The brain as a generative model: information-theoretic surprise in learning and action

Our environment is rich with statistical regularities, such as a sudden cold gust of wind indicating a potential change in weather. A combination of theoretical work and empirical evidence suggests that humans embed this information in an internal representation of the world. This generative model is used to perform probabilistic inference, which may be approximated through surprise minimization. This process rests on current beliefs enabling predictions, with expectation violation amounting to surprise. Through repeated interaction with the world, beliefs become more accurate and grow more certain over time. Perception and learning may be accounted for by minimizing surprise of current observations, while action is proposed to minimize expected surprise of future events. This framework thus shows promise as a common formulation for different brain functions. The work presented here adopts information-theoretic quantities of surprise to investigate both perceptual learning and action. We recorded electroencephalography (EEG) of participants in a somatosensory roving-stimulus paradigm and performed trial-by-trial modeling of cortical dynamics. Bayesian model selection suggests early processing in somatosensory cortices to encode confidence-corrected surprise and subsequently Bayesian surprise. This suggests the somatosensory system to signal surprise of observations and update a probabilistic model learning transition probabilities. We also extended this framework to include audition and vision in a multi-modal roving-stimulus study. Next, we studied action by investigating a sensitivity to expected Bayesian surprise. Interestingly, this quantity is also known as information gain and arises as an incentive to reduce uncertainty in the active inference framework, which can correspond to surprise minimization. In comparing active inference to a classical reinforcement learning model on the two-step decision-making task, we provided initial evidence for active inference to better account for human model-based behaviour. This appeared to relate to participants’ sensitivity to expected Bayesian surprise and contributed to explaining exploration behaviour not accounted for by the reinforcement learning model. Overall, our findings provide evidence for information-theoretic surprise as a model for perceptual learning signals while also guiding human action.Unsere Umwelt ist reich an statistischen Regelmäßigkeiten, wie z. B. ein plötzlicher kalter Windstoß, der einen möglichen Wetterumschwung ankündigt. Eine Kombination aus theoretischen Arbeiten und empirischen Erkenntnissen legt nahe, dass der Mensch diese Informationen in eine interne Darstellung der Welt einbettet. Dieses generative Modell wird verwendet, um probabilistische Inferenz durchzuführen, die durch Minimierung von Überraschungen angenähert werden kann. Der Prozess beruht auf aktuellen Annahmen, die Vorhersagen ermöglichen, wobei eine Verletzung der Erwartungen einer Überraschung gleichkommt. Durch wiederholte Interaktion mit der Welt nehmen die Annahmen mit der Zeit an Genauigkeit und Gewissheit zu. Es wird angenommen, dass Wahrnehmung und Lernen durch die Minimierung von Überraschungen bei aktuellen Beobachtungen erklärt werden können, während Handlung erwartete Überraschungen für zukünftige Beobachtungen minimiert. Dieser Rahmen ist daher als gemeinsame Bezeichnung für verschiedene Gehirnfunktionen vielversprechend. In der hier vorgestellten Arbeit werden informationstheoretische Größen der Überraschung verwendet, um sowohl Wahrnehmungslernen als auch Handeln zu untersuchen. Wir haben die Elektroenzephalographie (EEG) von Teilnehmern in einem somatosensorischen Paradigma aufgezeichnet und eine trial-by-trial Modellierung der kortikalen Dynamik durchgeführt. Die Bayes'sche Modellauswahl deutet darauf hin, dass frühe Verarbeitung in den somatosensorischen Kortizes confidence corrected surprise und Bayesian surprise kodiert. Dies legt nahe, dass das somatosensorische System die Überraschung über Beobachtungen signalisiert und ein probabilistisches Modell aktualisiert, welches wiederum Wahrscheinlichkeiten in Bezug auf Übergänge zwischen Reizen lernt. In einer weiteren multimodalen Roving-Stimulus-Studie haben wir diesen Rahmen auch auf die auditorische und visuelle Modalität ausgeweitet. Als Nächstes untersuchten wir Handlungen, indem wir die Empfindlichkeit gegenüber der erwarteten Bayesian surprise betrachteten. Interessanterweise ist diese informationstheoretische Größe auch als Informationsgewinn bekannt und stellt, im Rahmen von active inference, einen Anreiz dar, Unsicherheit zu reduzieren. Dies wiederum kann einer Minimierung der Überraschung entsprechen. Durch den Vergleich von active inference mit einem klassischen Modell des Verstärkungslernens (reinforcement learning) bei der zweistufigen Entscheidungsaufgabe konnten wir erste Belege dafür liefern, dass active inference menschliches modellbasiertes Verhalten besser abbildet. Dies scheint mit der Sensibilität der Teilnehmer gegenüber der erwarteten Bayesian surprise zusammenzuhängen und trägt zur Erklärung des Explorationsverhaltens bei, das jedoch nicht vom reinforcement learning-Modell erklärt werden kann. Insgesamt liefern unsere Ergebnisse Hinweise für Formulierungen der informationstheoretischen Überraschung als Modell für Signale wahrnehmungsbasierten Lernens, die auch menschliches Handeln steuern

Neural surprise in somatosensory Bayesian learning

Tracking statistical regularities of the environment is important for shaping human behavior and perception. Evidence suggests that the brain learns environmental dependencies using Bayesian principles. However, much remains unknown about the employed algorithms, for somesthesis in particular. Here, we describe the cortical dynamics of the somatosensory learning system to investigate both the form of the generative model as well as its neural surprise signatures. Specifically, we recorded EEG data from 40 participants subjected to a somatosensory roving-stimulus paradigm and performed single-trial modeling across peri-stimulus time in both sensor and source space. Our Bayesian model selection procedure indicates that evoked potentials are best described by a non-hierarchical learning model that tracks transitions between observations using leaky integration. From around 70ms post-stimulus onset, secondary somatosensory cortices are found to represent confidence-corrected surprise as a measure of model inadequacy. Indications of Bayesian surprise encoding, reflecting model updating, are found in primary somatosensory cortex from around 140ms. This dissociation is compatible with the idea that early surprise signals may control subsequent model update rates. In sum, our findings support the hypothesis that early somatosensory processing reflects Bayesian perceptual learning and contribute to an understanding of its underlying mechanisms

Mismatch responses: Probing probabilistic inference in the brain

Sensory signals are governed by statistical regularities and carry valuable information about the unfolding of environmental events. The brain is thought to capitalize on the probabilistic nature of sequential inputs to infer on the underlying (hidden) dynamics driving sensory stimulation. Mis-match responses (MMRs) such as the mismatch negativity (MMN) and the P3 constitute prominent neuronal signatures which are increasingly interpreted as reflecting a mismatch between the current sensory input and the brain’s generative model of incoming stimuli. As such, MMRs might be viewed as signatures of probabilistic inference in the brain and their response dynamics can provide insights into the underlying computational principles. However, given the dominance of the auditory modality in MMR research, the specifics of brain responses to probabilistic sequences across sensory modalities and especially in the somatosensory domain are not well characterized. The work presented here investigates MMRs across the auditory, visual and somatosensory modality by means of electroencephalography (EEG) and functional magnetic resonance imaging (fMRI). We designed probabilistic stimulus sequences to elicit and characterize MMRs and employed computational modeling of response dynamics to inspect different aspects of the brain’s generative model of the sensory environment. In the first study, we used a volatile roving stimulus paradigm to elicit somatosensory MMRs and performed single-trial modeling of EEG signals in sensor and source space. Model comparison suggested that responses reflect Bayesian inference based on the estimation of transition probability and limited information integration of the recent past in order to adapt to a changing environment. The results indicated that somatosensory MMRs reflect an initial mismatch between sensory input and model beliefs represented by confidence-corrected surprise (CS) followed by model adjustment dynamics represented by Bayesian surprise (BS). For the second and third study we designed a tri-modal roving stimulus paradigm to delineate modality specific and modality general features of mismatch processing. Computational modeling of EEG signals in study 2 suggested that single-trial dynamics reflect Bayesian inference based on estimation of uni-modal transition probabilities as well as cross-modal conditional dependencies. While early mismatch processing around the MMN tended to reflect CS, later MMRs around the P3 rather reflect BS, in correspondence to the somatosensory study. Finally, the fMRI results of study 3 showed that MMRs are generated by an interaction of modality specific regions in higher order sensory cortices and a modality general fronto-parietal network. Inferior parietal regions in particular were sensitive to expectation violations with respect to the cross-modal contingencies in the stimulus sequences. Overall, our results indicate that MMRs across the senses reflect processes of probabilistic inference in a complex and inherently multi-modal environment.Sensorische Signale sind durch statistische Regularitäten bestimmt und beinhalten wertvolle Informationen über die Entwicklung von Umweltereignissen. Es wird angenommen, dass das Gehirn die Wahrscheinlichkeitseigenschaften sequenzieller Reize nutzt um auf die zugrundeliegenden (verborgenen) Dynamiken zu schließen, welche sensorische Stimulation verursachen. Diskrepanz-Reaktionen ("Mismatch responses"; MMRs) wie die "mismatch negativity" (MMN) und die P3 sind bekannte neuronale Signaturen die vermehrt als Signale einer Diskrepanz zwischen der momentanen sensorischen Einspeisung und dem generativen Modell, welches das Gehirn von den eingehenden Reizen erstellt angesehen werden. Als solche können MMRs als Signaturen von wahrscheinlichkeitsbasierter Inferenz im Gehirn betrachtet werden und ihre Reaktionsdynamiken können Einblicke in die zugrundeliegenden komputationalen Prinzipien geben. Angesichts der Dominanz der auditorischen Modalität in der MMR-Forschung, sind allerdings die spezifischen Eigenschaften von Hirn-Reaktionen auf Wahrscheinlichkeitssequenzen über sensorische Modalitäten hinweg und vor allem in der somatosensorischen Modalität nicht gut charakterisiert. Die hier vorgestellte Arbeit untersucht MMRs über die auditorische, visuelle und somatosensorische Modalität hinweg anhand von Elektroenzephalographie (EEG) und funktioneller Magnetresonanztomographie (fMRT). Wir gestalteten wahrscheinlichkeitsbasierte Reizsequenzen, um MMRs auszulösen und zu charakterisieren und verwendeten komputationale Modellierung der Reaktionsdynamiken, um verschiedene Aspekte des generativen Modells des Gehirns von der sensorischen Umwelt zu untersuchen. In der ersten Studie verwendeten wir ein volatiles "Roving-Stimulus"-Paradigma, um somatosensorische MMRs auszulösen und modellierten die Einzel-Proben der EEG-Signale im sensorischen und Quell-Raum. Modellvergleiche legten nahe, dass die Reaktionen Bayes’sche Inferenz abbilden, basierend auf der Schätzung von Transitionswahrscheinlichkeiten und limitierter Integration von Information der jüngsten Vergangenheit, welche eine Anpassung an Umweltänderungen ermöglicht. Die Ergebnisse legen nahe, dass somatosen-sorische MMRs eine initiale Diskrepanz zwischen sensorischer Einspeisung und Modellüberzeugung reflektieren welche durch "confidence-corrected surprise" (CS) repräsentiert ist, gefolgt von Modelanpassungsdynamiken repräsentiert von "Bayesian surprise" (BS). Für die zweite und dritte Studie haben wir ein Tri-Modales "Roving-Stimulus"-Paradigma gestaltet, um modalitätsspezifische und modalitätsübergreifende Eigenschaften von Diskrepanzprozessierung zu umreißen. Komputationale Modellierung von EEG-Signalen in Studie 2 legte nahe, dass Einzel-Proben Dynamiken Bayes’sche Inferenz abbilden, basierend auf der Schätzung von unimodalen Transitionswahrscheinlichkeiten sowie modalitätsübergreifenden bedingten Abhängigkeiten. Während frühe Diskrepanzprozessierung um die MMN dazu tendierten CS zu reflektieren, so reflektierten spätere MMRs um die P3 eher BS, in Übereinstimmung mit der somatosensorischen Studie. Abschließend zeigten die fMRT-Ergebnisse der Studie 3 dass MMRs durch eine Interaktion von modalitätsspezifischen Regionen in sensorischen Kortizes höherer Ordnung mit einem modalitätsübergreifenden fronto-parietalen Netzwerk generiert werden. Inferior parietale Regionen im Speziellen waren sensitiv gegenüber Erwartungsverstoß in Bezug auf die modalitätsübergreifenden Wahrscheinlichkeiten in den Reizsequenzen. Insgesamt weisen unsere Ergebnisse darauf hin, dass MMRs über die Sinne hinweg Prozesse von wahrscheinlichkeitsbasierter Inferenz in einer komplexen und inhärent multi-modalen Umwelt darstellen

Physical but not virtual presence of others potentiates implicit and explicit learning

E-learning activities are becoming more and more common. Whilst it is well known that the physical presence of others motivates individuals to engage in perceptual and learning tasks, systematic investigations comparing the effects of physical and virtual co-presence of others on knowledge acquisition are still scarce. Here we investigate the effects of physical and virtual co-presence of others on explicit and implicit learning. In Experiment 1 (discovery sample), retrieval accuracy in a spatial memory task and EEG indexes (mismatch negativity-MMN) of implicit perceptual learning were recorded when participants were alone or in presence of another individual. In Experiment 2 (replicating sample), we added a “virtual” condition, where the same tasks were performed during a video-conference call. In both experiments, MMN was demonstrated to encode for perceptual learning as revealed by the significant correlation with Bayesian Surprise (a consolidated information-theoretic index of Bayesian learning). Furthermore, In Experiments 1 and 2 physical co-presence systematically ameliorated memorization performances and increased MMN indexes related to implicit learning. These positive effects were absent in the virtual condition, thus suggesting that only physical, but not virtual co-presence is effective in potentiating learning dynamics

EEG mismatch responses in a multimodal roving stimulus paradigm provide evidence for probabilistic inference across audition, somatosensation, and vision

The human brain is constantly subjected to a multimodal stream of probabilistic sensory inputs. Electroencephalography (EEG) signatures, such as the mismatch negativity (MMN) and the P3, can give valuable insight into neuronal probabilistic inference. Although reported for different modalities, mismatch responses have largely been studied in isolation, with a strong focus on the auditory MMN. To investigate the extent to which early and late mismatch responses across modalities represent comparable signatures of uni- and cross-modal probabilistic inference in the hierarchically structured cortex, we recorded EEG from 32 participants undergoing a novel tri-modal roving stimulus paradigm. The employed sequences consisted of high and low intensity stimuli in the auditory, somatosensory and visual modalities and were governed by unimodal transition probabilities and cross-modal conditional dependencies. We found modality specific signatures of MMN (~100–200 ms) in all three modalities, which were source localized to the respective sensory cortices and shared right lateralized prefrontal sources. Additionally, we identified a cross-modal signature of mismatch processing in the P3a time range (~300–350 ms), for which a common network with frontal dominance was found. Across modalities, the mismatch responses showed highly comparable parametric effects of stimulus train length, which were driven by standard and deviant response modulations in opposite directions. Strikingly, P3a responses across modalities were increased for mispredicted stimuli with low cross-modal conditional probability, suggesting sensitivity to multimodal (global) predictive sequence properties. Finally, model comparisons indicated that the observed single trial dynamics were best captured by Bayesian learning models tracking unimodal stimulus transitions as well as cross-modal conditional dependencies

Preferred music listening is associated with perceptual learning enhancement at the expense of self-focused attention

Can preferred music listening improve following attentional and learning performances? Here we suggest that this may be the case. In Experiment 1, following preferred and non-preferred musical-piece listening, we recorded electrophysiological responses to an auditory roving-paradigm. We computed the mismatch negativity (MMN – the difference between responses to novel and repeated stimulation), as an index of perceptual learning, and we measured the correlation between trial-by-trial EEG responses and the fluctuations in Bayesian Surprise, as a quantification of the neural attunement with stimulus informational value. Furthermore, during music listening, we recorded oscillatory cortical activity. MMN and trial-by-trial correlation with Bayesian surprise were significantly larger after subjectively preferred versus non-preferred music, indicating the enhancement of perceptual learning. The analysis on oscillatory activity during music listening showed a selective alpha power increased in response to preferred music, an effect often related to cognitive enhancements. In Experiment 2, we explored whether this learning improvement was realized at the expense of self-focused attention. Therefore, after preferred versus non-preferred music listening, we collected Heart-Beat Detection (HBD) accuracy, as a measure of the attentional focus toward the self. HBD was significantly lowered following preferred music listening. Overall, our results suggest the presence of a specific neural mechanism that, in response to aesthetically pleasing stimuli, and through the modulation of alpha oscillatory activity, redirects neural resources away from the self and toward the environment. This attentional up-weighting of external stimuli might be fruitfully exploited in a wide area of human learning activities, including education, neurorehabilitation and therapy. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.3758/s13423-022-02127-8

The role of prediction in social neuroscience

Research has shown that the brain is constantly making predictions about future events. Theories of prediction in perception, action and learning suggest that the brain serves to reduce the discrepancies between expectation and actual experience, i.e., by reducing the prediction error. Forward models of action and perception propose the generation of a predictive internal representation of the expected sensory outcome, which is matched to the actual sensory feedback. Shared neural representations have been found when experiencing one's own and observing other's actions, rewards, errors, and emotions such as fear and pain. These general principles of the “predictive brain” are well established and have already begun to be applied to social aspects of cognition. The application and relevance of these predictive principles to social cognition are discussed in this article. Evidence is presented to argue that simple non-social cognitive processes can be extended to explain complex cognitive processes required for social interaction, with common neural activity seen for both social and non-social cognitions. A number of studies are included which demonstrate that bottom-up sensory input and top-down expectancies can be modulated by social information. The concept of competing social forward models and a partially distinct category of social prediction errors are introduced. The evolutionary implications of a “social predictive brain” are also mentioned, along with the implications on psychopathology. The review presents a number of testable hypotheses and novel comparisons that aim to stimulate further discussion and integration between currently disparate fields of research, with regard to computational models, behavioral and neurophysiological data. This promotes a relatively new platform for inquiry in social neuroscience with implications in social learning, theory of mind, empathy, the evolution of the social brain, and potential strategies for treating social cognitive deficits

Expectation violation and attention to pain jointly modulate neural gain in somatosensory cortex

The neural processing and experience of pain are influenced by both expectations and attention. For example, the amplitude of event-related pain responses is enhanced by both novel and unexpected pain, and by moving the focus of attention towards a painful stimulus. Under predictive coding, this congruence can be explained by appeal to a precision-weighting mechanism, which mediates bottom-up and top-down attentional processes by modulating the influence of feedforward and feedback signals throughout the cortical hierarchy. The influence of expectation and attention on pain processing can be mapped onto changes in effective connectivity between or within specific neuronal populations, using a canonical microcircuit (CMC) model of hierarchical processing. We thus implemented a CMC within dynamic causal modelling for magnetoencephalography in human subjects, to investigate how expectation violation and attention to pain modulate intrinsic (within-source) and extrinsic (between-source) connectivity in the somatosensory hierarchy. This enabled us to establish whether both expectancy and attentional processes are mediated by a similar precision-encoding mechanism within a network of somatosensory, frontal and parietal sources. We found that both unexpected and attended pain modulated the gain of superficial pyramidal cells in primary and secondary somatosensory cortex. This modulation occurred in the context of increased lateralized recurrent connectivity between somatosensory and fronto-parietal sources, driven by unexpected painful occurrences. Finally, the strength of effective connectivity parameters in S1, S2 and IFG predicted individual differences in subjective pain modulation ratings. Our findings suggest that neuromodulatory gain control in the somatosensory hierarchy underlies the influence of both expectation violation and attention on cortical processing and pain perception