Executive functioning moderates neural reward processing in youth

Abstract

Although executive functioning has traditionally been studied in "cool" settings removed from emotional contexts, it is highly relevant in "hot" emotionally salient settings such as reward processing. Furthermore, brain structures related to "cool" executive functioning and "hot" reward-related processes develop simultaneously, yet little is known about how executive functioning modulates neural processes related to reward processing during adolescence, a period of time when these systems are still developing. The present study examined how performance on "cool" behavioral executive functioning measures moderates neural reward processing. Youths (N = 43, M age = 13.74 years, SD = 1.81 years) completed a child-friendly monetary incentive delay task during fMRI acquisition that captures neural responses to reward anticipation and to reward receipt and omission. Performance on inhibitory control and cognitive flexibility measures, captured outside the scanner, was used to predict brain activation and seed-based connectivity (ventral striatum and amygdala). Across analyses, we found that executive functioning moderated youths' neural responses during both reward anticipation and performance feedback, predominantly with respect to amygdala connectivity with prefrontal/frontal and temporal structures, supporting previous theoretical models of brain development during adolescence. Overall, youths with worse executive functioning had more pronounced differences in neural activation and connectivity between task conditions compared with youths with better executive functioning. This study contributes to elucidating the relationship between "cool" and "hot" processes and our findings demonstrate that simple executive functioning skills moderate more complex processes that involve incorporation of numerous skills in an emotionally salient context, such as reward processing.

Neural mechanisms of reward processing in adolescent irritability

“…Table 1 lists participant characteristics for the final N = 52, as well as scores on symptoms measures (see below). Data from a subset of participants have been previously published (Kryza‐Lacombe, Christian, et al, 2020; Kryza‐Lacombe, Kiefer, et al., 2020; Liuzzi et al., 2020; Schwartz et al., 2019).…”

The effects of reward on children’s Stroop performance: Interactions with temperament

“…For instance, these patterns may reflect an actual negative, linear correlation between reward sensitivity and reward‐based change in early EFs, and thus a developmental shift in this association between early childhood and adulthood. While rewards impact EFs via arousal and attentional control (Botvinick & Braver, 2015; Padmala & Pessoa, 2011), EF also modulates brain activity that supports reward processing (Kryza‐Lacombe et al, 2021). Critically, EF and reward processing, as well as their respective neural substrates, exhibit distinct developmental trajectories (Somerville & Casey, 2010).…”

“…Importantly, motivation‐EF interactions are bidirectional in nature; rewards impact top‐down cognitive control as well as bottom‐up affective networks, while EF modulates reward processing and associated brain activity (Blair & Ursache, 2011; Kryza‐Lacombe et al, 2021; Somerville & Casey, 2010). Associations among reward processing and EF may therefore have different patterns across development, as executive and motivational systems exhibit distinct trajectories.…”