Variation in reward- and error-related neural measures attributable to age, gender, race, and ethnicity

Hill, Kaylin E.; Oumeziane, Belel Ait; Novak, Keisha; Rollock, David; Foti, Dan

doi:10.1016/j.ijpsycho.2017.12.009

Cited by 22 publications

(27 citation statements)

References 78 publications

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“…The RewP was also the only measure examined that significantly covaried with age, with younger adults showing larger amplitudes. Many prior studies examining covariation with the RewP (or separate win and loss waveforms) have focused on developmental samples, though studies that have extended the age range into middle and older adults observe a pattern similar to ours, with attenuation of the RewP over the course of adulthood 62,63 . Several existing studies used a slot paradigm design with all outcome information being delivered simultaneously (with trial outcomes defined based on number or proximity of stimuli in the final visual array) [59][60][61] .…”

Section: Discussionsupporting

confidence: 67%

Electrophysiological investigation of reward anticipation and outcome evaluation during slot machine play

Fryer

Roach

Holroyd

et al. 2020

Preprint

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Slot machines are a popular form of gambling, offering a tractable way to experimentally model reward processes. This study used a 3-reel slot paradigm to assess psychologically distinct phases of reward processing, reflecting anticipation, and early and late-stage outcome processing. EEG measures of winning, nearly missing (a losing outcome revealed at the final, third reel), and “totally” missing (a losing outcome revealed earlier, at the second reel) were collected from healthy adults (n=54). Condition effects were evaluated in: i) event-related potential (ERP) components reflecting anticipatory attention (stimulus preceding negativity, SPN) and outcome processing (reward positivity, RewP and late-positive potential, LPP) and ii) total power and phase synchrony of theta and delta band oscillations. Behaviorally, trial initiation was fastest after a near miss outcome and slowest after a winning outcome. As expected, a significant SPN was observed for possible wins (AA) vs. total misses (AB), consistent with reward anticipation. In addition, significantly larger win (AAA) vs. near miss (AAB) amplitudes were observed for the RewP and LPP to wins and LPP to near misses (vs. total misses) reflecting early and late-stage outcome processing effects. There was an effect of reel position on the RewP, with larger effects in the final reel (AAA-AAB) relative to the 2nd-reel locked difference waves (AA-AB). Across all outcomes, near misses elicited the largest and most phase-synchronized theta responses, while wins elicited larger and more phase-synchronized delta responses than total misses, with near misses not differing from wins or total misses. Phase locking measures contrasting win vs. near miss delta and theta synchronization, within time windows corresponding to ERP measurements, covaried with RewP, but not SPN or LPP, amplitude. Lastly, EEG measures showed differential relationships with age and self-reported consummatory pleasure. In the context of slot machine play, where reward anticipation and attainment place minimal demands on effort and skill, ERP and time-frequency methods capture distinct neurophysiological signatures of reward anticipation and outcome processing.

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Section: Discussionsupporting

confidence: 67%

Electrophysiological investigation of reward anticipation and outcome evaluation during slot machine play

Fryer

Roach

Holroyd

et al. 2020

Preprint

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“…Specifically, they have methodological implications by suggesting the importance of assessing and accounting for the ToD at which the ∆RewP‐focused study sessions are conducted. In addition, these age‐related results are in line with the recently underscored need for the inclusion of demographic variables as moderators as a standard practice in all psychophysiological studies, in order to fully understand their impact on the EEG/ERP variables of interest (Hill, Oumeziane, Novak, Rollock, & Foti, ).…”

Section: Discussionsupporting

confidence: 76%

Time of day differences in neural reward responsiveness in children

Tsypes

Gibb

2020

Psychophysiology

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The Reward Positivity (∆RewP) event‐related potential (ERP), generally quantified as the difference between neural responsiveness to monetary gains (RewP‐Gain) and losses (RewP‐Loss) is commonly used as an index of neural reward responsiveness. Despite the popularity of this ERP component in studies of reward processing, knowledge about the role of state‐related influences on the ∆RewP is limited. The present study examined whether ∆RewP amplitudes may differ based on when during the day they are assessed and whether age or sex would moderate this link. Participants were 188 children between the ages of 7 and 11 (47.3% female) without a lifetime history of a major depressive disorder or any anxiety disorder recruited from the community. Children completed the Doors task during which continuous electroencephalography was recorded to isolate the ∆RewP. To better isolate this ERP component from other temporally or spatially overlapping ERPs, we used temporospatial principal component analysis. We found that time of day (ToD) differences in the ∆RewP amplitude varied based on children's age. Specifically, older, compared to younger, children exhibited stronger responses to gains versus losses between 11:15 a.m. and 12:30 p.m. and after around 5:15 p.m. Further, these age‐related differences appeared to be driven specifically by older children's reduced neural responsiveness to losses. The findings have methodological implications by highlighting the importance of accounting for the ToD at which ∆RewP‐focused study sessions are conducted as well as for demographic characteristics of the participants, such as their age.

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“…Importantly, normal and pathological aging effects may impact reward processing neural signals. RewP magnitude shows a negative association with age among HC (9), and a depression-focused meta-analysis found that RewP blunting was most pronounced in younger depressed samples (42). Beyond reward processing, growing evidence supports hypotheses of accelerated brain aging in SZ (43)(44)(45)(46)(47), particularly early in the illness course (44,46), which may be due to abnormal brain maturation (48).…”

Section: Introductionmentioning

confidence: 96%

“…Reward processing deficits are a core feature of schizophrenia (SZ) (1)(2)(3)(4) that may underlie characteristic motivational impairments (3) and contribute to poor functional outcomes (5)(6)(7). Many reward-focused studies i) implement paradigms that confound reward processing with other cognitive or behavioral demands known to be impaired in SZ (4,8), ii) do not focus on key demographic variables (like age) (9), or iii) do not consider clinical variables that may be associated with accelerated brain changes (like illness phase) (10).…”

Section: Introductionmentioning

confidence: 99%

“…The reels sequentially populate, left to right, enabling parsing of anticipatory from early and late-consummatory signals. Because neurodevelopmental changes are central to SZ pathogenesis and healthy reward processing (51,57), we compared SZ and HC across a wide age range, with the goal of examining contributions of i) age through analyses of chronological age and BrainAGE (derived from reward ERPs), and ii) categorically-defined illness phase through recruitment of early illness (ESZ) and chronic (CSZ) patient groups (9,10).…”

Section: Introductionmentioning

confidence: 99%

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

Abram

Roach

Holroyd

et al. 2020

Preprint

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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.

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Variation in reward- and error-related neural measures attributable to age, gender, race, and ethnicity

Cited by 22 publications

References 78 publications

Electrophysiological investigation of reward anticipation and outcome evaluation during slot machine play

Electrophysiological investigation of reward anticipation and outcome evaluation during slot machine play

Time of day differences in neural reward responsiveness in children

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

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