Hierarchical reasoning by neural circuits in the frontal cortex

The brain circuits of strategic decisions Primates can compute and integrate low-level decisions to make strategic adjustments to higher-level decisions. The neural substrates and mechanisms that allow this process are not known. Sarafyazd and Jazayeri performed single-cell recordings in the dorsomedial frontal cortex and the anterior cingulate cortex of monkeys. They observed that the two brain areas, which have been implicated in error monitoring and the control of adaptive behavior, processed signals involved in causal inference. The anterior cingulate acted downstream of the dorsomedial frontal cortex. It used graded evidence derived from errors in low-level processes in a decision hierarchy to select between longer-term behavioral strategies. Science, this issue p. eaav8911 Macaque monkeys are capable of hierarchical decision-making. INTRODUCTION Research on the neurobiology of decision-making has emerged as a fertile ground for integrating cognitive, systems, computational, and, more recently, circuit and molecular neuroscience. However, examinations of the underlying neural mechanisms have been largely limited to categorizing stimuli under uncertainty or choosing among volatile rewards. To realize the broader impact of this integration, we need to understand the neural underpinnings of decision-making in more sophisticated behavioral paradigms that demand cognitive reasoning and characterize the computational principles that underlie such reasoning. RATIONALE Cognitive reasoning often involves making hierarchically organized decisions. For example, imagine you want to prepare a dish you once enjoyed at a restaurant. You try an online recipe, but the outcome falls short of expectations. You ask yourself, “Is it me or is this the wrong recipe? ” Depending on your confidence in your cooking skills, you may try the recipe a few more times, but if the results remain unsatisfactory, you may switch to another recipe. Behavioral studies have shown that humans reason about their failures by assessing their confidence after one or more attempts. However, the neural computations supporting this high-level reasoning strategy are not understood. We sought to characterize these computations in the frontal cortex of nonhuman primates. RESULTS We trained monkeys to perform a task comprised of two hierarchically organized decisions. In their first decision, monkeys had to choose between two stimulus-response contingency rules that alternated covertly throughout the experiment. Subsequently, monkeys had to make a perceptual judgment about a stimulus and respond according to the underlying contingency rule. In this task, making the wrong choice in either decision could lead to an error. Therefore, to correctly infer the cause of the error, one has to reason hierarchically and ask, “Did the rule change, or did I make a perceptual error? ” We found that monkeys, like humans, relied on their confidence to decide whether to attribute errors to themselves or to covert rule switches. They treated each failure as evidence for a covert rule switch but did so rationally by updating their belief about the underlying rule depending on their level of confidence in their perceptual judgments across multiple trials. To assess the animals’ behavior rigorously, we developed a model of hierarchical decision-making that was composed of two processes, one supporting perceptual decisions within each trial and another supporting decisions about covert rule switches across trials. The model was able to capture the animals’ behavior accurately and provided a quantitative account of how the belief about covert rule switches was updated. Next, we sought to characterize how neural computations in the frontal cortex could provide a substrate for representing and updating the belief about rule switches. We focused on anterior cingulate cortex (ACC) and dorsomedial frontal cortex (DMFC), which have been implicated in performance monitoring, adaptive reasoning, and strategic decision-making. Electrophysiological recordings indicated that neural activity in both areas reflected the animals’ belief about the rule on the basis of the outcome of the preceding trials. A detailed comparison of the nature of the signals in the two areas revealed that only ACC had a strong correlate of the animals’ decisions about rule switches. Further probing of these circuits using causal tools revealed that ACC operates downstream of DMFC, integrates trial-outcome information, and drives decisions about when a rule switch might have occurred. CONCLUSION Our behavioral results reveal that monkeys, like humans, can reason hierarchically and make rational decisions that rely on evidence at multiple time scales. This opens the possibility for a detailed examination of the neurobiology of hierarchical reasoning, which is a central theme in cognitive neuroscience. We were able to build on previous foundational work on models of decision-making to create a unified framework for understanding the computational principles of hierarchical reasoning. In addition, our neural recording and perturbation experiments revealed a distributed and hierarchically organized neural circuit in the frontal cortex, including DMFC and ACC, that is functionally responsible for hierarchical reasoning about errors. Confidence-based updating of beliefs in uncertain environments is an integral part of human cognition, and our discovery of its underlying computational principles and neural mechanisms is likely to help bridge the gap between research in cognitive and systems neuroscience. Cognitive error reasoning in the frontal cortex. In a hierarchical reasoning task comprised of two alternating rules (bottom), animals inferred covert rule switches by monitoring the outcome of their perceptual decisions about unreliable stimuli (middle). In nonhuman primates, this cognitive capacity was supported by circuit-level interactions in the frontal cortex computing the belief about rule switches on the basis of the outcome of the preceding trials (top). Humans process information hierarchically. In the presence of hierarchies, sources of failures are ambiguous. Humans resolve this ambiguity by assessing their confidence after one or more attempts. To understand the neural basis of this reasoning strategy, we recorded from dorsomedial frontal cortex (DMFC) and anterior cingulate cortex (ACC) of monkeys in a task in which negative outcomes were caused either by misjudging the stimulus or by a covert switch between two stimulus-response contingency rules. We found that both areas harbored a representation of evidence supporting a rule switch. Additional perturbation experiments revealed that ACC functioned downstream of DMFC and was directly and specifically involved in inferring covert rule switches. These results‏ reveal the computational principles of hierarchical reasoning, as implemented by cortical circuits.