Oscillatory gamma activity in humans: a possible role for object representation

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Abstract

The coherent representation of an object has been suggested to be established by the synchronization in the gamma range (20–100 Hz) of a distributed neural network. So-called ‘40-Hz’ activity in humans could reflect such a mechanism. We have presented here experimental evidence supporting this hypothesis, both in the visual and auditory modalities. However, different types of gamma activity should be distinguished, mainly the evoked 40-Hz response and the induced gamma activities. Only induced gamma activities seem to be related to coherent object representations. In addition, their topography depends on sensory modality and task, which is in line with the idea that they reflect the oscillatory synchronization of task-dependent networks. They can also be functionally and topographically distinguished from the classical evoked potentials and from the alpha rhythm. It was also proposed that the functional role of gamma oscillations is not restricted to object representation established through bottom-up mechanisms of feature binding, but also extends to the cases of internally driven representations and to the maintenance of information in memory.

Introduction

Synchronized oscillatory activity in the gamma range (30–100 Hz) could play a major role in linking the different areas involved in the same object representation into a unified, coherent percept. Indeed, the distributed nature of the network coding for a given object in a particular task is now well documented, in particular by many neuroimaging studies (for review see Courtney et al., 1997). Following the theoretical proposal from Milner, 1974, von der Malsburg and Schneider, 1986, the neural structures participating in this network might be dynamically linked by oscillatory synchronous firing. Over the last decade, this hypothesis has been supported by a growing body of experimental findings in anesthetized and awake animals (Gray et al., 1989, Kreiter and Singer, 1996; for review see Singer and Gray, 1995).

The inspection of the human EEG/MEG literature since the 1950s reveals numerous reports of gamma oscillatory activities in various sensory modalities and tasks (Galambos et al., 1981, Pantev et al., 1991, Pfurtscheller et al., 1994, among many others: Sem-Jacobsen et al., 1956, Sheer, 1989; for review see Tallon-Baudry and Bertrand, 1999). At first glance, these observations may appear rather disparate. Two major factors contribute to this impression: (1) different electrophysiological phenomena have been very often gathered under the same term ‘40-Hz activity’ in an undifferentiated manner; and (2) a common framework for interpretation is somehow lacking.

The three different types of 40-Hz activities observed in humans (namely, evoked, induced and steady-state responses) (Galambos, 1992) will be presented. Experimental evidence showing that induced gamma activity can be related to the generation of unified object representation will be given. The functional specificity of induced gamma oscillations, as compared to the evoked gamma response or classical evoked potential, will be assessed.

Section snippets

Steady-state response

Steady-state evoked potentials are obtained in response to periodically modulated stimuli (auditory, visual or somatosensory). They have a sinusoidal-like waveform at the driving stimulus frequency, and show amplitude maxima in different frequency bands, particularly at approximately 40 Hz. They could reflect the superposition of transient early evoked components (Galambos et al., 1981, Morgan et al., 1996).

Evoked gamma

A transient oscillatory evoked response has been observed in the first 100 ms following

Functional importance of visually induced gamma activity

If synchronized oscillatory activity indeed plays a role in linking together the different neural regions involved in the same object processing, it should be enhanced whenever a coherent percept is being built. So far, we have tested three different experimental paradigms involving the activation of an object representation.

In the first case (Tallon-Baudry et al., 1996), subjects were presented with coherent triangles or an incoherent control (Fig. 2a). Both coherent stimuli (illusory and real

Evoked 40-Hz response

A transient 40-Hz oscillatory component has been observed in the first 100 ms following a transient acoustic stimulus in the averaged evoked response from either electrical or magnetic signals. It consists of a small amplitude response, phase-locked to the stimulus onset and occurring in the same time range as the middle-latency auditory components (Fig. 5a). Pantev et al. (1991) revealed from magnetic recordings that this 40-Hz response is generated at least partially in the auditory cortex.

Conclusions

Do induced gamma activities and evoked potentials reflect distinct processes? Several arguments stand in favor of a clear distinction between these two phenomena. Indeed, the topographies of induced gamma and evoked potentials can be very different, as for example during the delay in the visual short-term memory experiment (Fig. 4), or fairly close, as in the acoustic frequency discrimination task (Fig. 6). The effects observed on induced gamma activity can occur at shorter latencies than those

Acknowledgements

This work was supported by grants from the Rhône-Alpes Region (1997–2000).

References (43)

  • J. Sinkkonen et al.

    Gabor filters: an informative way for analysing event-related brain activity

    J. Neurosci. Meth.

    (1995)
  • C. Tallon-Baudry et al.

    Oscillatory gamma activity in humans and its role in object representation

    Trends Cogni. Sci.

    (1999)
  • A. von Stein et al.

    Different frequencies for different scales of cortical integration

    Int. J. Psychophysiol.

    (2000)
  • O. Bertrand et al.

    Stimulus frequency dependence of the transient oscillatory auditory evoked responses (40 Hz) studied by electric and magnetic recordings in human

  • Bertrand, O., Tallon-Baudry, C., Pernier, J., 1999. Time-frequency analysis of oscillatory gamma-band activity: wavelet...
  • S.M. Courtney et al.

    Transient and sustained activity in a distributed neural system for human working memory

    Nature

    (1997)
  • M.N. Franowicz et al.

    Comparison of evoked potentials and highfrequency (gamma-band) oscillating potentials in rat auditory cortex

    J. Neurophysiol.

    (1995)
  • R. Galambos

    A comparison of certain gamma band (40-Hz) brain rhythms in cat and man

  • R. Galambos et al.

    A 40-Hz auditory potential recorded from the human scalp

    Proc. Natl. Acad. Sci. USA

    (1981)
  • C.M. Gray et al.

    Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties

    Nature

    (1989)
  • H. Jokeit et al.

    Different event-related patterns of gamma-band power in brain waves of fast- and slow-reacting subjects

    Proc. Natl. Acad. Sci. USA

    (1994)
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