Oscillatory power decreases and long-term memory: the information via desynchronization hypothesis

Abstract

The traditional belief is that brain oscillations are important for human long-term memory, because they induce synchronized firing between cell assemblies which shapes synaptic plasticity. Therefore, most prior studies focused on the role of synchronization for episodic memory, as reflected in theta (∼5 Hz) and gamma (>40 Hz) power increases. These studies, however, neglect the role that is played by neural desynchronization, which is usually reflected in power decreases in the alpha and beta frequency band (8-30 Hz). In this paper we present a first idea, derived from information theory that gives a mechanistic explanation of how neural desynchronization aids human memory encoding and retrieval. Thereby we will review current studies investigating the role of alpha and beta power decreases during long-term memory tasks and show that alpha and beta power decreases play an important and active role for human memory. Applying mathematical models of information theory, we demonstrate that neural desynchronization is positively related to the richness of information represented in the brain, thereby enabling encoding and retrieval of long-term memories. This information via desynchronization hypothesis makes several predictions, which can be tested in future experiments.

Keywords: EEG; MEG; alpha; beta; desynchronization; long-term memory; oscillations; synchronization.

Figure 1

The different frequency bands and their relation to memory. (A) A time-frequency power spectrum of a parietal electrode (Pz) is shown during a memory task. Time 0 indicates stimulus presentation. Power increases relative to baseline (red) can be seen in the theta and gamma frequency range, whereas relative power decreases (blue) emerge in the alpha and beta frequency range. (B) A schematic depiction of the power in the different frequency bands is shown and how they typically relate to memory. Blue refers to items for which memory succeeds (Memory+), red refers to items for which memory fails (Memory−).

Figure 2

Alpha/beta power during encoding. (A) Alpha/beta power decreases during encoding are more pronounced for words which are subsequently remembered (blue) than for words which are subsequently forgotten (red). (B) Alpha (left) and beta (right) SMEs are shown during deep (semantic) encoding. Negative SMEs were observed in both frequency bands from 500 to 1500 ms after stimulus onset. The gray bars indicate the time windows for plotting the corresponding topographies (bottom). Figure adapted from Hanslmayr et al. (2009a).

Figure 3

Beta power decrease and BOLD signal during memory formation. (A) The topography of the beta SME (left) is shown together with the source localization (right). Stronger power decreases for subsequently remembered in contrast to forgotten items was observed in the left inferior frontal gyrus (IFG). (B) The negative correlation between beta power and BOLD signal is shown in red, together with the SME in the fMRI, shown in green; yellow areas denote an overlap between fMRI SMEs and negative BOLD—beta power correlations. (C) The correlation between beta power and BOLD is shown for two regions within the left IFG as a function of subsequent memory (M+ vs. M−). Figure adapted from Hanslmayr et al. (2011b).

Figure 4

Alpha/beta power during memory retrieval. (A) Alpha/beta power decreases are typically more pronounced during recognition of old items (hits), compared to correctly identified new items (correct rejections). (B) Beta power during retrieval of positions (left) and objects (right) is shown. Black colors denote the difference in relative power decreases (ERD) between a condition in which two items (Fan1) or four items (Fan3) were recalled. The topographies on the lower left side denote the electrode positions showing a significant difference between the two Fan conditions. Note the different topographies between recall of positions and recall of objects. Figure reproduced with permission from Khader and Rösler (2011).

Figure 5

Alpha/beta power during selective retrieval. (A) Subjects encoded shape—color pairs. In one condition two colors were associated with a shape, in the other condition one color was associated with a shape. (B) During the selective retrieval phase the shape was presented together with a cue, specifying the to-be-retrieved target color. (C) Alpha/beta power (11.5–20 Hz) during selective retrieval is shown. The color bar denotes the difference in relative power (%) between the two-color and the one-color condition. Note the increase in alpha/beta power over the competitor hemisphere (comp) and the decrease in power over the target hemisphere (targ). Figure adapted from Waldhauser et al. (2012).

Figure 6

The link between desynchronization and information. (A) Firing rates for a population of neurons (N = 50) was simulated with either no synchrony (left panel), a low degree of synchrony (middle panel), or a high degree of synchrony (right panel). The total number of spikes in each population was the same. The lower panels plot the corresponding local field potentials (LFP). (B) The power (15 Hz) in the LFP increases as a function of synchrony. (C) Information, calculated with Shannon's Entropy, derived from the firing rates of the three neural populations is plotted. (D) The relation between LFP power and information is plotted for simulations with varying degrees of synchrony. Note the inverse relationship between information and synchrony/LFP-power.

Figure 7

Two different neural connection properties and their relation to synchrony and LTP are shown. (A) Two pyramidal neurons (P1 and P2) have excitatory projections to a down-stream neuron D. If these neurons fire in synchrony (as it happens at t1), their impact on the down-stream neuron adds up, thus increasing the likelihood of a discharge and LTP. If they fire asynchronously (t2 and t3) there is low probability that D will discharge and show LTP. (B) Neuron P1 has excitatory projections to the downstream neuron D, whereas neuron P2 has an indirect inhibitory projection to D, via an inhibitory interneuron I. In this case, synchronized firing (at t1) does not add up. Instead, only desynchronized firing (at t2) would lead to a depolarization of D, enhancing the likelihood of LTP. Figure inspired by Schneidman et al. (2011).