Human intracranial high-frequency activity during memory processing: neural oscillations or stochastic volatility?

Abstract

Intracranial high-frequency activity (HFA), which refers to fast fluctuations in electrophysiological recordings, increases during memory processing. Two views have emerged to explain this effect: (1) HFA reflects a synchronous signal, related to underlying gamma oscillations, that plays a mechanistic role in human memory and (2) HFA reflects an asynchronous signal that is a non-specific marker of brain activation. We review recent data supporting each of these views and conclude that HFA during memory processing is more consistent with an asynchronous signal. Memory-related HFA is therefore best conceptualized as a biomarker of neural activation that can functionally map memory with high spatial and temporal precision.

Figure 1. HFA–morphology and synchrony

A: Data from human visual cortex shows the spectral morphology of gamma oscillations (“bumps”) as well as broadband increases in asynchronous power. Data courtesy of [30]. B: The number of electrodes, from an early study of episodic memory formation, exhibiting significantly greater spectral power during successful encoding across frequencies from 2 to 64 Hz. Data from [25]. C: Averaged t-statistics across 98 patients comparing spectral power for successful versus unsuccessful encoding are shown. Error bars reflect ±1 SEM across patients. Yellow asterisks mark significant increases/decreases in power during encoding (t-test; p < 0.05; Bonferroni corrected). Data courtesy of [27]. D: Two power spectra during the encoding period of a memory test for items that were later remembered (red) and later forgotten (blue). The shape of the frequency spectrum reveals a flat, asynchronous increase in high frequency power. Data courtesy of Michael J. Kahana. E: During memory formation, large increases in HFA are not accompanied by increases in high-frequency synchrony. In fact, regions showing increases in HFA power display signifi-cant decreases in phase synchrony. Data courtesy of [44].

Figure 2. The neurological stages of episodic encoding and retrieval

A: In each panel, regions that exhibited a significant change in HFA during encoding and recall on a free recall memory task are shown. Color and grayscale renderings represent the percentage of nearby regions exhibiting significant effects and containing more than 5 patients, respectively. Radiological slice view is shown with right (R) and left (L) hemispheres labeled. Data modified from [4] and [27]. B: In the left medial temporal lobe (MTL), HFA correlated with overall memory performance across patients (r=0.3911, p=0.0015). C: Each panel describes a particular stage of neural activity during memory formation and retrieval. The text above each panel provides a putative behavioral/cognitive role of each stage.