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An Integrative Framework for Perceptual Disturbances in Psychosis

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An Integrative Framework for Perceptual Disturbances in Psychosis REVIEWS An integrative framework for perceptual disturbances in psychosis Guillermo Horga1* and Anissa Abi- Dargham 2* Abstract | Perceptual disturbances in psychosis, such as auditory verbal hallucinations, are associated with increased baseline activity in the associative auditory cortex and increased dopamine transmission in the associative striatum. Perceptual disturbances are also associated with perceptual biases that suggest increased reliance on prior expectations. We review theoretical models of perceptual inference and key supporting physiological evidence, as well as the anatomy of associative cortico–striatal loops that may be relevant to auditory perceptual inference. Integrating recent findings, we outline a working framework that bridges neurobiology and the phenomenology of perceptual disturbances via theoretical models of perceptual inference. Schizophrenia Explanations such as ‘hallucinations are caused by perceptual disturbances in psychosis represent an extreme A psychiatric illness overactive dopamine receptors’ are unsatisfactory variant of the perceptual biases that arise naturally characterized by a variety of because they leave an explanatory gap between the from the incorporation of prior knowledge. symptoms, including positive mental and the physical. How can dopamine cause a Here we present a selective review of the literature symptoms, negative symptoms 1 (for example, apathy and voice or a belief? — Paul C. Fletcher and Chris D. Frith on the pathophysiology of psychotic perceptual distur- amotivation) and cognitive bances, and outline an integrative framework grounded impairments (for example, Perceptual disturbances, including hallucinations or in models of normal perception that has the potential memory deficits). false percepts, are a defining and prevalent feature of to advance current conceptualizations of these puz- schizophrenia and other psychotic disorders. zling phenomena. In addition to our focus on percep- Psychotic disorders A group of disorders, including Perception is the subjective process by which neural tual models, we attempt to bridge a number of relevant schizophrenia and other systems represent, disambiguate and interpret sensory fields that historically have developed in parallel. Most disorders, such as bipolar inputs from the environment. Because sensory inputs relevantly, an extensive body of pharmacological and disorder, with psychotic are always conveyed with some level of noise or uncer- molecular- imaging studies have definitively established features, that present with psychotic or positive tainty, a key function of sensory systems is to reduce sen- a central role of excessive dopamine transmission in the 2 symptoms. sory uncertainty in order to facilitate accurate judgments striatum in psychosis . However, previous views of sen- that permit successful adaptation to the environment. sory processing in schizophrenia have mostly focused Auditory verbal To do so in an optimal way, sensory systems leverage on local cortical circuits and have de- emphasized the hallucinations the prior knowledge that an agent has acquired through contributions to perceptual disturbances in schizo- (AVH). Percepts of speech or voices without corresponding experience. Optimal sensory processing, however, does phrenia of neuromodulators such as dopamine and of speech stimuli. not imply error- free perceptual judgments. As we later their effects on basal ganglia circuits. These views may discuss in more detail, incorporating prior knowledge be partly influenced by traditional conceptions of sen- into percepts, although generally advantageous, biases sory systems as isolated brain modules, specialized for perception towards more likely sensory events: that passive stimulus detection through local processing, is, it implies perceptual- judgment errors on the side of that are immune to learning and cognitive influences3. likely scenarios. This predisposes healthy individuals to In turn, dopamine transmission in the striatum has 1Deparment of Psychiatry, Columbia University, and a plethora of perceptual distortions, such as seeing faces mostly been cast in terms of reward- based learning, New York State Psychiatric in clouds or experiencing a cell phone vibration in the despite the mounting evidence supporting a more gen- Institute, New York, NY, USA. absence of true vibration. Likewise, such incorporation eral role for striatal dopamine in perception and cogni- 2Department of Psychiatry, of prior knowledge may provide a point of vulnera- tion beyond reward- related processes. Similarly, striatal Stony Brook University, bility that, under the strain of pathological states, may function has been classically portrayed in terms of reward Stony Brook, NY, USA. result in qualitatively similar but more extreme biases. learning and action selection, and only recently has its *e- mail: HorgaG@ These extreme biases, in turn, may constitute the basic role in perceptual learning and perceptual decision mak- nyspi.columbia.edu; anissa.abi- dargham@ phenomenon behind perceptual disturbances such as ing come into focus. The view of perceptual disturbances stonybrookmedicine.edu auditory verbal hallucinations (AVH), or percepts of voices we present here instead aims to integrate recent insights https://doi.org/10.1038/ in the absence of speech stimuli. A critical aspect of our into the roles of dopamine and the basal ganglia within s41583-019-0234-1 proposed framework is thus centred on the notion that the the context of current theoretical models of perception. NATURE REVIEWS | NEUROSCIENCE VOLUME 20 | DECEMBER 2019 | 763 REVIEWS Positive symptoms Given the clinical predominance of auditory distur- commentary on the patient’s behaviour or a conver- Also known as psychotic bances, relative to disturbances in other sensory modal- sation between different familiar or unfamiliar voices. symptoms or psychosis; ities, in psychotic disorders, we focus mainly on relevant The content of hallucinated voices (that is, AVH) is symptoms that are added to pathways at the intersection between dopamine, basal variable, but commonly it exhibits a negative emotional the repertoire of usual experiences and that represent ganglia circuits and the auditory system. We build upon valence (for example, a derogatory tone) and is relevant 16 a loss of contact with reality prior theoretical accounts of psychosis that have capital- to the voice- hearer’s personal experience . In acute (that is, subjective experiences ized on computational modelling to bridge phenomenol- states, AVH are typically interpreted as real voices origi- that substantially deviate from ogy and neurobiology1,4,5. We place a special emphasis on nating in the external environment (that is, patients have what most perceive as the physiological basis for auditory perception and the no insight into their internal and dysfunctional origin) objective evidence), including hallucinations and delusions. candidate pathophysiological mechanisms that may lead and consequently provoke hallucination- related behav- to altered perceptual experiences in psychosis. iours, such as out- loud verbal responses to the voices Prodromal Specifically, some prominent models of psychosis (soliloquy) or other congruent behaviours (for example, Related to the psychosis emphasize aberrant reward signalling as the central factor checking whether the perceived voices are the next- prodrome or prodromal phase, 6,7 terms that refer to the phase linking dopamine dysfunction and psychotic symptoms , door neighbours’ voices heard through the wall). Other preceding the development of given the well- established role of dopamine in reward forms of psychosis, such as those induced by pro- full- blown symptoms of a prediction- error signalling8–10. However, it is generally dopaminergic drugs in Parkinson disease, contrast with psychotic disorder; typically accepted that dopamine has additional functions11. In this schizophrenia in that they feature visual hallucinations defined by the expression of vein, we focus on recent evidence for a role of dopamine more frequently than auditory hallucinations17, sug- attenuated forms of positive symptoms. in perceptual decision making and learning, and present gesting that auditory pathways are particularly relevant an alternative view of psychotic perceptual disturbances in the pathophysiology of psychotic disorders in the that emphasizes alterations in perceptual inference. schizophrenia spectrum18. Phenomenology Delusions and psychotic syndrome. In psychosis, percep- Patients with schizophrenia and other psychotic dis- tual disturbances such as hallucinations almost always orders report a wide range of perceptual disturbances. accompany other psychotic symptoms. They tend to These phenomena, in particular hallucinations, have co- occur and evolve in parallel with delusions, which long been documented and have become emblematic of are defined as tenacious false beliefs maintained in the mental illness from a sociocultural standpoint. Like other face of contradictory evidence. This clustering of hal- positive symptoms of psychosis, perceptual distortions lucinations with delusions is stronger than the correla- tend to develop progressively during adolescence or early tion of either of these individual symptoms with other adulthood12. They typically begin in attenuated forms, symptoms of schizophrenia (for example, amotivation during the prodromal pre-psychosis phase, and gradually or memory impairments), and thus defines a distinct evolve into overt distortions
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