Approximate, not Perfect Synchrony Maximizes the Downstream Effectiveness of Excitatory Neuronal Ensembles

The most basic functional role commonly ascribed to synchrony in the brain is that of amplifying excitatory neuronal signals. The reasoning is straightforward: When positive charge is injected into a leaky target neuron over a time window of positive duration, some of it will have time to leak back out before an action potential is triggered in the target, and it will in that sense be wasted. If the goal is to elicit a firing response in the target using as little charge as possible, it seems best to deliver the charge all at once, i.e., in perfect synchrony. In this article, we show that this reasoning is correct only if one assumes that the input ceases when the target crosses the firing threshold, but before it actually fires. If the input ceases later—for instance, in response to a feedback signal triggered by the firing of the target—the “most economical” way of delivering input (the way that requires the least total amount of input) is no longer precisely synchronous, but merely approximately so. If the target is a heterogeneous network, as it always is in the brain, then ceasing the input “when the target crosses the firing threshold” is not an option, because there is no single moment when the firing threshold is crossed. In this sense, precise synchrony is never optimal in the brain.