Review
Contributions of the prefrontal cortex to the neural basis of human decision making

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Abstract

The neural basis of decision making has been an elusive concept largely due to the many subprocesses associated with it. Recent efforts involving neuroimaging, neuropsychological studies, and animal work indicate that the prefrontal cortex plays a central role in several of these subprocesses. The frontal lobes are involved in tasks ranging from making binary choices to making multi-attribute decisions that require explicit deliberation and integration of diverse sources of information. In categorizing different aspects of decision making, a division of the prefrontal cortex into three primary regions is proposed. (1) The orbitofrontal and ventromedial areas are most relevant to deciding based on reward values and contribute affective information regarding decision attributes and options. (2) Dorsolateral prefrontal cortex is critical in making decisions that call for the consideration of multiple sources of information, and may recruit separable areas when making well defined versus poorly defined decisions. (3) The anterior and ventral cingulate cortex appear especially relevant in sorting among conflicting options, as well as signaling outcome-relevant information. This topic is broadly relevant to cognitive neuroscience as a discipline, as it generally comprises several aspects of cognition and may involve numerous brain regions depending on the situation. The review concludes with a summary of how these regions may interact in deciding and possible future research directions for the field.

Introduction

Decision making is required for behaviors ranging from simple movements to the complex consideration of multiple alternatives and reasoning about distant future consequences. The topic has long been studied in a variety of separate disciplines with an equally broad range of techniques, ranging from investigations of the neuronal correlates of binary choice in non-human primates to complex analyses of group decisions in applied settings. This breadth has resulted in a large gap so that research into the neural basis of decision making has often been limited to the simplest of decision processes and has remained largely disconnected from applications to complex human judgments, while high level decision research has remained heavily descriptive with theories of human decision making rarely making solid connections to neurophysiological underpinnings. Through recent efforts reviewed here, this state of decision research is beginning to change.

Investigations over the last decade have begun to view decision making from the perspective of cognitive neuroscience and are closing this longstanding gap between the ends of the decision research spectrum. This review describes studies that have managed to move toward a greater understanding of the neural systems contributing to decision making, while also capturing some of the cognitive complexity and relevance to deciding in everyday life that had previously been strictly the domain of purely descriptive decision research. Viewing complex human decision making in terms of the neural processing that underlies its potentially numerous subprocesses may be a critical next step in the effort to understand human decision making and most critically the mechanisms behind why people decide in the ways they do. This unified approach has the potential to move theories of human decision making towards incorporating the effects that neural system interactions have on reasoning and deciding. This unification may not only better inform theorists about the substrates of traditional findings in decision research, but also lead to integrating normal decision making with the disordered decision processes observed in a variety of patients with brain damage, individuals with mental illnesses, and drug abusers, leading to better characterizations of the behavioral deficits found in disordered populations.

From the neural perspective, this paper will argue that the prefrontal cortex is a key brain region in many aspects human decision making. Evidence for this claim includes an extensive neurological history of disordered decision making in patients who have sustained frontal lesions dating back to the now famous case of Phineas Gage. Additionally, many recent neuroimaging studies have investigated decision relevant subprocessing, finding prominent prefrontal activity regularly across a number of studies including those investigating abstract reward processing, guessing, planning, inductive reasoning, and manipulating complex information in working memory. In addition to the prominent role of the prefrontal cortex in deciding, it is further argued that this region may be fractionated according to both separable subprocesses relevant to deciding and the neural connectivity of separable prefrontal regions to other brain areas. This fractionation is not to be taken as an indication that there are autonomous subdivisions of the frontal lobes that carry out functions isolated from the rest of the brain, but rather that different areas of the prefrontal cortex appear to be engaged in separable multi-component neural systems involved in separable cognitive processes. As noted by Fuster [1], the frontal lobes should not be considered to be autonomous in carrying out cognitive processes, but rather they interact with many other brain areas.

The goal of this paper is to describe recent advances made in the investigation of neural decision making and present a picture of the neural processing in prefrontal regions that is relevant to complex human decision making. While the scientific study of decision making in the brain is relatively new, several intriguing areas of research have produced results that reveal many clues to its neural architecture.

Anatomically, there is evidence that different frontal regions contribute uniquely to different decision subprocesses. The orbitofrontal cortex (OFC) appears to be relevant in situations involving incentive gain [3], [4], [5], [6], best-guess estimations [7], [8], and the emotional experience associated with gains and losses. Studies of the OFC in non-human primates, humans with brain injury, and neuroimaging studies indicate that the region is heavily involved in processing many types of rewards and making rapid changes in behavior to accommodate environmental changes [2]. These abilities implicate the OFC in responding to outcomes in the environment, and adjusting behavior to fit different situations. The dorsolateral prefrontal cortex (DLPFC) tends to be most involved in manipulating decision relevant information on-line, and in conscious deliberation during decisions. Extensive research has implicated DLPFC in working memory [11], [12], [13], which is a cognitive requirement for maintaining decision goals, considering options, and integrating the two to predict future outcomes and probabilities of meeting goals. There is also evidence that the DLPFC is involved in deciding under uncertain circumstances that have no objectively correct answer [14], [15], [16], [17]. Other important frontal areas include the anterior cingulate (AC), involved in conflict processing [18], [19] and outcome relevant processing [66], [122] and the frontopolar cortex, which has been implicated in rule-based deciding [123], and self-generated information [124].

Section snippets

The prefrontal cortex

Recent analyses of the cytoarchitecture and connectivity of prefrontal areas have provided detailed descriptions of several of the prefrontal systems that appear to be important in processing decision-relevant information. This anatomical overview will serve as a reference point for the remainder of this paper and will be particularly relevant to the discussions of findings from neuroimaging. The content of this section is mostly restricted to prefrontal regions; however, some discussion of

The OFC: reward, emotion, and environmental adaptiveness

The OFC and ventromedial prefrontal regions may be viewed as an integration center for emotional content from other areas of the limbic system. They are involved in processing the reward value of environmental stimuli, a function central to decision making, as it may underlie the affective tinting that accompanies decision attributes, as well as the ‘gut feelings’ that have long been discussed in association with the act of making difficult decisions. Additionally, this area looks to be

Reward processing in the OFC

Research into the way humans make decisions has often focused on comparisons of risky and conservative behavior [50]. Such work inherently incorporates gains and losses, or rewards and punishments. Many important domains of decision research, including the study of risk taking behavior, the use of mental heuristics, and the framing effect have included precise manipulations of the degrees of potential rewards and punishments; thus reward and punishment have been central in characterizing human

Deficits in decision making tasks following OFC damage

Damage to the OFC has profound effects on human behavior, as described in the earlier section on patient deficits. Such damage may affect emotional states, social abilities, deciding, and reasoning. One of the core deficits of these patients is inability to appreciate and avoid possible negative future consequences of immediate actions. This has been referred to as a blindness to the future [9], which leads to an inability to avoid possible risks that may be incurred after deciding. Devastating

Further evidence for OFC involvement in decision making

The medial OFC and amygdala are closely related but evidence suggests that they have separable functions in risky decisions. Bechara et al. [63] assessed the differential behavioral effects of OFC and amygdala damage using their gambling task [61]. The medial OFC patient results replicated previous studies [61], [73], [74], showing that such patients are unable to decide advantageously and fail to show differential skin conductance activity in anticipation of risky choices. The results of the

DLPFC: reasoning, comparing, and evaluating

The DLPFC is known as one of the chief cortical areas responsible for maintaining and manipulating information in working memory. In addition to initial evidence from cell recording [91], [12], this phenomenon has also been well studied with functional neuroimaging [92], [93], [94], [95]. Working memory function has obvious value in decision making, as it is essential for maintaining a focus on goal hierarchies, monitoring the status of competing options, and possibly storing affective

Contributions of the AC to deciding

The AC cortex appears to be involved in decisions that are highly ambiguous. Recent neuroimaging results indicate that this area likely plays a key role in mental processing of situations in which there are conflicting options and high likelihood of making an error. An interpretation of AC function has recently been proposed by Botvinick et al. [18] that associates it instead with conflict monitoring. Additionally, AC activity appears to be relevant to various types of decisions that involve

Summary

The neural basis of decision making has long been elusive, and often considered to be too broad a problem to be tractable. The multitude of subprocesses that contribute to decision making and the many behaviors that involve some aspect of deciding add to the complexity. Recent interdisciplinary efforts involving neuroimaging, work with patients, electrophysiology, and work with animals have begun to make progress in solving some of the key questions about the mechanisms of decision making.

This

Acknowledgements

The author would like to thank Keith Holyoak, Matthew Lieberman, and Barbara Knowlton for their encouragement, helpful comments, and critical review of this manuscript. The manuscript also benefited greatly from the suggestions of two anonymous reviewers and the rapid pace of innovative research into the relevant topics. Fig. 4 was reprinted by permission of Elsevier Science from Neuropsychopharmacology by Rogers et al. [6], Neuropsychopharmacology, 20, 322–339, 1999 by American College of

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