A predictive coding account of bistable perception - a model-based fMRI study

In bistable vision, subjective perception wavers between two interpretations of a constant ambiguous stimulus. This dissociation between conscious perception and sensory stimulation has motivated various empirical studies on the neural correlates of bistable perception, but the neurocomputational mechanism behind endogenous perceptual transitions has remained elusive. Here, we recurred to a generic Bayesian framework of predictive coding and devised a model that casts endogenous perceptual transitions as a consequence of prediction errors emerging from residual evidence for the suppressed percept. Data simulations revealed close similarities between the model’s predictions and key temporal characteristics of perceptual bistability, indicating that the model was able to reproduce bistable perception. Fitting the predictive coding model to behavioural data from an fMRI-experiment on bistable perception, we found a correlation across participants between the model parameter encoding perceptual stabilization and the behaviourally measured frequency of perceptual transitions, corroborating that the model successfully accounted for participants’ perception. Formal model comparison with established models of bistable perception based on mutual inhibition and adaptation, noise or a combination of adaptation and noise was used for the validation of the predictive coding model against the established models. Most importantly, model-based analyses of the fMRI data revealed that prediction error time-courses derived from the predictive coding model correlated with neural signal time-courses in bilateral inferior frontal gyri and anterior insulae. Voxel-wise model selection indicated a superiority of the predictive coding model over conventional analysis approaches in explaining neural activity in these frontal areas, suggesting that frontal cortex encodes prediction errors that mediate endogenous perceptual transitions in bistable perception. Taken together, our current work provides a theoretical framework that allows for the analysis of behavioural and neural data using a predictive coding perspective on bistable perception. In this, our approach posits a crucial role of prediction error signalling for the resolution of perceptual ambiguities

Die Entstehung eindeutiger bewusster Wahrnehmung aus doppeldeutigen sensorischen Informationen

The research presented in this habilitation treatise seeks to understand the construction of unambiguous conscious experiences from ambiguous sensory information. Our work builds on the idea that the brain applies predictive processes to resolve the ambiguity inherent in sensory information. We developed a predictive coding algorithm that models the interaction of internal predictions with prediction errors driven by ambiguous sensory information. We combined model-based fMRI and TMS-induced virtual lesions to demonstrate that the processing of sensory ambiguity is not limited to feature-selective regions in sensory corteces, but involves supra-modal brain regions of the frontoparietal network. Our work proposes a key role for the inferior frontal cortex in regulating the access of conflicting information into conscious experience. Finally, we show that the interaction of internal predictions with external sensory information correlates with the severity of hallucinatory experiences in patients diagnosed with paranoid schizophrenia. In sum, the research presented in this habilitation treatise explains how the brain transforms ambiguous sensory data into unambiguous conscious experiences and suggests how alterations in this process may lead to hallucinations. Our computational and lesion-based approach advances the scientific understanding at two of the most important frontiers in contemporary neuroscience: the biology of consciousness and neurocomputational theories of psychosis

Perzeptuelle Wechsel bei bistabiler Wahrnehmung werden durch den Frontoparietalen Kortex mediiert

In bistable perception, ambiguous stimuli elicit spontaneous (endogenous) transitions between two mutually exclusive percepts while sensory stimulation remains constant. Such endogenous perceptual transitions have been studied in comparison with stimulus-induced changes in perception generated in a so- called “replay” condition. In the replay condition, perceptual transitions are created by a disambiguated version of the stimulus and designed to be as similar as possible to their ambiguous counterparts with respect to quality and timing. In a number of studies using functional magnetic resonance imaging (fMRI), the statistical comparison between endogenous and stimulus-induced perceptual transitions has shown that significantly higher “Blood Oxygen Level Dependent” (BOLD) responses in right hemispheric frontal and parietal brain areas are associated with endogenous perceptual transitions. The functional role of this frontoparietal network has remained controversial, however. On the one hand, it has been argued that this enhanced activity might reflect causal influences of regions in frontal and parietal cortex on the processing in sensory brain areas and thus point to the importance of “top-down” processes for bistable perception. On the other hand, it has been proposed that differences in the BOLD signals measured might result from discrepancies in the perceptual quality of transitions between the two conditions. This “bottom–up” explanation focuses above all on possibly longer durations of perceptual transitions in the bistable as compared to the replay condition, being reflected by differences in frontoparietal activity. The goal of this experiment was to disentangle these two hypotheses in a fMRI experiment on 15 healthy human participants. Using a rotating Lissajous figure, we elicited endogenous and stimulus-induced changes in perception, whereby participants rated the perceived duration of these events. Furthermore, we used “Statistical Parametric Mapping” (SPM) to test the BOLD activity associated with perceptual transitions in the bistable condition against the replay condition. Finally, we applied “Dynamic Causal Modeling” (DCM) in order to determine the neural model that most readily explains the observed BOLD signal in terms of effective connectivity. We replicated previous findings of enhanced activity in frontoparietal brain regions for endogeneous perceptual transitions whilst controlling for potential confounds of differences in transition duration between the two conditions. Our DCM results indicated that enhanced activity for perceptual transitions during bistability is associated with a modulation of “top-down” connectivity from frontal to visual cortex. Taken together, these findings suggest that activity in frontoparietal brain areas is crucially involved in perceptual transitions during bistable perception in terms of “top–down” connectivity.Während bistabiler Wahrnehmung rufen ambige Stimuli bei konstanter sensorischer Stimulation spontane (endogene) Wechsel zwischen zwei distinkten Wahrnehmungsinhalten hervor. Eine Möglichkeit der Erforschung dieser perzeptuellen Ereignisse besteht darin, endogene Wahrnehmungswechsel mit Stimulus-induzierten Änderungen der Wahrnehmungsinhalte zu vergleichen, welche in einer sogenannten „Replay“ Bedingung erzeugt werden. Diese experimentelle Bedingung versucht, durch eine disambiguierte Version des Stimulus die perzeptuellen Eigenschaften von Wahrnehmungswechseln der bistabilen Bedingung in Qualität und zeitlicher Abfolge möglichst genau nachzubilden. Der statistische Vergleich zwischen den mit endogenen und Stimulus–induzierten Wahrnehmungswechseln assoziierten „Blood Oxygen Level Dependent“ (BOLD) Signalen der funktionellen Magnetresonanztomographie (fMRT) erbrachte in einer Reihe von Studien eine signifikant höhere Aktivität in rechtshemisphärisch lokalisierten frontalen und parietalen Gehirnarealen für endogene perzeptuelle Wechsel. Die funktionelle Bedeutung dieses frontoparietalen Netzwerks blieb bislang jedoch umstritten. Einerseits wird angenommen, die erhöhte Aktivität von Regionen im frontalen und parietalen Kortex spiegele deren kausale Beteiligung an der Verarbeitung des ambigen Stimulus in sensorischen Gehirnarealen wider und liefere damit einen Hinweis auf die Bedeutung von „top–down“ Prozessen für die bistabile Wahrnehmung. Andererseits wird argumentiert, eine solche frontoparietale Aktivität resultiere aus den unterschiedlichen perzeptuellen Eigenschaften der Wahrnehmungswechsel in beiden Bedingungen. Dieser „bottom–up“ Ansatz verwies insbesondere auf die im Vergleich zur „Replay“ Bedingung möglicherweise längere zeitliche Ausdehnung von Wahrnehmungswechseln in der bistabilen Bedingung, welche sich in einer erhöhten frontoparietalen Aktivität niederschlagen könne. Das Ziel der vorliegenden Untersuchung war es, diese beiden Hypothesen in einem fMRT Experiment an 15 gesunden Probanden voneinander abzugrenzen. Hierzu haben wir mit Hilfe einer rotierenden Lissajous–Figur spontane und Stimulus–induzierte Wahrnehmungswechsel erzeugt und die zeitliche Ausdehnung dieser Ereignisse von den Studienteilnehmern bewerten lassen. Des Weiteren haben wir die mit den Wahrnehmungswechseln assoziierten BOLD Signale in beiden Bedingungen unter Verwendung von „Statistical Parametric Mapping“ (SPM) gegeneinander getestet. Schließen haben wir mit Hilfe von „Dynamic Causal Modeling“ (DCM) dasjenige neuronale Modell identifiziert, welches den Zeitverlauf des BOLD Signales während unseres Experiments im Sinne effektiver Konnektivität am besten erklärt. Im Gegensatz zu früheren Studien konnten wir potentielle Störfaktoren im Sinne einer unterschiedlichen zeitlichen Ausdehnung der Wahrnehmungswechsel zwischen beiden Bedingungen ausschließen. Eine erhöhte frontoparietale Aktivität für endogene Wahrnehmungswechsel konnten wir hingegen bestätigen. Die Ergebnisse unserer DCM Analyse zeigten, dass die erhöhte BOLD Aktivität für bistabile Wahrnehmungswechsel mit einer Modulation der Konnektivität vom frontalen zum visuellen Kortex einhergeht. Zusammenfassend legen diese Befunde nahe, dass die Aktivität in frontoparietalen Gehirnarealen im Sinne einer „top–down“ Konnektivität entscheidend an perzeptuellen Wechseln der bistabilen Wahrnehmung beteiligt ist

Bistable perception alternates between internal and external modes of sensory processing

Perceptual history can exert pronounced effects on the contents of conscious experience: when confronted with completely ambiguous stimuli, perception does not waver at random between diverging stimulus interpretations but sticks with recent percepts for prolonged intervals. Here, we investigated the relevance of perceptual history in situations more similar to everyday experience, where sensory stimuli are usually not completely ambiguous. Using partially ambiguous visual stimuli, we found that the balance between past and present is not stable over time but slowly fluctuates between two opposing modes. For time periods of up to several minutes, perception was either largely determined by perceptual history or driven predominantly by disambiguating sensory evidence. Computational modeling suggested that the construction of unambiguous conscious experiences is modulated by slow fluctuations between internally and externally oriented modes of sensory processing

Perceptual stability of the Lissajous figure is modulated by the speed of illusory rotation (Weilnhammer et al. 2016)

This fileset contains the raw Matlab data files (*.mat) and the corresponding Matlab script (*.m) for the analysis. It also contains data (*.csv) which were submitted to the rm-ANOVA.<br

Perceptual Stability of the Lissajous Figure Is Modulated by the Speed of Illusory Rotation.

Lissajous figures represent ambiguous structure-from-motion stimuli rotating in depth and have proven to be a versatile tool to explore the cognitive and neural mechanisms underlying bistable perception. They are generated by the intersection of two sinusoids with perpendicular axes and increasing phase-shift whose frequency determines the speed of illusory 3D rotation. Recently, we found that Lissajous figures of higher shifting frequencies elicited longer perceptual phase durations and tentatively proposed a "representational momentum" account. In this study, our aim was twofold. First, we aimed to gather more behavioral evidence related to the perceptual dynamics of the Lissajous figure by simultaneously varying its shifting frequency and size. Using a conventional analysis, we investigated the effects of our experimental manipulations on transition probability (i.e., the probability that the current percept will change at the next critical stimulus configuration). Second, we sought to test the impact of our experimental factors on the occurrence of transitions in bistable perception by means of a Bayesian approach that can be used to directly quantify the impact of contextual cues on perceptual stability. We thereby estimated the implicit prediction of perceptual stability and how it is modulated by experimental manipulations

Correction: Psychotic Experiences and Overhasty Inferences Are Related to Maladaptive Learning.

[This corrects the article DOI: 10.1371/journal.pcbi.1005328.]

Lissajous figure and distribution of perceptual phase durations.

<p>(A) Lissajous are generated by the intersection of two sinusoids with perpendicular axes and increasing phase-shift whose frequency determines the speed of illusory 3D rotation. Following their introduction to experimental psychology, Lissajous figures were originally studied by means of twin-oscillators and analog cathode ray oscillographs in the 1940s and 1950s [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0160772#pone.0160772.ref006" target="_blank">6</a>]. (B) Perceptual phase duration across all participants, runs and conditions. Distributions with a sharp rise and a long tail are typical of bistable perception.</p