Reward processing electrophysiology in schizophrenia: Effects of age and illness phase

Abstract

Background: Reward processing abnormalities may underlie characteristic pleasure and motivational impairments in schizophrenia. Some neural measures of reward processing show strong age-related modulation, highlighting the importance of considering age effects on reward sensitivity. We compared event-related potentials (ERPs) reflecting reward anticipation (stimulus-preceding negativity, SPN) and evaluation (reward positivity, RewP; late-positive potential, LPP) across individuals with schizophrenia (SZ) and healthy controls (HC), with an emphasis on examining effects of chronological age, brain age (i.e., predicted age based on neurobiological measures), and illness phase.Methods: Subjects underwent EEG while completing a slot-machine task for which rewards were not dependent on performance accuracy, speed, or other preparatory demands. Slot-machine task EEG responses were compared between 54 SZ and 54 HC individuals, ages 19 to 65. Reward-related ERPs were analyzed with respect to chronological age, categorically-defined illness phase (early; ESZ versus chronic schizophrenia; CSZ), and were used to model brain age relative to chronological age.Results: Illness phase-focused analyses indicated there were no group differences in average SPN or RewP amplitudes. However, a group x reward outcome interaction revealed that ESZ differed from HC in later outcome processing, reflected by greater LPP responses following loss versus reward (a reversal of the HC pattern). While brain age estimates did not differ among groups, depressive symptoms in SZ were associated with older brain age estimates while controlling for negative symptoms.Conclusions: ESZ and CSZ did not differ from HC in reward anticipation or early outcome processing during a cognitively undemanding reward task, highlighting areas of preserved functioning. However, ESZ showed altered later reward outcome evaluation, pointing to selective reward deficits during the early illness phase of schizophrenia. Further, an association between ERP-derived brain age and depressive symptoms in SZ extends prior findings linking depression with reward-related ERP blunting. Taken together, both illness phase and age may impact reward processing in SZ, and brain aging may offer a promising, novel marker of reward dysfunction that warrants further study.

Alpha Event-related Desynchronization During Reward Processing in Schizophrenia

“…It is therefore worth emphasizing that given our relatively passive slot machine task design, in which reward outcome did not depend on participant performance or decision-making, we observe alpha ERD alterations in schizophrenia even when reward attainment places minimal demands on higher-order cognitive processes. This finding is of particular interest as our group has previously shown intact reward anticipation and early outcome reward processing in this same experimental cohort(32); event-related potential analyses in our group’s earlier work demonstrated no differences between SZ and HC in either the stimulus preceding negativity (SPN), a pre-stimulus onset ERP reflecting reward anticipation, or the reward positivity (RewP), an early (~250ms) evolving ERP reflecting early reward feedback processing. This intact RewP is in line with prior studies examining feedback processing in SZ and supports current conceptualizations that patients with schizophrenia have intact hedonic responses.…”

“…Negative symptoms were evaluated in the SZ group using the Positive and Negative Syndrome Scale (PANSS (cite). In addition to a negative symptom total score, we also used the PANSS to compute a Depression composite score based on a previously validated five-factor model shown to correlate with depression in SZ (35), similar to our previous work (32); the composite is derived by summing the anxiety (G2), guilt (G3), and depression (G6) items from the general psychopathology subscale. Trait rumination was assessed in both the HC and SZ groups with the Rumination Response Scale (RRS) (36).…”

“…Prior work from our group using this task did not focus on alpha band, but instead established expected condition effects in heathy controls, including outcome modulations of oscillatory power in response to wins (delta) and losses (theta) (31); and also time-domain event-related potential comparisons between SZ and healthy control (HC) groups that revealed intact anticipatory (stimulus preceding negativity) and early outcome (reward positivity), with late in outcome processing (late positive potential)(32). In the current study, we hypothesized that alpha ERD would be deficient during reward processing in SZ (i.e., less alpha suppression to wins, relative to near miss losses), and that ERD deficits would correlate with negative symptoms.…”