Charles F. Geier

Immaturities in Reward Processing and Its Influence on Inhibitory Control in Adolescence

The nature of immature reward processing and the influence of rewards on basic elements of cognitive control during adolescence are currently not well understood. Here, during functional magnetic resonance imaging, healthy adolescents and adults performed a modified antisaccade task in which trial-by-trial reward contingencies were manipulated. The use of a novel fast, event-related design enabled developmental differences in brain function underlying temporally distinct stages of reward processing and response inhibition to be assessed. Reward trials compared with neutral trials resulted in faster correct inhibitory responses across ages and in fewer inhibitory errors in adolescents. During reward trials, the blood oxygen level–dependent signal was attenuated in the ventral striatum in adolescents during cue assessment, then overactive during response preparation, suggesting limitations during adolescence in reward assessment and heightened reactivity in anticipation of reward compared with adults. Importantly, heightened activity in the frontal cortex along the precentral sulcus was also observed in adolescents during reward-trial response preparation, suggesting reward modulation of oculomotor control regions supporting correct inhibitory responding. Collectively, this work characterizes specific immaturities in adolescent brain systems that support reward processing and describes the influence of reward on inhibitory control. In sum, our findings suggest mechanisms that may underlie adolescents’ vulnerability to poor decision-making and risk-taking behavior.

Development of eye-movement control

Cognitive control of behavior continues to improve through adolescence in parallel with important brain maturational processes including synaptic pruning and myelination, which allow for efficient neuronal computations and the functional integration of widely distributed circuitries supporting top-down control of behavior. This is also a time when psychiatric disorders, such as schizophrenia and mood disorders, emerge reflecting a particularly vulnerability to impairments in development during adolescence. Oculomotor studies provide a unique neuroscientific approach to make precise associations between cognitive control and brain circuitry during development that can inform us of impaired systems in psychopathology. In this review, we first describe the development of pursuit, fixation, and visually-guided saccadic eye movements, which collectively indicate early maturation of basic sensorimotor processes supporting reflexive, exogenously-driven eye movements. We then describe the literature on the development of the cognitive control of eye movements as reflected in the ability to inhibit a prepotent eye movement in the antisaccade task, as well as making an eye movement guided by on-line spatial information in working memory in the oculomotor delayed response task. Results indicate that the ability to make eye movements in a voluntary fashion driven by endogenous plans shows a protracted development into adolescence. Characterizing the transition through adolescence to adult-level cognitive control of behavior can inform models aimed at understanding the neurodevelopmental basis of psychiatric disorders.

Development of Working Memory Maintenance

The neural circuitry supporting mature visual spatial working memory (VSWM) has been well delineated in nonhuman primates and in human adults. However, we still have limited understanding about developmental change through adolescence in this network. We present results from a fast event-related functional MRI (fMRI) study aimed at characterizing developmental changes in brain mechanisms supporting VSWM across different delay periods. Forty-three healthy subjects (17 adults, 18-30 yr; 13 adolescents, 13-17 yr; 13 children, 8-12 yr) were scanned as they performed an oculomotor delayed response (ODR) task with short (2.5 s) and long (10 s) delay period trials. Results showed that all age groups recruited a common network of regions to support both delay trials, including frontal, parietal, and temporal regions, indicative of a core circuitry needed to perform the task. Several age-related differences were found in the recruitment of regions, supporting short delay trials, including fronto-caudal areas, which could contribute to known differences in initial memory-guided saccade precision. To support extended delay trials, adults primarily recruited additional posterior parietal cortex (PPC), whereas children and adolescents recruited a considerably more extensive distributed circuitry. Our findings indicate that brain processes supporting basic aspects of working memory across cortex are established by childhood. We also find evidence for continued immaturities in systems supporting working memory precision, reflected by differences in the circuitry recruited by children and by continued refinement of fronto-insular-temporal regions recruited by adolescents. Taken together, these results suggest distinct developmental changes in the circuitry supporting visual spatial working memory.

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

ABSTRACT 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.

Adolescent brain maturation and smoking: what we know and where we're headed.

Smoking is a leading cause of mortality and morbidity worldwide. Smoking initiation often occurs during adolescence. This paper reviews and synthesizes adolescent development and nicotine dependence literatures to provide an account of adolescent smoking from onset to compulsive use. We extend neurobiological models of adolescent risk-taking, that focus on the interplay between incentive processing and cognitive control brain systems, through incorporating psychosocial and contextual factors specific to smoking, to suggest that adolescents are more vulnerable than adults to cigarette use generally, but that individual differences exist placing some adolescents at increased risk for smoking. Upon smoking, adolescents are more likely to continue smoking due to the increased positive effects induced by nicotine during this period. Continued use during adolescence, may be best understood as reflecting drug-related changes to neural systems underlying incentive processing and cognitive control, resulting in decision-making that is biased towards continued smoking. Persistent changes following nicotine exposure that may underlie continued dependence are described. We highlight ways that interventions may benefit from a consideration of cognitive-neuroscience findings.

Dissociated Effects of Anticipating Smoking versus Monetary Reward in the Caudate as a Function of Smoking Abstinence

BACKGROUND Theories of addiction suggest that chronic smoking may be associated with both hypersensitivity to smoking and related cues and hyposensitivity to alternative reinforcers. However, neural responses to smoking and nonsmoking rewards are rarely evaluated within the same paradigm, leaving the extent to which both processes operate simultaneously uncertain. Behavioral evidence and theoretical models suggest that dysregulated reward processing may be more pronounced during deprivation from nicotine, but neuroimaging evidence on the effects of deprivation on reward processing is limited. The current study examined the impact of deprivation from smoking on neural processing of both smoking and monetary rewards. METHODS Two separate functional magnetic resonance imaging scans were performed in 38 daily smokers, one after smoking without restriction and one following 24 hours of abstinence. A rewarded guessing task was conducted during each scan to evaluate striatal blood oxygen level-dependent response during anticipation of both smoking and monetary rewards. RESULTS A significant reward type by abstinence interaction was observed in the bilateral caudate and medial prefrontal cortex during reward anticipation. The blood oxygen level-dependent response to anticipation of smoking reward was significantly higher and anticipation of monetary rewards was significantly lower during abstinence compared with nonabstinence. Attenuation of monetary reward-related activation during abstinence was significantly correlated with abstinence-induced increases in craving and withdrawal. CONCLUSIONS These results provide the first direct evidence of dissociated effects of smoking versus monetary rewards as a function of abstinence. The findings suggest an important neural pathway that may underlie the choice to smoke in lieu of alternative reinforcement during a quit attempt.

Developmental Effects of Incentives on Response Inhibition

Inhibitory control and incentive processes underlie decision making, yet few studies have explicitly examined their interaction across development. Here, the effects of potential rewards and losses on inhibitory control in 64 adolescents (13- to 17-year-olds) and 42 young adults (18- to 29-year-olds) were examined using an incentivized antisaccade task. Notably, measures were implemented to minimize age-related differences in reward valuation and potentially confounding motivation effects. Incentives affected antisaccade metrics differently across the age groups. Younger adolescents generated more errors than adults on reward trials, but all groups performed well on loss trials. Adolescent saccade latencies also differed from adults across the range of reward trials. Overall, results suggest persistent immaturities in the integration of reward and inhibitory control processes across adolescence.

Methodological approaches in developmental neuroimaging studies

Pediatric neuroimaging is increasingly providing insights into the neural basis of cognitive development. Indeed, we have now arrived at a stage where we can begin to identify optimal methodological and statistical approaches to the acquisition and analysis of developmental imaging data. In this article, we describe a number of these approaches and how their selection impacts the ability to examine and interpret developmental effects. We describe preferred approaches to task selection, definition of age groups, selection of fMRI designs, definition of regions of interest (ROI), optimal baseline measures, and treatment of timecourse data. Consideration of these aspects of developmental neuroimaging reveals that unlike single‐group neuroimaging studies, developmental studies pose unique challenges that impact study planning, task design, data analysis, and the interpretation of findings. Hum Brain Mapp , 2010.

Effects of incentives, age, and behavior on brain activation during inhibitory control: a longitudinal fMRI study.

Highlights • Reward-modulated cognitive control is supported by amygdalar incentive processing.• NAcc activation supports inhibitory control in youths.• NAcc activation hinders inhibitory control in adults.

The Teenage Brain Cognitive Control and Motivation

Adolescence is associated with heightened mortality rates due in large measure to negative consequences from risky behaviors. Theories of adolescent risk taking posit that it is driven by immature cognitive control coupled with heightened reward reactivity, yet surprisingly few empirical studies have examined these neurobiological systems together. In this article, we describe a series of studies from our laboratory aimed at further delineating the maturation of cognitive control through adolescence, as well as how rewards influence a key aspect of cognitive control: response inhibition. Our findings indicate that adolescents can exert adult-like control over their behavior but that they have limitations regarding the consistency with which they can generate optimal responses compared with adults. Moreover, we demonstrate that the brain circuitry supporting mature cognitive (inhibitory) control is still undergoing development. Our work using the rewarded antisaccade task, a paradigm that enables concurrent assessment of rewards and inhibitory control, indicates that adolescents show delayed but heightened responses in key reward regions along with concurrent activation in brain systems that support behaviors leading to reward acquisition. Considered together, our results highlight adolescent-specific differences in the integration of basic brain processes that may underlie decision making and more complex risk taking in adolescence.