Catherine Tallon-Baudry

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.

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 an 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.

Neural Dissociation between Visual Awareness and Spatial Attention

To what extent does what we consciously see depend on where we attend to? Psychologists have long stressed the tight relationship between visual awareness and spatial attention at the behavioral level. However, the amount of overlap between their neural correlates remains a matter of debate. We recorded magnetoencephalographic signals while human subjects attended toward or away from faint stimuli that were reported as consciously seen only half of the time. Visually identical stimuli could thus be attended or not and consciously seen or not. Although attended stimuli were consciously seen slightly more often than unattended ones, the factorial analysis of stimulus-induced oscillatory brain activity revealed distinct and independent neural correlates of visual awareness and spatial attention at different frequencies in the gamma range (30–150 Hz). Whether attended or not, consciously seen stimuli induced increased mid-frequency gamma-band activity over the contralateral visual cortex, whereas spatial attention modulated high-frequency gamma-band activity in response to both consciously seen and unseen stimuli. A parametric analysis of the data at the single-trial level confirmed that the awareness-related mid-frequency activity drove the seen–unseen decision but also revealed a small influence of the attention-related high-frequency activity on the decision. These results suggest that subjective visual experience is shaped by the cumulative contribution of two processes operating independently at the neural level, one reflecting visual awareness per se and the other reflecting spatial attention.

The many faces of the gamma band response to complex visual stimuli.

While much is known about the functional architecture of the visual system, little is known about its large-scale dynamics during perception. This study describes this dynamics with a high spatial, temporal and spectral resolution. We recorded depth EEG of epileptic patients performing a face detection task and found that the stimuli induced strong modulations in the gamma band (40 Hz to 200 Hz) in selective occipital, parietal and temporal sites, in particular the fusiform gyrus, the lateral occipital gyrus and the intra-parietal sulcus. Occipito-temporal sites were the first to be activated, closely followed by the parietal sites, while portions of the primary visual cortex seemed to deactivate temporarily. Some of those effects were found to be correlated across distant sites, suggesting that a coordinated balance between regional gamma activations and deactivations could be involved during visual perception.

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.

An attention modulated response to disgust in human ventral anterior insula

The human brain is expert in analyzing rapidly and precisely facial features, especially emotional expressions representing a powerful communication vector. The involvement of insula in disgust recognition has been reported in behavioral and functional imaging studies. However, we do not know whether specific insular fields are involved in disgust processing nor what the processing time course is. Using depth electrodes implanted during presurgical evaluation of patients with drug‐refractory temporal lobe epilepsy, we recorded intracerebral event‐related potentials to human facial emotional expressions, that is, fear, disgust, happiness, surprise, and neutral expression. We studied evoked responses in 13 patients with insular contacts to specify the insular fields involved in disgust processing and assess the timing of their activation. We showed that specific potentials to disgust beginning 300 milliseconds after stimulus onset and lasting 200 milliseconds were evoked in the ventral anterior insula in four patients. The occurrence and latency of event‐related potentials to disgust in the ventral anterior insula were affected by selective attention. The analysis of spatial and temporal characteristics of insular responses to disgust facial expression lead us to underline the crucial role of ventral anterior insula in the categorization of facial emotional expressions, particularly the disgust. Ann Neurol 2003

The roles of gamma-band oscillatory synchrony in human visual cognition.

Oscillatory synchrony in the gamma (30-120 Hz) range has initially been related both theoretically and experimentally to visual grouping. Its functional role in human visual cognition turns out to be much broader, especially when attention, memory or awareness are concerned. Induced gamma oscillations are thus not related to a single cognitive function, and are probably better understood in terms of a population mechanism taking advantage of the neurons fine temporal tuning: the 10-30 ms time precision imposed by gamma-band rhythms could favor the selective transmission of synchronized information (attention) and foster synaptic plasticity (memory). Besides, gamma oscillatory synchrony also seems related to the emergence of visual awareness. The recent discovery that gamma oscillations could appear simultaneously in distinct areas at distinct frequencies and with different functional correlates further suggests the existence of a flexible multiplexing schema, integrating frequency bands within the gamma range but also at lower frequency bands. Understanding how and when oscillations at different frequencies interact has become a major challenge for the years to come.

Visual Grouping and the Focusing of Attention Induce Gamma-band Oscillations at Different Frequencies in Human Magnetoencephalogram Signals

Neural oscillatory synchrony could implement grouping processes, act as an attentional filter, or foster the storage of information in short-term memory. Do these findings indicate that oscillatory synchrony is an unspecific epiphenomenon occurring in any demanding task, or that oscillatory synchrony is a fundamental mechanism involved whenever neural cooperation is requested? If the latter hypothesis is true, then oscillatory synchrony should be specific, with distinct visual processes eliciting different types of oscillations. We recorded magnetoencephalogram (MEG) signals while manipulating the grouping properties of a visual display on the one hand, and the focusing of attention to memorize part of this display on the other hand. Grouping-related gamma oscillations were present in all conditions but modulated by the grouping properties of the stimulus (one or two groups) in the high gamma-band (70120 Hz) at central occipital locations. Attention-related gamma oscillations appeared as an additional component whenever attentional focusing was requested in the low gamma-band (4466 Hz) at parietal locations. Our results thus reveal the existence of a functional specialization in the gamma range, with grouping-related oscillations showing up at higher frequencies than attention-related oscillations. The pattern of oscillatory synchrony is thus specific of the visual process it is associated with. Our results further suggest that both grouping processes and focused attention rely on a common implementation process, namely, gamma-band oscillatory synchrony, a finding that could account for the fact that coherent percepts are more likely to catch attention than incoherent ones.

Olfactory learning modifies the expression of odour-induced oscillatory responses in the gamma (60-90 Hz) and beta (15-40 Hz) bands in the rat olfactory bulb

This study addressed the question of the possible functional relevance of two different oscillatory activities, beta and gamma (15–40 and 60–90 Hz, respectively) for perception and memory processes in olfactory areas of mammals. Local field potentials were recorded near relay olfactory bulb neurons while rats performed an olfactory discrimination task. Signals reflected the mass activity from this region and characteristics of oscillatory activities were used as an index of local synchrony. Beta and gamma oscillatory activities were quantified by time‐frequency methods before during and after odour sampling. In rats early in their training, olfactory sampling was associated with a significant decrease in power in the gamma band in parallel with a weak but significant increase in the beta band (centred on 27 Hz). Several days later, in well‐trained rats, the gamma oscillatory depression was significantly enhanced both in duration and amplitude. It appeared within the 500 ms time period preceding odour onset and was further reduced during the odour period. Concurrently the beta oscillatory response (now centred on 24 Hz) during odour sampling was amplified by a twofold factor. The beta band response was modulated according to the chemical nature of the stimuli and rats behavioural response. This study showed for the first time that odour sampling in behaving animals is associated with a clear shift in the olfactory bulb neuronal activity from a gamma to a beta oscillatory regime. Moreover, the data stress the importance of studying the odour‐induced beta activity and its relation to perception and memory.

How Ongoing Fluctuations in Human Visual Cortex Predict Perceptual Awareness: Baseline Shift versus Decision Bias

Visual perception fluctuates across repeated presentations of the same near-threshold stimulus. These perceptual fluctuations have often been attributed to baseline shifts—i.e., ongoing modulations of neuronal activity in visual areas—driven by top-down attention. Using magnetoencephalography, we directly tested whether ongoing attentional modulations could fully account for the perceptual impact of prestimulus activity on a subsequent seen–unseen decision. We found that prestimulus gamma-band fluctuations in lateral occipital areas (LO) predicted visual awareness, but did not reflect the focus of spatial attention. Moreover, these prestimulus signals influenced the decision outcome independently from the strength of the following visual response, suggesting that baseline shifts alone could not explain their perceptual impact. Using a straightforward decision-making model based on the accumulation of sensory evidence over time, we show that prestimulus gamma-band fluctuations in LO behave as a decision bias at stimulus onset, irrespectively of subsequent stimulus processing. In contrast, spatial attention suppressed prestimulus alpha-band signals in the same region, and produced a sustained baseline shift that also predicted the outcome of the seen–unseen decision. Together, our results indicate that prestimulus fluctuations in visual areas can influence the conscious detection of an upcoming stimulus via two distinct mechanisms: an attention-driven baseline shift in the alpha range, and a decision bias in the gamma range.