Developmental changes in brain function underlying the influence of reward processing on inhibitory control

Adolescence is a period marked by changes in motivational and cognitive brain systems. However, the development of the interactions between reward and cognitive control processing are just beginning to be understood. Using event-related functional neuroimaging and an incentive modulated antisaccade task, we compared blood-oxygen level dependent activity underlying motivated response inhibition in children, adolescents, and adults. Behaviorally, children and adolescents performed significantly worse than adults during neutral trials. However, children and adolescents showed significant performance increases during reward trials. Adults showed no performance changes across conditions. fMRI results demonstrated that all groups recruited a similar circuitry to support task performance, including regions typically associated with rewards (striatum and orbital frontal cortex), and regions known to be involved in inhibitory control (putative frontal and supplementary eye fields, and posterior parietal cortex, and prefrontal loci). During rewarded trials adolescents showed increased activity in striatal regions, while adults demonstrated heightened activation in the OFC relative to children and adolescents. Children showed greater reliance on prefrontal executive regions that may be related to increased effort in inhibiting responses. Overall, these results indicate that response inhibition is enhanced with reward contingencies over development. Adolescents’ heightened response in striatal regions may be one factor contributing to reward-biased decision making and perhaps risk taking behavior.     

Pubertal development underlies optimization of inhibitory control through specialization of ventrolateral prefrontal cortex

Inhibitory control improves into young adulthood after specialization of relevant brain systems during adolescence. However, the biological mechanisms supporting this unique transition are not well understood. Given that adolescence is defined by puberty, we examined relative contributions of chronological age and pubertal maturation to inhibitory control development. 105 8–19-year-olds completed 1–5 longitudinal visits (227 visits total) in which pubertal development was assessed via self-reported Tanner stage and inhibitory control was assessed with an in-scanner antisaccade task. As expected, percentage and latency of correct antisaccade responses improved with age and pubertal stage. When controlling for pubertal stage, chronological age was distinctly associated with correct response rate. In contrast, pubertal stage was uniquely associated with antisaccade latency even when controlling for age. Chronological age was associated with fMRI task activation in several regions including the right dorsolateral prefrontal cortex, while puberty was associated with right ventrolateral prefrontal cortex (VLPFC) activation. Furthermore, task-related connectivity between VLPFC and cingulate was associated with both pubertal stage and response latency. These results suggest that while age-related developmental processes may support maturation of brain systems underlying the ability to inhibit a response, puberty may play a larger role in the effectiveness of generating cognitive control responses.     

Self-referential processing influences functional activation during cognitive control: an fMRI study

Rostral anterior cingulate cortex (rACC) plays a central role in the pathophysiology of major depressive disorder (MDD). As we reported in our previous study (Wagner et al., 2006), patients with MDD were characterized by an inability to deactivate this region during cognitive processing leading to a compensatory prefrontal hyperactivation. This hyperactivation in rACC may be related to a deficient inhibitory control of negative self-referential processes, which in turn may interfere with cognitive control task execution and the underlying fronto-cingulate network activation. To test this assumption, a functional magnetic resonance imaging study was conducted in 34 healthy subjects. Univariate and functional connectivity analyses in statistical parametric mapping software 8 were used. Self-referential stimuli and the Stroop task were presented in an event-related design. As hypothesized, rACC was specifically engaged during negative self-referential processing (SRP) and was significantly related to the degree of depressive symptoms in participants. BOLD signal in rACC showed increased valence-dependent (negative vs neutral SRP) interaction with BOLD signal in prefrontal and dorsal anterior cingulate regions during Stroop task performance. This result provides strong support for the notion that enhanced rACC interacts with brain regions involved in cognitive control processes and substantiates our previous interpretation of increased rACC and prefrontal activation in patients during Stroop task.     

Contributions of dopamine-related basal ganglia neurophysiology to the developmental effects of incentives on inhibitory control

Inhibitory control can be less reliable in adolescence, however, in the presence of rewards, adolescents’ performance often improves to adult levels. Dopamine is known to play a role in signaling rewards and supporting cognition, but its role in the enhancing effects of reward on adolescent cognition and inhibitory control remains unknown. Here, we assessed the contribution of basal ganglia dopamine-related neurophysiology using longitudinal MR-based assessments of tissue iron in rewarded inhibitory control, using an antisaccade task. In line with prior work, we show that neutral performance improves with age, and incentives enhance performance in adolescents to that of adults. We find that basal ganglia tissue iron is associated with individual differences in the magnitude of this reward boost, which is strongest in those with high levels of tissue iron, predominantly in adolescence. Our results provide novel evidence that basal ganglia neurophysiology supports developmental effects of rewards on cognition, which can inform neurodevelopmental models of the role of dopamine in reward processing during adolescence.     

Kids,candy, brain and behavior: Age differences in responses to candy gains and losses

The development of reward-related neural systems, from adolescence through adulthood, has received much recent attention in the developmental neuroimaging literature. However, few studies have investigated behavioral and neural responses to both gains and losses in pre-pubertal child populations. To address this gap in the literature, in the present study healthy children aged 7–11 years and young-adults completed an fMRI card-guessing game using candy pieces delivered post-scan as an incentive. Age differences in behavioral and neural responses to candy gains/losses were investigated. Adults and children displayed similar responses to gains, but robust age differences were observed following candy losses within the caudate, thalamus, insula, and hippocampus. Interestingly, when task behavior was included as a factor in post hoc mediation analyses, activation following loss within the caudate/thalamus related to task behavior and relationships with age were no longer significant. Conversely, relationships between response to loss and age within the hippocampus and insula remained significant even when controlling for behavior, with children showing heightened loss responses within the dorsal/posterior insula. These results suggest that both age and task behavior influence responses within the extended reward circuitry, and that children seem to be more sensitive than adults to loss feedback particularly within the dorsal/posterior insula.     

Developmental effects of decision-making on sensitivity to reward: An fMRI study

Studies comparing neural correlates of reward processing across development yield inconsistent findings. This challenges theories characterizing adolescents as globally hypo- or hypersensitive to rewards. Developmental differences in reward sensitivity may fluctuate based on reward magnitude, and on whether rewards require decision-making. We examined whether these factors modulate developmental differences in neural response during reward anticipation and/or receipt in 26 adolescents (14.05±2.37yrs) and 26 adults (31.25±8.23yrs). Brain activity was assessed with fMRI during reward anticipation, when subjects made responses with-vs.-without decision-making, to obtain large-vs.-small rewards, and during reward receipt. When reward-receipt required decision-making, neural activity did not differ by age. However, when reward receipt did not require decision-making, neural activity varied by development, reward magnitude, and stage of the reward task. During anticipation, adolescents, but not adults, exhibited greater activity in the insula, extending into putamen, and cingulate gyrus for large-vs.-small incentives. During feedback, adults, but not adolescents, exhibited greater activity in the precuneus for large-vs.-small incentives. These data indicate that age-related differences in reward sensitivity cannot be characterized by global hypo- or hyper-responsivity. Instead, neural responding in striatum, prefrontal cortex and precuneus is influenced by both situational demands and developmental factors. This suggests nuanced maturational effects in adolescent reward sensitivity.     

Negative impact of daily screen use on inhibitory control network in preadolescence: A two-year follow-up study

The COVID-19 pandemic has made an unprecedented shift in children’s daily lives. Children are increasingly spending time with screens to learn and connect with others. As the online environment rapidly substitutes in-person experience, understanding children’s neuropsychological trajectories associated with screen experiences is important. Previous findings suggest that excessive screen use can lead children to prefer more immediate rewards over delayed outcomes. We hypothesized that increased screen time delays a child’s development of inhibitory control system in the brain (i.e., fronto-striatal circuitry). By analyzing neuropsychological data from 8324 children (9–11ys) from the ABCD Study, we found that children who had more screen time showed a higher reward orientation and weaker fronto-striatal connectivity. Importantly, we found that the daily screen exposure mediated the effect of reward sensitivity on the development of the inhibitory control system in the brain over a two year period. These findings suggest possible negative long-term impacts of increased daily screen time on children’s neuropsychological development. The results further demonstrated that screen time influences dorsal striatum connectivity, which suggests that the effect of daily screen use is a habitual seeking behavior. The study provides neural and behavioral evidence for the negative impact of daily screen use on developing children.     

How the aging brain translates motivational incentive into action: the role of individual differences in striato-cortical white matter pathways

The anticipation of reward enhances actions that lead to those rewards, but individuals differ in how effectively motivational incentives modulate their actions. Such individual differences are particularly prominent in aging. In order to account for such inter-individual variability among older adults, we approach the neurobiological mechanisms of motivated behavior from an individual differences perspective focusing on white matter pathways in the aging brain. Using analyses of probabilistic tractography seeded in the striatum, we report that the estimated strength of cortico-striatal and intra-striatal white matter pathways among older adults correlated with how effectively motivational incentives modulated their actions. Specifically, individual differences in the extent to which elderly participants utilized reward cues to prepare and perform more efficient antisaccades predicted structural connectivity of the striatum with cortical areas involved in reward anticipation and oculomotor control. These striatal connectivity profiles endow us with a network account for individual differences in motivated behavior among older adults. More generally, the data suggest that capturing individual differences may be crucial to better understand developmental trajectories in motivated behavior.     

Measures of frontal functioning and the emergence of inhibitory control processes at 10 months of age

During the first year, infants begin to exhibit initial evidence of working memory and inhibitory control in conjunction with substantial maturation of the frontal cortex and corresponding neural circuitry. Currently, relatively little is known about the neural and autonomic resources that are recruited in response to increased executive demands during the first year of development. To this end, we recorded electroencephalogram (EEG; 6-9 Hz) and electrocardiogram from 10-month-olds during a working memory and inhibitory control task (looking A-not-B). Analyses compared measures of frontal functioning (EEG power, EEG coherence, heart rate) during nonreversal (working memory) and reversal (working memory+inhibitory control) trials. The increased cognitive demand of inhibitory control processing was associated with increases in heart rate and frontal coherence (medial frontal-lateral frontal, medial frontal-temporal, medial frontal-medial parietal, and medial frontal-occipital electrode pairs). Thus, synchronized activity across distributed cortical regions appeared to be essential to inhibitory control processes during infancy. The addition of inhibitory control processes, however, was not associated with any changes in neuronal activity (EEG power). These findings are discussed in relation to other neuroscience findings and provide insight into the development of integrated frontal functioning in infancy.     

Maternal parenting behavior and functional connectivity development in children: A longitudinal fMRI study

Parenting behavior is associated with internalizing symptoms in children, and cross-sectional research suggests that this association may be mediated by the influence of parenting on the development of frontoamygdala circuitry. However, longitudinal studies are lacking. Moreover, there is a paucity of studies that have investigated parenting and large-scale networks implicated in affective functioning. In this longitudinal study, data from 95 (52 female) children and their mothers were included. Children underwent magnetic resonance imaging that included a 6 min resting state sequence at wave 1 (mean age = 8.4 years) and wave 2 (mean age = 9.9 years). At wave 1, observational measures of positive and negative maternal behavior were collected during mother-child interactions. Region-of-interest analysis of the amygdala, and independent component and dual-regression analyses of the Default Mode Network (DMN), Executive Control Network (ECN) and the Salience Network (SN) were carried out. We identified developmental effects as a function of parenting: positive parenting was associated with decreased coactivation of the superior parietal lobule with the ECN at wave 2 compared to wave 1. Thus our findings provide preliminary longitudinal evidence that positive maternal behavior is associated with maturation of the connectivity between higher-order control networks.     

Neural processes of reward and punishment processing in childhood and adolescence: An event-related potential study on age differences

Reward and punishment processing are subject to substantial developmental changes during youth. However, little is known about the neurophysiological correlates that are associated with these developmental changes, particularly with regard to both anticipatory and outcome processing stages. Thus, the aim of this study was to address this research gap in a sample of typically developing children and adolescents.Fifty-four children and adolescents (8–18 years) performed a Monetary Incentive Delay Task comprising a monetary reward and punishment condition. Using event-related brain potential recordings, the cue-P3 and the stimulus-preceding negativity (SPN) were analyzed during the anticipation phase, while the Reward Positivity and the feedback-P3 were analyzed during the outcome phase.When anticipating monetary loss or no gain, SPN amplitude in the right hemisphere decreased with age. Moreover, exploratory analyses revealed a decrease in feedback-P3 amplitudes in response to monetary loss with increasing age. No other group differences were observed.Age-related changes in the SPN and fP3 component suggest that sensitivity to negative outcomes decreases from childhood to late adolescence, supporting the notion that adolescence is associated with reduced harm-avoidance. Longitudinal research including young adults is needed to substantiate our findings and its clinical implications regarding disturbed developmental trajectories in psychiatric populations.     

An fMRI study of sex differences in brain activation during object naming

We present a neuroimaging experiment that examines whether males and females use distinct brain systems while performing a confrontational naming task, with specific attention to the possibility of laterality differences, as suggested by some theories of sex differences in language processing. We further address whether sex-based differences in functional brain organization might interact with object category distinctions, given that previous behavioral studies have shown some consistent processing differences between the sexes with respect to tools versus plants. Functional magnetic resonance imaging (fMRI) data were collected from 26 participants (13 males and 13 females). Main effect and interaction analyses reveal no discernable laterality differences between the sexes. All other results, however, were consistent with previous object-naming studies. Global effects revealed dominant foci in fusiform gyrus, left posterior middle temporal gyrus, left basal ganglia/thalamus, left middle/inferior frontal gyri, left frontal operculum, left supplementary motor area/dorsal anterior cingulate, and left pre-central gyrus. Main contrasts for tools versus plants were likewise consistent with previous fMRI studies. Although men and women showed no discernable activation differences, hemispheric or otherwise, when collapsed across object categories, sex-by-category analyses showed selective activation for females in dorsal anterior cingulate gyrus and left posterior middle temporal gyrus for tools, and selective activation for males in left posterior middle temporal gyrus for plants. We discuss the relevance of these sex-by-category effects to previous behavioral findings and theories that relate to vocabulary differences between the sexes.     

Maltreatment and brain development: The effects of abuse and neglect on longitudinal trajectories of neural activation during risk processing and cognitive control

The profound effects of child maltreatment on brain functioning have been documented. Yet, little is known about whether distinct maltreatment experiences are differentially related to underlying neural processes of risky decision making: valuation and control. Using conditional growth curve modeling, we compared a cumulative approach versus a dimensional approach (relative effects of abuse and neglect) to examine the link between child maltreatment and brain development. The sample included 167 adolescents (13–14 years at Time 1, 53 % male), assessed annually four times. Risk processing was assessed by blood-oxygen-level-dependent responses (BOLD) during a lottery choice task, and cognitive control by BOLD responses during the Multi-Source Interference Task. Cumulative maltreatment effects on insula and dorsolateral anterior cingulate cortex (dACC) activation during risk processing were not significant. However, neglect (but not abuse) was associated with slower developmental increases in insula and dACC activation. In contrast, cumulative maltreatment effects on fronto-parietal activation during cognitive control were significant, and abuse (but not neglect) was associated with steeper developmental decreases in fronto-parietal activation. The results suggest neglect effects on detrimental neurodevelopment of the valuation system and abuse effects on accelerated neurodevelopment of the control system, highlighting differential effects of distinct neglect versus abuse adverse experiences on neurodevelopment.     

Adolescent harm avoidance as a longitudinal predictor of maladaptive cognitive emotion regulation in adulthood: The mediating role of inhibitory control

The current study investigates the effect of adolescent harm avoidance (HA) on maladaptive cognitive emotion regulation strategies (mCER) in early adulthood. The mediating role of inhibitory control and the moderating effect of gender on this link were also examined. Longitudinal data from 261 adolescents (147 female) were collected in three phases (T0, T1 and T2) over approximately 10 years. Results revealed that, after controlling for HA in adulthood (T2), female adolescents' HA (T0) significantly predicted mCER strategies after 10 years (T2), whereas male adolescents' HA only predicted catastrophizing. In addition, attentional impulsivity (T1) significantly mediated the relation between HA and mCER, though only among women. There was no significant indirect effect for emotional interference and stop-signal reaction time. Results revealed gender and measure specific associations between HA and inhibitory control and suggest that HA could induce inhibitory deficits leading to mCER.     

Temporal discounting for self and friends in adolescence: A fMRI study

Adolescence is characterized by impulsivity but also by increased importance of friendships. This study took the novel perspective of testing temporal discounting in a fMRI task where choices could affect outcomes for 96 adolescents (aged 10–20-years) themselves and their best friend. Decisions either benefitted themselves (i.e., the Self Immediate – Self Delay’ condition) or their friend (i.e., ‘Friend Immediate – Friend Delay’ condition); or juxtaposed rewards for themselves and their friends (i.e., the ‘Self Immediate – Friend Delay’ or ‘Friend Immediate – Self Delay’ conditions). We observed that younger adolescents were more impulsive; and all participants were more impulsive when this was associated with an immediate benefit for friends. Individual differences analyses revealed increased activity in the subgenual anterior cingulate cortex extending in the ventral striatum for immediate relative to delayed reward choices for self. Temporal choices were associated with activity in the prefrontal cortex, parietal cortex, insula, and ventral striatum, but only activity in the right inferior parietal lobe was associated with age. Finally, temporal delay choices for friends relative to self were associated with increased activity in the temporo-parietal junction and precuneus. Overall, this study shows a unique role of the social context in adolescents’ temporal decision making.     

Enhanced reward sensitivity and decreased loss sensitivity in Internet addicts: An fMRI study during a guessing task

As the world’s fastest growing “addiction”, Internet addiction should be studied to unravel the potential heterogeneity. The present study is set to examine reward and punishment processing in Internet addicts as compared to healthy controls while they subjectively experience monetary gain and loss during the performance of a guessing task. The results showed that Internet addicts associated with increased activation in orbitofrontal cortex in gain trials and decreased anterior cingulate activation in loss trials than normal controls. The results suggested that Internet addicts have enhanced reward sensitivity and decreased loss sensitivity than normal comparisons.