Behavioral and Cognitive Neuroscience Reviews http://bcn.sagepub.com/ The Cognitive Neuroscience of Human Decision Making: A Review and Conceptual Framework Lesley K. Fellows Behav Cogn Neurosci Rev 2004 3: 159 DOI: 10.1177/1534582304273251 The online version of this article can be found at: http://bcn.sagepub.com/content/3/3/159 Published by: http://www.sagepublications.com Additional services and information for Behavioral and Cognitive Neuroscience Reviews can be found at: Email Alerts: http://bcn.sagepub.com/cgi/alerts Subscriptions: http://bcn.sagepub.com/subscriptions Reprints: http://www.sagepub.com/journalsReprints.nav Permissions: http://www.sagepub.com/journalsPermissions.nav Citations: http://bcn.sagepub.com/content/3/3/159.refs.html >> Version of Record - Jan 14, 2005 What is This? Downloaded from bcn.sagepub.com at MCGILL UNIVERSITY LIBRARY on July 18, 2012 10.1177/1534582304273251BEHAVIORALFellows / HUMAN AND DECISION COGNITIVE MAKING NEUROSCIENCE REVIEWS The Cognitive Neuroscience of Human Decision Making: A Review and Conceptual Framework Lesley K. Fellows Montreal Neurological Institute Decision making, the process of choosing between options, is a tions of decision-making research in disciplines as varied fundamental human behavior that has been studied intensively as cognitive psychology, economics, and computer sci- by disciplines ranging from cognitive psychology to economics. ence (Baron, 1994; Kahneman, Slovic, & Tversky, 1982; Despite the importance of this behavior, the neural substrates of Lipshitz, Klein, Orasanu, & Salas, 2001; Stirling, 2003), decision making are only beginning to be understood. Impaired which may be very useful in guiding this fledgling field. decision making is recognized in neuropsychiatric conditions This article will attempt to clarify what is known about such as dementia and drug addiction, and the inconsistencies the neural bases of human decision making and what is and biases of healthy decision makers have been intensively stud- not. First, the literature on decision making in patients ied. However, the tools of cognitive neuroscience have only with frontal lobe damage will be reviewed. In the past sev- recently been applied to understanding the brain basis of this eral years, this work has had an important impact on the complex behavior. This article reviews the literature on the cogni- study of both normal and pathological decision making. tive neuroscience of human decision making, focusing on the However, the inconsistencies and difficulties in inter- roles of the frontal lobes, and provides a conceptual framework preting this growing body of work highlight the need for for organizing this disparate body of work. a more systematic approach. Although there is no true consensus model of decision making, consistent features can be found in theories emerging from various disci- Key Words: executive function, prefrontal cortex, fron- plines. These recurring themes can be distilled into a tal lobes, amygdala, reward, impulsivity useful framework for beginning to understand how the general processes of decision making may be repre- Decision making is a vital component of human sented in the brain. In the second part of this article, I behavior. Like other executive processes, it involves the will propose such a framework and review the cognitive synthesis of a variety of kinds of information: multimodal neuroscience literature that addresses these more sensory inputs, autonomic and emotional responses, fundamental aspects of decision making. past associations, and future goals. These inputs must be integrated with information about uncertainty, timing, cost-benefit, and risk and then applied to select appro- NEUROANATOMY priate actions. This processing has further practical con- The cognitive neuroscience literature on decision straints: It must be completed rapidly and must retain making has focused on a limited set of brain regions. some degree of flexibility to be useful in a changing envi- ronment. Despite this daunting complexity, recent work using a variety of methods has begun to elucidate the Author’s Note: This work was supported by National Institutes of Health Grant R21 NS045074, a clinician-scientist award from the Cana- component processes underlying decision making and dian Institutes of Health Research, and an award from the Fonds de la to localize these processes in the human brain. recherche en sante de Quebec. I would like to thank Martha Farah and This is a new focus for cognitive neuroscience. Andrea Heberlein for comments on earlier drafts of the article. Inroads have been made in understanding elements of Behavioral and Cognitive Neuroscience Reviews decision making, but the connections between these ele- Volume 3 Number 3, September 2004 159-172 DOI: 10.1177/1534582304273251 ments remain unclear. However, there are long tradi- © 2004 Sage Publications 159 Downloaded from bcn.sagepub.com at MCGILL UNIVERSITY LIBRARY on July 18, 2012 160 BEHAVIORAL AND COGNITIVE NEUROSCIENCE REVIEWS Figure 1: Ventral and Lateral Views of the Frontal Lobes, Showing the Approximate Borders of the Various Sectors Described in the Text. There has been particular interest in the role of the nected, emphasizing the synthetic and integrative role of prefrontal cortex in general and the ventromedial the region in general (Barbas, 2000). The cortical anat- prefrontal cortex in particular. The terminology used to omy is summarized in Figure 1; for additional accessible describe these regions can be confusing. Although strict reviews of this anatomy, see Mesulam (2003) and Stuss boundaries are rarely defined, the ventromedial frontal and Levine (2002). lobe (VMF) includes the medial portion of orbitofrontal Several subcortical structures have been implicated in cortex (OFC) and the ventral portion of the medial wall decision making. The amygdala appears to have a role, of the frontal lobes. The lateral OFC is often grouped perhaps in part through its important interconnections with the ventral portion of the lateral convexity of the with the OFC. Recent work has also begun to examine frontal lobe and labeled the ventrolateral frontal lobe the role of mesolimbic and mesocortical dopaminergic (VLF), although this distinction is more frequent in projections (arising in the substantia nigra and ventral functional imaging than in lesion studies. Most com- tegmental area of the midbrain and terminating in the monly, these ventral areas are contrasted with ventral striatum-nucleus accumbens, dorsal striatum dorsolateral prefrontal cortex (DLF; for a detailed dis- [caudate-putamen], and prefrontal cortex) that have cussion of the relationship between these areas and been implicated in reward and addiction (Schultz, 2002; Brodmann’s nomenclature, see Chiavaras, LeGoualher, Wise, 2002). There is also some work supporting a role Evans, & Petrides, 2001; Petrides & Pandya, 1999, 2002). for prefrontal serotonin in aspects of reinforcement- This broad division of prefrontal cortex is a reason- driven learning and deciding (Clarke, Dalley, Crofts, able starting point because, generally speaking, these Robbins, & Roberts, 2004; Rogers et al., 2003; Rogers, three cortical areas have different cytoarchitecture and Owen, et al., 1999). different patterns of connectivity, both in humans This should not be viewed as a definitive list of the (Petrides & Pandya, 1999, 2002) and in nonhuman pri- neuroanatomical substrates of decision making but mates (Barbas, 2000; Dombrowski, Hilgetag, & Barbas, rather as a useful starting point for understanding the 2001). Ventral medial prefrontal and caudal existing literature. It reflects the biases of the initial orbitofrontal regions are classified as paralimbic cortex. investigators in this relatively new field, primarily driven These cortical areas are closely connected to limbic by clinical observations of patients with focal brain dam- structures such as the amygdala and hypothalamus, pro- age and more recently by the results of functional imag- vide descending inputs to midbrain structures including ing studies of reward processing in humans and the periaqueductal gray and substantia nigra, and receive insight that the poor choices of substance abusers sug- polymodal sensory inputs (An, Bandler, Ongur, & Price, gests a role for the reward circuitry first identified in ani- 1998; Barbas, 2000; Ghashghaei & Barbas, 2002; Ongur, mal models of addiction in normal and pathologic An, & Price, 1998; Price, Carmichael, & Drevets, 1996; human decision making (Bechara & Damasio, 2002; Rempel-Clower & Barbas, 1998). In contrast, DLF is Bechara, Dolan, & Hindes, 2002; Cavedini, Riboldi, heteromodal association cortex, with more restricted Keller, D’Annucci, & Bellodi, 2002; Grant, Contoreggi, sensory inputs, and has been implicated in working & London, 2000). Indeed, recent single-unit work in memory and selective attentional processes. However, monkeys has demonstrated reward-sensitive neurons in all areas of the prefrontal cortex are heavily intercon- a variety of other regions, including the sensory Downloaded from bcn.sagepub.com at MCGILL UNIVERSITY LIBRARY on July 18, 2012 Fellows / HUMAN DECISION MAKING 161 thalamus (Komura et al., 2001) and parietal cortex (Platt Weber, Hsee, & Welch, 2001). Such reports have empha- & Glimcher, 1999; Sugrue, Corrado, & Newsome, 2004). sized impairments in the emotional aspect of decision making. Empirical studies of elements of decision mak- LESIONS ing following frontal lobe damage have been under- taken more recently (e.g.,