Christopher H. Chatham

A unified framework for inhibitory control

Inhibiting unwanted thoughts, actions and emotions figures centrally in daily life, and the prefrontal cortex (PFC) is widely viewed as a source of this inhibitory control. We argue that the function of the PFC is best understood in terms of representing and actively maintaining abstract information, such as goals, which produces two types of inhibitory effects on other brain regions. Inhibition of some subcortical regions takes a directed global form, with prefrontal regions providing contextual information relevant to when to inhibit all processing in a region. Inhibition within neocortical (and some subcortical) regions takes an indirect competitive form, with prefrontal regions providing excitation of goal-relevant options. These distinctions are crucial for understanding the mechanisms of inhibition and how they can be impaired or improved.

Developing Cognitive Control Three Key Transitions

The ability to flexibly break out of routine behaviors develops gradually and is essential for success in life. In this article, we discuss three key developmental transitions toward more flexible behavior. First, children develop an increasing ability to overcome habits by engaging cognitive control in response to environmental signals. Second, children shift from recruiting cognitive control reactively, as needed in the moment, to recruiting cognitive control proactively, in preparation for needing it. Third, children shift from relying on environmental signals for engaging cognitive control to becoming more self-directed. All three transitions can be understood in terms of the development of increasingly active and abstract goal representations in the prefrontal cortex.

Pupillometric and behavioral markers of a developmental shift in the temporal dynamics of cognitive control.

The capacity to anticipate and prepare for future events is thought to be critical for cognitive control. Dominant accounts of cognitive control treat the developing system as merely a weaker version of the adult system, progressively strengthening over time. Using the AX Continuous Performance Task (AX-CPT) in combination with high-resolution pupillometry, we find that whereas 8-year-old children resemble adults in their proactive use of cognitive control, 3.5-year-old children exhibit a qualitatively different, reactive form of cognitive control, responding to events only as they unfold and retrieving information from memory as needed in the moment. These results demonstrate the need to reconsider the origins of cognitive control and the basis for childrens behaviors across domains.

Cognitive control reflects context monitoring, not motoric stopping, in response inhibition.

The inhibition of unwanted behaviors is considered an effortful and controlled ability. However, inhibition also requires the detection of contexts indicating that old behaviors may be inappropriate – in other words, inhibition requires the ability to monitor context in the service of goals, which we refer to as context-monitoring. Using behavioral, neuroimaging, electrophysiological and computational approaches, we tested whether motoric stopping per se is the cognitively-controlled process supporting response inhibition, or whether context-monitoring may fill this role. Our results demonstrate that inhibition does not require control mechanisms beyond those involved in context-monitoring, and that such control mechanisms are the same regardless of stopping demands. These results challenge dominant accounts of inhibitory control, which posit that motoric stopping is the cognitively-controlled process of response inhibition, and clarify emerging debates on the frontal substrates of response inhibition by replacing the centrality of controlled mechanisms for motoric stopping with context-monitoring.

From an executive network to executive control: A computational model of the n-back task

A paradigmatic test of executive control, the n-back task, is known to recruit a widely distributed parietal, frontal, and striatal “executive network,” and is thought to require an equally wide array of executive functions. The mapping of functions onto substrates in such a complex task presents a significant challenge to any theoretical framework for executive control. To address this challenge, we developed a biologically constrained model of the n-back task that emergently develops the ability to appropriately gate, bind, and maintain information in working memory in the course of learning to perform the task. Furthermore, the model is sensitive to proactive interference in ways that match findings from neuroimaging and shows a U-shaped performance curve after manipulation of prefrontal dopaminergic mechanisms similar to that observed in studies of genetic polymorphisms and pharmacological manipulations. Our model represents a formal computational link between anatomical, functional neuroimaging, genetic, behavioral, and theoretical levels of analysis in the study of executive control. In addition, the model specifies one way in which the pFC, BG, parietal, and sensory cortices may learn to cooperate and give rise to executive control.

The Practice of Going Helps Children to Stop: The Importance of Context Monitoring in Inhibitory Control

How do we stop ourselves during ongoing action? Recent work implies that stopping per se is easy given sufficient monitoring of contextual cues signaling the need to change action. We test key implications of this idea for improving inhibitory control. Seven- to 9-year-old children practiced stopping an ongoing action or monitoring for cues that signaled the need to go again. Both groups subsequently showed better response inhibition in a Stop-Signal task than active controls, and practice monitoring yielded a dose-response relationship. When monitoring practice was optimized to occur while children engaged in responding, the greatest benefits were observed-even greater than from practicing stopping itself. These findings demonstrate the importance of monitoring processes in developing response inhibition and suggest promising new directions for interventions.

Working memory management and predicted utility

Given the limited capacity of working memory (WM), its resources should be allocated strategically. One strategy is filtering, whereby access to WM is granted preferentially to items with the greatest utility. However, reallocation of WM resources might be required if the utility of maintained information subsequently declines. Here, we present behavioral, computational, and neuroimaging evidence that human participants track changes in the predicted utility of information in WM. First, participants demonstrated behavioral costs when the utility of items already maintained in WM declined and resources should be reallocated. An adapted Q-learning model indicated that these costs scaled with the historical utility of individual items. Finally, model-based neuroimaging demonstrated that frontal cortex tracked the utility of items to be maintained in WM, whereas ventral striatum tracked changes in the utility of items maintained in WM to the degree that these items are no longer useful. Our findings suggest that frontostriatal mechanisms track the utility of information in WM, and that these dynamics may predict delays in the removal of information from WM.

A developmental window into trade-offs in executive function: The case of task switching versus response inhibition in 6-year-olds

Good executive function has been linked to many positive outcomes in academic performance, health, and social competence. However, some aspects of executive function may interfere with other cognitive processes. Childhood provides a unique test case for investigating such cognitive trade-offs, given the dramatic failures and developments observed during this period. For example, most children categorically switch or perseverate when asked to switch between rules on a card-sorting task. To test potential trade-offs with the development of task switching abilities, we compared 6-year-olds who switched versus perseverated in a card-sorting task on two aspects of inhibitory control: response inhibition (via a stop signal task) and interference control (via a Simon task). Across two studies, switchers showed worse response inhibition than perseverators, consistent with the idea of cognitive trade-offs; however, switchers showed better interference control than perseverators, consistent with prior work documenting benefits associated with the development of executive function. This pattern of positive and negative associations may reflect aspects of working memory (active maintenance of current goals, and clearing of prior goals) that help children focus on a single task goal but hurt in situations with conflicting goals. Implications for understanding components of executive function and their relationships across development are discussed.

Parallel temporal dynamics in hierarchical cognitive control

Cognitive control allows us to follow abstract rules in order to choose appropriate responses given our desired outcomes. Cognitive control is often conceptualized as a hierarchical decision process, wherein decisions made at higher, more abstract levels of control asymmetrically influence lower-level decisions. These influences could evolve sequentially across multiple levels of a hierarchical decision, consistent with much prior evidence for central bottlenecks and seriality in decision-making processes. However, here, we show that multiple levels of hierarchical cognitive control are processed primarily in parallel. Human participants selected responses to stimuli using a complex, multiply contingent (third order) rule structure. A response deadline procedure allowed assessment of the accuracy and timing of decisions made at each level of the hierarchy. In contrast to a serial decision process, error rates across levels of the decision mostly declined simultaneously and at identical rates, with only a slight tendency to complete the highest level decision first. Simulations with a biologically plausible neural network model demonstrate how such parallel processing could emerge from a previously developed hierarchically nested frontostriatal architecture. Our results support a parallel processing model of cognitive control, in which uncertainty on multiple levels of a decision is reduced simultaneously.

Working memory gating mechanisms explain developmental change in rule-guided behavior

Cognitive control requires choosing contextual information to update into working memory (input gating), maintaining it there (maintenance) stable against distraction, and then choosing which subset of maintained information to use in guiding action (output gating). Recent work has raised the possibility that the development of rule-guided behavior, in the transition from childhood to adolescence, is linked specifically to changes in the gating components of working memory (Amso, Haas, McShane, & Badre, 2014). Given the importance of effective rule-guided behavior for decision making in this developmental transition, we used hierarchical rule tasks to probe the precise developmental dynamics of working memory gating. This mechanistic precision informs ongoing efforts to train cognitive control and working memory operations across typical and atypical development. The results of Experiment 1 verified that the development of rule-guided behavior is uniquely linked to increasing hierarchical complexity but not to increasing maintenance demands across 1st, 2nd, and 3rd order rule tasks. Experiment 2 then investigated whether this developmental trajectory in rule-guided behavior is best explained by change in input gating or output gating. Further, as input versus output gating also tend to correlate with a more proactive versus reactive control strategy in these tasks, we assessed developmental change in the degree to which these two processes were deployed efficiently given the task. Experiment 2 shows that the developmental change observed in Experiment 1 and in Amso et al. (2014) is likely a result of increased efficacy of output gating processes, as well as greater strategic efficiency in that adolescents opt for this costly process less often than children.