The brain exhibits organized fluctuations of neural activity, even in the absence of tasks or sensory input. A prominent type of such spontaneous activity is the alpha rhythm, which influences perception and interacts with other ongoing neural activity. It is currently hypothesized that states of decreased prestimulus α oscillations indicate enhanced neural excitability, resulting in improved perceptual acuity. Nevertheless, it remains debated how changes in excitability manifest at the behavioral level in perceptual tasks. We addressed this issue by comparing two alternative models describing the effect of spontaneous α power on signal detection. The first model assumes that decreased α power increases baseline excitability, amplifying the response to both signal and noise, predicting a liberal detection criterion with no effect on sensitivity. The second model predicts that decreased α power increases the trial-by-trial precision of the sensory response, resulting in improved sensitivity. We tested these models in two EEG experiments in humans where we analyzed the effects of prestimulus α power on visual detection and discrimination using a signal detection framework. Both experiments provide strong evidence that decreased α power reflects a more liberal detection criterion, rather than improved sensitivity, consistent with the baseline model. In other words, when the task requires detecting stimulus presence versus absence, reduced α oscillations make observers more likely to report the stimulus regardless of actual stimulus presence. Contrary to previous interpretations, these results suggest that states of decreased α oscillations increase the global baseline excitability of sensory systems without affecting perceptual acuity.SIGNIFICANCE STATEMENTSpontaneous fluctuations of brain activity explain why a faint sensory stimulus is sometimes perceived and sometimes not. The prevailing view is that heightened neural excitability, indexed by decreased α oscillations, promotes better perceptual performance. Here, we provide evidence that heightened neural excitability instead reflects a state of biased perception, during which a person is more likely to see a stimulus, whether or not it is actually present. Therefore, we propose that changes in neural excitability leave the precision of sensory processing unaffected. These results establish the link between spontaneous brain activity and the variability in human perception.
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 (70-120 Hz) at central occipital locations. Attention-related gamma oscillations appeared as an additional component whenever attentional focusing was requested in the low gamma-band (44-66 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.
The ongoing state of the brain radically affects how it processes sensory information. How does this ongoing brain activity interact with the processing of external stimuli? Spontaneous oscillations in the alpha range are thought to inhibit sensory processing, but little is known about the psychophysical mechanisms of this inhibition. We recorded ongoing brain activity with EEG while human observers performed a visual detection task with stimuli of different contrast intensities. To move beyond qualitative description, we formally compared psychometric functions obtained under different levels of ongoing alpha power and evaluated the inhibitory effect of ongoing alpha oscillations in terms of contrast or response gain models. This procedure opens the way to understanding the actual functional mechanisms by which ongoing brain activity affects visual performance. We found that strong prestimulus occipital alpha oscillations-but not more anterior mu oscillations-reduce performance most strongly for stimuli of the highest intensities tested. This inhibitory effect is best explained by a divisive reduction of response gain. Ongoing occipital alpha oscillations thus reflect changes in the visual system's input/output transformation that are independent of the sensory input to the system. They selectively scale the system's response, rather than change its sensitivity to sensory information.
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