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

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.

Reward learning capacity in a community sample of individuals who use cannabis.

“…These criteria can include: the removal of trials where response time was faster than 150 ms and slower than 1,500 ms (Bogdan & Pizzagalli, 2006;Whitton et al, 2016) or 2,500 ms (AhnAllen et al, 2012;Dillon et al, 2022;, and additional outliers outside the range of ±3SD from the mean. Participants may be removed from analyses if they had more than 20 outlier trials per block based on reaction time (AhnAllen et al, 2012;Dillon et al, 2022;Liverant et al, 2014); others set this cutoff as 10 per block (Kaiser et al, 2018;Patel et al, 2020;Whitton et al, 2018Whitton et al, , 2021. Some studies specified the requirement of receiving at least 25 rich rewarded stimuli per block (AhnAllen et al, 2012;Liverant et al, 2014), no fewer than 6 lean rewarded stimuli (Dillon et al, 2022) and/or a rich/lean reward ratio of no less than 2 (Dillon et al, 2022;Kaiser et al, 2018).…”

“…Some studies specified the requirement of receiving at least 25 rich rewarded stimuli per block (AhnAllen et al, 2012;Liverant et al, 2014), no fewer than 6 lean rewarded stimuli (Dillon et al, 2022) and/or a rich/lean reward ratio of no less than 2 (Dillon et al, 2022;Kaiser et al, 2018). Others also removed participants with accuracy scores below 55% (Janes et al, 2015;Kaiser et al, 2018;Whitton et al, 2018Whitton et al, , 2021 or 60% (AhnAllen et al, 2012;Liverant et al, 2014), and some studies did not indicate the application of any quality control checks (Hou et al, 2020;. Lawn et al, (2016) used several of the aforementioned criteria, that when applied to our dataset, did not change the non-significant group differences in response bias across blocks (see Manuscript Supplementary Material).…”

Comparative Analysis of Dopaminergic and Cholinergic Mechanisms of Sensory and Sensorimotor Gating in Healthy Individuals and in Patients With Schizophrenia

“…Nicotine intake (smoking) was found to enhance sensory gating in healthy individuals with baseline low rates of P50 suppression (mainly, in carriers of Val/Val variant of COMT rs4680 polymorphism) and in patients with schizophrenia, but not in bipolar disorder (Whitton et al, 2021 ). In healthy persons, the effect of nicotine on P50 gating was relatively modest and was significantly enhanced after combined nicotine and MAO-A inhibitor compared to placebo and to the nicotine-alone condition (Smith et al, 2015 ).…”