Review
Is synchronized neuronal gamma activity relevant for selective attention?

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Abstract

Today, much evidence exists that sensory feature binding is accomplished by phase synchronization of induced neuronal gamma activity (30–80 Hz). Recent studies furthermore suggest that phase synchronization of induced gamma activity may represent a general mechanism enabling transient associations of neural assemblies and thus may play a central role in cortical information processing. Here, we describe findings indicating that synchronized gamma activity is moreover specifically involved in selective attention. While feature binding appears to depend primarily on induced gamma synchronization, attentional processes seem to involve both induced and evoked gamma oscillations. Yet it is still an open question, as to which top-down and bottom-up processes are associated with attentional modulation of gamma activity. A possible mechanism to project influences from attentional control structures to areas concerned with stimulus representation and vice versa, may be neuronal synchronization and the resulting firing rate changes of coincidence-detecting neurons in target areas.

Introduction

According to William James [44], attention is “the taking possession by the mind in clear and vivid form, of one out of what seem several simultaneously possibly objects or trains of thought.” Focused or selective attention allows selection of certain items from the stream of information processing. In general, brain processes which are at the focus of attention, enter awareness [66], [92]. In a strict sense, one does not become immediately aware of a stimulus or one’s own response, but only slightly after one has selected it [52], [74]. Studies on selective attention are mainly concerned with perceptual selection, i.e. selection of sensory information [16], [57]. Several mechanisms underlying perceptual selection have been proposed. The most obvious mechanism is selection based on firing rates and several experimental studies support this hypothesis [85]. A principal drawback of this mechanism is that it interferes with the rate coding of stimulus properties, which is the prime modulatory influence on firing rates. Another possible candidate, however not yet supported by much experimental evidence, is the implementation of so-called shifter-circuits that gate bottom-up processing streams [4]. Recently, it has been proposed that synchronization of neural firing may accomplish attentional selection in an effective manner, in particular perceptual selection [68]. This mechanism could provide an additional coding dimension independent of rate coding. Precise synchronization of neural firing within the millisecond range is associated with phase synchronization of gamma activity, i.e. high frequency EEG activity above 30 Hz [22]. As described in the following, there is already significant evidence in support of the idea that gamma synchronization may represent a general mechanism enabling transient association of neural assemblies. However, recent findings reported below indicate that, in addition, synchronized gamma activity may indeed play a specific role in selective attention.

Section snippets

Synchronization of gamma activity: a neural coupling mechanism

Phase synchronization of neuronal gamma activity is regarded as the most probable mechanism underlying so-called feature binding. It is well known that different features of a visual object are processed in different submodules of the visual system, for example color in V4 and motion in MT (V5) [26]. Each sensory submodule contains a complete map of the respective feature. A central neuroscientific problem has been how these different aspects are bound together to become one coherent

Synchronized gamma oscillations: role in selective attention

But is there any evidence that synchronized gamma activity is also specifically involved in selective attention, i.e. the ability to focus on a subset of items during information processing? Several recent studies support this view. With respect to visual selective attention, an enhancement of scalp recorded induced gamma activity was reported when subjects attended to a certain stimulus or when they perceived a Gestalt [38], [63]. In intracranial recordings from area V4 in monkeys, increased

Critical viewpoints

Contrary to the data described above, some groups investigating monkey visual cortex have either failed to find functional modulations of synchronized gamma oscillations or have failed to find gamma synchronization at all [49], [87], [99]. Other authors have attributed these discrepancies in experimental findings to the fact that recordings were from different cortical sites or layers [53], that diverse techniques to analyse synchronization were used, in particular different time windows for

Discussion and outlook

In conclusion, the majority of experimental data point to the view that phase synchronization of gamma activity not only seems to be a general mechanism underlying cortical information processing, but also appears to be particularly involved in attentional processes. As described above, in several studies, increased synchronization within the gamma range was reported during conditions of focused attention compared to control conditions, i.e. the degree of gamma synchronization seems to be

Acknowledgements

We thank Dr Laura Parkes for comments on an earlier version of the manuscript.

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