Mechanisms of Zero-Lag Synchronization in Cortical Motifs

Zero-lag synchronization between distant cortical areas has been observed in a diversity of experimental data sets and between many different regions of the brain. Several computational mechanisms have been proposed to account for such isochronous synchronization in the presence of long conduction delays: Of these, the phenomenon of “dynamical relaying” – a mechanism that relies on a specific network motif – has proven to be the most robust with respect to parameter mismatch and system noise. Surprisingly, despite a contrary belief in the community, the common driving motif is an unreliable means of establishing zero-lag synchrony. Although dynamical relaying has been validated in empirical and computational studies, the deeper dynamical mechanisms and comparison to dynamics on other motifs is lacking. By systematically comparing synchronization on a variety of small motifs, we establish that the presence of a single reciprocally connected pair – a “resonance pair” – plays a crucial role in disambiguating those motifs that foster zero-lag synchrony in the presence of conduction delays (such as dynamical relaying) from those that do not (such as the common driving triad). Remarkably, minor structural changes to the common driving motif that incorporate a reciprocal pair recover robust zero-lag synchrony. The findings are observed in computational models of spiking neurons, populations of spiking neurons and neural mass models, and arise whether the oscillatory systems are periodic, chaotic, noise-free or driven by stochastic inputs. The influence of the resonance pair is also robust to parameter mismatch and asymmetrical time delays amongst the elements of the motif. We call this manner of facilitating zero-lag synchrony resonance-induced synchronization, outline the conditions for its occurrence, and propose that it may be a general mechanism to promote zero-lag synchrony in the brain.Author Summary: Understanding large-scale neuronal dynamics – and how they relate to the cortical anatomy – is one of the key areas of neuroscience research. Despite a wealth of recent research, the key principles of this relationship have yet to be established. Here we employ computational modeling to study neuronal dynamics on small subgraphs – or motifs – across a hierarchy of spatial scales. We establish a novel organizing principle that we term a “resonance pair” (two mutually coupled nodes), which promotes stable, zero-lag synchrony amongst motif nodes. The bidirectional coupling between a resonance pair acts to mutually adjust their dynamics onto a common and relatively stable synchronized regime, which then propagates and stabilizes the synchronization of other nodes within the motif. Remarkably, we find that this effect can propagate along chains of coupled nodes and hence holds the potential to promote stable zero-lag synchrony in larger sub-networks of cortical systems. Our findings hence suggest a potential unifying account of the existence of zero-lag synchrony, an important phenomenon that may underlie crucial cognitive processes in the brain. Moreover, such pairs of mutually coupled oscillators are found in a wide variety of physical and biological systems suggesting a new, broadly relevant and unifying principle.