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Oscillatory Synchrony

From a neural point of view, building a coherent percept can be compared to a jigsaw puzzle. The pieces of the puzzle are the bits of sensory information that are scattered in different sensory areas: the color of an object, for instance, is analyzed in one brain region, and its motion in another one. But how are these pieces put back together again to form the coherent percept we experience? This problem, also known as the feature binding problem, could be solved by oscillatory synchrony: All neurons dealing with the same perceptual object would synchronize their firing on an oscillatory mode—in other words, alternate collectively between epochs of activity and rest—much as a group of drummers would follow a given rhythm. In this view, the temporal structure of neural activity becomes a fundamental property of the neural code.

Binding features together in an object is crucial, but distinguishing objects from one another is equally important. Oscillatory synchrony may be relevant for scene segmentation: In response to a picture of a woman carrying a dog, for instance, neurons responding to the woman would synchronize their discharge at a given frequency, whereas neurons responding to the dog would synchronize their discharge at a different frequency—as two groups of drummers could beat two distinct rhythms. In addition to scene analysis, oscillatory synchrony may also prove useful for other cognitive functions, such as attention, memory, and awareness. This entry describes neural oscillations and measuring oscillatory potentials.

Neural Oscillations

A typical experimental test of the role of oscillatory synchrony in feature binding involves two physically similar perceptual configurations: one leading to a coherent percept (e.g., dots defining the contours of a triangle) but not the other (randomly placed dots). Oscillatory synchrony is larger in response to the coherent stimulus: It could thus be involved in grouping together different sensory features in a coherent perceptual whole. This finding has been replicated a number of times in the visual modality, using a variety of stimulus configurations and recording methods, in both humans and animals. The role of oscillatory synchrony in other sensory modalities, as well as in cross-modal integration (e.g., integrating the sound of a bark with the picture of a dog), is also well documented. Direct tests of the role of oscillatory synchrony in segmentation are more scarce, especially in humans.

Because oscillatory synchrony has been primarily involved in feature binding, it has been proposed as a mechanism linking direct neural activity to subjective experience. Thus, it has often been considered as a potential neural correlate of (or prerequisite to) awareness. Oscillatory synchrony shows an additional interesting feature: It is by definition a group property, in line with the idea that awareness cannot be reduced to activity in a single module, area, or neuron, but emerges from dynamical interactions within the brain. This appealing theoretical proposal remains quite difficult to validate experimentally in an irrefutable manner, although a growing body of evidence points in this direction.

The oscillations related to grouping and awareness are quite fast, in what is called the gamma range, between 30 and 100 hertz (Hz). This means that an oscillation period lasts between 10 and 30 milliseconds (ms). This corresponds to a temporal window of crucial importance for neural integration: All inputs arriving on a given neuron within 10 to 30 ms add up and are likely to generate a response in this neuron. On the other hand, the same number of inputs arriving over a longer period of time (e.g., 100 ms) will not add up to generate a response. In other words, inputs that are synchronized are more likely to be selected for further processing than nonsynchronized inputs: This is the definition of an attentional selection mechanism. Experimentally, attention-related gamma oscillations have indeed been described, both in monkeys and humans. In addition, synaptic plasticity—the fundamental mechanism by which learning takes place and new memories are formed—can be highly sensitive to input timing, in particular within 10 to 30 ms. A growing number of experimental data in humans and monkeys corroborate the involvement of oscillatory synchrony in memory formation, in both the visual and auditory modality. For instance, items that elicit larger gamma oscillations when seen for the first time are more likely to be recalled later.

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