Review
INMED/TINS special issue
Human gamma-frequency oscillations associated with attention and memory

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Both theoretical and experimental animal work supports the hypothesis that transient oscillatory synchronization of neuronal assemblies at gamma frequencies (30–100 Hz) is closely associated with sensory processing. Recent data from recordings in animals and humans have suggested that gamma-frequency activity also has an important role in attention and both working and long-term memory. The involvement of gamma-band synchronization in various cognitive paradigms in humans is currently being investigated using intracranial and high-density electro- and magnetoencephalography recordings. Here, we discuss recent findings demonstrating human gamma-frequency activity associated with attention and memory in both sensory and non-sensory areas. Because oscillatory gamma-frequency activity has an important role in neuronal communication and synaptic plasticity, it could provide a key for understanding neuronal processing in both local and distributed cortical networks engaged in complex cognitive functions. This review is part of the INMED/TINS special issue Physiogenic and pathogenic oscillations: the beauty and the beast, based on presentations at the annual INMED/TINS symposium (http://inmednet.com).

Introduction

In recent years, fast cortical oscillatory activity in the gamma-frequency band (30–100 Hz), as recorded in humans using electro- or magnetoencephalography (EEG or MEG, respectively), has received increasing interest because of its association with various cognitive functions in healthy humans 1, 2, 3 and a possible role in psychiatric and neurological dysfunctions 4, 5. Although the coordinated activity of large numbers of neurons is required to produce oscillatory gamma-frequency activity in EEG and MEG recordings, its functional role remains unclear. The current understanding of fast oscillations is that they reflect synchronous activity of large ensembles of rhythmically firing neurons, which can be observed at multiple spatial scales, from single-unit recordings to the scalp EEG (Box 1).

From a physiological perspective, there are strong arguments for synchronization in the gamma-frequency band being important for neuronal communication. If a neuron receives input from several other neurons, this drive is enhanced if the spiking inputs are coincident because the synchronization enables the postsynaptic potentials to integrate [6] (Box 2, Figure Ia). The duration of an excitatory postsynaptic potential (PSP) is approximately τPSP ∼10 ms [7], which defines the timeframe of temporal integration. Thus, gamma-frequency oscillations with a duration of 10–30 ms will provide a ‘tighter’ synchronization than will oscillations in lower frequency bands (Box 2, Figure Ia). Because this principle enables a group of neurons to exert a stronger drive when synchronized on downstream networks, it has been proposed that long-distance neuronal communication is reflected by phase synchronization 6, 8, 9, 10.

The hypothesis that synchronous firing of a group of cells increases their functional impact has been the cornerstone of various theories of the role of oscillatory gamma-frequency activity. For instance, the ‘binding problem’ addresses the physiological mechanisms responsible for combining different features in a visual scene to form a coherent percept. It has been proposed that the binding problem can be solved by synchronous firing of neurons encoding the features to be combined [11]. The synchronized neurons will additionally provide a stronger drive to downstream visual areas, enabling a coherent percept to propagate. Electrophysiological recordings in both humans and animals have provided experimental support for feature binding being achieved by neuronal synchronization in the gamma-frequency band 12, 13, 14, 15, 16, 17, 18, 19, 20. Furthermore, in the locust, odour discrimination is impaired if oscillatory synchronization is blocked pharmacologically [21].

In agreement with the hypothesis that synchronization is important for neuronal communication, it has been proposed that gamma-frequency synchronization serves as a mechanism for gain control [6]. Because an increase in neuronal synchronization results in amplification of the drive exerted on downstream areas, the gain with respect to neuronal firing increases too (Box 2, Figure Ib). As addressed below, gain control by neuronal synchronization might provide the neuronal substrate for directed attention. Finally, it has been proposed that sustained neuronal firing in the gamma-frequency range is responsible for active maintenance of representations in working memory. This hypothesis has received support from animal recordings [22] and, as reviewed below, also human research 23, 24, 25, 26, 27, 28. All of the mechanisms addressed above pertain to dynamic changes in the pattern of neuronal firing. However, stable, long-lasting modifications of synaptic connections are another essential component of neuronal processing. Experimental work has demonstrated an intricate connection between neuronal firing and the phase of ongoing gamma-frequency oscillations in relation to synaptic plasticity (Box 1, Figure Id) [29]. As discussed below, oscillatory gamma-band activity has also been associated with encoding and recall of long-term memory.

In summary, there are several theories suggesting that gamma-band synchronization has a pivotal role in attention and memory. These theories have received partial support from animal research; however, it remains to be determined whether the same mechanisms are present in humans when complex cognitive tasks are applied. Recent technical developments in human electrophysiological research have provided the tools for addressing this question. Beyond advances in recording techniques, these developments include better source-modelling methods for localizing oscillatory brain activity from EEG and MEG signals and the application of novel signal-processing techniques for detection of transient neural oscillations. Using these techniques, it has become possible to study human gamma-band neural synchronization in various cortical regions, such as the primary visual cortex, Broca's area and pars opercularis. This emerging line of research is reviewed here to better understand the role of gamma-frequency synchronization in human attention and memory.

Section snippets

Gamma-frequency activity during attentional selection and stimulus encoding

Because of the limited processing capacities of human sensory systems, attention helps to select stimulus features relevant for behavioural goals from a rich and noisy environment. At the physiological level, attention appears to operate by increasing the relative ability of neurons representing attended stimuli in sensory cortices to influence downstream cortical areas [30]. One proposed mechanism involves neural synchronization: as already mentioned, a neuron receiving multiple synaptic

Gamma-frequency activity during maintenance of working and short-term memory

Short-term memory is defined as the capacity to retain and manipulate information that is no longer accessible in the environment. Following the hypothesis that the representation of a specific stimulus relies on a synchronously oscillating assembly of neurons, a memory trace could be established by sustained oscillations in the absence of external stimulation (Box 2, Figure Ic). This provides a putative mechanism for maintenance of short-term or working memory of neuronal representations in

Gamma-frequency activity and long-term memory

From a physiological perspective, there are several reasons to believe that synchronized activity in the gamma-frequency band should have a role in encoding long-term memory through the modification of synaptic connections. First, it has been argued that the neuronal synchronization of representations in sensory areas results in a stronger synaptic drive to downstream areas [6]. As a consequence, the stronger drive results in stronger neuronal firing, promoting synaptic plasticity. Second, it

Concluding remarks

Although the studies reviewed here point to an important role of activity in the gamma band, it should be emphasized that oscillatory brain activity is produced in other frequency bands too. In particular, theta-band activity is modulated by both working 51, 52 and long-term memory tasks 44, 45, 53. Interestingly, recent iEEG studies reported that gamma-frequency power is modulated by the phase of theta-frequency oscillations 54, 55. This finding is consistent with theoretical work proposing

Acknowledgements

This work was funded by the Volkswagen Foundation Grant I/79876 and Netherlands Organization for Scientific Research Innovative Research Incentive Schemes 864.03.007. All authors contributed equally to this paper.

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