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Far in space and yet in synchrony: a neuronal mechanism for zero-lag long-range synchronization in the brain

By C. MIRASSO, R. VICENTE, G. PIPA, L. L. GOLLO, I. FISCHER
Neuroscince 2009, Chicago, USA 2009

Multi-electrode recordings have revealed that distant neuronal populations synchronize their activity patterns at zero-lag during certain stages of cognitive acts. These isochronous firings among remote cerebral cortical areas occur although the axonal conduction delays can amount to several tens of milliseconds. It is not clear yet which mechanism is responsible for giving rise to the isochronous discharge of widely distributed neurons, despite of such latencies. Several mechanisms have been pointed out as partially responsible for the enhancement of such synchrony. Inhibitory synapses and gap junctions have been proposed to stabilize the synchronous firing of cells under some specific conditions and for a limited range of delays [1]. In the case of the hippocampus a canonical circuit of excitatory and inhibitory neurons have been shown to successfully reproduce the experimental findings of long-range synchrony among hippocampal neurons [2]. Synaptic  plasticity mechanisms have also been shown to stabilize synchronous gamma oscillations between distant cortical areas by reinforcing the connections the delay of which matches the period of the oscillatory activity [3].
In this work we investigate the synchronization properties of a simple network motif and found that, even in the presence of large axonal conduction delays, distant neuronal populations self-organize into lag-free oscillations [4]. According to our results cortico-cortical association fibers as well as certain cortico-thalamocortical
loops represent ideal circuits to circumvent the phase-shifts and time-lags associated with conduction delays.
[1] N. Kopell and G. Ermentrout, Chemical and electrical synapses perform complementary roles in the synchronization of interneuronal networks. Proc. Natl. Acad. Sci. 101, 15482 (2004).
[2] R. Traub et al., A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature 383, 621 (1996).
[3] A. Knoblauch and F. Sommer, Synaptic plasticity, conduction delays, and inter-areal phase relations of spike activity in a model of reciprocally connected areas. Neurocomputing 52-54, 301 (2003).
[4] R. Vicente et al., Dynamical relaying can yield zero time lag neuronal synchrony despite long conduction delays, Proc. Natl. Acad. Sci. 105, 17157 (2008).