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The brainweb: Phase synchronization and large-scale integration

Key Points

  • The large-scale integration problem refers to the series of processes whereby the nervous system coordinates activity that is distributed over distant brain regions to produce a unified cognitive moment. One of the most plausible candidate mechanisms behind large-scale integration is the formation of dynamic links among brain regions, links that are mediated by phase synchronization. Phase synchronization refers to the relation between the temporal structures of the neural signals regardless of signal amplitude. Two signals are said to be synchronous if their rhythms coincide.

  • Neural assemblies — distributed networks of neurons linked by reciprocal connections — provide a conceptual framework for the integration of distributed neural activity. Large-scale integration commonly involves neural assemblies separated by long distances.

  • Converging evidence indicates that phase synchrony is probably involved in brain integration. Electrophysiological analyses in cats and primates have shown that the emergence of phase synchrony over widespread cortical domain correlates with the occurrence of attentive and perceptuomotor behaviours, as well as during the execution of a learning task. Analogous findings have been made in humans using electroencephalographic and magnetoencephalographic techniques.

  • Although the evidence for phase synchronization as a mechanism for large-scale integration is well grounded, it is only correlative. Direct proof that changes in synchronous activity can affect behaviour remains to be established in most cases. Similarly, the cellular mechanisms of synchronization, the interplay between slow and fast brain rhythms, and the role of parallel phase synchronization over different frequency bands constitute topics for future research.

Abstract

The emergence of a unified cognitive moment relies on the coordination of scattered mosaics of functionally specialized brain regions. Here we review the mechanisms of large-scale integration that counterbalance the distributed anatomical and functional organization of brain activity to enable the emergence of coherent behaviour and cognition. Although the mechanisms involved in large-scale integration are still largely unknown, we argue that the most plausible candidate is the formation of dynamic links mediated by synchrony over multiple frequency bands.

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Figure 1
Figure 2: Neural synchrony as a multiscale phenomenon.
Figure 3: Long-range integration studies I.
Figure 4: Long-range integration studies II.
Figure 5: Interdependence between different frequency components from local field potentials recorded from the cortex of a behaving cat.

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Acknowledgements

Thanks to Jean-Baptiste Poline for this help concerning metabolic imaging methods. This work was partly supported by the Ministère de l'Education et la Recherche (Action Cognitique) and the Fundacion Puelma (E.R.).

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ENCYCLOPEDIA OF LIFE SCIENCES

Brain imaging: localization of brain functions

Brain imaging: observing ongoing neural activity

Glossary

INVERSE PROBLEM

Mathematical analysis aimed at localizing the neural sources of the electromagnetic field measured at the scalp surface.

CORTICAL COLUMN

Cylinder of cortex with a diameter up to 1 mm that groups neurons with strong reciprocal connections.

BETA RHYTHM

Neural rhythmic activity (12–25 cycles per second).

GAMMA RHYTHM

Neural rhythmic activity (about 25–70 cycles per second).

TIME–FREQUENCY ANALYSIS

Mathematical techniques used to estimate the spectral components (amplitude, frequency and phase) of short non-stationary signals (for example, Wavelets, ARMA, Hilbert).

CROSS-CORRELATION

Probability for a neuron to spike as a function of the latency of the last spike of a second neuron.

GO–NO-GO PARADIGM

Task in which the subject must produce a motor response for one class of stimulus while ignoring others.

BINOCULAR RIVALRY TASK

Task in which each eye of the subject is shown a different image. This results in a bistable visual experience.

THETA RHYTHM

Neural rhythmic activity (4–8 cycles per second).

PARKINSONIAN TREMOR

Abnormal rhythmic muscular activity (4–8 Hz) observed in Parkinsonian patients.

ALPHA RHYTHM

Neural rhythmic activity (8–12 cycles per second).

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Varela, F., Lachaux, JP., Rodriguez, E. et al. The brainweb: Phase synchronization and large-scale integration. Nat Rev Neurosci 2, 229–239 (2001). https://doi.org/10.1038/35067550

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