Paradox lost? Exploring the role of alpha oscillations during externally vs. internally directed attention and the implications for idling and inhibition hypotheses

Abstract

Although slow waves of the electroencephalogram (EEG) have been associated with attentional processes, the functional significance of the alpha component in the EEG (8.1–12 Hz) remains uncertain. Conventionally, synchronisation in the alpha frequency range is taken to be a marker of cognitive inactivity, i.e. ‘cortical idling’. However, it has been suggested that alpha may index the active inhibition of sensory information during internally directed attentional tasks such as mental imagery. More recently, this idea has been amended to encompass the notion of alpha synchronisation as a means of inhibition of non-task relevant cortical areas irrespective of the direction of attention. Here we test the adequacy of the one idling and two inhibition hypotheses about alpha. In two experiments we investigated the relation between alpha and internally vs. externally directed attention using mental imagery vs. sensory-intake paradigms. Results from both experiments showed a clear relationship between alpha and both attentional factors and increased task demands. At various scalp sites alpha amplitudes were greater during internally directed attention and during increased load, results incompatible with alpha reflecting cortical idling and more in keeping with suggestions of active inhibition necessary for internally driven mental operations.

Introduction

The human electroencephalograph (EEG) has proven a useful tool in the examination of the brain's attentional networks. The purpose of the present study is to help delineate various interpretations of the alpha component of the human EEG in terms of the distinction between internally directed and externally directed attention.

Traditionally it has been argued that the alpha rhythm reflects a generalised idling condition of the brain, calm yet alert (Adrian and Matthews, 1934). In support of this many studies have noted a task-related decrease in alpha power, both over occipital sites during visual stimulation and scanning tasks (Berger, 1929, Berger, 1930, Mann et al., 1996) and over sensorimotor areas during movement or somatosensory tasks (see Pfurtscheller et al., 1996 for a review).

However, there have been other studies whose observations have been anomalous to the alpha-as-idling findings. Cole and Ray, 1985, Ray and Cole, 1985b, Ray and Cole, 1985a explored the effects of the direction of attention within the framework of the intake-rejection hypothesis (Lacey et al., 1963, Lacey, 1967, Lacey and Lacey, 1970). This hypothesis introduced the notion of sensory ‘intake’ tasks (i.e. externally directed attention) and non-sensory ‘rejection’ processes (i.e. internally directed attention), such as mental arithmetic, mental imagery and working memory tasks. The rejection aspect of the theory related to the proposal that in order for example, to facilitate mental imagery, one needs to inhibit or ‘reject’ incoming sensory information. Ray and Cole, 1985b, Ray and Cole, 1985a found increased alpha power in rejection tasks such as mental imagery and arithmetic especially at parietal sites.

Similar to the findings of Ray and Cole, 1985a, Klinger et al., 1973 observed that imagination was associated with increased alpha, Schupp et al. (1994) reported lower alpha power for perceptual tasks as opposed to mental imagery, an association has been observed between average alpha amplitude and mental rotation ability Williams et al., 1995, Klimesch et al., 1990 found that participants who did well in memory tests had higher average alpha frequencies than those who did poorly, indicating the possible importance of alpha mechanisms for memory systems.

Klimesch et al. have since hypothesised a wider role for alpha oscillatory networks of various cognitive processes that involve both attention and memory. The basic principle involved here is that activation of this network would lead to alpha desynchronisation (see Klimesch, 1997 for a review). More recently, Klimesch et al., 1999, Klimesch et al., 2000 have proposed that alpha synchronisation may index inhibitory processes serving to increase signal to noise ratios—the greater the task demands within this network, the more inhibition needed, the greater the synchronisation. Klimesch's proposals are compatible with the notion of ‘surround inhibition’ wherein active cortical areas, indexed by alpha desynchronisation are surrounded by a ‘doughnut’ of alpha synchronisation or inhibition (Suffczynski et al., 2001). Thus, the surrounding inhibition, controlled by thalamo-cortical and reticular nucleus pacemaker cells, acts to increase the gain on the focally active area of alpha desynchronisation in a manner in keeping with Crick's spotlight of attention hypothesis (Crick, 1984). These findings suggest that alpha activity is not a simple index of cortical idling, but that it is a measure of active processing necessary for internally driven mental operations.

Thus there exists a lack of consensus in the literature regarding the functional significance (if any) of oscillations in the traditional alpha bandwidth of 8–12 Hz. The conventional view that alpha reflects a state of cortical idling (Adrian and Matthews, 1934, Pfurtscheller et al., 1996) has been modified to accommodate findings of increased alpha power during certain internal tasks, such that it is proposed that alpha indexes early inhibition of sensory input mechanisms (Ray and Cole, 1985b, Ray and Cole, 1985a). More recently this idea has been broadened to propose alpha as a mechanism for increasing signal to noise ratios within the cortex by means of inhibition of unnecessary or conflicting processes to the task in hand (Klimesch et al., 1999, Klimesch et al., 2000).

In order to tease apart these competing theories experimentally, we employed tasks that manipulated both cognitive processing requirements (difficulty) and direction of attention (externally vs. internally directed attention). In our first experiment we tested the hypotheses that alpha indexes cortical idling by determining whether alpha power over sensory areas decreases not only during external as opposed to internal tasks, but also as a function of increasing task demands. We also tested the alternative hypothesis that alpha power reflects the inhibition of sensory input mechanisms necessary for internally directed attention, by testing whether alpha power was greater during internal as opposed to external tasks, and that during sensory-intake tasks (but not during internally directed attention) alpha increases in line with increasing task demands over task-irrelevant areas. Finally, we tested the hypothesis that alpha is an index of a more generalised inhibition system serving to increase signal to noise ratios, by testing whether alpha power increases during internally directed attention and as task demands increase during sensory-intake tasks, and also that it increases with task demands during internally directed attention.