Smoking as a Common Modulator of Sensory Gating and Reward Learning in Individuals with Psychotic Disorders.

Alexis E Whitton,Kathryn E Lewandowski,Mei-Hua Hall

doi:10.3390/brainsci11121581

Alexis E Whitton, Kathryn E Lewandowski + Show 1 more

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https://doi.org/10.3390/brainsci11121581

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Abstract

Motivational and perceptual disturbances co-occur in psychosis and have been linked to aberrations in reward learning and sensory gating, respectively. Although traditionally studied independently, when viewed through a predictive coding framework, these processes can both be linked to dysfunction in striatal dopaminergic prediction error signaling. This study examined whether reward learning and sensory gating are correlated in individuals with psychotic disorders, and whether nicotine—a psychostimulant that amplifies phasic striatal dopamine firing—is a common modulator of these two processes. We recruited 183 patients with psychotic disorders (79 schizophrenia, 104 psychotic bipolar disorder) and 129 controls and assessed reward learning (behavioral probabilistic reward task), sensory gating (P50 event-related potential), and smoking history. Reward learning and sensory gating were correlated across the sample. Smoking influenced reward learning and sensory gating in both patient groups; however, the effects were in opposite directions. Specifically, smoking was associated with improved performance in individuals with schizophrenia but impaired performance in individuals with psychotic bipolar disorder. These findings suggest that reward learning and sensory gating are linked and modulated by smoking. However, disorder-specific associations with smoking suggest that nicotine may expose pathophysiological differences in the architecture and function of prediction error circuitry in these overlapping yet distinct psychotic disorders.

Highlights

Disturbances in motivation and perception are hallmark features of schizophrenia and other psychotic disorders
We found that smokers and non-smokers differed from one another in a consistent manner across both sensory gating and probabilistic reward task (PRT) performance, interestingly, opposing effects were observed in the schizophrenia and bipolar disorder groups
Performance in the schizophrenia group, it was associated with impaired sensory gating and PRT performance in the bipolar disorder group (Figure 3A,B left panel), the latter impairment was mitigated in individuals with bipolar disorder who were taking dopamine D2 receptor antagonists (Figure 3A,B right panel)

Summary

Introduction

Disturbances in motivation and perception are hallmark features of schizophrenia and other psychotic disorders. They frequently co-occur within the same individual, these disturbances have been traditionally studied as separate entities. Research emanating from the field of computational neuroscience has postulated predictive coding accounts of psychosis, which cast motivational and perceptual disturbances in a more unified light. Such accounts posit that psychosis results from “a decreased precision in the encoding of prior beliefs relative to the sensory data, thereby garnering maladaptive inferences” [1]; Rather than being pathophysiologically distinct, motivational and perceptual disturbances may be governed by a common learning mechanism (for a review, see [2]), perhaps arising from aberrant phasic striatal dopamine signaling [3]

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