Review
Dopamine modulates neural networks involved in effort-based decision-making

https://doi.org/10.1016/j.neubiorev.2008.10.010Get rights and content

Abstract

Recent animal and human studies suggest that the dorsal anterior cingulate cortex (dACC) and its related subcortical structures including nucleus accumbens (NAc) are in the center of a brain network that determines and pursues the best option from available alternatives. Specifically, the involvement of the dACC network in decision-making can be categorized under two broad processes of evaluation and execution. The former aims to determine the most cost-effective option while the latter aims to attain the preferred option. The present article reviews neural and molecular findings to show that the dopamine system might modulate this dACC network at multiple levels to optimize both processes. Several lines of evidence suggest that the dopamine system has a bimodal effect, allows the network to compare different representations in the evaluation phase, and focuses the network on the preferred representation in the execution phase. This is apparently achieved by modulating other neurotransmission systems and by transmitting different signals via D1 vs. D2 receptor subtypes and phasic vs. tonic firing.

Introduction

All animals continuously face decision-making circumstances in which they must choose between two or more options. Making apt decisions is vital as it has a significant impact on key evolutionary outcomes such as survival and reproduction (Gibson and Langen, 1996, Krebs, 1978, Mulder, 1990). Decision-making is a complex process and involves different variables. Recent studies have started to shed light on the neurobiology of decision-making. However, such studies vary widely and include investigations conducted across different species from rats to humans, with investigative methods ranging from the behavioral through to the neural and molecular levels. The aim of the present article is to review the previous findings, using a common framework and terminology. We focus specifically on the decisions that are made to solve a current problem and not on those that are aimed at long-term outcomes. The review also focuses on the decisions that are made to exploit the available options to greatest benefit, rather than those that are adventurous and explore novel alternatives. We provide evidence that decision-making is related to a brain network centered on the dorsal anterior cingulate cortex (dACC) and its related subcortical structures. We also consider how the dopamine system modulates this network at multiple levels to facilitate an optimal decision.

Section snippets

Neural network of decision-making

There are considerable connections between the anterior cingulate cortex (ACC) and the striatum including the nucleus accumbens (NAc) across mammalian species. Reciprocal connections between these brain regions were described in humans more than two decades ago (Alexander et al., 1986); the ACC projects to the NAc, which projects back to the ACC via the mediodorsal (Ongur and Price, 2000, Ray and Price, 1993, Yeterian and Pandya, 1988) and anteroventral nuclei of the thalamus (Xiaob and Barbas,

Molecular basis of decision-making

Assuming that the dACC-striatum-thalamus circuit and its dopamine system are involved in decision-making, the next question is how dopamine modulates this circuit to facilitate an optimal decision. Below, we first review different cortico-basal ganglia models to illustrate an overall view of how the dopamine system modulates the network. Then, we review dopamine studies to provide clues on how this system can facilitate progression of different aspects of decision-making at the molecular level.

Conclusions and implications

Decision-making requires processing of a variety of different variables. These variables can be categorized under two broad processes of evaluation and execution. The former consists of outcome appraisal and cost–benefit analysis and aims to determine the best possible option while the latter consists of motivation and action sequencing and aims to attain the preferred option. Recent animal and human studies suggest that the dACC and its related subcortical structures are at the center of a

Acknowledgements

Dr Yücel is supported by a NH&MRC Clinical Career Development Award (ID: 509345). Prof Pantelis's research is supported by NHMRC Program Grant (ID: 350241). The authors thank Dr. Alex Fornito for his helpful comments on the manuscript.

References (169)

  • M.S. Cousins et al.

    Nucleus accumbens dopamine depletions alter relative response allocation in a T-maze cost/benefit task

    Behavioural Brain Research

    (1996)
  • H.D. Critchley et al.

    Anterior cingulate activity during error and autonomic response

    Neuroimage

    (2005)
  • D.P. Daberkow et al.

    Relation between methamphetamine-induced monoamine depletions in the striatum and sequential motor learning

    Pharmacology, Biochemistry and Behavior

    (2005)
  • E.R. de Bruijn et al.

    Effects of antipsychotic and antidepressant drugs on action monitoring in healthy volunteers

    Brain Research

    (2006)
  • M.R. DeLong

    Primate models of movement disorders of basal ganglia origin

    Trends in Neurosciences

    (1990)
  • N.U. Dosenbach et al.

    A core system for the implementation of task sets

    Neuron

    (2006)
  • M. Ernst et al.

    Choice selection and reward anticipation: an fMRI study

    Neuropsychologia

    (2004)
  • N. Eshel et al.

    Neural substrates of choice selection in adults and adolescents: development of the ventrolateral prefrontal and anterior cingulate cortices

    Neuropsychologia

    (2007)
  • R.M. Gibson et al.

    How do animals choose their mates?

    Trends in Ecology & Evolution

    (1996)
  • P.S. Goldman-Rakic et al.

    D(1) receptors in prefrontal cells and circuits

    Brain Research. Brain Research Reviews

    (2000)
  • A.A. Grace

    Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia

    Neuroscience

    (1991)
  • A.A. Grace et al.

    Regulation of firing of dopaminergic neurons and control of goal-directed behaviors

    Trends in Neurosciences

    (2007)
  • A.M. Graybiel

    The basal ganglia: learning new tricks and loving it

    Current Opinion in Neurobiology

    (2005)
  • Y.L. Hurd et al.

    D1 and D2 dopamine receptor mRNA expression in whole hemisphere sections of the human brain

    Journal of Chemical Neuroanatomy

    (2001)
  • A. Kacelnik et al.

    Risk-sensitivity: crossroads for theories of decision making

    Trends in Cognitive Sciences

    (1997)
  • K.A. Keay et al.

    Parallel circuits mediating distinct emotional coping reactions to different types of stress

    Neuroscience and Biobehavioral Reviews

    (2001)
  • S. Kheramin et al.

    Role of the orbital prefrontal cortex in choice between delayed and uncertain reinforcers: a quantitative analysis

    Behavioural Processes

    (2003)
  • B. Knutson et al.

    Amphetamine modulates human incentive processing

    Neuron

    (2004)
  • B. Knutson et al.

    FMRI visualization of brain activity during a monetary incentive delay task

    Neuroimage

    (2000)
  • J.S. Lonstein et al.

    Site and behavioral specificity of periaqueductal gray lesions on postpartum sexual, maternal, and aggressive behaviors in rats

    Brain Research

    (1998)
  • A.A. Marsh et al.

    Response options and expectations of reward in decision-making: the differential roles of dorsal and rostral anterior cingulate cortex

    Neuroimage

    (2007)
  • J.W. Mink

    The basal ganglia: focused selection and inhibition of competing motor programs

    Progress in Neurobiology

    (1996)
  • R.J. Morecraft et al.

    Convergence of limbic input to the cingulate motor cortex in the rhesus monkey

    Brain Research Bulletin

    (1998)
  • K.L. Nowend et al.

    D1 or D2 antagonism in nucleus accumbens core or dorsomedial shell suppresses lever pressing for food but leads to compensatory increases in chow consumption

    Pharmacology, Biochemistry and Behavior

    (2001)
  • G.E. Alexander et al.

    Parallel organization of functionally segregated circuits linking basal ganglia and cortex

    Annual Review of Neuroscience

    (1986)
  • C. Amiez et al.

    Anterior cingulate error-related activity is modulated by predicted reward

    European Journal of Neuroscience

    (2005)
  • X. An et al.

    Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in macaque monkeys

    Journal of Comparative Neurology

    (1998)
  • C. Baleydier et al.

    The duality of the cingulate gyrus in monkey. Neuroanatomical study and functional hypothesis

    Brain

    (1980)
  • T.D. Barnes et al.

    Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories

    Nature

    (2005)
  • A. Bechara et al.

    Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making

    Journal of Neuroscience

    (1999)
  • A. Bechara et al.

    Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions

    Brain

    (2000)
  • G.S. Berns et al.

    A computational model of how the basal ganglia produce sequences

    Journal of Cognitive Neuroscience

    (1998)
  • S.M. Beurze et al.

    Integration of target and effector information in the human brain during reach planning

    Journal of Neurophysiology

    (2007)
  • G. Bezzina et al.

    Effects of quinolinic acid-induced lesions of the nucleus accumbens core on inter-temporal choice: a quantitative analysis

    Psychopharmacology

    (2007)
  • K. Blair et al.

    Choosing the lesser of two evils, the better of two goods: specifying the roles of ventromedial prefrontal cortex and dorsal anterior cingulate in object choice

    Journal of Neuroscience

    (2006)
  • R.M. Bilder et al.

    The catechol-O-methyltransferase polymorphism: relations to the tonic-phasic dopamine hypothesis and neuropsychiatric phenotypes

    Neuropsychopharmacology

    (2004)
  • S. Both et al.

    Effect of a single dose of levodopa on sexual response in men and women

    Neuropsychopharmacology

    (2005)
  • M. Botvinick et al.

    Conflict monitoring versus selection-for-action in anterior cingulate cortex

    Nature

    (1999)
  • J.W. Brown et al.

    Learned predictions of error likelihood in the anterior cingulate cortex

    Science

    (2005)
  • G. Bush et al.

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

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

    (2002)
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