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A neurobiological theory of meaning in perception. Part 3. Multiple cortical areas synchronize without loss of local autonomy


Information transfer and integration among functionally distinct areas of cerebral cortex of oscillatory activity requires some degree of phase synchrony of the trains of action potentials that carry the information prior to the integration. However, propagation delays are obligatory. Delays vary with the lengths and conduction velocities of the axons carrying the information, causing phase dispersion. In order to determine how synchrony is achieved despite dispersion, we recorded EEG signals from multiple electrode arrays on five cortical areas in cats and rabbits, that had been trained to discriminate visual or auditory conditioned stimuli. Analysis by time-lagged correlation, multiple correlation and PCA, showed that maximal correlation was at zero lag and averaged .7, indicating that 50% of the power in the gamma range among the five areas was at zero lag irrespective of phase or frequency. There were no stimulus-related episodes of transiently increased phase locking among the areas, nor EEG "bursts" of transiently increased amplitude above the sustained level of synchrony. Three operations were identified to account for the sustained correlation. Cortices broadcast their outputs over divergent-convergent axonal pathways that performed spatial ensemble averaging; synaptic interactions between excitatory and inhibitory neurons in cortex operated as band pass filters for gamma; and signal coarse-graining by pulse frequency modulation at trigger zones enhanced correlation. The conclusion is that these three operations enable continuous linkage of multiple cortical areas by activity in the gamma range, providing the basis for coordinated cortical output to other parts of the brain, despite varying axonal conduction delays, something like the back plane of a main frame computer.

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