The Argument for Multiplexed Synchrony

Although the spike-timing dependent specificity of neural firing is an established phenomenon, many seem to doubt the idea that more global forms of phase coding (i.e., "multiplexed synchrony," in which populations of neurons will fire at specific phases of a particular firing rhythm) is neurally plausible. In contrast, authors such as Jensen, Lisman, and Idiart have championed the idea that brain functions like working memory can be understood as emerging from multiplexed theta and gamma oscillations in neocortex. Beyond the theoretical and computational possibility that such a mechanism exists, what empirical evidence supports this idea?

This question is addressed by John Lisman in a 2005 article from Hippocampus. He reviews several pieces of evidence in support of the multiplexing hypothesis, such as:

1) Both theta and gamma oscillations occur together in hippocampus, and furthermore, theta rhythms modulate the amplitude of gamma rhythms;

2) The frequency of the dominant oscillation within each of these bands is correlated with the other frequencies, such that a shift in one of them seems to be accompanied by a proportional shift in the other;

3) A phenomenon called "phase procession" is known to occur in awake rats that are exploring a radial arm maze; as they traverse the maze, hippocampal neurons with sensitivity to regions that were just visited fire just out of phase with neurons sensitive to regions that are about to be visited. This suggests that the mechanisms driving synchronous firing do have the temporal precision necessary to generate "multiplexed" phase relationships.

4) The average differences in phase between these differentially-tuned hippocampal neural ensembles always corresponds to a particular fraction of theta; the actual position of a rat can be optimally reconstructed by analyzing the spike timing of these neurons in terms of where they fall within 5 or 6 "phase bins" - i.e., does a particular neural ensembled fire within the first 1/5 of a theta cycle, or the second 1/5? Using a phase bin size of 5 or 6 resulted in a more accurate reconstruction of a rat's actual position than a similar analysis that divides spike timing into 4 or less bins, and was not significantly less accurate than dividing spike timing into 7 or more bins.

5) Measurements of memory scanning from the Sternberg task suggest that memories in this task are searched sequentially and exhaustively, with memory scanning time corresponding roughly to the period of one gamma cycle.

Based on this evidence, it is unreasonable to insist that neural networks do not have the temporal precision to accomplish multiplexed synchrony. It's also unreasonable to claim that noise may have deleterious effects on these abilities - based on the the paper reviewed in this post, we know that "noise" recorded in vivo shows some properties that in some cases might actually increase the information capacity of the neural code. And if anyone should point to the fragility of this mechanism, let's remember that synchronous oscillations are seen to spontaneously emerge both in embodied computational models as well as in hippocampus culture.

Of course, it is still possible to claim that synchronous firing is merely a harmless correlate, rather than a cause, of cognitive functions. But such a claim would contradict evidence reviewed in this post on how recognition memory can be enhanced with slow-wave visual flicker - in other words, that an enhancement of a particular rhythm can enhance cognitive function. Evidence reviewed in this post also suggests a casual role for synchronous firing, in that presentation of auditory rhythms at harmonics of these neural oscillations seems to quicken reaction time. And we know from the paper reviewed in this post that synchrony probably does have a causal role in at least one aspect of cortical function - the rather important function of actually gating sensory information into cortex.

Unfortunately, it seems not possible to disrupt synchronous firing selectively while leaving other cognitive functions intact. For example, muscimol and pentobarbital are known to disrupt gamma and theta rhythms, but clearly have cognitive effects as well. Exploration of the role of muscarinic agonists, such as carbachol, and other drugs like piracetam (which have been shown to elevate the density of muscarinic-cholinoreceptors in frontal cortex) on synchronous oscillations may also prove fruitful in further establishing the link between theta/gamma oscillations and cognition. Unfortunately, drugs like these can always be claimed to act on cognitive functions directly by some pathway that does not primarily involve synchrony; therefore pharmacology may be of limited use in establishing a causal role for synchrony.

In conclusion, a quick thought experiment: if a seagull is observed to flap its wings in synchrony, and be able to fly, one might doubt that synchrony per se is important. Instead, one might point to something else that is accomplished in the process of sychronous wing-flapping, such as symmetric turbulent air flows. Even if every seagull ever observed must flap its wings synchronously in order to fly, it is still possible to doubt that synchronous wing-flaping per se is the feature that allows flight. And, in some sense this is true, because it is possible to construct flying machines that work without synchronous wing-flapping. Fundamentally, it is really the aerodynamics that matter, not synchronous wing-flapping. Nonetheless, it seems patently untrue to say that the synchrony of wing-flapping is merely a side effect of the ability of seagulls to fly.

Likewise, it is possible to construct computational models that work without synchronous oscillations. Fundamentally, one might argue that the information processing is what matters, not the specific implementation. Nonetheless, it seems unreasonable to say that synchrony of firing is merely a side effect of cognition.