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.visual perception | psychosis | top-down processing | predictive coding | schizophrenia

IMPORTANCE Cross-sectional and longitudinal studies have consistently reported associations between childhood trauma and psychotic experiences and disorders. However, few studies have examined whether the age of exposure or specific trauma types are differently associated with the risk of developing psychotic experiences. OBJECTIVE To examine whether exposure to trauma, assessed at multiple age periods between 0 and 17 years of age, is associated with an increased risk of psychotic experiences by age 18 years and whether this association varies according to trauma type as well as age and frequency of exposure. DESIGN, SETTING, AND PARTICIPANTS This study used data from the Avon Longitudinal Study of Parents and Children, a large population-based birth cohort in the United Kingdom that recruited women who resided in the Avon Health Authority area and had an expected delivery date between April 1, 1991, and December 31, 1992. Data on psychotic experiences were included in the study, along with trauma variables derived from assessments completed by the parents or self-reported by the participants. The variables represent exposure to any trauma type between ages 0 and 17 years; any trauma type within a distinct age period: early childhood (0-4.9 years), middle childhood (5-10.9 years), or adolescence (11-17 years); specific trauma types between ages 0 and 17 years; and specific trauma types within early childhood, middle childhood, or adolescence. Data were analyzed from January 9, 2017, to November 30, 2017. MAIN OUTCOMES AND MEASURES Suspected or definite psychotic experiences were assessed using the psychosis-like symptoms semistructured interview at age 12 years and then at age 18 years. RESULTS The sample of 4433 participants included 2504 (56.5%) females, with a mean (SD) age of 17.8 (0.38) years. Exposure to any trauma up to age 17 years was associated with increased odds of psychotic experiences at age 18 years (adjusted odds ratio, 2.91; 95% CI, 2.15-3.93). All trauma types from age 0 to 17 years were associated with an increased odds of psychotic experiences. The population-attributable fraction for childhood and adolescent trauma on psychotic experiences at age 18 years was 45% (95% CI, 25%-60%). Effect sizes for most trauma types were greater for exposure that was more proximal to the outcome, although CIs overlapped with those for more distal trauma. Evidence supported dose-response associations for exposure to multiple trauma types and at multiple age periods. In an analysis aimed at minimizing reverse causality, adolescent trauma was also associated with past-year incident psychotic experiences at age 18 years. CONCLUSIONS AND RELEVANCE These findings are consistent with the thesis that trauma could have a causal association with psychotic experiences; if so, identification of modifiable mediators is required to inform prevention strategies.

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Gaze direction is an important social signal in both human and nonhuman primates, providing information about conspecifics' attention, interests, and intentions. Single-unit recordings in macaques have revealed neurons selective for others' specific gaze direction. A parallel functional organization in the human brain is indicated by gaze-adaptation experiments, in which systematic distortions in gaze perception following prolonged exposure to static face images reveal dynamic interactions in local cortical circuitry. However, our understanding of the influence of high-level social cognition on these processes in monkeys and humans is still rudimentary. Here we show that the attribution of a mental state to another person determines the way in which the human brain codes observed gaze direction. Specifically, we convinced observers that prerecorded video sequences of an experimenter gazing left or right were a live video link to an adjacent room. The experimenter wore mirrored goggles that observers believed were either transparent such that the person could see, or opaque such that the person could not see. The effects of adaptation were enhanced under the former condition relative to the latter, indicating that high-level sociocognitive processes shape and modulate sensory coding of observed gaze direction.

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 sub-optimal 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.

Early stages of visual processing are carried out by neural circuits activated by simple and specific features, such as the orientation of an edge. A fundamental question in human vision is how the brain organises such intrinsically local information into meaningful properties of objects. Classic models of visual processing emphasise a one-directional flow of information from early feature-detectors to higher-level information-processing. By contrast to this view, and in line with predictive-coding models of perception, here, we provide evidence from human vision that high-level object representations dynamically interact with the earliest stages of cortical visual processing. In two experiments, we used ambiguous stimuli that, depending on the observer’s prior object-knowledge, can be perceived as either coherent objects or as a collection of meaningless patches. By manipulating object knowledge we were able to determine its impact on processing of low-level features while keeping sensory stimulation identical. Both studies demonstrate that perception of local features is facilitated in a manner consistent with an observer’s high-level object representation (i.e., with no effect on object-inconsistent features). Our results cannot be ascribed to attentional influences. Rather, they suggest that high-level object representations interact with and sharpen early feature-detectors, optimising their performance for the current perceptual context.

Research highlights▶ Levels of sensory-motor predictions vary gradually in the healthy population. ▶ Deficient predictions are related to a delusion-like style of thinking. ▶ The continuum between health and psychosis exists even on a sensory-motor level.