Dorsal Anterior Cingulate Cortex Encodes the Integrated Incentive Motivational Value of Cognitive Task Performance.

Humans can seamlessly combine value signals from diverse motivational incentives, yet it is not well understood how these signals are "bundled" in the brain to modulate cognitive control. The dorsal ACC (dACC) is theorized to integrate motivational value dimensions in the service of goal-directed action, although this hypothesis has yet to receive rigorous confirmation. In the present study, we examined the role of human dACC in motivational incentive integration. Healthy young adult men and women were scanned with fMRI while engaged in an experimental paradigm that quantifies the combined effects of liquid (e.g., juice, neutral, saltwater) and monetary incentives on cognitive task performance. Monetary incentives modulated trial-by-trial dACC activation, whereas block-related effects of liquid incentives on dACC activity were observed. When bundled together, incentive-related dACC modulation predicted fluctuations in both cognitive performance and self-report motivation ratings. Statistical mediation analyses suggest that dACC encoded the incentives in terms of their integrated subjective motivational value, and that this value signal was most proximally associated with task performance. Finally, we confirmed that these incentive integration effects were selectively present in dACC. Together, the results support an account in which dACC integrates motivational signals to compute the expected value of goal-directed cognitive control.SIGNIFICANCE STATEMENT How are primary and secondary incentives integrated in the brain to influence goal-directed behavior? Using an innovative experimental fMRI paradigm that combines motivational incentives that have historically been studied independently between species (e.g., monetary rewards for humans, food rewards for animals), we examine the relationship between incentive motivational value and cognitive control allocation. We find evidence that the integrated incentive motivational value of combined incentives is encoded in human dorsal ACC. Further, self-reported motivational shifts mediated the effects of incentive-modulated dorsal ACC activity on task performance, revealing convergence in how self-reported and experimentally induced motivation are encoded in the human brain. Our findings may inform future translational studies examining affective/motivational and cognitive impairments in psychopathology (e.g., anxiety, depression, addiction).

Distinct Neural Profiles of Frontoparietal Networks in Boys with ADHD and Boys with Persistent Depressive Disorder.

Working memory deficits are common in attention-deficit/hyperactivity disorder (ADHD) and depression-two common neurodevelopmental disorders with overlapping cognitive profiles but distinct clinical presentation. Multivariate techniques have previously been utilized to understand working memory processes in functional brain networks in healthy adults but have not yet been applied to investigate how working memory processes within the same networks differ within typical and atypical developing populations. We used multivariate pattern analysis (MVPA) to identify whether brain networks discriminated between spatial versus verbal working memory processes in ADHD and Persistent Depressive Disorder (PDD). Thirty-six male clinical participants and 19 typically developing (TD) boys participated in a fMRI scan while completing a verbal and a spatial working memory task. Within a priori functional brain networks (frontoparietal, default mode, salience), the TD group demonstrated differential response patterns to verbal and spatial working memory. The PDD group showed weaker differentiation than TD, with lower classification accuracies observed in primarily the left frontoparietal network. The neural profiles of the ADHD and PDD differed specifically in the SN where the ADHD group's neural profile suggests significantly less specificity in neural representations of spatial and verbal working memory. We highlight within-group classification as an innovative tool for understanding the neural mechanisms of how cognitive processes may deviate in clinical disorders, an important intermediary step towards improving translational psychiatry.

Dissociable influences of reward and punishment on adaptive cognitive control.

To invest effort into any cognitive task, people must be sufficiently motivated. Whereas prior research has focused primarily on how the cognitive control required to complete these tasks is motivated by the potential rewards for success, it is also known that control investment can be equally motivated by the potential negative consequence for failure. Previous theoretical and experimental work has yet to examine how positive and negative incentives differentially influence the manner and intensity with which people allocate control. Here, we develop and test a normative model of control allocation under conditions of varying positive and negative performance incentives. Our model predicts, and our empirical findings confirm, that rewards for success and punishment for failure should differentially influence adjustments to the evidence accumulation rate versus response threshold, respectively. This dissociation further enabled us to infer how motivated a given person was by the consequences of success versus failure.

Age-Related Differences in Motivational Integration and Cognitive Control.

Motivational incentives play an influential role in value-based decision-making and cognitive control. A compelling hypothesis in the literature suggests that the motivational value of diverse incentives are integrated in the brain into a common currency value signal that influences decision-making and behavior. To investigate whether motivational integration processes change during healthy aging, we tested older (N = 44) and younger (N = 54) adults in an innovative incentive integration task paradigm that establishes dissociable and additive effects of liquid (e.g., juice, neutral, saltwater) and monetary incentives on cognitive task performance. The results reveal that motivational incentives improve cognitive task performance in both older and younger adults, providing novel evidence demonstrating that age-related cognitive control deficits can be ameliorated with sufficient incentive motivation. Additional analyses revealed clear age-related differences in motivational integration. Younger adult task performance was modulated by both monetary and liquid incentives, whereas monetary reward effects were more gradual in older adults and more strongly impacted by trial-by-trial performance feedback. A surprising discovery was that older adults shifted attention from liquid valence toward monetary reward throughout task performance, but younger adults shifted attention from monetary reward toward integrating both monetary reward and liquid valence by the end of the task, suggesting differential strategic utilization of incentives. These data suggest that older adults may have impairments in incentive integration and employ different motivational strategies to improve cognitive task performance. The findings suggest potential candidate neural mechanisms that may serve as the locus of age-related change, providing targets for future cognitive neuroscience investigations.

Optimal behavioral hierarchy.

Human behavior has long been recognized to display hierarchical structure: actions fit together into subtasks, which cohere into extended goal-directed activities. Arranging actions hierarchically has well established benefits, allowing behaviors to be represented efficiently by the brain, and allowing solutions to new tasks to be discovered easily. However, these payoffs depend on the particular way in which actions are organized into a hierarchy, the specific way in which tasks are carved up into subtasks. We provide a mathematical account for what makes some hierarchies better than others, an account that allows an optimal hierarchy to be identified for any set of tasks. We then present results from four behavioral experiments, suggesting that human learners spontaneously discover optimal action hierarchies.

Motivational context determines the impact of aversive outcomes on mental effort allocation.

It is well known that people will exert effort on a task if sufficiently motivated, but how they distribute these efforts across different strategies (e.g., efficiency vs. caution) remains uncertain. Past work has shown that people invest effort differently for potential positive outcomes (rewards) versus potential negative outcomes (penalties). However, this research failed to account for differences in the context in which negative outcomes motivate someone - either as punishment or reinforcement. It is therefore unclear whether effort profiles differ as a function of outcome valence, motivational context, or both. Using computational modeling and our novel Multi-Incentive Control Task, we show that the influence of aversive outcomes on one's effort profile is entirely determined by their motivational context. Participants (N:91) favored increased caution in response to larger penalties for incorrect responses, and favored increased efficiency in response to larger reinforcement for correct responses, whether positively or negatively incentivized.

An fMRI protocol for administering liquid incentives to human participants.

This protocol describes the materials and approaches for administering liquid incentives to human participants during fMRI scanning. We first describe preparation of the liquid solutions (e.g., neutral solution and saltwater) and liquid delivery setups. We then detail steps to connect the setups to the computer-controlled syringe pump in the MRI control room, followed by procedures for testing the syringe pump dispensing a liquid bolus during the task. Description of custom software and required adapters for implementing the liquid setup are included. For complete details on the use and execution of this protocol, please refer to Yee et al. (2021).

Aversive motivation and cognitive control.

Aversive motivation plays a prominent role in driving individuals to exert cognitive control. However, the complexity of behavioral responses attributed to aversive incentives creates significant challenges for developing a clear understanding of the neural mechanisms of this motivation-control interaction. We review the animal learning, systems neuroscience, and computational literatures to highlight the importance of experimental paradigms that incorporate both motivational context manipulations and mixed motivational components (e.g., bundling of appetitive and aversive incentives). Specifically, we postulate that to understand aversive incentive effects on cognitive control allocation, a critical contextual factor is whether such incentives are associated with negative reinforcement or punishment. We further illustrate how the inclusion of mixed motivational components in experimental paradigms enables increased precision in the measurement of aversive influences on cognitive control. A sharpened experimental and theoretical focus regarding the manipulation and assessment of distinct motivational dimensions promises to advance understanding of the neural, monoaminergic, and computational mechanisms that underlie the interaction of motivation and cognitive control.

Dissociable Effects of Monetary, Liquid, and Social Incentives on Motivation and Cognitive Control.

Humans are social creatures and, as such, can be motivated by aspects of social life (e.g., approval from others) to guide decision-making in everyday contexts. Indeed, a common view is that people may have stronger orientation toward social goals or incentives relative to other incentive modalities, such as food or money. However, current studies have only rarely addressed how social incentives compare to other types of rewards in motivating goal-directed behavior. The current study tested this claim; across two separate experiments, the effects of liquid and social incentives were compared in terms of their subsequent impact on task performance and self-reported affect and motivation. Critically, valenced social incentives offered both ecological validity (short video clips-Experiment 1) and continuity with prior stimuli used in the social reward and motivation literature (static images-Experiment 2) when examining their effect on behavior. Across both studies, the results replicate and extend prior work, demonstrating robust effects of liquid incentives on task performance and self-reported affect and motivation, while also supporting an interpretation of weaker motivational and affective effects for social incentives. These patterns of results highlight the complex and wide-ranging effects of social incentives and call into question the effectiveness of social incentives, relative to other incentive modalities, in motivating behavior.

Interactions of Motivation and Cognitive Control.

There is general agreement that both motivation and cognitive control play critical roles in shaping goal-directed behavior, but only recently has scientific interest focused around the question of motivation-control interactions. Here we briefly survey this literature, organizing contemporary findings around three issues: 1) whether motivation preferentially impacts cognitive control processes, 2) the neural mechanisms that underlie motivation-cognition interactions, and 3) why motivation might be relevant for overcoming the costs of control. Dopamine (DA) is discussed as a key neuromodulator in these motivation-cognition interactions. We conclude by highlighting open issues, specifically Pavlovian versus instrumental control distinctions and effects of motivational valence and conflict, which could benefit from future research attention.

Humans Integrate Monetary and Liquid Incentives to Motivate Cognitive Task Performance.

It is unequivocal that a wide variety of incentives can motivate behavior. However, few studies have explicitly examined whether and how different incentives are integrated in terms of their motivational influence. The current study examines the combined effects of monetary and liquid incentives on cognitive processing, and whether appetitive and aversive incentives have distinct influences. We introduce a novel task paradigm, in which participants perform cued task-switching for monetary rewards that vary parametrically across trials, with liquid incentives serving as post-trial performance feedback. Critically, the symbolic meaning of the liquid was held constant (indicating successful reward attainment), while liquid valence was blocked. In the first experiment, monetary rewards combined additively with appetitive liquid feedback to improve subject task performance. Aversive liquid feedback counteracted monetary reward effects in low monetary reward trials, particularly in a subset of participants who tended to avoid responding under these conditions. Self-report motivation ratings predicted behavioral performance above and beyond experimental effects. A follow-up experiment replicated the predictive power of motivation ratings even when only appetitive liquids were used, suggesting that ratings reflect idiosyncratic subjective values of, rather than categorical differences between, the liquid incentives. Together, the findings indicate an integrative relationship between primary and secondary incentives and potentially dissociable influences in modulating motivational value, while informing hypotheses regarding candidate neural mechanisms.

Neural correlates of letter reversal in children and adults.

Children often make letter reversal errors when first learning to read and write, even for letters whose reversed forms do not appear in normal print. However, the brain basis of such letter reversal in children learning to read is unknown. The present study compared the neuroanatomical correlates (via functional magnetic resonance imaging) and the electrophysiological correlates (via event-related potentials or ERPs) of this phenomenon in children, ages 5-12, relative to young adults. When viewing reversed letters relative to typically oriented letters, adults exhibited widespread occipital, parietal, and temporal lobe activations, including activation in the functionally localized visual word form area (VWFA) in left occipito-temporal cortex. Adults exhibited significantly greater activation than children in all of these regions; children only exhibited such activation in a limited frontal region. Similarly, on the P1 and N170 ERP components, adults exhibited significantly greater differences between typical and reversed letters than children, who failed to exhibit significant differences between typical and reversed letters. These findings indicate that adults distinguish typical and reversed letters in the early stages of specialized brain processing of print, but that children do not recognize this distinction during the early stages of processing. Specialized brain processes responsible for early stages of letter perception that distinguish between typical and reversed letters may develop slowly and remain immature even in older children who no longer produce letter reversals in their writing.