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Resonance, oscillation and the intrinsic frequency preferences of neurons

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Abstract

The realization that different behavioural and perceptual states of the brain are associated with different brain rhythms has sparked growing interest in the oscillatory behaviours of neurons. Recent research has uncovered a close association between electrical oscillations and resonance in neurons. Resonance is an easily measurable property that describes the ability of neurons to respond selectively to inputs at preferred frequencies. A variety of ionic mechanisms support resonance and oscillation in neurons. Understanding the basic principles involved in the production of resonance allows for a simplified classification of these mechanisms. The characterization of resonance and frequency preference captures those essential properties of neurons that can serve as a substrate for coordinating network activity around a particular frequency in the brain.

Section snippets

Resonance as a probe of frequency preference

The use of frequency-response analysis for understanding neuronal function was pioneered by Cole4, who used it, before the advent of voltage clamp techniques, to describe some of the basic events concerned with the generation of action potentials in the giant axon of the squid. Research using frequency-domain techniques was then carried forward by researchers who wished to study emergent electrical phenomena in single neurons by using Fourier techniques to tease apart the components of the

How to make resonance: rules of thumb

The examples above show there are diverse ways to create resonance and oscillations in neurons. Fortunately, there are some simple regularities that govern these processes. In particular, as in the dual mechanism that underlies the depolarized resonance in neocortical cells, there is often a dissociation between the basic mechanisms responsible for the existence of resonance and the subsequent amplification of resonance to generate oscillations. This allows the study of these processes in

Amplifying currents, amplified resonance and oscillation

Although the rules for identifying resonant currents have been explained, the story is not yet complete. What is missing is the concept of an amplifying current. Such a current is essentially the inverse of a resonant current. Its reversal potential lies near the top, rather than the base, of its voltage-activation curve (Fig. 3); and it therefore actively potentiates, rather than opposes, voltage changes (cf. parts b and c in Fig. 2a). In addition, it activates quickly, rather than slowly,

Concluding remarks

There are many different ways to construct a resonance or frequency preference in neurons. Despite the differences, however, an underlying theme emerges that allows a simple classification of the oscillatory characteristics of neurons. To summarize, there are three classes of frequency-dependent mechanism in central neurons: (1) solitary resonances caused by unaided resonant currents; (2) amplified resonances that arise from the interaction of resonant and amplifying mechanisms; and (3)

Acknowledgements

The authors’ research was supported by The Israel Science Foundation and The European Commision.

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