Rule-guided Behavior Research Articles

On what it means to automatize a rule

The results of two experiments are reported that included a combined total of approximately 633,000 categorization trials. The experiments investigated the nature of what is automatized after lengthy practice with a rule-guided behavior. The results of both experiments suggest that an abstract rule, if interpreted as a verbal-based strategy, was not automatized during training, but rather the automatization linked a set of stimuli with similar values on one visual dimension to a common motor response. The experiments were designed to test and refine a recent neurocomputational model of how rule-guided behaviors become automatic (Kovacs, Hélie, Tran, & Ashby, 2021). The model assumes that rule-guided behaviors are initially controlled by a distributed neural network centered on rule units in prefrontal cortex, and that in addition to initiating behavior, this network also trains a faster and more direct network that includes projections from visual cortex directly to the rule-sensitive neurons in premotor cortex. The present results support this model and suggest that the projections from visual cortex to prefrontal and premotor cortex are restricted to visual representations of the relevant stimulus dimension only.

‘We Are Not Bad People’- Bricolage and the Rise of Community Forest Institutions in Burkina Faso

From a critical institutionalism and institutional bricolage perspective, this article analyses what drives institutional change in the commons and the outcomes for forest and people. It builds on the comparison of three neighbouring villages in Burkina Faso that in 1989, expecting higher returns, agreed to release their common lands for the creation of a community forest called Chantier d’Amenagement Forestier (CAF) within an international forestry project. The project created new bureaucratic institutions to replace the pre-existing customary and socially embedded system. Decades later, the three villages display different institutional change pathways and outcomes: one village abandoned the CAF, converted, and sold its forest and land; another maintained the CAF; and a third operates in-between. Using qualitative research methods, we ask why and how these different change trajectories and outcomes occurred among villages of identical cultural and sociopolitical background. The results show that poor design and implementation of the new bureaucratic institutions, as well as their disrespect of customary and socially embedded rules, led to forestland disputes between the villages. The bureaucratic institutions failed to solve those disputes, effectively manage the forest, and share the benefits equitably. This caused local people’s discontent and prompted actions for change. Actors in diverse ways made use of their social networks, agency, and power relations within and between the villages to either reshape, re-interpret or reject the new forest institutions. These processes of institutional bricolage led to highly diverse trajectories of change. The findings demonstrate the crucial role of locals as agents of change from below and question universal claims in institutional theory on how institutions induce rule-guided behaviour and create path dependencies.

Emergence of abstract rules in the primate brain.

Various aspects of human cognition are shaped and enriched by abstract rules, which help to describe, link and classify discrete events and experiences into meaningful concepts. However, where and how these entities emerge in the primate brain and the neuronal mechanisms underlying them remain the subject of extensive research and debate. Evidence from imaging studies in humans and single-neuron recordings in monkeys suggests a pivotal role for the prefrontal cortex in the representation of abstract rules; however, behavioural studies in lesioned monkeys and data from neuropsychological examinations of patients with prefrontal damage indicate substantial functional dissociations and task dependency in the contribution of prefrontal cortical regions to rule-guided behaviour. This Review describes our current understanding of the dynamic emergence of abstract rules in primate cognition, and of the distributed neural network that supports abstract rule formation, maintenance, revision and task-dependent implementation.

The value of proactive goal setting and choice in 3- to 7-year-olds' use of working memory gating strategies in a naturalistic task.

Rule-guided behavior depends on the ability to strategically update and act on content held in working memory. Proactive and reactive control strategies were contrasted across two experiments using an adapted input/output gating paradigm (Neuron, 81, 2014 and 930). Behavioral accuracies of 3-, 5-, and 7-year-olds were higher when a contextual cue appeared at the beginning of the task (input gating) rather than at the end (output gating). This finding supports prior work in older children, suggesting that children are better when input gating but rely on the more effortful output gating strategy for goal-oriented action selection (Cognition, 155, 2016 and 8). A manipulation was added to investigate whether children's use of working memory strategies becomes more flexible when task goals are specified internally rather than externally provided by the experimenter. A shift toward more proactive control was observed when children chose the task goal among two alternatives. Scan path analyses of saccadic eye movement indicated that giving children agency and choice over the task goal resulted in less use of a reactive strategy than when the goal was determined by the experimenter.

Enhanced Theta and High-Gamma Coupling during Late Stage of Rule Switching Task in Rat Hippocampus

Hippocampal oscillations, particularly theta (6–12 Hz) and gamma (30–90 Hz) frequency bands, play an important role in several cognitive functions. Theta and gamma oscillations show cross-frequency coupling (CFC), wherein the phase of theta rhythm modulates the amplitude of the gamma oscillation, and this CFC is believed to reflect cell assembly dynamics in cognitive processes. Previous studies have reported that CFC strength correlates with the learning process. However, details on these dynamic correlations have not been elucidated. In the present study, we analyzed local field potentials recorded from the rat hippocampus during the learning of a rule-switching task. The modulation index, an index of the CFC strength, became higher in rule-guided behavior than in the no rule condition. The enhanced coupling between theta and high-gamma oscillations (60–90 Hz) changed during the late stage of learning. In contrast, the coupling between theta and low-gamma oscillations (30–60 Hz) did not show any changes during learning. These results suggest that the coupling between theta and gamma bands occurs during rule learning and that high- and low-gamma bands play different roles in rule switching.

The relationship between cognitive enrichment and cognitive control: A systematic investigation of environmental influences on development through socioeconomic status.

We measured the impact of socioeconomic status (SES) on cognitive processes. We examined cognitive control, specifically working memory (WM), in a sample of N=141 7- to 17-year-olds using rule-guided behavior tasks. Our hypothesis is based on computational modeling data that suggest that the development of flexible cognitive control requires variable experiences in which to implement rule-guided action. We found that not all experiences that correlated with SES in our sample impacted task performance, and not all experiential variables that impacted performance were associated with SES. Of the experiential variables associated with task performance, only cognitive enrichment opportunities worked indirectly through SES to affect WM as tested with rule-guided behavior tasks. We discuss the data in the context of necessary precision in SES research.

Eye movements provide insight into individual differences in children's analogical reasoning strategies

Analogical reasoning is considered a key driver of cognitive development and is a strong predictor of academic achievement. However, it is difficult for young children, who are prone to focusing on perceptual and semantic similarities among items rather than relational commonalities. For example, in a classic A:B::C:? propositional analogy task, children must inhibit attention towards items that are visually or semantically similar to C, and instead focus on finding a relational match to the A:B pair. Competing theories of reasoning development attribute improvements in children's performance to gains in either executive functioning or semantic knowledge. Here, we sought to identify key drivers of the development of analogical reasoning ability by using eye gaze patterns to infer problem-solving strategies used by six-year-old children and adults. Children had a greater tendency than adults to focus on the immediate task goal and constrain their search based on the C item. However, large individual differences existed within children, and more successful reasoners were able to maintain the broader goal in mind and constrain their search by initially focusing on the A:B pair before turning to C and the response choices. When children adopted this strategy, their attention was drawn more readily to the correct response option. Individual differences in children's reasoning ability were also related to rule-guided behavior but not to semantic knowledge. These findings suggest that both developmental improvements and individual differences in performance are driven by the use of more efficient reasoning strategies regarding which information is prioritized from the start, rather than the ability to disengage from attractive lure items.

Neuromodulation of Prefrontal Cortex in Non-Human Primates by Dopaminergic Receptors during Rule-Guided Flexible Behavior and Cognitive Control.

The prefrontal cortex (PFC) is indispensable for several higher-order cognitive and executive capacities of primates, including representation of salient stimuli in working memory (WM), maintenance of cognitive task set, inhibition of inappropriate responses and rule-guided flexible behavior. PFC networks are subject to robust neuromodulation from ascending catecholaminergic systems. Disruption of these systems in PFC has been implicated in cognitive deficits associated with several neuropsychiatric disorders. Over the past four decades, a considerable body of work has examined the influence of dopamine on macaque PFC activity representing spatial WM. There has also been burgeoning interest in neuromodulation of PFC circuits involved in other cognitive functions of PFC, including representation of rules to guide flexible behavior. Here, we review recent neuropharmacological investigations conducted in our laboratory and others of the role of PFC dopamine receptors in regulating rule-guided behavior in non-human primates. Employing iontophoresis, we examined the effects of local manipulation of dopaminergic subtypes on neuronal activity during performance of rule-guided pro- and antisaccades, an experimental paradigm sensitive to PFC integrity, wherein deficits in performance are reliably observed in many neuropsychiatric disorders. We found dissociable effects of dopamine receptors on neuronal activity for rule representation and oculomotor responses and discuss these findings in the context of prior studies that have examined the role of dopamine in spatial delayed response tasks, attention, target selection, abstract rules, visuomotor learning and reward. The findings we describe here highlight the common features, as well as heterogeneity and context dependence of dopaminergic neuromodulation in regulating the efficacy of cognitive functions of PFC in health and disease.

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.

Functional Specialization within Macaque Dorsolateral Prefrontal Cortex for the Maintenance of Task Rules and Cognitive Control

The abilities of switching between and maintaining task rules are fundamental aspects of goal-oriented behavior. The PFC is thought to implement the cognitive processes underling such rule-based behavior, but the specific contributions of the several cytoarchitecturally distinct subfields of PFC remain poorly understood. Here, we used bilateral cryogenic deactivation to investigate the relative contributions of two regions of the dorsolateral PFC (dlPFC)--the inferior dlPFC (idlPFC) area, consisting of the cortex lining the caudal principal sulcus, and the dorsally adjacent superior dlPFC (sdlPFC)--to different aspects of rule-based behavior. Macaque monkeys performed two variants of a task that required them to alternate unpredictably between eye movements toward (prosaccade) or away from (antisaccade) a visual stimulus. In one version of the task, the current rule was overtly cued. In the second, the task rule was uncued, and successful performance required the animals to detect rule changes on the basis of reward outcome and subsequently maintain the current task rule within working memory. Deactivation of the idlPFC impaired the monkeys' ability to perform pro- and antisaccades in the uncued task only. In contrast, deactivation of the sdlPFC had no effect on performance in either task. Combined deactivation of idlPFC and sdlPFC impaired performance on antisaccade, but not prosaccade, trials in both task variants. These results suggest that the idlPFC is required for mnemonic processes involved in maintenance of task rules, whereas both idlPFC and sdlPFC together are necessary for the deployment of the cognitive control required to perform antisaccades. Together, these data support the concept of a functional specialization of subregions within the dlPFC for rule-guided behavior.

Working memory updating and the development of rule-guided behavior

The transition from middle childhood into adolescence is marked by both increasing independence and also extensive change in the daily requirements of familial demands, social pressures, and academic achievement. To manage this increased complexity, children must develop the ability to use abstract rules that guide the choice of behavior across a range of circumstances. Here, we tested children through adults in a task that requires increasing levels of rule abstraction, while separately manipulating competition among alternatives in working memory. We found that age-related differences in rule-guided behavior can be explained in terms of improvement in rule abstraction, which we suggest involves a working memory updating mechanism. Furthermore, family socioeconomic status (SES) predicted change in rule-guided behavior, such that higher SES predicted better performance with development. We discuss these results within a working memory gating framework for abstract rule-guided behavior.

Targeted training of the decision rule benefits rule-guided behavior in Parkinson’s disease

The impact of Parkinson's disease (PD) on rule-guided behavior has received considerable attention in cognitive neuroscience. The majority of research has used PD as a model of dysfunction in frontostriatal networks, but very few attempts have been made to investigate the possibility of adapting common experimental techniques in an effort to identify the conditions that are most likely to facilitate successful performance. The present study investigated a targeted training paradigm designed to facilitate rule learning and application using rule-based categorization as a model task. Participants received targeted training in which there was no selective-attention demand (i.e., stimuli varied along a single, relevant dimension) or nontargeted training in which there was selective-attention demand (i.e., stimuli varied along a relevant dimension as well as an irrelevant dimension). Following training, all participants were tested on a rule-based task with selective-attention demand. During the test phase, PD patients who received targeted training performed similarly to control participants and outperformed patients who did not receive targeted training. As a preliminary test of the generalizability of the benefit of targeted training, a subset of the PD patients were tested on the Wisconsin card sorting task (WCST). PD patients who received targeted training outperformed PD patients who did not receive targeted training on several WCST performance measures. These data further characterize the contribution of frontostriatal circuitry to rule-guided behavior. Importantly, these data also suggest that PD patient impairment, on selective-attention-demanding tasks of rule-guided behavior, is not inevitable and highlight the potential benefit of targeted training.

Chronic treatment with the serotonin 2A/2C receptor antagonist SR 46349B enhances the retention and efficiency of rule-guided behavior in mice

Animal studies have established that drugs activating the serotonin 2A (5-HT2A) receptor can enhance learning and memory in a variety of classical and operant conditioning tasks. Unfortunately, long-term agonism typically results in receptor downregulation, which can negate such nootropic effects. Conversely, chronic antagonism can act to increase receptor density, an adaptation which, in principle, should enhance cognition in a manner similar to acute agonism. In this study, we questioned whether chronic treatment with the 5-HT2A receptor antagonist, SR 46349B, a drug known to increase 5-HT2A receptor density in vivo, would improve cognitive performance in normal mice. To address this question, we administered SR 46349B to mice for 4days following initial training on a simple rule-based reward acquisition task. We subsequently tested their recall of this task and, finally, their ability to adapt to a reversal in reward contingency (reversal learning). For comparison, two additional groups were treated with the 5-HT2A/2C receptor agonist, DOI, which downregulates the 5-HT2A receptor. SR 46349B improved retention of the previously-learned task but did not affect reversal learning. Subjects treated with SR 46349B also completed trials faster and with greater motor efficiency than vehicle- or DOI-treated subjects. We hypothesize that long-term drug treatments resulting in 5-HT2A receptor up-regulation may be useful in enhancing recall of learned behaviors and, thus, may have potential for treating cognitive impairment associated with neurodegenerative disorders.

On the neural basis of rule-guided behavior

Human behavior emerges from a complex dynamic interaction between graded and context-sensitive neural processes, the biomechanics of our bodies, and the vicissitudes of our environments. These coupled processes bear little resemblance to the iterated application of simple symbolic rules. Still, there are circumstances under which our behavior appears to be guided by explicit mental rules. A prototypical case is when succinct verbal instructions are communicated and are promptly followed by another. How does the brain support such rule-guided behavior? How are explicit rules represented in the brain? How are rule representations shaped by experience? What neural processes form the foundation of our ability to systematically represent and apply rules from the vast range of possible rules? This article reviews a line of research that has sought a computational cognitive neuroscience account of rule-guided behavior in terms of the functioning of the prefrontal cortex, the basal ganglia, and related brain systems.

Flexible rule use: Common neural substrates in children and adults

Flexible rule-guided behavior develops gradually, and requires the ability to remember the rules, switch between them as needed, and implement them in the face of competing information. Our goals for this study were twofold: first, to assess whether these components of rule-guided behavior are separable at the neural level, and second, to identify age-related differences in one or more component that could support the emergence of increasingly accurate and flexible rule use over development. We collected event-related fMRI data while 36 children aged 8–13 and adults aged 20–27 performed a task that manipulated rule representation, rule switching, and stimulus incongruency. Several regions – left dorsolateral prefrontal cortex (DLPFC), left posterior parietal cortex, and pre-supplementary motor area – were engaged by both the rule representation and the rule-switching manipulations. These regions were engaged similarly across age groups, though contrasting timecourses of activation in left DLPFC suggest that children updated task rules more slowly than did adults. These findings support the idea that common networks can contribute to a variety of executive functions, and that some developmental changes take the form of changes in temporal dynamics rather than qualitative changes in the network of brain regions engaged.

Functional localization within the prefrontal cortex: missing the forest for the trees?

Anatomical and functional studies of the prefrontal cortex (PFC) have identified multiple PFC subregions. We argue that the PFC is involved in cognitive functions exceeding the sum of specific functions attributed to its subregions. These can be revealed either by lesions of the whole PFC, or more specifically by selective disconnection of the PFC from certain types of information (for example, visual) allowing the investigation of PFC function in toto. Recent studies in macaque monkeys using the latter approach lead to a second conclusion: that the PFC, as a whole, could be fundamentally specialized for representing events that are extended in time. The representation of temporally complex events might underlie PFC involvement in general intelligence, decision-making, and executive function.

Monkeys Quickly Learn and Generalize Visual Categories without Lateral Prefrontal Cortex

Categorization is a basic mental process that helps individuals distinguish among groups of negative and positive objects, e.g., poisons and nutrients, or predators and prey. Monkey experiments have suggested that lateral prefrontal cortex (LPFC) participates in learning and processing visual categories. However, in humans category specific visual agnosia follows inferior temporal cortex but not LPFC damage. Here, we use a new behavioral approach to show that both normal monkeys and those with bilateral removal of LPFC learn and generalize perceptual categories of related visual stimuli rapidly without explicit instruction. These results strongly indicate that visual categorization occurs at some earlier stage of feed-forward processing, presumably in temporal cortex, without top-down information from LPFC.

The interplay between formality and informality in managed learning networks

This paper offers an empirical exploration of group-level knowledge practices in a university-managed learning network of small and medium sized enterprises. Managed learning networks are an example of an intermediate form of network relationship with both formal and informal elements. The aim of the paper is to help understand the implications of the degree of formality/informality for group-based learning. This is based on a multi-dimensional conception of formalisation that focuses specifically on two dimensions: firstly, formality as a feature of rule-guided behaviour and secondly, as a characteristic of the social and emotional dynamics of groups. The interplay between these dimensions is examined and an initial framework suggesting the implications of alternative configurations for group learning is proposed.

Rat Prefrontal Cortical Neurons Selectively Code Strategy Switches

Multiple memory systems are distinguished by different sets of neuronal circuits and operating principles optimized to solve different problems across mammalian species (Tulving and Schacter, 1994). When a rat selects an arm in a plus maze, for example, the choice can be guided by distinct neural systems (White and Wise, 1999) that encode different relationships among perceived stimuli, actions, and reward. Thus, egocentric or stimulus-response associations require striatal circuits, whereas spatial or episodic learning requires hippocampal circuits (Packard et al., 1989). Although these memory systems function in parallel (Packard and McGaugh, 1996), they can also interact competitively or synergistically (Kim and Ragozzino, 2005). The neuronal mechanisms that coordinate these multiple memory systems are not fully known, but converging evidence suggests that the prefrontal cortex (PFC) is central. The PFC is crucial for abstract, rule-guided behavior in primates and for switching rapidly between memory strategies in rats. We now report that rat medial PFC neuronal activity predicts switching between hippocampus- and caudate-dependent memory strategies. Prelimbic (PL) and infralimbic (IL) neuronal activity changed as rats switched memory strategies even as the rats performed identical behaviors but did not change when rats learned new contingencies using the same strategy. PL dynamics anticipated learning performance whereas IL lagged, suggesting that the two regions help initiate and establish new strategies, respectively. These neuronal dynamics suggest that the PFC contributes to the coordination of memory strategies by integrating the predictive relationships among stimuli, actions, and reward.

Prefrontal cortex and rule abstraction: Where and whether? Theoretical comment on Moore et al. (2009).

The primate dorsolateral prefrontal cortex is implicated in diverse aspects of behavioral regulation, cognitive control, and memory. However, direct neuropsychological evidence supporting a requirement of this area in functions other than spatial working memory has been scarce. T. L. Moore, S. P. Schettler, R. J. Killiany, D. L. Rosene, and M. B. Moss have shown, for the first time, that lesions of dorsolateral prefrontal cortex in the rhesus monkey (including areas 9 and 46) substantially impair performance in a test of executive function modeled on the Wisconsin Card Sorting Task. The pattern of impairment is consistent with a role for dorsolateral prefrontal areas in rule abstraction but may relate to a role for this area in rule maintenance as well. Interestingly, monkeys with dorsolateral prefrontal lesions do not appear to perseverate in their use of particular rules in the task, different from the common impairment associated with frontal lobe damage in humans. These findings indicate that dorsolateral prefrontal cortex is necessary for some aspects of rule-guided behavior in the primate brain and help illuminate the involvement of different prefrontal areas in different aspects of executive function and rule-guided behavior.