Alpha Oscillations Shape Sensory Representation and Perceptual Sensitivity.

Alpha activity (8-14 Hz) is the dominant rhythm in the awake brain and is thought to play an important role in setting the internal state of the brain. Previous work has associated states of decreased alpha power with enhanced neural excitability. However, evidence is mixed on whether and how such excitability enhancement modulates sensory signals of interest versus noise differently, and what, if any, are the consequences for subsequent perception. Here, human subjects (male and female) performed a visual detection task in which we manipulated their decision criteria in a blockwise manner. Although our manipulation led to substantial criterion shifts, these shifts were not reflected in prestimulus alpha band changes. Rather, lower prestimulus alpha power in occipital-parietal areas improved perceptual sensitivity and enhanced information content decodable from neural activity patterns. Additionally, oscillatory alpha phase immediately before stimulus presentation modulated accuracy. Together, our results suggest that alpha band dynamics modulate sensory signals of interest more strongly than noise.SIGNIFICANCE STATEMENT The internal state of our brain fluctuates, giving rise to variability in perception and action. Neural oscillations, most prominently in the alpha band, have been suggested to play a role in setting this internal state. Here, we show that ongoing alpha band activity in occipital-parietal regions predicts the quality of visual information decodable in neural activity patterns and subsequently the human observer's sensitivity in a visual detection task. Our results provide comprehensive evidence that visual representation is modulated by ongoing alpha band activity and advance our understanding on how, when faced with unchanging external stimuli, internal neural fluctuations influence perception and behavior.

Pre-stimulus alpha-band phase gates early visual cortex responses.

Alpha-band (8-13 Hz) oscillations have been shown to phasically inhibit perceptual reports in human observers, yet the underlying physiological mechanism of this effect is debated. According to contrasting models, based primarily on animal experiments, alpha activity is thought to either originate from specialized cells in the visual thalamus and periodically inhibit the relay of visual information to the primary visual cortex (V1) in a feedforward manner, or to propagate from higher visual areas back to V1 in a feedback manner. Human neurophysiological evidence in favor of either hypothesis, both, or neither, has been limited. To help address this issue, we explored the link between pre-stimulus alpha phase and visual electroencephalography (EEG) responses thought to arise from afferent input onto human V1. Specially-designed visual stimuli were used to elicit large amplitude C1 event-related potentials (ERP), with polarity, topography, and timing indicative of striate genesis. Single-trial circular-linear associations between pre-stimulus phase and post-stimulus global field power (GFP) during the C1 time window revealed significant effects peaking in the alpha frequency band. Control analyses ruling out the potential confound of post-stimulus data bleeding into the pre-stimulus window demonstrated that GFP amplitude decreases as pre-stimulus alpha phase deviates from an individual's preferred phase. These findings demonstrate an early locus - suggesting that the phase of pre-stimulus alpha oscillations could modulate visual processing by gating the feedforward flow of sensory input between the thalamus and V1, although other models are potentially compatible.

Ongoing neural oscillations influence behavior and sensory representations by suppressing neuronal excitability.

The ability to process and respond to external input is critical for adaptive behavior. Why, then, do neural and behavioral responses vary across repeated presentations of the same sensory input? Ongoing fluctuations of neuronal excitability are currently hypothesized to underlie the trial-by-trial variability in sensory processing. To test this, we capitalized on intracranial electrophysiology in neurosurgical patients performing an auditory discrimination task with visual cues: specifically, we examined the interaction between prestimulus alpha oscillations, excitability, task performance, and decoded neural stimulus representations. We found that strong prestimulus oscillations in the alpha+ band (i.e., alpha and neighboring frequencies), rather than the aperiodic signal, correlated with a low excitability state, indexed by reduced broadband high-frequency activity. This state was related to slower reaction times and reduced neural stimulus encoding strength. We propose that the alpha+ rhythm modulates excitability, thereby resulting in variability in behavior and sensory representations despite identical input.

Spontaneous Neural Oscillations Bias Perception by Modulating Baseline Excitability.

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 STATEMENT: Spontaneous 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.

Prestimulus alpha-band power biases visual discrimination confidence, but not accuracy.

The magnitude of power in the alpha-band (8-13Hz) of the electroencephalogram (EEG) prior to the onset of a near threshold visual stimulus predicts performance. Together with other findings, this has been interpreted as evidence that alpha-band dynamics reflect cortical excitability. We reasoned, however, that non-specific changes in excitability would be expected to influence signal and noise in the same way, leaving actual discriminability unchanged. Indeed, using a two-choice orientation discrimination task, we found that discrimination accuracy was unaffected by fluctuations in prestimulus alpha power. Decision confidence, on the other hand, was strongly negatively correlated with prestimulus alpha power. This finding constitutes a clear dissociation between objective and subjective measures of visual perception as a function of prestimulus cortical excitability. This dissociation is predicted by a model where the balance of evidence supporting each choice drives objective performance but only the magnitude of evidence supporting the selected choice drives subjective reports, suggesting that human perceptual confidence can be suboptimal with respect to tracking objective accuracy.

Spontaneous Brain Oscillations and Perceptual Decision-Making.

Making rapid decisions on the basis of sensory information is essential to everyday behaviors. Why, then, are perceptual decisions so variable despite unchanging inputs? Spontaneous neural oscillations have emerged as a key predictor of trial-to-trial perceptual variability. New work casting these effects in the framework of models of perceptual decision-making has driven novel insight into how the amplitude of spontaneous oscillations impact decision-making. This synthesis reveals that the amplitude of ongoing low-frequency oscillations (<30 Hz), particularly in the alpha-band (8-13 Hz), bias sensory responses and change conscious perception but not, surprisingly, the underlying sensitivity of perception. A key model-based insight is that various decision thresholds do not adapt to alpha-related changes in sensory activity, demonstrating a seeming suboptimality of decision mechanisms in tracking endogenous changes in sensory responses.

Multiple mechanisms link prestimulus neural oscillations to sensory responses.

Spontaneous fluctuations of neural activity may explain why sensory responses vary across repeated presentations of the same physical stimulus. To test this hypothesis, we recorded electroencephalography in humans during stimulation with identical visual stimuli and analyzed how prestimulus neural oscillations modulate different stages of sensory processing reflected by distinct components of the event-related potential (ERP). We found that strong prestimulus alpha- and beta-band power resulted in a suppression of early ERP components (C1 and N150) and in an amplification of late components (after 0.4 s), even after controlling for fluctuations in 1/f aperiodic signal and sleepiness. Whereas functional inhibition of sensory processing underlies the reduction of early ERP responses, we found that the modulation of non-zero-mean oscillations (baseline shift) accounted for the amplification of late responses. Distinguishing between these two mechanisms is crucial for understanding how internal brain states modulate the processing of incoming sensory information.

Moment-to-Moment Fluctuations in Neuronal Excitability Bias Subjective Perception Rather than Strategic Decision-Making.

Perceiving an external stimulus depends not only on the physical features of the stimulus, but also fundamentally on the current state of neuronal excitability, indexed by the power of ongoing alpha-band and beta-band oscillations (8-30 Hz). Recent studies suggest that heightened excitability does not improve perceptual precision, but biases observers to report the presence of a stimulus regardless of its physical presence. It is unknown whether this bias is due to changes in observers' subjective perceptual experience (perceptual bias) or their perception-independent decision-making strategy (decision bias). We tested these alternative interpretations in an EEG experiment in which male and female human participants performed two-interval forced choice (2IFC) detection and discrimination. According to signal detection theory, perceptual bias only affects 2IFC detection, but not discrimination, while interval decision bias should be task independent. We found that correct detection was more likely when excitability before the stimulus-present interval exceeded that before the stimulus-absent interval (i.e., 8-17 Hz power was weaker before the stimulus-present interval), consistent with an effect of excitability on perceptual bias. By contrast, discrimination accuracy was unaffected by excitability fluctuations between intervals, ruling out an effect on interval decision bias. We conclude that the current state of neuronal excitability biases the perceptual experience itself, rather than the decision process.