A mechanism for cognitive dynamics: neuronal communication through neuronal coherence

https://doi.org/10.1016/j.tics.2005.08.011Get rights and content

At any one moment, many neuronal groups in our brain are active. Microelectrode recordings have characterized the activation of single neurons and fMRI has unveiled brain-wide activation patterns. Now it is time to understand how the many active neuronal groups interact with each other and how their communication is flexibly modulated to bring about our cognitive dynamics. I hypothesize that neuronal communication is mechanistically subserved by neuronal coherence. Activated neuronal groups oscillate and thereby undergo rhythmic excitability fluctuations that produce temporal windows for communication. Only coherently oscillating neuronal groups can interact effectively, because their communication windows for input and for output are open at the same times. Thus, a flexible pattern of coherence defines a flexible communication structure, which subserves our cognitive flexibility.

Introduction

Because we are equipped with mechanisms of selective attention, we can do tasks such as the following: we can fixate on a central cross and press a button only when a green dot is flashed to the right while ignoring the same dot anywhere else in the visual field. And we can switch attention to do this task at any other spatial position, now ignoring the formerly relevant position. Although in both conditions, the same physical stimuli are given and the same behavioral responses are issued, there is obviously a strong cognitive control over the routing of information from sensory to motor areas. Conceptually, the effect of cognitive top-down control is a modification in the communication structure between brain areas.

But how do groups of neurons communicate? And how do top-down influences modify the communication structure within a few hundred milliseconds when anatomical connections stay unchanged on that timescale? Although we still know very little about neuronal communication mechanisms, we often have an implicit concept or model about it. In very general terms, the dominant model of neuronal communication is that a neuron sends its message (encoded in e.g. action potential rate or in the degree of action potential synchronization) down its axons to all neurons to which it is anatomically connected. Those receiving neurons combine (e.g. sum and threshold) all the different inputs that they receive from all neurons to which they have connections. An important aspect of this model is that both the distribution and the reception of neuronal signals is governed solely by the structure of the anatomical connections, that is, there is no further communication structure beyond the one imposed by anatomical connectedness. However, cognitive functions require flexibility in the routing of signals through the brain. They require a flexible effective communication structure on top of the anatomical communication structure that is fixed, at least on the timescale at which cognitive demands change.

In this article, I hypothesize that this effective communication structure is mechanistically implemented by the pattern of coherence among neuronal groups, that is, the pattern of phase-locking among oscillations in the communicating neuronal groups. Specifically, I hypothesize that neuronal communication between two neuronal groups mechanistically depends on coherence between them and the absence of neuronal coherence prevents communication. I will address this hypothesis as the ‘communication-through-coherence’ (CTC) hypothesis. It is based on two realizations: first, activated neuronal groups have the intrinsic property to oscillate 1, 2. Second, those oscillations constitute rhythmic modulations in neuronal excitability that affect both the likelihood of spike output and the sensitivity to synaptic input. Thus, rhythmic excitability peaks constitute rhythmically reoccurring temporal windows for communication. Only coherently oscillating (or phase-locked) neuronal groups can communicate effectively, because their communication windows for input and for output are open at the same times.

Previous work has hypothesized that neuronal coherence (or phase-locking or synchronization) could provide a tag that binds those neurons that represent the same perceptual object 3, 4, 5, 6, 7. This binding tag would be a flexible code for linking neurons into assemblies and thereby greatly enlarging the representational capacity of a given pool of neurons. This hypothesis is known as the binding-by-synchronization (BBS) hypothesis. The CTC and the BBS hypotheses are fully compatible with each other, but they are also clearly distinct. Whereas the BBS hypothesis is primarily suggesting a representational code, the CTC hypothesis considers the mechanistic consequences of neuronal oscillations for neuronal communication. It suggests that at the heart of our cognitive dynamic is a dynamic communication structure and that the neuronal substrate is the flexible neuronal coherence pattern.

In the following, I will first review neurophysiological data that suggest an important role of synchronous neuronal oscillations for neuronal communication. I will then present some evidence that directly suggests that neuronal coherence can serve neuronal communication and can be dynamically modulated by cognitive demands. Finally, I will review neurophysiological data about the attentional modulation of synchronous neuronal oscillations and speculate about the detailed implementation of a flexible communication structure through a flexible coherence pattern.

Section snippets

Neuronal communication through firing rate modulation

The predominant, but often only implicit, model of neuronal communication is that a neuronal group sends a message through enhancing its firing rate and the receiving group of neurons integrates this input over some time window and modulates its firing rate accordingly [8] (Figure 1a). Probably the most important reason why this model is dominant is that many experiments have demonstrated modulations in firing rate that correlate in a meaningful way with either stimulus parameters or cognitive

Neuronal communication through neuronal coherence

In this article, I explore the potential that neuronal oscillations offer as mechanisms for neuronal communication and propose that neuronal communication is not only subserved by oscillatory synchronization within the group of neurons sending a message, but also by coherence (or phase-locking) between the oscillations in the sending group and the receiving group (Figure 3a). The central argument is that activated neuronal groups have the intrinsic property to oscillate 1, 2. Those oscillations

Cortico-spinal coherence subserves cortico-spinal communication

There is also experimental evidence that the coherence between neuronal groups subserves their communication. Several studies have demonstrated coherence between different areas involved in visuo-motor transformations, starting from early visual areas and reaching through parietal cortex and motor cortex to the spinal cord 34, 35, 36, 37, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49. A recent study tested directly one prediction of the CTC hypothesis, namely that neuronal coherence has a functional

Coherence, competition and binding

Although the study on cortico-spinal coherence demonstrates that neuronal communication is rendered more effective through neuronal gamma-band coherence, it did not yet address another prediction of the CTC hypothesis, namely that neuronal coherence renders neuronal communication also selective. I am not aware of experimental evidence that tests this prediction directly, but let us speculate about a scenario in which such a potential mechanism might have profound importance.

It has been shown

Acknowledgements

I would like to thank Nancy Kopell and Wolf Singer for helpful discussions and comments. Supported by The Netherlands Organization for Scientific Research, grants 452–03–344 and The Human Frontier Science Program Organization, grant RGP0070/2003.

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