Attention and awareness in synchrony.

Interactions between functional areas are often considered to account for subtle aspects of cognitive functions, although direct experimental evidence is scarce. A recent study by Gross et al. relates the strength of synchrony between human parietal, frontal and occipital regions to the availability of attentional resources. These results support the current view that attention and awareness emerge from dynamic interactions in distributed networks.

Oscillatory synchrony between human extrastriate areas during visual short-term memory maintenance.

How do we keep an object in mind? Based on evidence from animal electrophysiology and human brain-imaging techniques, it is commonly held that short-term memory relies on sustained activity in a network distributed over sensory and prefrontal cortices. How does neural firing persist in such a distributed network in the absence of visual input? Hebb's influential but so far unproved proposal, developed more than 50 years ago, is that sustained activation in short-term memory networks is maintained by reverberating activity in neuronal loops. We hypothesized that synchronized oscillatory activity, proposed to provide a dynamic link between distributed areas, could not only coordinate activity in the network but also establish reentrant loops in the system to enable both sustained firing and temporal coincidence of inputs. We show in human intracranial recordings that limited regions of extrastriate visual areas, separated by several centimeters, become synchronized in an oscillatory mode during the rehearsal of an object in visual short-term memory. Synchrony occurs specifically in the beta range (15-25 Hz) and disappears in a control condition. These findings thus confirm experimentally the hypothesis of a functional role of synchronized oscillatory activity in the coordination of distributed neural activity in humans, and support Hebb's popular but unproved concept of short-term memory maintenance by reentrant activity within the activated network.

Cortical mapping of gamma oscillations in areas V1 and V4 of the macaque monkey.

To characterize the temporal and spatial parameters of gamma activity evoked by visual stimuli in areas V1 and V4 of the monkey cortex, we recorded the electrocorticogram (ECoG) with an implanted array of 28 and 31 subdural electrodes placed over the surface of the operculum in two anesthetized monkeys. This intermediate level of recordings should help to bridge the gap between multiunit and scalp recordings. Both averaged and single-trial responses to small flashed stimuli, for which we varied the retinotopic position, the luminance and the color, were analyzed in the time-frequency domain using a wavelet-based decomposition of the signal. Large gamma oscillations (40-55 Hz), not phase locked to stimulus onset, were observed during the whole stimulus presentation, whereas visual evoked potentials (VEPs) were present mainly at stimulus onset and offset. Cortical mapping showed that both activities were restricted in spatial extent and followed the retinotopic organization of area V1 on the operculum, thus strongly suggesting they were generated in the underlying cortex. Oscillatory burst detection in single trials showed that one to two bursts lasting from 100 ms to 500 ms occurred in the first 500 ms following stimulus onset, and that bursts occurring during the subsequent phases of the response had a smaller amplitude and duration. Finally, we showed that gamma activity was stronger with higher luminances and for red than for green, yellow, or white stimuli of same luminance. In one animal we recorded gamma activity over area V4. This was of lower magnitude than the activity recorded over V1 and was delayed by 40 ms with respect to the beginning of gamma activity in V1, in contrast with the VEPs that were delayed by 20 ms only. Both gamma oscillations and early VEP followed the retinotopic organization of V4 over the prelunate gyrus. The results show that gamma oscillations are dependent upon the same parameters as the VEPs (retinotopic position, luminance, and color). However, the differences in the time course of VEPs and gamma activity (transient vs. sustained) suggests that these two responses may reflect different cell populations, different networks, or different firing modes.

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

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.

Sustained and transient oscillatory responses in the gamma and beta bands in a visual short-term memory task in humans.

In a visual delayed matching-to-sample task, compared to a control condition, we had previously identified different components of the human EEG that could reflect the rehearsal of an object representation in short-term memory (Tallon-Baudry et al., 1998). These components were induced oscillatory activities in the gamma (24-60 Hz) and beta (15-20 Hz) bands, peaking during the delay at occipital and frontal electrodes, and two negativities in the evoked potentials. Sustained activities (lasting until the end of the delay) are more likely to reflect the continuous rehearsing process in memory than transient (ending before the end of the delay) activities. Nevertheless, since the delay duration we used in our previous experiment was fixed and rather short, it was difficult to discriminate between sustained and transient components. Here we used the same delayed matching-to-sample task, but with variable delay durations. The same oscillatory components in the gamma and beta bands were observed again during the delay. The only components that showed a sustained time course compatible with a memory rehearsing process were the occipital gamma and frontal beta induced activities. These two activities slowly decreased with increasing delay duration, while the performance of the subjects decreased in parallel. No sustained response could be found in the evoked potentials. These results support the hypothesis that objects representations in visual short-term memory consist of oscillating synchronized cell assemblies.

A ring-shaped distribution of dipoles as a source model of induced gamma-band activity.

As opposed to slow waves, spontaneous and stimulus-induced oscillations in the gamma-band show no polarity reversal in cortical depth, which cannot be explained by the classical equivalent current dipole model usually proposed as a model of pyramidal cell synaptic activity. Here we propose a ring-shaped distribution of dipoles as a source model for these fast oscillations. This distribution generates a field potential that does not reverse through cortical depth. Such a geometry could correspond to horizontally oriented dendritic fields. Moreover, this distribution generates a potential field, but no, or weak, magnetic field on the scalp surface, which corresponds to the observation that visually-induced gamma-band oscillations are detectable in EEG data, but not in simultaneously recorded MEG data.

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

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.

Induced gamma-band activity during the delay of a visual short-term memory task in humans.

It has been hypothesized that visual objects could be represented in the brain by a distributed cell assembly synchronized on an oscillatory mode in the gamma-band (20-80 Hz). If this hypothesis is correct, then oscillatory gamma-band activity should appear in any task requiring the activation of an object representation, and in particular when an object representation is held active in short-term memory: sustained gamma-band activity is thus expected during the delay of a delayed-matching-to-sample task. EEG was recorded while subjects performed such a task. Induced (e.g., appearing with a jitter in latency from one trial to the next) gamma-band activity was observed during the delay. In a control task, in which no memorization was required, this activity disappeared. Furthermore, this gamma-band activity during the rehearsal of the first stimulus representation in short-term memory peaked at both occipitotemporal and frontal electrodes. This topography fits with the idea of a synchronized cortical network centered on prefrontal and ventral visual areas. Activities in the alpha band, in the 15-20 Hz band, and in the averaged evoked potential were also analyzed. The gamma-band activity during the delay can be distinguished from all of these other components of the response, on the basis of either its variations or its topography. It thus seems to be a specific functional component of the response that could correspond to the rehearsal of an object representation in short-term memory.

Combined EEG and MEG recordings of visual 40 Hz responses to illusory triangles in human.

EEG and MEG were simultaneously recorded to study the visual gamma-band (30-70 Hz) responses. The electrical gamma-band response phase-locked to stimulus onset can be subdivided into a central component at 39 Hz and an occipital component at 36 Hz. A new high-frequency magnetic phase-locked response recorded over the occipital lobe is described. Its topography is complex and probably reflects the activity of multiple sources. Both electrical and magnetic high-frequency responses differ in topography from the low-frequency responses in the same latency range, suggesting that at least partially distinct sources are involved. The existence of a non-phase-locked 40 Hz component around 280 ms is confirmed in EEG data but is not detectable in MEG data.

Oscillatory gamma-band (30-70 Hz) activity induced by a visual search task in humans.

The coherent representation of an object in the visual system has been suggested to be achieved by the synchronization in the gamma-band (30-70 Hz) of a distributed neuronal assembly. Here we measure variations of high-frequency activity on the human scalp. The experiment is designed to allow the comparison of two different perceptions of the same picture. In the first condition, an apparently meaningless picture that contained a hidden Dalmatian, a neutral stimulus, and a target stimulus (twirled blobs) are presented. After the subject has been trained to perceive the hidden dog and its mirror image, the second part of the recordings is performed (condition 2). The same neutral stimulus is presented, intermixed with the picture of the dog and its mirror image (target stimulus). Early (95 msec) phase-locked (or stimulus-locked) gamma-band oscillations do not vary with stimulus type but can be subdivided into an anterior component (38 Hz) and a posterior component (35 Hz). Nonphase-locked gamma-band oscillations appear with a latency jitter around 280 msec after stimulus onset and disappear in averaged data. They increase in amplitude in response to both target stimuli. They also globally increase in the second condition compared with the first one. It is suggested that this gamma-band energy increase reflects both bottom-up (binding of elementary features) and top-down (search for the hidden dog) activation of the same neural assembly coding for the Dalmatian. The relationships between high- and low-frequency components of the response are discussed, and a possible functional role of each component is suggested.

Stimulus specificity of phase-locked and non-phase-locked 40 Hz visual responses in human.

Considerable interest has been raised by non-phase-locked episodes of synchronization in the gamma-band (30-60 Hz). One of their putative roles in the visual modality is feature-binding. We tested the stimulus specificity of high-frequency oscillations in humans using three types of visual stimuli: two coherent stimuli (a Kanizsa and a real triangle) and a noncoherent stimulus ("no-triangle stimulus"). The task of the subject was to count the occurrences of a curved illusory triangle. A time-frequency analysis of single-trial EEG data recorded from eight human subjects was performed to characterize phase-locked as well as non-phase-locked high-frequency activities. We found in early phase-locked 40 Hz component, maximal at electrodes Cz-C4, which does not vary with stimulation type. We describe a second 40 Hz component, appearing around 280 msec, that is not phase-locked to stimulus onset. This component is stronger in response to a coherent triangle, whether real or illusory: it could reflect, therefore, a mechanism of feature binding based on high-frequency synchronization. Because both the illusory and the real triangle are more target-like, it could also correspond to an oscillatory mechanism for testing the match between stimulus and target. At the same latencies, the low-frequency evoked response components phase-locked to stimulus onset behave differently, suggesting that low- and high-frequency activities have different functional roles.