Review
Human gamma-band activity: A review on cognitive and behavioral correlates and network models

https://doi.org/10.1016/j.neubiorev.2009.09.001Get rights and content

Abstract

Gamma-band oscillations (roughly 30–100 Hz) in human and animal EEG have received considerable attention in the past due to their correlations with cognitive processes. Here, we want to sketch how some of the higher cognitive functions can be explained by memory processes which are known to modulate gamma activity. Especially, the function of binding together the multiple features of a perceived object requires a comparison with contents stored in memory. In addition, we review recent findings about the actual behavioral relevance of human gamma-band activity. Interestingly, rather simple models of spiking neurons are not only able to generate oscillatory activity within the gamma-band range, but even show modulations of these oscillations in line with findings from human experiments.

Introduction

Since the discovery of the electroencephalogram (EEG) by Berger (1929), oscillatory patterns can be observed in brain electrical activity. The most prominent oscillation in spontaneous EEG can be found in a frequency band of 8–12 Hz, which was considered by Berger as the basic rhythm and was named alpha-rhythm. Alpha oscillations appear with large amplitudes between 10 and 50 mV. The chronologically next identified frequency range between 12 and 30 Hz was named by Berger consequently with the Greek letter beta. Faster oscillations in the human EEG between 30 and 80 Hz could be identified only later, since the amplitudes of EEG oscillations decrease with increasing frequencies. The term gamma activity was coined for this higher frequency band. After it had been identified, the gamma frequency range was demonstrated to correlate with many cognitive functions which will be the topic of this review.

Section snippets

Cognitive functions of gamma-band activity

Before addressing the cognitive aspects of human EEG gamma oscillations, we need to briefly introduce an important property of these responses. In response to sensory stimulation, a gamma-band response (GBR) is typically evoked. This has been shown for auditory (Pantev, 1995), visual (Hoogenboom et al., 2006), and somatosensory (Chen and Herrmann, 2001) stimuli in humans and for olfactory stimuli in animals (Eeckman and Freeman, 1990). At an early latency, these stimuli evoke a GBR that can be

Behavioral and perceptual relevance of gamma oscillations

The section above clearly points out numerous task-dependent modulations of GBRs in different experimental conditions, tasks, and modalities. However, there is much less evidence for the actual behavioral and perceptual relevance of these oscillations. More precisely, as suggested by Sejnowski and Paulsen (2006), if oscillations are essential for and related to perception and behavioral responses, these processes should be impaired by disturbing the oscillations which should lead to behavioral

Neural mechanisms of gamma-band activity

In this section we will explore several models that have been proposed to account for the emergence of gamma-band activity.

In a series of studies on hippocampal brain slices, Traub et al. (1998) and Whittington et al. (2000) demonstrated that neural networks that include mutually interconnected inhibitory interneurons synchronize at high frequencies, predominantly in the gamma-band. They studied two extreme cases that are replicated in Fig. 4. Clearly, if a network does not incorporate any

Conclusions

In conclusion, we want to stress four aspects of human gamma-band activity. First of all, they reflect cognitive processes – among which memory-matches seem to be most prominent and probably fundamental for others, such as attention, binding, object representation, and language. Secondly, these cognitive modulations cannot only be found on the late induced GBR but already on the early evoked GBR which is generated in early sensory cortices. Thus, GBRs provide evidence that already very early

Acknowledgments

IF was supported by the BMBF Bernstein Group for Computational Neuroscience. CSH and DL were supported by the Deutsche Forschungsgemeinschaft (grants HE3353/2 and SFB-TRR/31-A09).

References (136)

  • A.C. Chen et al.

    Perception of pain coincides with the spatial expansion of electroencephalographic dynamics in human subjects

    Neurosci. Lett.

    (2001)
  • T. Demiralp et al.

    Gamma amplitudes are coupled to theta phase in human EEG during visual perception

    Int. J. Psychophysiol.

    (2007)
  • F.H. Eeckman et al.

    Correlations between unit firing and EEG in the rat olfactory system

    Brain Res.

    (1990)
  • C. Eulitz et al.

    Oscillatory neuromagnetic activity induced by language and non-language stimuli

    Brain Res. Cogn. Brain Res.

    (1996)
  • R. Freunberger et al.

    Gamma oscillatory activity in a visual discrimination task

    Brain Res. Bull.

    (2007)
  • P. Fries et al.

    The gamma cycle

    Trends Neurosci.

    (2007)
  • I. Fründ et al.

    EEG oscillations in the gamma and alpha range respond differently to spatial frequency

    Vision Res.

    (2007)
  • I. Fründ et al.

    Evoked gamma oscillations in human scalp EEG are test-retest reliable

    Clin. Neurophysiol.

    (2007)
  • T. Gruber et al.

    Effects of picture repetition on induced gamma band responses, evoked potentials, and phase synchrony in the human EEG

    Brain Res. Cogn. Brain Res.

    (2002)
  • T. Gruber et al.

    Oscillatory brain activity in the human EEG during indirect and direct memory tasks

    Brain Res.

    (2006)
  • T. Gruber et al.

    Brain electrical tomography (BET) analysis of induced gamma band responses during a simple object recognition task

    Neuroimage

    (2006)
  • A.R. Haig et al.

    Peak gamma latency correlated with reaction time in a conventional oddball paradigm

    Clin. Neurophysiol.

    (1999)
  • S. Hanslmayr et al.

    Prestimulus oscillations predict visual perception performance between and within subjects

    Neuroimage

    (2007)
  • P. Heil

    First-spike latency of auditory neurons revisited

    Curr. Opin. Neurobiol.

    (2004)
  • C.S. Herrmann et al.

    Adaptive frequency decomposition of EEG with subsequent expert system analysis

    Comput. Biol. Med.

    (2001)
  • C.S. Herrmann et al.

    Human EEG gamma oscillations in neuropsychiatric disorders

    Clin. Neurophysiol.

    (2005)
  • C.S. Herrmann et al.

    Gamma responses and ERPs in a visual classification task

    Clin. Neurophysiol.

    (1999)
  • C.S. Herrmann et al.

    Cognitive functions of gamma-band activity: memory match and utilization

    Trends Cogn. Sci.

    (2004)
  • N. Hoogenboom et al.

    Localizing human visual gamma-band activity in frequency, time and space

    Neuroimage

    (2006)
  • B.H. Jansen et al.

    Phase synchronization of the ongoing EEG and auditory EP generation

    Clin. Neurophysiol.

    (2003)
  • O. Jensen et al.

    Human gamma-frequency oscillations associated with attention and memory

    Trends Neurosci.

    (2007)
  • J. Kaiser et al.

    Gamma-band activity over early sensory areas predicts detection of changes in audiovisual speech stimuli

    Neuroimage

    (2006)
  • J. Kaiser et al.

    Dynamics of gamma-band activity in human magnetoencephalogram during auditory pattern working memory

    Neuroimage

    (2003)
  • W. Khoe et al.

    Exogenous attentional selection of transparent superimposed surfaces modulates early event-related potentials

    Vision Res.

    (2005)
  • E. Körner et al.

    A model of computation in neocortical architecture

    Neural Networks

    (1999)
  • R. Kupper et al.

    Spike-latency codes and the effect of saccades

    Neurocomputing

    (2005)
  • D. Lenz et al.

    Human EEG very high frequency oscillations reflect the number of matches with a template in auditory short-term memory

    Brain Res.

    (2008)
  • D. Lenz et al.

    Enhanced gamma-band activity in ADHD patients lacks correlation with memory performance found in healthy children

    Brain Res.

    (2008)
  • D. Lenz et al.

    What’s that sound? Matches with auditory long-term memory induce gamma activity in human EEG

    Int. J. Psychophysiol.

    (2007)
  • R. Llinás et al.

    Rhythmic and dysrhythmic thalamocortical dynamics: GABA systems and the edge effect

    Trends Neurosci.

    (2005)
  • S. Makeig et al.

    Mining event-related brain dynamics

    Trends Cogn. Sci.

    (2004)
  • J. Martinovic et al.

    Induced gamma-band activity is related to the time point of object identification

    Brain Res.

    (2008)
  • M. Morup et al.

    Parallel factor analysis as an exploratory tool for wavelet transformed event-related EEG

    Neuroimage

    (2006)
  • M.J. Musselwhite et al.

    The influence of spatial frequency on the reaction times and evoked potentials recorded to grating pattern stimuli

    Vision Res.

    (1985)
  • F.W. Ohl et al.

    Learning-induced plasticity in animal and human auditory cortex

    Curr. Opin. Neurobiol.

    (2005)
  • K. Ohla et al.

    Early electrophysiological markers of visual awareness in the human brain

    Neuroimage

    (2007)
  • E.D. Adrian

    Olfactory reactions in the brain of the hedgehog

    J. Physiol.

    (1942)
  • F. Andersson et al.

    Early visual evoked potentials are modulated by eye position in humans induced by whole body rotations

    BMC Neurosci.

    (2004)
  • N. Axmacher et al.

    Sustained neural activity patterns during working memory in the human medial temporal lobe

    J. Neurosci.

    (2007)
  • E. Başar et al.

    The associations between 40 Hz-EEG and the middle latency response of the auditory evoked potential

    Int. J. Neurosci.

    (1987)
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