A Hierarchy of Functional States in Working Memory.

Extensive research has examined how information is maintained in working memory (WM), but it remains unknown how WM is used to guide behavior. We addressed this question by combining human electrophysiology (50 subjects, male and female) with pattern analyses, cognitive modeling, and a task requiring the prolonged maintenance of two WM items and priority shifts between them. This enabled us to discern neural states coding for memories that were selected to guide the next decision from states coding for concurrently held memories that were maintained for later use, and to examine how these states contribute to WM-based decisions. Selected memories were encoded in a functionally active state. This state was reflected in spontaneous brain activity during the delay period, closely tracked moment-to-moment fluctuations in the quality of evidence integration, and also predicted when memories would interfere with each other. In contrast, concurrently held memories were encoded in a functionally latent state. This state was reflected only in stimulus-evoked brain activity, tracked memory precision at longer timescales, but did not engage with ongoing decision dynamics. Intriguingly, the two functional states were highly flexible, as priority could be dynamically shifted back and forth between memories without degrading their precision. These results delineate a hierarchy of functional states, whereby latent memories supporting general maintenance are transformed into active decision circuits to guide flexible behavior.SIGNIFICANCE STATEMENT Working memory enables maintenance of information that is no longer available in the environment. Abundant neuroscientific work has examined where in the brain working memories are stored, but it remains unknown how they are represented and used to guide behavior. Our study shows that working memories are represented in qualitatively different formats, depending on behavioral priorities. Memories that are selected for guiding behavior are encoded in an active state that transforms sensory input into decision variables, whereas other concurrently held memories are encoded in a latent state that supports precise maintenance without affecting ongoing cognition. These results dissociate mechanisms supporting memory storage and usage, and open the door to reveal not only where memories are stored but also how.

10 Simple Rules for a Supportive Lab Environment.

The transition to principal investigator (PI), or lab leader, can be challenging, partially due to the need to fulfil new managerial and leadership responsibilities. One key aspect of this role, which is often not explicitly discussed, is creating a supportive lab environment. Here, we present ten simple rules to guide the new PI in the development of their own positive and thriving lab atmosphere. These rules were written and voted on collaboratively, by the students and mentees of Professor Mark Stokes, who inspired this piece.

Reward Boosts Neural Coding of Task Rules to Optimize Cognitive Flexibility.

Cognitive flexibility is critical for intelligent behavior. However, its execution is effortful and often suboptimal. Recent work indicates that flexible behavior can be improved by the prospect of reward, which suggests that rewards optimize flexible control processes. Here we investigated how different reward prospects influence neural encoding of task rule information to optimize cognitive flexibility. We applied representational similarity analysis to human electroencephalograms, recorded while female and male participants performed a rule-guided decision-making task. During the task, the prospect of reward varied from trial to trial. Participants made faster, more accurate judgements on high-reward trials. Critically, high reward boosted neural coding of the active task rule, and the extent of this increase was associated with improvements in task performance. Additionally, the effect of high reward on task rule coding was most pronounced on switch trials, where rules were updated relative to the previous trial. These results suggest that reward prospect can promote cognitive performance by strengthening neural coding of task rule information, helping to improve cognitive flexibility during complex behavior.SIGNIFICANCE STATEMENT The importance of motivation is evident in the ubiquity with which reward prospect guides adaptive behavior and the striking number of neurological conditions associated with motivational impairments. In this study, we investigated how dynamic changes in motivation, as manipulated through reward, shape neural coding for task rules during a flexible decision-making task. The results of this work suggest that motivation to obtain reward modulates the encoding of task rules needed for flexible behavior. The extent to which reward increased task rule coding also tracked improvements in behavioral performance under high-reward conditions. These findings help to inform how motivation shapes neural processing in the healthy human brain.

Causal Evidence for Learning-Dependent Frontal Lobe Contributions to Cognitive Control.

The lateral prefrontal cortex (LPFC) plays a central role in the prioritization of sensory input based on task relevance. Such top-down control of perception is of fundamental importance in goal-directed behavior, but can also be costly when deployed excessively, necessitating a mechanism that regulates control engagement to align it with changing environmental demands. We have recently introduced the "flexible control model" (FCM), which explains this regulation as resulting from a self-adjusting reinforcement-learning mechanism that infers latent statistical structure in dynamic task environments to predict forthcoming states. From this perspective, LPFC-based control is engaged as a function of anticipated cognitive demand, a notion for which we previously obtained correlative neuroimaging evidence. Here, we put this hypothesis to a rigorous, causal test by combining the FCM with a transcranial magnetic stimulation (TMS) intervention that transiently perturbed the LPFC. Human participants (male and female) completed a nonstationary version of the Stroop task with dynamically changing probabilities of conflict between task-relevant and task-irrelevant stimulus features. TMS was given on each trial before stimulus onset either over the LPFC or over a control site. In the control condition, we observed adaptive performance fluctuations consistent with demand predictions that were inferred from recent and remote trial history and effectively captured by our model. Critically, TMS over the LPFC eliminated these fluctuations while leaving basic cognitive and motor functions intact. These results provide causal evidence for a learning-based account of cognitive control and delineate the nature of the signals that regulate top-down biases over stimulus processing.SIGNIFICANCE STATEMENT A core function of the human prefrontal cortex is to control the signal flow in sensory brain regions to prioritize processing of task-relevant information. Abundant work suggests that such control is flexibly recruited to accommodate dynamically changing environmental demands, yet the nature of the signals that serve to engage control remains unknown. Here, we combined computational modeling with noninvasive brain stimulation to show that changes in control engagement are captured by a self-adjusting reinforcement-learning mechanism that tracks changing environmental statistics to predict forthcoming processing demands and that transient perturbation of the prefrontal cortex abolishes these adjustments. These findings delineate the learning signals that underpin adaptive engagement of prefrontal control functions and provide causal evidence for their relevance in behavioral control.

Neural Coding for Instruction-Based Task Sets in Human Frontoparietal and Visual Cortex.

Task preparation has traditionally been thought to rely upon persistent representations of instructions that permit their execution after delays. Accumulating evidence suggests, however, that accurate retention of task knowledge can be insufficient for successful performance. Here, we hypothesized that instructed facts would be organized into a task set; a temporary coding scheme that proactively tunes sensorimotor pathways according to instructions to enable highly efficient "reflex-like" performance. We devised a paradigm requiring either implementation or memorization of novel stimulus-response mapping instructions, and used multivoxel pattern analysis of neuroimaging data to compare neural coding of instructions during the pretarget phase. Although participants could retain instructions under both demands, we observed striking differences in their representation. To-be-memorized instructions could only be decoded from mid-occipital and posterior parietal cortices, consistent with previous work on visual short-term memory storage. In contrast, to-be-implemented instructions could also be decoded from frontoparietal "multiple-demand" regions, and dedicated visual areas, implicated in processing instructed stimuli. Neural specificity in the latter moreover correlated with performance speed only when instructions were prepared, likely reflecting the preconfiguration of instructed decision circuits. Together, these data illuminate how the brain proactively optimizes performance, and help dissociate neural mechanisms supporting task control and short-term memory storage.

Co-Activation-Based Parcellation of the Lateral Prefrontal Cortex Delineates the Inferior Frontal Junction Area.

The inferior frontal junction (IFJ) area, a small region in the posterior lateral prefrontal cortex (LPFC), has received increasing interest in recent years due to its central involvement in the control of action, attention, and memory. Yet, both its function and anatomy remain controversial. Here, we employed a meta-analytic parcellation of the left LPFC to show that the IFJ can be isolated based on its specific functional connections. A seed region, oriented along the left inferior frontal sulcus (IFS), was subdivided via cluster analyses of voxel-wise whole-brain co-activation patterns. The ensuing clusters were characterized by their unique connections, the functional profiles of associated experiments, and an independent topic mapping approach. A cluster at the posterior end of the IFS matched previous descriptions of the IFJ in location and extent and could be distinguished from a more caudal cluster involved in motor control, a more ventral cluster involved in linguistic processing, and 3 more rostral clusters involved in other aspects of cognitive control. Overall, our findings highlight that the IFJ constitutes a core functional unit within the frontal lobe and delineate its borders. Implications for the IFJ's role in human cognition and the organizational principles of the frontal lobe are discussed.

Transcranial magnetic stimulation dissociates prefrontal and parietal contributions to task preparation.

Cognitive control is thought to rely upon a set of distributed brain regions within frontoparietal cortex, but the functional contributions of these regions remain elusive. Here, we investigated the disruptive effects of transcranial magnetic stimulation (TMS) over the human prefrontal and parietal cortices in task preparation at different abstraction levels. While participants completed a task-switching paradigm that assessed the reconfiguration of task goals and response sets independently, TMS was applied over the left inferior frontal junction (IFJ) and over the left intraparietal sulcus (IPS) during task preparation. In Experiment 1, TMS over the IFJ caused interference with the updating of task goals, while leaving the updating of response sets unaffected. In Experiment 2, TMS over the IPS created the opposite pattern of results, perturbing only the ability to update response sets, but not task goals. Experiment 3 furthermore revealed that TMS over the IPS interfered with task goal updating when the pulses are delivered at a later point in time during preparation. This dissociation of abstract and action-related components not only reveals distinct cognitive control processes during task preparation, but also sheds new light on how prefrontal and parietal areas might work in concert to support flexible and goal-oriented control of behavior.

Do tasks matter in task switching? Dissociating domain-general from context-specific brain activity.

Throughout the past decade, the task-switching paradigm has been used extensively as a tool to delineate the neural mechanisms underlying flexible and goal-directed action control. Yet, given a large number of experimental procedures, the task-switching literature has yielded considerable inconsistencies calling for a systematic evaluation of the impact of methodological parameters. In the present study, we examine a fundamental and implicit assumption that has guided previous research on task switching. Does switch-related brain activation (i.e., the contrast between preparatory activity on switch versus repetition trials) reflect abstract cognitive control processes that are independent of specific task demands, and thus equivalent across different types of tasks? To answer this question, we compared the data of two fMRI studies that examined updating of task goals and/or stimulus-response mappings under almost identical protocols, but using entirely different tasks. In line with an abstract control process view, our results show that the vast majority of switch-related brain activity is insensitive to the context in which it occurs. The only region that exhibited a reliable contextual modulation was the anterior cingulate cortex, indicating that its contribution to preparatory adjustments might be linked to specific task demands.

More than associations: an ideomotor perspective on mirror neurons.

In this commentary, we propose an extension of the associative approach of mirror neurons, namely, ideomotor theory. Ideomotor theory assumes that actions are controlled by anticipatory representations of their sensory consequences. As we outline below, this extension is necessary to clarify a number of empirical observations that are difficult to explain from a purely associative perspective.

Goal-seeking compresses neural codes for space in the human hippocampus and orbitofrontal cortex.

Humans can navigate flexibly to meet their goals. Here, we asked how the neural representation of allocentric space is distorted by goal-directed behavior. Participants navigated an agent to two successive goal locations in a grid world environment comprising four interlinked rooms, with a contextual cue indicating the conditional dependence of one goal location on another. Examining the neural geometry by which room and context were encoded in fMRI signals, we found that map-like representations of the environment emerged in both hippocampus and neocortex. Cognitive maps in hippocampus and orbitofrontal cortices were compressed so that locations cued as goals were coded together in neural state space, and these distortions predicted successful learning. This effect was captured by a computational model in which current and prospective locations are jointly encoded in a place code, providing a theory of how goals warp the neural representation of space in macroscopic neural signals.

Theoretical distinction between functional states in working memory and their corresponding neural states.

Working memory (WM) is important for guiding behaviour, but not always for the next possible action. Here we define a WM item that is currently relevant for guiding behaviour as the functionally "active" item; whereas items maintained in WM, but not immediately relevant to behaviour, are defined as functionally "latent". Traditional neurophysiological theories of WM proposed that content is maintained via persistent neural activity (e.g., stable attractors); however, more recent theories have highlighted the potential role for "activity-silent" mechanisms (e.g., short-term synaptic plasticity). Given these somewhat parallel dichotomies, functionally active and latent cognitive states of WM have been associated with storage based on persistent-activity and activity-silent neural mechanisms, respectively. However, in this article we caution against a one-to-one correspondence between functional and activity states. We argue that the principal theoretical requirement for active and latent WM is that the corresponding neural states play qualitatively different functional roles. We consider a number of candidate solutions, and conclude that the neurophysiological mechanisms for functionally active and latent WM items are theoretically independent of the distinction between persistent activity-based and activity-silent forms of WM storage.

Controlling the self: the role of the dorsal frontomedian cortex in intentional inhibition.

Intentional inhibition refers to the suppression of ongoing behavior on the basis of internally-generated decisions. This ability to cancel planned actions at the last moment is thought to be critical for self-control and has been related to activation in a circumscribed region of the dorsal frontomedian cortex (dFMC). Preliminary theories of intentional inhibition were based on studies that exclusively examined the cancellation of motor responses, and consequently concluded that this region serves the suppression of motor output. Yet recent evidence suggests that the dFMC is also involved in inhibitory control over more abstract internal states such as emotions or desires that have no immediate behavioral output. In this review, we therefore wish to put forth a new integrative perspective on the role of the dFMC in human self-control. We will argue that by virtue of its anatomical location and functional connections, this area may subserve the disengagement from current urges and impulses, thus facilitating successful exertions of self-control across a wide range of contexts by overcoming a self-focused perspective. We will discuss the fit of this view of the dFMC with the existing literature, identify critical experimental determinants for engaging the dFMC in intentional inhibition, and outline promising perspectives for future research.

Priming determinist beliefs diminishes implicit (but not explicit) components of self-agency.

Weakening belief in the concept of free will yields pronounced effects upon social behavior, typically promoting selfish and aggressive over pro-social and helping tendencies. Belief manipulations have furthermore been shown to modulate basic and unconscious processes involved in motor control and self-regulation. Yet, to date, it remains unclear how high-level beliefs can impact such a wide range of behaviors. Here, we tested the hypothesis that priming disbelief in free will diminishes the sense of agency, i.e., the intrinsic sensation of being in control of one's own actions. To this end, we measured participants' implicit and explicit self-agency under both anti-free will and control conditions. Priming disbelief in free will reduced implicit but not explicit components of agency. These findings suggest that free will beliefs have a causal impact on the pre-reflective feeling of being in control of one's actions, and solidify previous proposals that implicit and explicit agency components tap into distinct facets of action awareness.

Power to the will: how exerting physical effort boosts the sense of agency.

The sense of agency refers to the experience of being in control of one's actions and their consequences. The 19th century French philosopher Maine de Biran proposed that the sensation of effort might provide an internal cue for distinguishing self-caused from other changes in the environment. The present study is the first to empirically test the philosophical idea that effort promotes self-agency. We used intentional binding, which refers to the subjective temporal attraction between an action and its sensory consequences, as an implicit measure of the sense of agency. Effort was manipulated independent of the primary task by requiring participants to pull stretch bands of varying resistance levels. We found that intentional binding was enhanced under conditions of increased effort. This suggests not only that the experience of effort directly contributes to the sense of agency, but also that the integration of effort as an agency cue is non-specific to the effort requirement of the action itself.

On the influence of reward on action-effect binding.

Ideomotor theory states that the formation of anticipatory representations about the perceptual consequences of an action [i.e., action-effect (A-E) binding] provides the functional basis of voluntary action control. A host of studies have demonstrated that A-E binding occurs fast and effortlessly, yet little is known about cognitive and affective factors that influence this learning process. In the present study, we sought to test whether the motivational value of an action modulates the acquisition of A-E associations. To this end, we linked specific actions with monetary incentives during the acquisition of novel A-E mappings. In a subsequent test phase, the degree of binding was assessed by presenting the former effect stimuli as task-irrelevant response primes in a forced-choice response task, absent reward. Binding, as indexed by response priming through the former action-effects, was only found for reward-related A-E mappings. Moreover, the degree to which reward associations modulated the binding strength was predicted by individuals' trait sensitivity to reward. These observations indicate that the association of actions and their immediate outcomes depends on the motivational value of the action during learning, as well as on the motivational disposition of the individual. On a larger scale, these findings also highlight the link between ideomotor theories and reinforcement-learning theories, providing an interesting perspective for future research on anticipatory regulation of behavior.