Zero-lag synchronous dynamics in triplets of interconnected cortical areas

Oscillatory and synchronized activities involving widespread populations of neurons in neocortex are associated with the execution of complex sensorimotor tasks and have been proposed to participate in the 'binding' of sensory attributes during perceptual synthesis. How the brain constructs these coherent firing patterns remains largely unknown. Several mechanisms of intracortical synchronization have been considered, in particular mutual inhibition and reciprocal excitation. These mechanisms fail to account for the zero-lag correlations observed among areas located at different levels in the visual hierarchy because the asymmetric laminar organization of ascending and descending connections in this hierarchy would predict systematic inter-areal phase lags. Here we show through detailed computer simulations that, when triplets rather than pairs of reciprocally connected areas in a cortical hierarchy are considered, zero-lag synchronization emerges naturally from their three-way interactions. These simulations were motivated by the observation that most areas in the cat and macaque monkey visual cortex are organized in such triplets. Our results suggest that patterns of anatomical connections in the mammalian neocortex provide a structural basis for the multi-level synchronization of neuronal activity. (C) 2001 Elsevier Science Ltd. All rights reserved.