Local and global reward learning in the lateral frontal cortex show differential development during human adolescence

Abstract

Reward-guided choice is fundamental for adaptive behaviour and depends on several component processes supported by prefrontal cortex. Here, across three studies, we show that two such component processes, linking reward to specific choices and estimating the global reward state, develop during human adolescence and are linked to the lateral portions of the prefrontal cortex. These processes reflect the assignment of rewards contingently to local choices, or noncontingently, to choices that make up the global reward history. Using matched experimental tasks and analysis platforms, we show the influence of both mechanisms increase during adolescence (study 1) and that lesions to lateral frontal cortex (that included and/or disconnected both orbitofrontal and insula cortex) in human adult patients (study 2) and macaque monkeys (study 3) impair both local and global reward learning. Developmental effects were distinguishable from the influence of a decision bias on choice behaviour, known to depend on medial prefrontal cortex. Differences in local and global assignments of reward to choices across adolescence, in the context of delayed grey matter maturation of the lateral orbitofrontal and anterior insula cortex, may underlie changes in adaptive behaviour.

Beta and theta oscillations track effort and previous reward in human basal ganglia and prefrontal cortex during decision making

“…We also found that previous reward enhanced the effects of current reward and effort on decision making. This results aligns with prior evidence that it may provide context for the current decision, potentially as a direct comparison with the current reward 63 or as a measure of recent reward history that captures the richness of the environment or global reward state 21,65 . Although the rewards on consecutive trials were independent in our laboratory paradigm, PFC likely tracks reward context because rewards have strong temporal correlations in real world environments.…”

Beta and theta oscillations track effort and previous reward in the human basal ganglia and prefrontal cortex during decision making

“…We also found that previous reward enhanced the effects of current reward and effort on decision making. This result aligns with prior evidence that it may provide context for the current decision, potentially as a direct comparison with the current reward ( 67 ) or as a measure of recent reward history that captures the richness of the environment or global reward state ( 24 , 69 ). Although the rewards on consecutive trials were independent in our laboratory paradigm, PFC likely tracks reward context because rewards have strong temporal correlations in real-world environments.…”

Different functions of physical effort: A scoping review of the value of physical effort in physical activity and sports

“…Compared to adults who predominantly exert effort strategically as an instrument to maximize rewards and minimize effort (Rodman et al, 2021), adolescents seem less sensitive to effort costs, thus, exerting more effort than a task requires (Sullivan-Toole et al, 2019). These differences might be influenced by changes in striving for autonomy (e.g., Steinberg & Morris, 2001) and in the neural (e.g., Wittmann et al, 2023) or hormonal system (e.g., Buchanan et al, 1992;Cyranowski et al, 2000) during adolescence, and on the other hand, rising opportunity costs of effort with aging (Cardini & Freund, 2021).…”