Theta Oscillations in Human Memory

Abstract

Theta frequency (4-8 Hz) fluctuations of the local field potential have long been implicated in learning and memory. Human studies of episodic memory, however, have provided mixed evidence for theta's role in successful learning and remembering. Re-evaluating these conflicting findings leads us to conclude that: (i) successful memory is associated both with increased narrow-band theta oscillations and a broad-band tilt of the power spectrum; (ii) theta oscillations specifically support associative memory, whereas the spectral tilt reflects a general index of activation; and (iii) different cognitive contrasts (generalized versus specific to memory), recording techniques (invasive versus noninvasive), and referencing schemes (local versus global) alter the balance between the two phenomena to make one or the other more easily detectable.

Keywords: SME; associative memory; intracranial EEG; spectral tilt; theta.

Figure 1.. Formation of associative memories via theta oscillations.

A. Spatial navigation constitutes a sequential set of sensory inputs that correspond to locations in space. Neural representations of a location become stronger the closer the observer is to that location. Locations exist as 2 (or 3) dimensional coordinates. B. Episodic memory, such as learning a list of nouns, consists of a sequential set of inputs that correspond to semantic and temporal features of encountered words. Words exist as locations in a multidimensional semantic/temporal feature space. C. Theta oscillations serve to organize sequential inputs, by representing multiple locations or items within a single theta cycle [5]. The current location or item is represented most strongly, but prior and forthcoming representations are also activated, though to a lesser degree (Panel C adapted from [2]). See Box 2 and for further details.

Figure 2.. Theta effects in human episodic memory.

The matrix is organized by recording technique (invasive vs. non-invasive, columns) and analysis technique (memory success vs. measures of associative memory, rows). “Memory success” refers to encoding contrasts between subsequently remembered and forgotten items (subsequent memory effect, SME) or to retrieval contrasts between correct memory retrieval and events where no retrieval occurs (i.e. “deliberation” in free recall, misses or correct rejections in recognition tasks). “Associative memory contrast” refers to analytic methods that compare correct encoding or retrieval trials based on a measure of episodic association, such as the amount of retrieved/encoded context, memory accuracy, or vividness of recall. Red indicates the given study reported significant increases in theta power, blue means theta decreases, and purple means the study reported significant increases and decreases (see supplemental materials for a more detailed description of these studies). [–,–,–,–,,,,,–123].

Figure 3.. Narrow-band low frequency oscillations during memory processing.

We describe two scenarios that could result in the observed low-frequency power decreases associated with successful memory processing: one in which the decrease is driven by a tilt of the background spectrum, which may be observed despite an increase in narrow-band oscillations in the successful compared to the unsuccessful condition (Hypothesis #1); and another one in which a decrease in power during successful vs. unsuccessful encoding occurs due to a true reduction in narrow-band oscillations (Hypothesis #2).

Figure 4.. Opposing directions of theta power and phase synchrony.

A. Top: Local and narrowband increases in theta power, as detected by a subset of intracranial electrodes (red circles), specifically underlie increases in long-range phase synchronization. Surrounding electrodes exhibit decreases in power due to tilt-related factors and show no significant change in their long-range synchrony with other regions. Averaged across electrodes, an increase in phase synchronization and decrease in power is observed. Bottom: All electrodes show a decrease in power, driven either by spectral tilt alone or narrowband increases in theta that are overwhelmed by the strength of the tilt. Due to increases in narrowband theta, or another mechanism entirely, such decreases in power co-occur with increases in long-range phase synchronization. B. In the case of Hypothesis #2, decreases in power can occur alongside increases in connectivity so long as the overall level of theta power is still sufficient to achieve inter-regional phase locking.

Figure 5.. Physiological origins of the scalp vs. intracranial theta discrepancy.

A. A possible contribution to the dissociation between theta findings between scalp and intracranial EEG is the tendency for scalp EEG to integrate signals over much larger areas of cortex, and thereby reflect not only theta amplitude but also the degree of large-scale theta synchronization. Under this model, theta amplitude can decrease in good memory states (blue-colored circles), but long-range synchronization may increase (red lines). Intracranial measurements reflect highly local activity and therefore exhibit decreases, while scalp EEG reflects larger-scale synchronization and shows increases. Notably, increases in long-range synchronization occur due to increases in narrowband theta power that are obscured in the average by a spectral tilt (orange box). B. Electrode referencing schemes can also affect measurements of theta power. In a “monopolar” style referencing scheme, such as the common average, intracranial electrodes may detect local increases in theta power (red circles). Similarly, scalp EEG electrodes sum these increases over wide areas of cortex. The high-pass spatial filtering properties of the bipolar reference tend to reduce or abolish this effect, potentially obscuring findings of memory-related theta increases.