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

No changes in parieto-occipital alpha during neural phase locking to visual quasi-periodic theta-, alpha-, and beta-band stimulation

Recent studies have probed the role of the parieto‐occipital alpha rhythm (8 – 12 Hz) in human visual perception through attempts to drive its neural generators. To that end, paradigms have used high‐intensity strictly‐periodic visual stimulation that created strong predictions about future stimulus occurrences and repeatedly demonstrated perceptual consequences in line with an entrainment of parieto‐occipital alpha. Our study, in turn, examined the case of alpha entrainment by non‐predictive low‐intensity quasi‐periodic visual stimulation within theta‐ (4 – 7 Hz), alpha‐ (8 – 13 Hz) and beta (14 – 20 Hz) frequency bands, i.e. a class of stimuli that resemble the temporal characteristics of naturally occurring visual input more closely. We have previously reported substantial neural phase‐locking in EEG recording during all three stimulation conditions. Here, we studied to what extent this phase‐locking reflected an entrainment of intrinsic alpha rhythms in the same dataset. Specifically, we tested whether quasi‐periodic visual stimulation affected several properties of parieto‐occipital alpha generators. Speaking against an entrainment of intrinsic alpha rhythms by non‐predictive low‐intensity quasi‐periodic visual stimulation, we found none of these properties to show differences between stimulation frequency bands. In particular, alpha band generators did not show increased sensitivity to alpha band stimulation and Bayesian inference corroborated evidence against an influence of stimulation frequency. Our results set boundary conditions for when and how to expect effects of entrainment of alpha generators and suggest that the parieto‐occipital alpha rhythm may be more inert to external influences than previously thought

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

Spontane neuronale Oszillationen beeinflussen Wahrnehmung durch Modulation von Baseline-Erregbarkeit

Spontaneous fluctuations of brain activity explain why a faint sensory stimulus is sometimes perceived and sometimes not. The predominant view is that heightened neural excitability, indexed by reduced spontaneous oscillations in the alpha frequency band (8-12 Hz), reflect a state of improved perceptual acuity. In this dissertation I present two EEG experiments and a systematic literature review that challenge this view by showing that reduced spontaneous oscillations reflect a state of biased, rather than improved, perception. In the first EEG experiment, I analysed the influence of spontaneous neural oscillations in a yes/no detection task with stimulus present and absent trials. States of reduced alpha oscillations preceded stimulus present reports in both stimulus present (i.e. hits) and absent trials (i.e. false alarms). According to signal detection theory, this is equivalent to a liberal detection criterion, rather than improved sensitivity/acuity. In the second EEG experiment, I compared the perceptual influence of spontaneous neural oscillations in detection and discrimination. Although I replicated the finding that states of reduced alpha oscillations boost the number of hits in detection, I found that spontaneous alpha oscillations had no effect on the proportion of correct discrimination responses. In addition to the EEG experiments, I conducted a systematic literature review on studies analysing the effect of spontaneous alpha oscillations on visual perceptual performance. I categorised the studies based on whether they used behavioural measures that were dependent (e.g. number of hits and false alarms) or Independent (e.g. detection sensitivity or the proportion of correct discrimination responses) of detection criterion. I found that most studies using criterion-dependent measures Report an effect of spontaneous alpha oscillations on perception, consistent with the results from the detection tasks of both EEG experiments. By contrast, most studies using criterion-independent measures report no effect of spontaneous alpha oscillations on perception. Thus, these studies confirm the null effect on detection sensitivity in the first EEG experiment and on discrimination accuracy in the second EEG experiment. Contrary to the predominant view, these findings indicate that heightened neural excitability, indexed by reduced alpha oscillations, is paralleled by a heightened sensorybaseline excitability. This results in a state of biased perception during which a person is more likely to see a stimulus, whether or not it is actually present.Spontane Fluktuationen der Hirnaktivität erklären, weshalb ein schwacher sensorischer Reiz manchmal wahrgenommen wird und manchmal nicht. Die vorherrschende Ansicht ist, dass gesteigerte neuronale Erregbarkeit/Excitability höhere Wahrnehmungsschärfe reflektiert. Gesteigerte neuronale Erregbarkeit wird durch reduzierte spontane Oszillationen im Alpha- Frequenzbereich (8-12 Hz) gemessen. In dieser Dissertation werden oben genannte Annahmen in Frage gestellt, indem ich zwei EEG Experimente und eine systematische Literaturübersicht präsentiere, die zeigen, dass reduzierte spontane Oszillationen die Wahrnehmungstendenz beeinflussen, aber nicht Wahrnehmungsschärfe verbessern. Im ersten EEG Experiment wurde der Einfluss spontaner neuronaler Oszillationen in einer ja/nein Detektionsaufgabe analysiert, in der der Reiz in einigen Durchläufen anwesend und in anderen abwesend war. Wenn Probanden zwischen Stimulusanwesenheit und -Abwesenheit entscheiden müssen, lassen verringerte Alphaoszillationen diese Probanden mit größerer Wahrscheinlichkeit einen Stimulus berichten, unabhängig davon ob tatsächlich einer präsentiert wurde oder nicht. In der Signalentdeckungstheorie ist dieses Antwortverhalten mit einem liberaleren Antwortkriterium gleichzustellen und nicht mit einer verbesserte Wahrnehmungsschärfe. Im zweiten EEG Experiment wurde der Einfluss spontaner neuronaler Oszillationen auf visuelle Detektion und Diskrimination untersucht. Wie von der Signalentdeckungstheorie vorhergesagt, zeigten die Ergebnisse auch hier, dass reduzierte Alpha-oszillationen die Anzahl der Treffer in der Detektionsaufgabe erhöhen, jedoch keinen Effekt auf den Anteil korrekter Antworten in der Diskriminationsaufgabe haben. Zusätzlich zu den EEG Experimenten wurde eine systematische Literaturübersicht erstellt, die den Einfluss spontaner Alpha-oszillationen auf visuelle Leistung untersucht. Die Studien wurden kategorisiert auf Basis davon, ob die behaviorale Methodik abhängig (z.B. Anzahl Treffer und falscher Alarme) oder unabhängig (z.B. Detektionssensitivität oder Anteil korrekter Diskriminationsantworten) vom Antwortkriterium war. Die meisten Studien, die Methoden verwendeten die vom Antwortkriterium abhängig waren, fanden einen Effekt von spontanen Alphaoszillationen auf Wahrnehmung, so wie auch unsere oben genannten EEG Experimente. Im Gegensatz dazu fanden die meisten Studien keinen Effekt von spontanen Alpha-oszillationen auf Wahrnehmung, die Methoden verwendeten die unabhängig vom Antwortkriterium war. Daher bestätigen diese Studien den Null- Effekt auf Detektionssensitivität im ersten EEG Experiment und auf Diskriminationsgenauigkeit im zweiten EEG Experiment. Im Gegensatz zu bisherigen Interpretationen legen unsere Resultate nahe, dass die kurzzeitige Steigerung der neuronalen Erregbarkeit, gemessen in reduzierten Alphaoszillationen, mit einer Steigerung der sensorischen Baseline- Erregbarkeit einhergeht. Die Folge erhöhter sensorischer Erregbarkeit ist eine Veränderung der Wahrnehmungstendenz, so dass wir einen Reiz mit größerer Wahrscheinlichkeit wahrnehmen, unabhängig davon ob tatsächlich ein Reiz anwesend ist oder nicht

Raw - Session 1

first session of the experimen

Raw - Session 2

second session of the experimen

Spontaneous Neural Oscillations Bias Perception by Modulating Baseline Excitability

International audienceThe 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

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