Neurocognitive mechanisms of cognitive control: The role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning

doi:10.1016/j.bandc.2004.09.016

Brain and Cognition

Volume 56, Issue 2, November 2004, Pages 129-140

https://doi.org/10.1016/j.bandc.2004.09.016 Get rights and content

Abstract

Convergent evidence highlights the differential contributions of various regions of the prefrontal cortex in the service of cognitive control, but little is understood about how the brain determines and communicates the need to recruit cognitive control, and how such signals instigate the implementation of appropriate performance adjustments. Here we review recent progress from cognitive neuroscience in examining some of the main constituent processes of cognitive control as involved in dynamic decision making: goal-directed action selection, response activation and inhibition, performance monitoring, and reward-based learning. Medial frontal cortex is found to be involved in performance monitoring: evaluating outcome vis-à-vis expectancy, and detecting performance errors or conflicting response tendencies. Lateral and orbitofrontal divisions of prefrontal cortex are involved in subsequently implementing appropriate adjustments.

Introduction

Flexible goal-directed behavior requires an adaptive cognitive control system for selecting contextually relevant information, and for organizing and optimizing processing pathways. In goal-directed behavior, decision-making (deciding which action to take) is biased by the anticipation of the action’s outcome. Differences between anticipated and actual outcome can be used to optimize behavior. Evaluating the adequacy and success of performance is instrumental in determining and implementing appropriate behavioral adjustments. For instance, if anticipated reward is not delivered this can be used to learn regularities in action-reward contingencies; negative feedback can be used to shift from one set of stimulus-response translation rules to another; detection of a performance error may be used to tighten control (e.g., shift to a more conservative speed/accuracy balance). Evidence from cognitive neuroscience is beginning to converge on differential contributions of various regions of the prefrontal cortex (PFC) in the service of cognitive control, but conspicuously little is known about how the brain determines and communicates the need to recruit cognitive control, and how such signals instigate the implementation of appropriate performance adjustments. Here we review evidence from recent reports on some of the main constituent processes of cognitive control as involved in dynamic decision making: goal-directed action selection, response activation and inhibition, performance monitoring, and reward-based learning.

Clearly, the agent that selects, activates, inhibits, monitors, and learns is ‘the individual’ rather than the PFC. It is, therefore, essential to specify more precisely the way in which such decision-making operations are supported by PFC; this, in turn, requires an understanding of the functional anatomy and effective connectivity of PFC. The next section will describe in some detail the current state of affairs and advancements in this regard. This framework will provide the background for the present review.

Section snippets

Anatomy and connectivity of the PFC

The main gyri of PFC in humans roughly comprise three main anatomical divisions: the lateral gyri (superior, middle, and inferior frontal gyri), the orbitofrontal gyri (medial and lateral), and the medial wall (medial frontal gyrus and cingulate gyrus). More conventional, but along similar lines, a cytoarchitectonic partitioning of PFC yields again three main divisions: lateral PFC, orbitofrontal cortex (OFC), and medial frontal cortex (MFC). Using the dimensions medial/lateral, rostral/caudal,

Functional specialization within PFC

Hardwired connections (whether or not potentiated by extensive learning and experience) between sensory stimuli and corresponding responses afford rapid performance of natural, stereotyped, or well-trained behaviors without demanding much attention. However, these behaviors are typically rigid, resisting generalization to novel situations, and thus need to be overruled when our goals and intentions require an alternative behavioral repertoire. When goal-directed action selection is needed (such

Goal-directed action-selection and reward-based association learning

The neurocognitive processes involved in decision making are especially relevant in choices that involve some perplexity, that is, when the alternatives are difficult to distinguish, have uncertain pay-offs or require prior knowledge to resolve them (Schall, 2001). Whereas choice refers to the final commitment to one alternative, decision refers to the preceding deliberation about the alternatives, the process that leads to a particular choice. By reinforcing the patterns of PFC activity

Response activation and response inhibition

Especially when the selected action has to compete for activation with strong alternatives, cognitive control may be needed to resist interference from these alternatives and ensure the timely and uninterrupted activation of the selected response (cf. Miller & Cohen, 2001). Inhibitory control is postulated as one of the mechanisms by which PFC exerts its coordinating effects on subsidiary processes implemented by posterior cortical and subcortical regions to optimize behavior. Inhibition can be

Performance monitoring

Flexible adjustments of behavior and reward-based association learning require the continuous assessment of ongoing actions and the outcomes of these actions. The ability to monitor and compare ongoing actions and performance outcomes with internal goals and standards is critical for optimizing decision making. According to a recent review of primate and human studies, largely overlapping brain areas, clustering in the rostral cingulate zone (RCZ, the posterior MFC border zone between the

The relation between performance monitoring and performance adjustment

Response errors have been reported to be consistently foreshadowed by modulation of RCZ activity during the immediately preceding (correct) response (Allain et al., in press, Ridderinkhof et al., 2003). This modulation, as expressed in event-related brain potentials, may reflect a transient disengagement of the monitoring system, resulting in occasional failures to implement appropriate control adjustments, and hence errors. Consistent with the monitor-disengagement notion, the behavioral

A special edition

This review paper sets the stage for a special issue of Brain and Cognition dedicated to neurocognitive mechanisms of performance monitoring and inhibitory control. The special issue was inspired by a symposium organized by the present guest editors in Amsterdam, April 2003, with financial support from the EPOS graduate school and the Netherlands Organization for Scientific Research. The articles in this special issue are all invited, but fully peer-reviewed to meet the high standards of Brain

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Neurocognitive mechanisms of cognitive control: The role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning

Abstract

Introduction

Section snippets

Anatomy and connectivity of the PFC

Functional specialization within PFC

Goal-directed action-selection and reward-based association learning

Response activation and response inhibition

Performance monitoring

The relation between performance monitoring and performance adjustment

A special edition

Biological Psychiatry

Trends in Cognitive Sciences

Acta Psychologica

Neuroscience and Biobehavioral Reviews

Neuron

Neuron

Neuroimage

Brain and Cognition

Brain and Cognition

Journal of the American Academy of Child and Adolescent Psychiatry

Neuropsychologia

Brain and Cognition

Trends in Neurosciences

Brain and Cognition

NeuroImage

Neuroscience Letters

Trends in Neurosciences

Brain and Cognition

Neuron

Neuropsychologia

Neuron

Current Opinion in Neurobiology

Behavioral and Brain Research

Brain and Cognition

NeuroImage

Brain and Cognition

Neuroscience Letters

Seminars in Neuroscience

Neuroimage

Neuroimage

Brain Research

Neuron

Neuron

Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans

Nature Neuroscience

Architecture and intrinsic connections of the prefrontal cortex in the rhesus-monkey

Journal of Comparative Neurology

Prefrontal cortex and decision-making in a mixed strategy game

Nature Neuroscience

Emotion, decision-making and the orbitofrontal cortex

Cerebral Cortex

Conflict monitoring and cognitive control

Psychological Review

Neural mechanisms of transient and sustained cognitive control during task switching

Neuron

Executive control in the Simon effect: An electropmyographic and distributional analysis

Psychological Research

Suppression of task-related saccades by electrical stimulation in the primate’s frontal eye field

Journal of Neurophysiology

Dorsal anterior cingulate cortex: A role in reward-based decision-making

Proceedings of the National Academy of Sciences of the United States of America

Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys

Journal of Comparative Neurology

Quantitative brain magnetic resonance imaging in attention-deficit hyperactivity disorder

Archives of General Psychiatry

Anterior cingulate cortex, error detection, and the on line monitoring of performance

Science

Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging

Journal of Neuroscience

Human cingulate cortex and autonomic control: Converging neuroimaging and clinical evidence

Brain

Movement-related neuronal activity selectively coding either direction or muscle pattern in three motor areas of the monkey

Journal of Neurophysiology