Goal-directed learning in adolescence: neurocognitive development and contextual influences.

Adolescence is a time during which we transition to independence, explore new activities and begin pursuit of major life goals. Goal-directed learning, in which we learn to perform actions that enable us to obtain desired outcomes, is central to many of these processes. Currently, our understanding of goal-directed learning in adolescence is itself in a state of transition, with the scientific community grappling with inconsistent results. When we examine metrics of goal-directed learning through the second decade of life, we find that many studies agree there are steady gains in performance in the teenage years, but others report that adolescent goal-directed learning is already adult-like, and some find adolescents can outperform adults. To explain the current variability in results, sophisticated experimental designs are being applied to test learning in different contexts. There is also increasing recognition that individuals of different ages and in different states will draw on different neurocognitive systems to support goal-directed learning. Through adoption of more nuanced approaches, we can be better prepared to recognize and harness adolescent strengths and to decipher the purpose (or goals) of adolescence itself.

Fluency generating emotion words correlates with verbal measures but not emotion regulation, alexithymia, or depressive symptoms.

How do you feel? To answer this question, one must first think of potential emotion words before choosing the best fit. However, we have little insight into how the ability to rapidly bring to mind emotion words-emotion fluency-relates to emotion functioning or general verbal abilities. In this study, we measured emotion fluency by counting how many emotion words participants could generate in 60 s. Participants (N = 151 in 2011-2012) also completed a behavioral measure of verbal fluency (i.e., how many words starting with "P" or "J" participants could produce in 60 s), a cognitive reappraisal emotion regulation task, and emotion functioning questionnaires. In preregistered analyses, we found that participants produced more negative emotion words than positive words and more positive words than neutral words in the emotion fluency task. As hypothesized, emotion fluency was positively related to verbal fluency, but contrary to hypotheses, emotion fluency was not related to self-reported or task-based emotion functioning (e.g., alexithymia, depression, and emotion regulation ability). As such, in community samples, emotion fluency may reflect general cognitive abilities rather than processes crucial to emotional well-being. While emotion fluency as measured here does not track indices of well-being, future research is needed to investigate potential contexts in which verbal fluency for emotion words may be key to emotion regulation. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Information about others' choices selectively alters risk tolerance and medial prefrontal cortex activation across adolescence and young adulthood.

Adolescence is associated with major changes in the cognitive, emotional and social domains. One domain in which these processes intersect is decision-making. Previous research has shown that individuals' attitudes towards risk and ambiguity shape their decision-making, and information about others' choices can influence individuals' decisions. However, it is currently unknown how information about others' choices influences risk and ambiguity attitudes separately, and the degree to which others' choices shape decision-making differentially across development from adolescence to young adulthood. The current study used a computational modeling framework to test how information about others' choices influences these attitudes. Participants, aged 14-22 years, made a series of risky and ambiguous choices while undergoing fMRI scanning. On some trials, they viewed risky or safe choices of others. Results showed that participants aligned their choices toward the choice preferences of others. Moreover, the tendency to align choices was expressed in changes in risk attitude, but not ambiguity attitude. The change in risk attitude was positively related to neural activation in the medial prefrontal cortex. Results did not show age related differences in behavior and corresponding neural activation, indicating that the manner in which adolescents are influenced by peers is not ubiquitous but rather, is highly context-dependent.

History of conditioned reward association disrupts inhibitory control: an examination of neural correlates.

The neural processes that support inhibitory control in the face of stimuli with a history of reward association are not yet well understood. Yet, the ability to flexibly adapt behavior to changing reward-contingency contexts is important for daily functioning and warrants further investigation. This study aimed to characterize neural and behavioral impacts of stimuli with a history of conditioned reward association on motor inhibitory control in healthy young adults by investigating group-level effects as well as individual variation in the ability to inhibit responses to stimuli with a reward history. Participants (N = 41) first completed a reward conditioning phase, during which responses to rewarded stimuli were associated with money and responses to unrewarded stimuli were not. Rewarded and unrewarded stimuli from training were carried forward as No-Go targets in a subsequent go/no-go task to test the effect of reward history on inhibitory control. Participants underwent functional brain imaging during the go/no-go portion of the task. On average, a history of reward conditioning disrupted inhibitory control. Compared to inhibition of responses to stimuli with no reward history, trials that required inhibition of responses to previously rewarded stimuli were associated with greater activity in frontal and striatal regions, including the inferior frontal gyrus, insula, striatum, and thalamus. Activity in the insula and thalamus during false alarms and in the ventromedial prefrontal cortex during correctly withheld trials predicted behavioral performance on the task. Overall, these results suggest that reward history serves to disrupt inhibitory control and provide evidence for diverging roles of the insula and ventromedial prefrontal cortex while inhibiting responses to stimuli with a reward history.

Examining cognitive control and reward interactions in adolescent externalizing symptoms.

During adolescence, rapid development and reorganization of the dopaminergic system supports increasingly sophisticated reward learning and the ability to exert behavioral control. Disruptions in the ability to exert control over previously rewarded behavior may underlie some forms of adolescent psychopathology. Specifically, symptoms of externalizing psychopathology may be associated with difficulties in flexibly adapting behavior in the context of reward. However, the direct interaction of cognitive control and reward learning in adolescent psychopathology symptoms has not yet been investigated. The present study used a Research Domain Criteria framework to investigate whether behavioral and neuronal indices of inhibition to previously rewarded stimuli underlie individual differences in externalizing symptoms in N = 61 typically developing adolescents. Using a task that integrates the Monetary Incentive Delay and Go-No-Go paradigms, we observed a positive association between externalizing symptoms and activation of the left middle frontal gyrus during response inhibition to cues with a history of reward. These associations were robust to controls for internalizing symptoms and neural recruitment during inhibition of cues with no reward history. Our findings suggest that inhibitory control over stimuli with a history of reward may be a useful marker for future inquiry into the development of externalizing psychopathology in adolescence.

Registration-free analysis of diffusion MRI tractography data across subjects through the human lifespan.

Diffusion MRI tractography produces massive sets of streamlines that need to be clustered into anatomically meaningful white-matter bundles. Conventional clustering techniques group streamlines based on their proximity in Euclidean space. We have developed AnatomiCuts, an unsupervised method for clustering tractography streamlines based on their neighboring anatomical structures, rather than their coordinates in Euclidean space. In this work, we show that the anatomical similarity metric used in AnatomiCuts can be extended to find corresponding clusters across subjects and across hemispheres, without inter-subject or inter-hemispheric registration. Our proposed approach enables group-wise tract cluster analysis, as well as studies of hemispheric asymmetry. We evaluate our approach on data from the pilot MGH-Harvard-USC Lifespan Human Connectome project, showing improved correspondence in tract clusters across 184 subjects aged 8-90. Our method shows up to 38% improvement in the overlap of corresponding clusters when comparing subjects with large age differences. The techniques presented here do not require registration to a template and can thus be applied to populations with large inter-subject variability, e.g., due to brain development, aging, or neurological disorders.

Stress impacts the fidelity but not strength of emotional memories.

Psychological stress during memory encoding influences resulting memory representations. However, open questions remain regarding how stress interacts with emotional memory. This interaction has mainly been studied by characterizing the correct identification of previously observed material (memory "hits"), with few studies investigating how stress influences the endorsement of unobserved material as remembered (memory "false alarms"). While hits can provide information about the presence or strength of a memory representation, false alarms provide insight into memory fidelity, indicating to what extent stored memories are confused with similar information presented at retrieval. This study examined the effects of stress on long-term memory for negative and neutral images, considering the separate contributions of hits and false alarms. Participants viewed images after repeated exposure to either a stress or a control manipulation. Stress impaired memory performance for negative pictures and enhanced memory performance for neutral pictures. These effects were driven by false alarms rather than hits: stressed participants false alarmed more often for negative and less often for neutral images. These data suggest that stress undermines the benefits of emotion on memory by changing individuals' susceptibility towards false alarms, and highlight the need to consider both memory strength and fidelity to characterize differences in memory performance.

Developmental patterns of change in the influence of safe and risky peer choices on risky decision-making.

Adolescents take more risks when peers monitor their behavior. However, it is largely unknown how different types of peer influence affect adolescent decision-making. In this study, we investigate how information about previous choices of peers differentially influences decision-making in adolescence and young adulthood. Participants (N = 99, age range 12-22) completed an economic choice task in which choice options were systematically varied on levels of risk and ambiguity. On each trial, participants selected between a safer choice (low variability in outcome) and a riskier choice (high variability in outcome). Participants made choices in three conditions: a solo condition in which they made choices with no additional information, a social condition in which they saw choices of supposed peers, and a computer condition in which they saw choices of a computer. Results showed that participants' choices conform to the choices made by the peers, but not a computer. Furthermore, when peers chose the safe option, late adolescents were especially likely to make a safe choice. Conversely, when the peer made a risky choice, late adolescents were least likely to follow choices made by the peer. We did not find evidence for differential influence of social information on decisions depending on their level of risk and ambiguity. These results show that information about previous decisions of peers are a powerful modifier for behavior and that the effect of peers on adolescents' decisions is less ubiquitous and more specific than previously assumed.

Development of Prefrontal Cortical Connectivity and the Enduring Effect of Learned Value on Cognitive Control.

Inhibitory control, the capacity to suppress an inappropriate response, is a process employed for guiding action selection in the service of goal-directed behavior. Under neutral circumstances, inhibitory control success improves from childhood to adulthood and has been associated with developmental shifts in functional activation and connectivity of the PFC. However, the ability to exercise inhibitory control is challenged in certain contexts by including appetitive cues, a phenomenon that may be particularly pronounced in youths. Here, we examine the magnitude and temporal persistence of learned value's influence on inhibitory control in a cross-sectional sample of 8- to 25-year-olds. Participants first underwent conditioning of a motor approach response to two initially neutral cues, with one cue reinforced with monetary reward and the other with no monetary outcome. Subsequently, during fMRI, participants reencountered these cues as no-go targets in a nonreinforced go/no-go paradigm. Although the influence of learned value increasingly disrupted inhibitory control with increasing age, in young adults this pattern remitted over the course of the task, whereas during adolescence the impairing effect of reward history persisted. Successful no-go performance to the previously rewarded target was related to greater recruitment of the right inferior frontal gyrus and age-related increase in functional connectivity between the inferior frontal gyrus and the ventromedial PFC for the previously rewarded no-go target over the control target. Together, results indicate the complex influence of value on goals over development relies upon the increased coordination of distinct higher-order regions in the PFC.

Adolescent Development of Value-Guided Goal Pursuit.

Adolescents are challenged to orchestrate goal-directed actions in increasingly independent and consequential ways. In doing so, it is advantageous to use information about value to select which goals to pursue and how much effort to devote to them. Here, we examine age-related changes in how individuals use value signals to orchestrate goal-directed behavior. Drawing on emerging literature on value-guided cognitive control and reinforcement learning, we demonstrate how value and task difficulty modulate the execution of goal-directed action in complex ways across development from childhood to adulthood. We propose that the scope of value-guided goal pursuit expands with age to include increasingly challenging cognitive demands, and scaffolds on the emergence of functional integration within brain networks supporting valuation, cognition, and action.

Dynamic Flexibility in Striatal-Cortical Circuits Supports Reinforcement Learning.

Complex learned behaviors must involve the integrated action of distributed brain circuits. Although the contributions of individual regions to learning have been extensively investigated, much less is known about how distributed brain networks orchestrate their activity over the course of learning. To address this gap, we used fMRI combined with tools from dynamic network neuroscience to obtain time-resolved descriptions of network coordination during reinforcement learning in humans. We found that learning to associate visual cues with reward involves dynamic changes in network coupling between the striatum and distributed brain regions, including visual, orbitofrontal, and ventromedial prefrontal cortex (n = 22; 13 females). Moreover, we found that this flexibility in striatal network coupling correlates with participants' learning rate and inverse temperature, two parameters derived from reinforcement learning models. Finally, we found that episodic learning, measured separately in the same participants at the same time, was related to dynamic connectivity in distinct brain networks. These results suggest that dynamic changes in striatal-centered networks provide a mechanism for information integration during reinforcement learning.SIGNIFICANCE STATEMENT Learning from the outcomes of actions, referred to as reinforcement learning, is an essential part of life. The roles of individual brain regions in reinforcement learning have been well characterized in terms of updating values for actions or cues. Missing from this account, however, is an understanding of how different brain areas interact during learning to integrate sensory and value information. Here we characterize flexible striatal-cortical network dynamics that relate to reinforcement learning behavior.

Consequences for peers differentially bias computations about risk across development.

Adolescents routinely take risks that impact the well-being of the friends they are with. However, it remains unclear when and how consequences for friends factor into decisions to take risks. Here we used an economic decision-making task to test whether risky choices are guided by the positive and negative consequences they promise for peers. Across a large developmental sample of participants ages 12-25, we show that risky decision computations increasingly assimilate friends' outcomes throughout adolescence into early adulthood in an asymmetric manner that overemphasizes protecting friends from incurring loss. Whereas adults accommodated friend outcomes to a greater degree when the friend was present and witnessing these choices, adolescents did so regardless of whether a friend could witness their decisions, highlighting the fundamentality of adolescent social motivations. By demonstrating that outcomes for another individual can powerfully tune an actor's risk tolerance, these results identify a key factor underlying peer-related motivations for risky behavior, with implications for the law and risk-prevention. (PsycINFO Database Record

An Upside to Reward Sensitivity: The Hippocampus Supports Enhanced Reinforcement Learning in Adolescence.

Adolescents are notorious for engaging in reward-seeking behaviors, a tendency attributed to heightened activity in the brain's reward systems during adolescence. It has been suggested that reward sensitivity in adolescence might be adaptive, but evidence of an adaptive role has been scarce. Using a probabilistic reinforcement learning task combined with reinforcement learning models and fMRI, we found that adolescents showed better reinforcement learning and a stronger link between reinforcement learning and episodic memory for rewarding outcomes. This behavioral benefit was related to heightened prediction error-related BOLD activity in the hippocampus and to stronger functional connectivity between the hippocampus and the striatum at the time of reinforcement. These findings reveal an important role for the hippocampus in reinforcement learning in adolescence and suggest that reward sensitivity in adolescence is related to adaptive differences in how adolescents learn from experience.

Transfer of learning relates to intrinsic connectivity between hippocampus, ventromedial prefrontal cortex, and large-scale networks.

An important aspect of adaptive learning is the ability to flexibly use past experiences to guide new decisions. When facing a new decision, some people automatically leverage previously learned associations, while others do not. This variability in transfer of learning across individuals has been demonstrated repeatedly and has important implications for understanding adaptive behavior, yet the source of these individual differences remains poorly understood. In particular, it is unknown why such variability in transfer emerges even among homogeneous groups of young healthy participants who do not vary on other learning-related measures. Here we hypothesized that individual differences in the transfer of learning could be related to relatively stable differences in intrinsic brain connectivity, which could constrain how individuals learn. To test this, we obtained a behavioral measure of memory-based transfer outside of the scanner and on a separate day acquired resting-state functional MRI images in 42 participants. We then analyzed connectivity across independent component analysis-derived brain networks during rest, and tested whether intrinsic connectivity in learning-related networks was associated with transfer. We found that individual differences in transfer were related to intrinsic connectivity between the hippocampus and the ventromedial prefrontal cortex, and between these regions and large-scale functional brain networks. Together, the findings demonstrate a novel role for intrinsic brain dynamics in flexible learning-guided behavior, both within a set of functionally specific regions known to be important for learning, as well as between these regions and the default and frontoparietal networks, which are thought to serve more general cognitive functions.

Probing behavioral responses to food: development of a food-specific go/no-go task.

The ability to exert self-control in the face of appetitive, alluring cues is a critical component of healthy development. The development of behavioral measures that use disease-relevant stimuli can greatly improve our understanding of cue-specific impairments in self-control. To produce such a tool relevant to the study of eating and weight disorders, we modified the traditional go/no-go task to include food and non-food targets. To confirm that performance on this new task was consistent with other go/no-go tasks, it was given to 147 healthy, normal weight volunteers between the ages of 5 and 30. High-resolution photos of food or toys were used as the target and nontarget stimuli. Consistent with expectations, overall improvements in accuracy were seen from childhood to adulthood. Participants responded more quickly and made more commission errors to food cues compared to nonfood cues (F(1,140)=21.76, P<0.001), although no behavioral differences were seen between low- and high-calorie food cues for this non-obese, healthy developmental sample. This novel food-specific go/no-go task may be used to track the development of self-control in the context of food cues and to evaluate deviations or deficits in the development of this ability in individuals at risk for eating problem behaviors and disorders.