Trends in Neurosciences
Volume 38, Issue 11, November 2015, Pages 725-740
Journal home page for Trends in Neurosciences

Review
Neural Cross-Frequency Coupling: Connecting Architectures, Mechanisms, and Functions

https://doi.org/10.1016/j.tins.2015.09.001Get rights and content

Trends

Cross-frequency coupling (CFC), in other words the association of multiple frequency neural oscillations, is present across different frequency bands and neural systems.

Circuit mechanisms determine CFC characteristics: oscillations generated in distinct versus overlapping circuits, and continuously active versus intermittent fast oscillation (FO).

Dynamic network properties determine CFC signatures: phase–phase coupling occur under weakly coupling and do not co-occur with phase–frequency coupling; phase–amplitude coupling is present when the FO is intermittent or sparse spiking; amplitude–amplitude coupling requires asymmetrical slow oscillations.

CFC is mechanistically implicated in three cognitive operations: multi-item representation, long-distance communication, and stimulus parsing.

Modeling shows that theta–gamma CFC is an intracortical mechanism for parsing speech.

Neural oscillations are ubiquitously observed in the mammalian brain, but it has proven difficult to tie oscillatory patterns to specific cognitive operations. Notably, the coupling between neural oscillations at different timescales has recently received much attention, both from experimentalists and theoreticians. We review the mechanisms underlying various forms of this cross-frequency coupling. We show that different types of neural oscillators and cross-frequency interactions yield distinct signatures in neural dynamics. Finally, we associate these mechanisms with several putative functions of cross-frequency coupling, including neural representations of multiple environmental items, communication over distant areas, internal clocking of neural processes, and modulation of neural processing based on temporal predictions.

Section snippets

Mechanistic and Functional Characteristics of Cross-Frequency Coupling

Brain oscillations are observed in vivo and in vitro in almost any neuronal population of the neo- and paleocortex. While it is relatively easy to measure oscillations and observe their modulations in various sensory states and cognitive operations, it remains largely unclear what role, if any, they play in neural information processing or, more generally, in cognition 1, 2. An intriguing feature of neural oscillations is that rhythms of distinct frequencies show specific coupling properties 3,

Multi-Item or Sequence Encoding

Many neural systems need to concurrently maintain active representations of distinct items, while avoiding interferences: these can be objects in the visual field, items in working memory, or sequences of motor commands in a complex movement [4]. Neural oscillations offer a potentially efficient tool for multi-item representation by temporally clustering spikes pertaining to each item within distinct oscillations phases. This principle allows downstream neural systems to read-out a given item

Synchronization of Fast Oscillations for Long-Distance Communication

One of the most prominent roles assigned to neural oscillations is to mediate selective neural communication between areas, with in-phase regions communicating more efficiently than out-of-phase ones [73]. Gamma rhythms have predominantly been implicated in this so-called ‘communication through coherence’ mechanism, especially for bottom-up processes [74]. However, fast oscillations only synchronize at a local scale. By contrast, slower rhythms (<10 Hz) may synchronize between distant areas 75,

Temporal Parsing of Continuous Stimuli

Many biological stimuli are characterized by an intrinsic quasi-rhythmic temporal structure, or are processed in a rhythmic mode. Speech is marked with syllabic contours, odors are sniffed at the respiratory rhythm, visual scenes are explored at the pace of saccades, etc. 81, 82. While slow oscillations in sensory areas reflect the rhythm of the sensory signal or of sensory sampling, fast gamma oscillations underpin fine-grained sensory processing in a bottom-up fashion 28, 39, 74, 83. The

Concluding Remarks

The coupling between neural oscillations may take a variety of forms, emerge from different architectures, and underpin distinct functions. However, causal relationships between neural CFC and cognitive functions are yet to be demonstrated. We hope that, by clarifying the concepts and the relationships between mechanisms and function, the framework we outlined here will stimulate original research and hence contribute to filling conceptual and empirical gaps. Essential future developments in

Glossary

Amplitude–amplitude coupling (AAC)
coupling between the amplitudes of a slow oscillation (SO) and a fast oscillation (FO).
Cross-frequency coupling (CFC)
dynamical interactions between neural oscillations operating in different frequency bands.
Dense-spiking oscillation
oscillation generated by synchrony in a neural population in which each neuron in the population emits one spike per cycle at a specific phase.
Interneuronal gamma (ING) oscillation
gamma neural oscillation (>30 Hz) arising from

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