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The role of phase synchronization in memory processes

Key Points

  • The term 'phase' denotes the angle corresponding to the momentary deflection of an oscillation. Phase synchronization of neural oscillations refers to the correlation of phase values between two brain regions.

  • Electroencephalography and local field potential oscillations reflect fluctuations in neuronal membrane potential and are thus related to changes in neural excitability and to spike timing. Therefore, phase synchronization between two brain regions reflects correlations of neural excitability and spike timing.

  • Correlated changes in neural excitability and spike timing are the basis for two major functions of phase synchronization: neural communication and spike timing-dependent plasticity. It is still an open question, however, how these functions interact with each other.

  • Increased phase synchronization has been observed during various memory processes, including working memory maintenance and long-term memory encoding and retrieval. Neural plasticity is probably most relevant for long-term memory formation, whereas neural communication is likely to play a part during both working and long-term memory processes.

  • Recent studies suggest that working and long-term memory operations, which have long been considered separately, are supported by overlapping brain regions, particularly the hippocampus. Phase synchronization could constitute a common neural signature of both working memory maintenance and long-term memory formation.

  • Computer models propose that cross-frequency coupling of the amplitude (and possibly even phases) of gamma oscillations to phases of theta oscillations supports the representation of multiple items in working memory. Indeed, modulations of cross-frequency phase–phase and phase–amplitude coupling have been observed depending on working memory operations.

  • Further data indicate that cross-frequency phase–amplitude and phase–phase coupling may also support long-term memory encoding of sequences and cued recall of spatial positions. Cross-frequency phase–phase and phase–amplitude coupling may constitute mechanisms that support the exchange of object representations between working and long-term memory.

  • Taken together, both empirical and theoretical evidence suggests that phase synchronization and complementary phase-based mechanisms provide a common 'neural protocol' for various memory-related operations.

Abstract

In recent years, studies ranging from single-unit recordings in animals to electroencephalography and magnetoencephalography studies in humans have demonstrated the pivotal role of phase synchronization in memory processes. Phase synchronization — here referring to the synchronization of oscillatory phases between different brain regions — supports both working memory and long-term memory and acts by facilitating neural communication and by promoting neural plasticity. There is evidence that processes underlying working and long-term memory might interact in the medial temporal lobe. We propose that this is accomplished by neural operations involving phase–phase and phase–amplitude synchronization. A deeper understanding of how phase synchronization supports the flexibility of and interaction between memory systems may yield new insights into the functions of phase synchronization in general.

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Figure 1: Putative functions of phase synchronization.
Figure 2: Patterns of phase synchronization during working and long-term memory.
Figure 3: Cross-frequency phase–phase and phase–amplitude coupling.
Figure 4: An integrative view of memory-related synchronization mechanisms.

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Acknowledgements

This work is supported by grants from the German Research Foundation (SFB TR3, project A9 and DFG project FE366/5-1). We thank J. Jitsev, P. Klaver, N. Maier, L. Melloni, P. Sauseng and B. Staresina for valuable comments on an earlier draft of this manuscript.

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Glossary

Local field potential

A neural voltage fluctuation recorded from the extracellular space, which mainly originates from postsynaptic potentials.

Neural oscillation

A periodic and continuous (wave-like) variation of a neural signal.

Oscillatory phase

The angle that corresponds to the momentary deflection of an oscillation (referring to the cosine function; for example, 0° at the peak and 180° at the trough of an oscillation).

Gamma frequency range

The frequency range between 30–100Hz.

Inactivation time constant

A variable controlling the temporal characteristics of the spontaneous inactivation of an ion channel, as described by an exponential decay function.

Coincidence-sensitive neurons

Neurons that predominantly discharge action potentials if simultaneously activated by multiple presynaptic neurons, defining a narrow time window for activation.

Hebbian learning

A cellular mechanism of learning, proposed by Donald Hebb, according to which the connection between a presynaptic and a postsynaptic cell is strengthened if the presynaptic cell is successful in activating a postsynaptic cell.

Spike timing-dependent plasticity

A special kind of neural plasticity that depends on time delays between the action potentials of the presynaptic and the postsynaptic neuron.

Spike–field coherence

The preferential firing of action potentials predominantly during a specific phase range of field potential oscillations.

Theta frequency range

The frequency range between 3–8Hz.

Spike doublets

Two action potentials that are separated by a brief temporal interval.

Material-specific buffer for short-term storage

A specialized short-term maintenance system for verbal (phonological loop) or spatial (visuo-spatial sketchpad) information.

Beta frequency range

The frequency range between 12–30Hz.

Spectral coherence

A traditional measure of synchronization between two brain regions, which comprises both the synchronization of phases and the co-variation of power (squared amplitude) of neural oscillations.

Declarative memory

Memory of consciously accessible content — for example, memory of experiences with their specific temporal and spatial contexts (episodic memory), and memory of facts (semantic memory).

Delta frequency range

The frequency range between 1–3Hz.

Aversive conditioning

A type of unconscious (non-declarative) learning that occurs when a stimulus (for example, a specific tone) is repeatedly accompanied by an unpleasant sensation such as an electric shock. After learning, presentation of the stimulus alone induces the physiological response associated with the unpleasant sensation.

Delayed matching-to-sample task

A typical working memory paradigm in which information about a single test item has to be maintained for several seconds. Afterwards, subjects have to indicate whether a probe item matches the test item.

Place cell

A hippocampal neuron that specifically responds to stimuli in certain spatial locations. Its firing rate increases when an animal or subject approaches the respective location.

Alpha frequency range

The frequency range between 8–12Hz.

Microelectrode recording

An electrophysiological recording with a microelectrode (which has a diameter of several μm) that enable researchers to measure individual action potentials in animals or humans.

Macroelectrode recording

An electrophysiological recording using macroelectrodes (contact size in the mm range), which allow electroencephalography recordings from within the animal or human brain.

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Fell, J., Axmacher, N. The role of phase synchronization in memory processes. Nat Rev Neurosci 12, 105–118 (2011). https://doi.org/10.1038/nrn2979

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