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New vistas for α-frequency band oscillations

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The amplitude of α-frequency band (8–14 Hz) activity in the human electroencephalogram is suppressed by eye opening, visual stimuli and visual scanning, whereas it is enhanced during internal tasks, such as mental calculation and working memory. α-Frequency band oscillations have hence been thought to reflect idling or inhibition of task-irrelevant cortical areas. However, recent data on α-amplitude and, in particular, α-phase dynamics posit a direct and active role for α-frequency band rhythmicity in the mechanisms of attention and consciousness. We propose that simultaneous α-, β- (14–30 Hz) and γ- (30–70 Hz) frequency band oscillations are required for unified cognitive operations, and hypothesize that cross-frequency phase synchrony between α, β and γ oscillations coordinates the selection and maintenance of neuronal object representations during working memory, perception and consciousness.

Introduction

Hans Berger was among the first to witness electroencephalogram (EEG) rhythms in the α- (8–14 Hz) and β- (14–30 Hz) frequency bands [1]. During the following four decades, the parieto-occipital α rhythm was found to be attenuated by eye opening, visual stimuli and by increased attentiveness. These findings inspired the idea of α oscillations functioning as an ‘idling’ rhythm that characterizes an alert-but-still brain state [2]. Today, the idling hypothesis has been largely overtaken by a framework where the amplitude of α oscillations reflects a level of cortical inhibition 3, 4, 5, 6, 7. Accumulating data on α phase dynamics 8, 9, 10, 11, 12, however, add a twist to the story; endogenous as well as stimulus-locked α-band phase correlations seem to have a direct role in the neuronal machinery underlying behavioral-level phenomena, such as attention, STM and sensory awareness. These findings challenge the inhibition hypothesis, as well as the prevailing interpretation of α amplitude dynamics.

Section snippets

Do large-amplitude α oscillations reflect cortical inhibition?

Early on, the α-band oscillations were observed to be strengthened during internal tasks, such as mental arithmetic and visual imagery, which was interpreted by Ray and Cole [3] to reflect rejection of sensory information intake. This idea was advanced into an α-inhibition hypothesis by Klimesch [4] and Pfurtscheller 5, 6, who proposed that small α amplitudes are a signature of regions of active neuronal processing, whereas large-amplitude α oscillations reflect the inhibition and disengagement

Alpha-frequency band phase correlations

Compared with the large body of data on α-amplitude dynamics, investigations on α-phase dynamics have remained infrequent, although this line of research is now rapidly gaining popularity. Phase synchrony is essential in the formation of transient neuronal assemblies [24], in communication therein [25] and, consequently, in large-scale integration [26]. Phase interactions thus define functional networks in the cerebral cortex. Therefore, we propose here that it is the phase (Box 1), not

Thalamic burst discharges during α-frequency band oscillations

At the cellular level, the concept of α-frequency band inhibition has been largely based on an association between sleep-state α spindles and burst discharges of thalamocortical neurons [6]. Thalamocortical relay neurons have long been known to operate in two distinct modes: in a depolarized state they tonically fire single spikes, whereas following a period of hyperpolarization (∼−70 mV), long enough to de-inactivate T-type calcium channels, they discharge spike bursts (interspike intervals 2–5 

Phase reset of ongoing α oscillations

The classical event-related potentials (ERPs) are influenced by both peristimulus amplitude and phase dynamics (Box 1). In contrast with the classical view of ERPs revealing stimulus-evoked components from ongoing ‘noise’, several human EEG studies suggest that some early ERP components, N1 in particular, at least partly emerge from a stimulus-caused phase reset of ongoing θ 44, 45 and α oscillations 44, 45, 46 (Box 1, Figure Ib, c). These findings place a large body of data on the N1 component

Phase synchrony among α, β and γ oscillations

In recent years, β- and γ-frequency band oscillations have attracted widespread interest. Transient synchronization of neuronal activity seems to be a key mechanism in the binding of anatomically distributed feature processing into coherent perceptual objects, where it is often associated with β or γ oscillations [24]. Also, the phenomenology of γ oscillations in the human EEG is in line with a role in the formation of neuronal object representations [51], and, accordingly, γ oscillations are

Discrete perception and action

When visual objects are presented serially at fixation, humans can recognize and categorize them at rates up to 8–12 Hz 67, 68. In a continuous wagon wheel illusion experiment, illusory reversals are most probable at wheel-motion frequencies of ∼10 Hz, which is suggestive of discrete perceptual sampling [69] (Figure 2c). Similarly, rats sample and discriminate odors at a rate of 8 Hz [70] and use active whisking at 7–14 Hz for tactile perception [34]. Hence, perception seems to operate in discrete

Discrete cognition: α oscillations in the ‘global neuronal workspace’

According to the current dogma of neuronal network dynamics, synchronous γ-frequency band assemblies account for ‘active’ neuronal processing, whereas the roles of α oscillations are in the inhibition and ‘inactivation’ of task-irrelevant cortical regions. However, as discussed here, an accumulating body of evidence emphasizes a direct involvement of α oscillations in the mechanisms of top-down modulation, attention and consciousness.

Neural correlates of consciousness (NCC) are widely

Acknowledgements

This work was supported by the Academy of Finland and by the Ella and Georg Ehrnrooth Foundation.

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