Perception's shadow: long-distance synchronization of human brain activity

Abstract

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^1,2,3,4. Results of several experiments in animals provide support for this idea (see, for example, refs 4,5,6,7,8,9,10). In humans, gamma oscillations have been described both on the scalp^{11,12,13,14,15,16} (measured by electroencephalography and magnetoencephalography) and in intracortical recordings¹⁷, 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 another³.