-field potential (LFP) computed relative to each spike. Middle panel, z score from a Rayleigh test, which measured LFP phase uniformity at the time of each spike, as a function of frequency and time offset. White ‘×’ indicates the frequency of peak phase locking. Right panel, firing rate of this cell as a function of instantaneous theta phase at the frequency of peak phase locking. Adapted, with permission, from Ref. [30]. B. The activity of a neuron from one patient's auditory cortex whose spiking was tightly coupled to the amplitude of simultaneous gamma oscillations (r = 0.84). Ticks in top row indicate individual action potentials. Middle row depicts the LFP signal filtered to only include frequencies below 130 Hz. Bottom row indicates LFP gamma power (black) and neuronal firing rate (blue), showing that these two measures are closely related. Adapted, with permission, from Ref. [17].

Figure 4. Gamma-band correlates of specific cognitive representations

A. The activity of an electrode from left-temporal cortex that exhibited significant variations in high-gamma (65–128 Hz) amplitude according to the identity of the stimulus that was viewed. Blue line indicates the gamma amplitude after viewing ‘F,’ red indicates the gamma amplitude after viewing ‘D,’ and orange indicates the mean gamma power across all letters. Shaded rectangles indicate timepoints where this effect is significant (gray indicates p < 0.05, black indicates p < 10^-5). B. Right panel indicates the mean high-gamma power for each letter at the timepoint of peak letter-related differences (indicated by the black dashed line in left panel). Modified, with permission, from Ref. [53].