Elsevier

Brain Research Reviews

Volume 53, Issue 1, January 2007, Pages 63-88
Brain Research Reviews

Review
EEG alpha oscillations: The inhibition–timing hypothesis

https://doi.org/10.1016/j.brainresrev.2006.06.003Get rights and content

Abstract

The traditional belief is that the event-related alpha response can solely be described in terms of suppression or event-related desynchronization (ERD). Recent research, however, has shown that under certain conditions alpha responds reliably with an increase in amplitudes (event-related synchronization or ERS). ERS is elicited in situations, where subjects withhold or control the execution of a response and is obtained over sites that probably are under, or exert top-down control. Thus, we assume that alpha ERS reflects top-down, inhibitory control processes. This assumption leads over to the timing aspect of our hypothesis. By the very nature of an oscillation, rhythmic amplitude changes reflect rhythmic changes in excitation of a population of neurons. Thus, the time and direction of a change – described by phase – is functionally related to the timing of neuronal activation processes. A variety of findings supports this view and shows, e.g., that alpha phase coherence increases between task-relevant sites and that phase lag lies within a time range that is consistent with neuronal transmission speed. Another implication is that phase reset will be a powerful mechanism for the event-related timing of cortical processes. Empirical evidence suggests that the extent of phase locking is a functionally sensitive measure that is related to cognitive performance. Our general conclusion is that alpha ERS plays an active role for the inhibitory control and timing of cortical processing whereas ERD reflects the gradual release of inhibition associated with the emergence of complex spreading activation processes.

Section snippets

Introduction: basic principles underlying the inhibition–timing hypothesis

Osocillations reflect rhythmic changes in the (relative) level of depolarization in the (dendritic and somatic) membrane potentials of masses of neurons. Consequently, they reflect phases of low versus high excitability. The basic principle (shown in Fig. 1) can be illustrated by considering the phase of oscillatory activity together with the level of excitation in excitatory neurons. For simplicity, we assume that oscillatory activity is induced by inhibitory cells and reflects rhythmic

Alpha desynchronization (ERD) as a functional correlate of brain activation

The well-known alpha response – power suppression during eyes opening (described since the early days of EEG research, cf. Berger, 1929) – suggests that light stimulation (bottom-up processing) is responsible for the decrease of the large amplitudes which can be observed particularly at posterior recording sites during closed eyes. Most interestingly, this interpretation is questioned by the simple fact that alpha suppression can also be observed solely in response to eyes opening (a top-down

The timing aspect

As discussed in Section 2, an increase in rhythmic activity results in two different effects, in a general decrease in firing rate and an increase in rhythmic discharges (cf. Figs. 1A with B). We assume that the first effect reflects inhibition as discussed in Section 3. The second effect, however, underlies the timing of neuronal activity and will be discussed in this section.

The crucial aspect – as outlined in Fig. 1 – is that an increase in inhibition (driving an oscillation) is accompanied

The physiological basis of alpha oscillations

Since several decades, it was suggested that the thalamus plays a key role in the generation of cortical oscillations and sleep spindles in particular (Andersen and Andersson, 1968). Thus, it was tempting to assume that alpha, as the dominant oscillation in the human scalp EEG, also is generated by thalamic nuclei. This view has led to the idea that the cortex might be passively driven by a ‘thalamic pacemaker’ (cf. Basar et al., 1997, for a review). The seminal work by Lopes da Silva et al.,

Elaboration of the alpha inhibition–timing (AIT) hypothesis and critical questions

We have focused on two basic aspects, one referring to the state, the other to the timing of information processing. With respect to the first aspect, experimental evidence shows consistently that ERD reaches a maximum during a time window in which (conscious) task-related processes take place, whereas ERS can be observed when certain aspects of task performance are under top-down control. Although both cases reflect states of information processing, their functional difference can be best

Conclusions

The general line of our argumentation is that alpha – like other oscillations – is an active phenomenon but reflects – in contrast to other oscillations, a certain type of top-down process. The active role of alpha is seen in a mechanism that also may underlie the functional role of other oscillations: Synchronization in the alpha frequency range helps neurons in distributed networks to effectively activate common target cells. We think that this timing mechanism plays an important role in the

Acknowledgment

This research was supported by the Austrian Science Fund (FWF), P-16849-B022.

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