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.

This article presents, for the first time, a practical method for the direct quantification of frequency-specific synchronization (i.e., transient phase-locking) between two neuroelectric signals. The motivation for its development is to be able to examine the role of neural synchronies as a putative mechanism for long-range neural integration during cognitive tasks. The method, called phase-locking statistics (PLS), measures the significance of the phase covariance between two signals with a reasonable time-resolution (<100 ms). Unlike the more traditional method of spectral coherence, PLS separates the phase and amplitude components and can be directly interpreted in the framework of neural integration. To validate synchrony values against background fluctuations, PLS uses surrogate data and thus makes no a priori assumptions on the nature of the experimental data. We also apply PLS to investigate intracortical recordings from an epileptic patient performing a visual discrimination task. We find large-scale synchronies in the gamma band (45 Hz), e.g., between hippocampus and frontal gyrus, and local synchronies, within a limbic region, a few cm apart. We argue that whereas long-scale effects do reflect cognitive processing, short-scale synchronies are likely to be due to volume conduction. We discuss ways to separate such conduction effects from true signal synchrony.

Transient periods of synchronization of oscillating neuronal discharges in the frequency range 30-80 Hz (gamma oscillations) have been proposed to act as an integrative mechanism that may bring a widely distributed set of neurons together into a coherent ensemble that underlies a cognitive act. Results of several experiments in animals provide support for this idea. In humans, gamma oscillations have been described both on the scalp (measured by electroencephalography and magnetoencephalography) and in intracortical recordings, but no direct participation of synchrony in a cognitive task has been demonstrated so far. Here we record electrical brain activity from subjects who are viewing ambiguous visual stimuli (perceived either as faces or as meaningless shapes). We show for the first time, to our knowledge, that only face perception induces a long-distance pattern of synchronization, corresponding to the moment of perception itself and to the ensuing motor response. A period of strong desynchronization marks the transition between the moment of perception and the motor response. We suggest that this desynchronization reflects a process of active uncoupling of the underlying neural ensembles that is necessary to proceed from one cognitive state to another.

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