Review
Oscillatory gamma activity in humans and its role in object representation

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Abstract

We experience objects as whole, complete entities irrespective of whether they are perceived by our sensory systems or are recalled from memory. However, it is also known that many of the properties of objects are encoded and processed in different areas of the brain. How then, do coherent representations emerge? One theory suggests that rhythmic synchronization of neural discharges in the gamma band (around 40 Hz) may provide the necessary spatial and temporal links that bind together the processing in different brain areas to build a coherent percept. In this article we propose that this mechanism could also be used more generally for the construction of object representations that are driven by sensory input or internal, top-down processes. The review will focus on the literature on gamma oscillatory activities in humans and will describe the different types of gamma responses and how to analyze them. Converging evidence that suggests that one particular type of gamma activity (induced gamma activity) is observed during the construction of an object representation will be discussed.

Section snippets

When is induced-gamma activity observed?

Induced-gamma activity has been observed in response to sensory stimuli and during motor tasks in a variety of human EEG and MEG experiments. We now briefly review the somewhat disparate induced-gamma literature organized according to the type of task in which the subject is engaged. All the studies listed below point towards a modulation of induced gamma strength by the perceptive and cognitive parameters of the task; however they do not address the issue of the functional role of induced

Induced gamma and bottom-up feature-binding

If induced gamma activity reflects a binding mechanism, it should be enhanced when a coherent percept is created in response to a given stimulus. This hypothesis can be tested by evaluating the strength of the gamma signal that is induced by stimuli that share the same physical properties but do, or do not, lead to the perception of a coherent percept. Using protocols taken from animal studies9, two different groups have reported an increase in the strength of the gamma signal in the scalp EEG

Induced gamma and object representation

As outlined in the introduction, an object representation can be directly built from the sensory input by bottom-up processes, but might also be expected to be activated, retrieved, or rehearsed through top-down processes. To examine the latter, we investigated the variations in gamma strength that occur when an internal representation of a picture or a tone is needed to correctly perform a task. When searching for someone in a crowd, we know in advance who we are looking for – in other words,

Induced gamma oscillations: the signature of object representation?

In all the studies described above, the variations of induced gamma activity are predicted by the representational hypothesis. Thus, there is growing experimental evidence pointing toward a functional role for induced gamma activity in binding together the areas involved in an object representation, whether generated through bottom-up or top-down processes. Alternative explanations can be found for each experiment individually (attentional selection of the stimuli looking like the target in the

Neural substrate of induced gamma activity

Where do these oscillations recorded on the scalp originate? One could argue that muscular activity might account for these signals. However, several arguments can be put forward that rule out this interpretation. Since induced gamma activity shows task-dependent time courses and topographies, it seems unlikely that it could reflect muscle activity alone. Furthermore, the functional effects are confined to a fairly narrow frequency range (30–50 Hz), whereas muscle activity usually has a broader

Gamma oscillations and spike synchronization

In order to better understand the neural substrate of induced gamma oscillations, we still need to fill the gap between the macroscopic approaches based on scalp EEG recordings reviewed here, and the spike-train synchronizations observed in animal studies at a microscopic scale in single or multiple-unit recordings14, 16, 61, 62. At the present time the results of these two approaches are difficult to compare because of the very different spatial sampling and experimental paradigms used. Signal

Conclusion

The representational hypothesis presented here is derived from the feature-binding hypothesis from the animal literature and postulates that fast oscillatory synchronization of brain areas underlies the construction of a task-relevant object representation. When searching for experimental evidence in human EEG/MEG recordings to support this hypothesis, two types of oscillatory activity in the gamma-range should be distinguished (1) an early, transient 40-Hz evoked response and (2) a

Outstanding questions

  • What is the functional significance of the transient decrease of gamma strength observed after a sensory stimulus, in the time range where the major components of the evoked responses occur?

  • Is multi-sensory integration also achieved through oscillatory synchronization?

  • Induced gamma activity seems to underlie the activation of fine object representations. Can more crude representations be established more quickly through other mechanisms?

  • Is it possible to bridge the gap between oscillatory

Acknowledgements

This work was supported by grants from Human Frontier Science Program (1995–1998) and the Rhône-Alpes Region (1997–2000). We thank J. Pernier for his contribution to the neural source model and many helpful discussions, C. Pantev from Münster University for his collaboration in MEG recordings, M. Huotilainen for her comments on the manuscript, and J.F. Echallier and P.E. Aguerra for their helpful technical assistance.

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