Forms of prediction in the nervous system.

The idea that predictions shape how we perceive and comprehend the world has become increasingly influential in the field of systems neuroscience. It also forms an important framework for understanding neuropsychiatric disorders, which are proposed to be the result of disturbances in the mechanisms through which prior information influences perception and belief, leading to the production of suboptimal models of the world. There is a widespread tendency to conceptualize the influence of predictions exclusively in terms of 'top-down' processes, whereby predictions generated in higher-level areas exert their influence on lower-level areas within an information processing hierarchy. However, this excludes from consideration the predictive information embedded in the 'bottom-up' stream of information processing. We describe evidence for the importance of this distinction and argue that it is critical for the development of the predictive processing framework and, ultimately, for an understanding of the perturbations that drive the emergence of neuropsychiatric symptoms and experiences.

Publisher Correction: Forms of prediction in the nervous system.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

White matter microstructure in face and body networks predicts facial expression and body posture perception across development.

Facial expression and body posture recognition have protracted developmental trajectories. Interactions between face and body perception, such as the influence of body posture on facial expression perception, also change with development. While the brain regions underpinning face and body processing are well-defined, little is known about how white-matter tracts linking these regions relate to perceptual development. Here, we obtained complementary diffusion magnetic resonance imaging (MRI) measures (fractional anisotropy [FA], spherical mean Sµ ), and a quantitative MRI myelin-proxy measure (R1), within white-matter tracts of face- and body-selective networks in children and adolescents and related these to perceptual development. In tracts linking occipital and fusiform face areas, facial expression perception was predicted by age-related maturation, as measured by Sµ and R1, as well as age-independent individual differences in microstructure, captured by FA and R1. Tract microstructure measures linking posterior superior temporal sulcus body region with anterior temporal lobe (ATL) were related to the influence of body on facial expression perception, supporting ATL as a site of face and body network convergence. Overall, our results highlight age-dependent and age-independent constraints that white-matter microstructure poses on perceptual abilities during development and the importance of complementary microstructural measures in linking brain structure and behaviour.

Semantic object-scene inconsistencies affect eye movements, but not in the way predicted by contextualized meaning maps.

Semantic information is important in eye movement control. An important semantic influence on gaze guidance relates to object-scene relationships: objects that are semantically inconsistent with the scene attract more fixations than consistent objects. One interpretation of this effect is that fixations are driven toward inconsistent objects because they are semantically more informative. We tested this explanation using contextualized meaning maps, a method that is based on crowd-sourced ratings to quantify the spatial distribution of context-sensitive "meaning" in images. In Experiment 1, we compared gaze data and contextualized meaning maps for images, in which objects-scene consistency was manipulated. Observers fixated more on inconsistent versus consistent objects. However, contextualized meaning maps did not assign higher meaning to image regions that contained semantic inconsistencies. In Experiment 2, a large number of raters evaluated image-regions, which were deliberately selected for their content and expected meaningfulness. The results suggest that the same scene locations were experienced as slightly less meaningful when they contained inconsistent compared to consistent objects. In summary, we demonstrated that - in the context of our rating task - semantically inconsistent objects are experienced as less meaningful than their consistent counterparts and that contextualized meaning maps do not capture prototypical influences of image meaning on gaze guidance.

Shift toward prior knowledge confers a perceptual advantage in early psychosis and psychosis-prone healthy individuals.

Many neuropsychiatric illnesses are associated with psychosis, i.e., hallucinations (perceptions in the absence of causative stimuli) and delusions (irrational, often bizarre beliefs). Current models of brain function view perception as a combination of two distinct sources of information: bottom-up sensory input and top-down influences from prior knowledge. This framework may explain hallucinations and delusions. Here, we characterized the balance between visual bottom-up and top-down processing in people with early psychosis (study 1) and in psychosis-prone, healthy individuals (study 2) to elucidate the mechanisms that might contribute to the emergence of psychotic experiences. Through a specialized mental-health service, we identified unmedicated individuals who experience early psychotic symptoms but fall below the threshold for a categorical diagnosis. We observed that, in early psychosis, there was a shift in information processing favoring prior knowledge over incoming sensory evidence. In the complementary study, we capitalized on subtle variations in perception and belief in the general population that exhibit graded similarity with psychotic experiences (schizotypy). We observed that the degree of psychosis proneness in healthy individuals, and, specifically, the presence of subtle perceptual alterations, is also associated with stronger reliance on prior knowledge. Although, in the current experimental studies, this shift conferred a performance benefit, under most natural viewing situations, it may provoke anomalous perceptual experiences. Overall, we show that early psychosis and psychosis proneness both entail a basic shift in visual information processing, favoring prior knowledge over incoming sensory evidence. The studies provide complementary insights to a mechanism by which psychotic symptoms may emerge.

The promises and pitfalls of applying computational models to neurological and psychiatric disorders.

Computational models have become an integral part of basic neuroscience and have facilitated some of the major advances in the field. More recently, such models have also been applied to the understanding of disruptions in brain function. In this review, using examples and a simple analogy, we discuss the potential for computational models to inform our understanding of brain function and dysfunction. We argue that they may provide, in unprecedented detail, an understanding of the neurobiological and mental basis of brain disorders and that such insights will be key to progress in diagnosis and treatment. However, there are also potential problems attending this approach. We highlight these and identify simple principles that should always govern the use of computational models in clinical neuroscience, noting especially the importance of a clear specification of a model's purpose and of the mapping between mathematical concepts and reality.

How to (and how not to) think about top-down influences on visual perception.

The question of whether cognition can influence perception has a long history in neuroscience and philosophy. Here, we outline a novel approach to this issue, arguing that it should be viewed within the framework of top-down information-processing. This approach leads to a reversal of the standard explanatory order of the cognitive penetration debate: we suggest studying top-down processing at various levels without preconceptions of perception or cognition. Once a clear picture has emerged about which processes have influences on those at lower levels, we can re-address the extent to which they should be considered perceptual or cognitive. Using top-down processing within the visual system as a model for higher-level influences, we argue that the current evidence indicates clear constraints on top-down influences at all stages of information processing; it does, however, not support the notion of a boundary between specific types of information-processing as proposed by the cognitive impenetrability hypothesis.

Evidence of absence: no relationship between behaviourally measured prediction error response and schizotypy.

INTRODUCTION: The predictive processing framework has attracted much interest in the field of schizophrenia research in recent years, with an increasing number of studies also carried out in healthy individuals with nonclinical psychosis-like experiences. The current research adopted a continuum approach to psychosis and aimed to investigate different types of prediction error responses in relation to psychometrically defined schizotypy. METHODS: One hundred and two healthy volunteers underwent a battery of behavioural tasks including (a) a force-matching task, (b) a Kamin blocking task, and (c) a reversal learning task together with three questionnaires measuring domains of schizotypy from different approaches. RESULTS: Neither frequentist nor Bayesian statistical methods supported the notion that alterations in prediction error responses were related to schizotypal traits in any of the three tasks. CONCLUSIONS: These null results suggest that deficits in predictive processing associated with clinical states of psychosis are not always present in healthy individuals with schizotypal traits.

A new predictive coding model for a more comprehensive account of delusions.

Attempts to understand psychosis-the experience of profoundly altered perceptions and beliefs-raise questions about how the brain models the world. Standard predictive coding approaches suggest that it does so by minimising mismatches between incoming sensory evidence and predictions. By adjusting predictions, we converge iteratively on a best guess of the nature of the reality. Recent arguments have shown that a modified version of this framework-hybrid predictive coding-provides a better model of how healthy agents make inferences about external reality. We suggest that this more comprehensive model gives us a richer understanding of psychosis compared with standard predictive coding accounts. In this Personal View, we briefly describe the hybrid predictive coding model and show how it offers a more comprehensive account of the phenomenology of delusions, thereby providing a potentially powerful new framework for computational psychiatric approaches to psychosis. We also make suggestions for future work that could be important in formalising this novel perspective.

Knowledge-driven perceptual organization reshapes information sampling via eye movements.

Humans constantly move their eyes to explore the environment. However, how image-computable features and object representations contribute to eye-movement control is an ongoing debate. Recent developments in object perception indicate a complex relationship between features and object representations, where image-independent object knowledge generates objecthood by reconfiguring how feature space is carved up. Here, we adopt this emerging perspective, asking whether object-oriented eye movements result from gaze being guided by image-computable features, or by the fact that these features are bound into an object representation. We recorded eye movements in response to stimuli that initially appear as meaningless patches but are experienced as coherent objects once relevant object knowledge has been acquired. We demonstrate that fixations on identical images are more object-centered, less dispersed, and more consistent across observers once these images are organized into objects. Gaze guidance also showed a shift from exploratory information sampling to exploitation of object-related image areas. These effects were evident from the first fixations onwards. Importantly, eye movements were not fully determined by knowledge-dependent object representations but were best explained by the integration of these representations with image-computable features. Overall, the results show how information sampling via eye movements is guided by a dynamic interaction between image-computable features and knowledge-driven perceptual organization. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Characterising modulatory effects of high-intensity high frequency transcranial random noise stimulation using the perceptual template model.

Neural noise is an inherent property of all nervous systems. However, our understanding of the mechanisms by which noise influences perception is still limited. To elucidate this relationship, we require techniques that can safely modulate noise in humans. Transcranial random noise stimulation (tRNS) has been proposed to induce noise into cortical processing areas according to the principles of stochastic resonance (SR). Specifically, it has been demonstrated that small to moderate intensities of noise improve performance. To date, however, high intensity tRNS effects on neural noise levels have not been directly quantified, nor have the detrimental effects proposed by SR been demonstrated in early visual function. Here, we applied 3 mA high-frequency tRNS to primary visual cortex during an orientation-discrimination task across increasing external noise levels and used the Perceptual Template Model to quantify the mechanisms by which noise changes perceptual performance in healthy observers. Results show that, at a group level, high-intensity tRNS worsened perceptual performance. Our computational analysis reveals that this change in performance was underpinned by an increased amount of additive noise and a reduced ability to filter external noise compared to sham stimulation. Interestingly, while most observers experienced detrimental effects, a subset of participants demonstrated improved performance. Preliminary evidence suggests that differences in baseline internal noise levels might account for these individual differences. Together, these results refine our understanding of the mechanisms underlying the influence of neural noise on perception and have important implications for the application of tRNS as a research tool.

A Computational Analysis of Abnormal Belief Updating Processes and Their Association With Psychotic Experiences and Childhood Trauma in a UK Birth Cohort.

BACKGROUND: Psychotic experiences emerge from abnormalities in perception and belief formation and occur more commonly in those experiencing childhood trauma. However, which precise aspects of belief formation are atypical in psychosis is not well understood. We used a computational modeling approach to characterize belief updating in young adults in the general population, examine their relationship with psychotic outcomes and trauma, and determine the extent to which they mediate the trauma-psychosis relationship. METHODS: We used data from 3360 individuals from the Avon Longitudinal Study of Parents and Children birth cohort who completed assessments for psychotic outcomes, depression, anxiety, and two belief updating tasks at age 24 and had data available on traumatic events assessed from birth to late adolescence. Unadjusted and adjusted regression and counterfactual mediation methods were used for the analyses. RESULTS: Basic behavioral measures of belief updating (draws-to-decision and disconfirmatory updating) were not associated with psychotic experiences. However, computational modeling revealed an association between increased decision noise with both psychotic experiences and trauma exposure, although <3% of the trauma-psychotic experience association was mediated by decision noise. Belief updating measures were also associated with intelligence and sociodemographic characteristics, confounding most of the associations with psychotic experiences. There was little evidence that belief updating parameters were differentially associated with delusions compared with hallucinations or that they were differentially associated with psychotic outcomes compared with depression or anxiety. CONCLUSIONS: These findings challenge the hypothesis that atypical belief updating mechanisms (as indexed by the computational models and behavioral measures we used) underlie the development of psychotic phenomena.

There is no evidence that meaning maps capture semantic information relevant to gaze guidance: Reply to Henderson, Hayes, Peacock, and Rehrig (2021).

The concerns raised by Henderson, Hayes, Peacock, and Rehrig (2021) are based on misconceptions of our work. We show that Meaning Maps (MMs) do not predict gaze guidance better than a state-of-the-art saliency model that is based on semantically-neutral, high-level features. We argue that there is therefore no evidence to date that MMs index anything beyond these features. Furthermore, we show that although alterations in meaning cause changes in gaze guidance, MMs fail to capture these alterations. We agree that semantic information is important in the guidance of eye-movements, but the contribution of MMs for understanding its role remains elusive.

Low-level, prediction-based sensory and motor processes are unimpaired in Autism.

A new promising account of human brain function suggests that sensory cortices try to optimise information processing via predictions that are based on prior experiences. The brain is thus likened to a probabilistic prediction machine. There has been a growing - though inconsistent - literature to suggest that features of autism spectrum conditions (ASCs) are associated with a deficit in modelling the world through such prediction-based inference. However empirical evidence for differences in low-level sensorimotor predictions in autism is still lacking. One approach to examining predictive processing in the sensorimotor domain is in the context of self-generated (predictable) as opposed to externally-generated (less predictable) effects. We employed two complementary tasks - forcematching and intentional binding - which examine self-versus externally-generated action effects in terms of sensory attenuation and intentional binding respectively in adults with and without autism. The results show that autism was associated with normal levels of sensory attenuation of internally-generated force and with unaltered temporal attraction of voluntary actions and their outcomes. Thus, our results do not support a general deficit in predictive processing in autism.

Meaning maps and saliency models based on deep convolutional neural networks are insensitive to image meaning when predicting human fixations.

Eye movements are vital for human vision, and it is therefore important to understand how observers decide where to look. Meaning maps (MMs), a technique to capture the distribution of semantic information across an image, have recently been proposed to support the hypothesis that meaning rather than image features guides human gaze. MMs have the potential to be an important tool far beyond eye-movements research. Here, we examine central assumptions underlying MMs. First, we compared the performance of MMs in predicting fixations to saliency models, showing that DeepGaze II - a deep neural network trained to predict fixations based on high-level features rather than meaning - outperforms MMs. Second, we show that whereas human observers respond to changes in meaning induced by manipulating object-context relationships, MMs and DeepGaze II do not. Together, these findings challenge central assumptions underlying the use of MMs to measure the distribution of meaning in images.

Childhood trauma and cognitive biases associated with psychosis: A systematic review and meta-analysis.

Childhood trauma is associated with an increased risk of psychosis, but the mechanisms that mediate this relationship are unknown. Exposure to trauma has been hypothesised to lead to cognitive biases that might have causal effects on psychotic symptoms. The literature on whether childhood trauma is associated with psychosis-related cognitive biases has not been comprehensively reviewed. A systematic review and meta-analysis or narrative synthesis of studies examining the association between childhood trauma and the following biases: external locus of control (LOC), external attribution, probabilistic reasoning, source monitoring, top-down processing, and bias against disconfirmatory evidence. Studies were assessed for quality, and sources of heterogeneity were explored. We included 25 studies from 3,465 studies identified. Individuals exposed to childhood trauma reported a more external LOC (14 studies: SMD Median = 0.40, Interquartile range 0.07 to 0.52), consistent with a narrative synthesis of 11 other studies of LOC. There was substantial heterogeneity in the meta-analysis (I2 = 93%) not explained by study characteristics examined. Narrative syntheses for other biases showed weaker, or no evidence of association with trauma. The quality of included studies was generally low. Our review provides some evidence of an association between childhood trauma and a more external LOC, but not with the other biases examined. The low quality and paucity of studies for most of the cognitive biases examined highlights the need for more rigorous studies to determine which biases occur after trauma, and whether they mediate an effect of childhood trauma on psychosis.

Facial expressions modulate the ontogenetic trajectory of gaze-following among monkeys.

Gaze-following, the tendency to direct one's attention to locations looked at by others, is a crucial aspect of social cognition in human and nonhuman primates. Whereas the development of gaze-following has been intensely studied in human infants, its early ontogeny in nonhuman primates has received little attention. Combining longitudinal and cross-sectional observational data from Barbary macaques at 'La Forêt des Singes', we show here that gaze-following among conspecifics develops within the first year of life with a rapid increase between 5 and 6 months, reaching adult levels at 1 year. Sex, rank, and relatedness of the animal whose gaze the subject followed did not affect gaze-following rates. Interestingly, however, the behavior was enhanced in all age classes if a gaze-cue was accompanied by a facial expression. Furthermore, the effect of facial expressions had a modulatory influence on the ontogenetic trajectory of gaze-following, suggesting that it is of functional significance in the development of the behavior. Follow-up analyses revealed that one specific facial expression that is given in response to social interactions between third parties was particularly efficient in eliciting gaze-following responses, indicating the importance of cues that are able to guide the acquisition of social information. Taken together, these results suggest that the development and the operation of gaze-following are tuned to the social and physical characteristics of a species' environment.

Inability to improve performance with control shows limited access to inner states.

Any repeatedly performed action is characterized by endogenous variability, affecting both speed and accuracy-for a large part presumably caused by fluctuations in underlying brain and body states. The current research questions concerned (a) whether such states are accessible to us and (b) whether we can act upon this information to reduce variability. For example, when playing a game of darts, there is an implicit assumption that people can wait to throw until they are in the right perceptual-attentional state. If this is true, taking away the ability to self-pace the game should worsen performance. We first tested precisely this assumption asking participants to play darts in a self-paced and a fixed-paced condition. There was no benefit of self-pacing, showing that participants were unable to use such control to improve their performance and reduce their variability. Next, we replicated these findings in 2 computer-based tasks, in which participants performed a rapid action-selection and a visual detection task in 1 self-paced and 3 forced-paced conditions. Over 4 different empirical tests, we show that the self-paced condition did not lead to improved performance or reduced variability, nor to reduced temporal dependencies in the reaction time (RT) series. Overall, it seems that, if people have any access to their fluctuating performance-relevant inner states, this access is limited and not relevant for upcoming performance. (PsycINFO Database Record (c) 2020 APA, all rights reserved).

Orienting asymmetries and lateralized processing of sounds in humans.

BACKGROUND: Lateralized processing of speech is a well studied phenomenon in humans. Both anatomical and neurophysiological studies support the view that nonhuman primates and other animal species also reveal hemispheric differences in areas involved in sound processing. In recent years, an increasing number of studies on a range of taxa have employed an orienting paradigm to investigate lateralized acoustic processing. In this paradigm, sounds are played directly from behind and the direction of turn is recorded. This assay rests on the assumption that a hemispheric asymmetry in processing is coupled to an orienting bias towards the contralateral side. To examine this largely untested assumption, speech stimuli as well as artificial sounds were presented to 224 right-handed human subjects shopping in supermarkets in Germany and in the UK. To verify the lateralized processing of the speech stimuli, we additionally assessed the brain activation in response to presentation of the different stimuli using functional magnetic resonance imaging (fMRI). RESULTS: In the naturalistic behavioural experiments, there was no difference in orienting behaviour in relation to the stimulus material (speech, artificial sounds). Contrary to our predictions, subjects revealed a significant left bias, irrespective of the sound category. This left bias was slightly but not significantly stronger in German subjects. The fMRI experiments confirmed that the speech stimuli evoked a significant left lateralized activation in BA44 compared to the artificial sounds. CONCLUSION: These findings suggest that in adult humans, orienting biases are not necessarily coupled with lateralized processing of acoustic stimuli. Our results -- as well as the inconsistent orienting biases found in different animal species -- suggest that the orienting assay should be used with caution. Apparently, attention biases, experience, and experimental conditions may all affect head turning responses. Because of the complexity of the interaction of factors, the use of the orienting assay to determine lateralized processing of sound stimuli is discouraged.

A hierarchical model of social perception: Psychophysical evidence suggests late rather than early integration of visual information from facial expression and body posture.

Facial expressions are one of the most important sources of information about another's emotional states. More recently, other cues such as body posture have been shown to influence how facial expressions are perceived. It has been argued that this biasing effect is underpinned by an early integration of visual information from facial expression and body posture. Here, we replicate this biasing effect, but, using a psychophysical procedure, show that adaptation to facial expressions is unaffected by body context. The integration of face and body information therefore occurs downstream of the sites of adaptation, known to be localised in high-level visual areas of the temporal lobe. Contrary to previous research, our findings thus provide direct evidence for late integration of information from facial expression and body posture. They are consistent with a hierarchical model of social perception, in which social signals from different sources are initially processed independently and in parallel by specialised visual mechanisms. Integration of these different inputs in later stages of the visual system then supports the emergence of the integrated whole-person percept that is consciously experienced.