Contributions of the nucleus accumbens and its subregions to different aspects of risk-based decision making

The nucleus accumbens (NAc) has been implicated in mediating different forms of decision making in humans and animals. In the present study, we observed that inactivation of the rat NAc, via infusion of GABA agonists, reduced preference for a large/risky option and increased response latencies on a probabilistic discounting task. Discrete inactivations of the NAc shell and core revealed further differences between these regions in mediating choice and response latencies, respectively. The effect on choice was attributable to reduced win–stay performance (i.e., choosing risky after a being rewarded for a risky choice on a preceding trial). Moreover, NAc inactivation altered choice only when the large/risky option had greater long-term value, in terms of the amount of food that could be obtained over multiple trials relative to the small/certain option. Inactivation of the NAc or the shell subregion also slightly reduced preference for larger rewards on a reward magnitude discrimination. Thus, the NAc seems to play a small role in biasing choice toward larger rewards, but its contribution to behavior is amplified when delivery of these rewards is uncertain, helping to direct response selection toward more favorable outcomes.

[1]  S. Killcross,et al.  Inactivation of the prelimbic, but not infralimbic, prefrontal cortex impairs the contextual control of response conflict in rats , 2007, The European journal of neuroscience.

[2]  S. Floresco,et al.  Dopaminergic regulation of limbic-striatal interplay. , 2007, Journal of psychiatry & neuroscience : JPN.

[3]  S. Floresco,et al.  Dissociable Roles for the Nucleus Accumbens Core and Shell in Regulating Set Shifting , 2006, The Journal of Neuroscience.

[4]  Rudolf N Cardinal,et al.  Effects of lesions of the nucleus accumbens core on choice between small certain rewards and large uncertain rewards in rats , 2005, BMC Neuroscience.

[5]  I. Weiner The "two-headed" latent inhibition model of schizophrenia: modeling positive and negative symptoms and their treatment , 2003, Psychopharmacology.

[6]  S. Floresco,et al.  Fundamental Contribution by the Basolateral Amygdala to Different Forms of Decision Making , 2009, The Journal of Neuroscience.

[7]  S. Floresco,et al.  Dopaminergic Modulation of Risk-Based Decision Making , 2009, Neuropsychopharmacology.

[8]  B. Balleine,et al.  The Role of the Nucleus Accumbens in Instrumental Conditioning: Evidence of a Functional Dissociation between Accumbens Core and Shell , 2001, The Journal of Neuroscience.

[9]  Camelia M. Kuhnen,et al.  Variability in Nucleus Accumbens Activity Mediates Age-Related Suboptimal Financial Risk Taking , 2010, The Journal of Neuroscience.

[10]  Sandra Jazbec,et al.  Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents , 2005, NeuroImage.

[11]  S. Floresco,et al.  Dopaminergic and Glutamatergic Regulation of Effort- and Delay-Based Decision Making , 2008, Neuropsychopharmacology.

[12]  John A. Detre,et al.  Neural correlates of voluntary and involuntary risk taking in the human brain: An fMRI Study of the Balloon Analog Risk Task (BART) , 2008, NeuroImage.

[13]  John R. C Christensen,et al.  Regional and temporal differences in real-time dopamine efflux in the nucleus accumbens during free-choice novelty , 1997, Brain Research.

[14]  J. Deakin,et al.  Effects of lesions of the orbitofrontal cortex on sensitivity to delayed and probabilistic reinforcement , 2002, Psychopharmacology.

[15]  S. Floresco,et al.  Prefrontal cortical contribution to risk-based decision making. , 2010, Cerebral cortex.

[16]  Bruce W. Smith,et al.  Neural Substrates of Reward Magnitude, Probability, and Risk during a Wheel of Fortune Decision-making Task Nih Public Access Cingulate Cortex in Decision-making , 2022 .

[17]  C. Pennartz,et al.  The nucleus accumbens as a complex of functionally distinct neuronal ensembles: An integration of behavioural, electrophysiological and anatomical data , 1994, Progress in Neurobiology.

[18]  C. Pennartz,et al.  Pharmacological Manipulation of Neuronal Ensemble Activity by Reverse Microdialysis in Freely Moving Rats: A Comparative Study of the Effects of Tetrodotoxin, Lidocaine, and Muscimol , 2007, Journal of Pharmacology and Experimental Therapeutics.

[19]  Joshua L. Jones,et al.  Phasic Nucleus Accumbens Dopamine Release Encodes Effort- and Delay-Related Costs , 2010, Biological Psychiatry.

[20]  M. Walton,et al.  Separate neural pathways process different decision costs , 2006, Nature Neuroscience.

[21]  Joshua L. Jones,et al.  Basolateral Amygdala Modulates Terminal Dopamine Release in the Nucleus Accumbens and Conditioned Responding , 2010, Biological Psychiatry.

[22]  S. Floresco,et al.  Modulation of Hippocampal and Amygdalar-Evoked Activity of Nucleus Accumbens Neurons by Dopamine: Cellular Mechanisms of Input Selection , 2001, The Journal of Neuroscience.

[23]  M. Bozkurt,et al.  Functional anatomy. , 1980, Equine veterinary journal.

[24]  Matthew T. Kaufman,et al.  Distributed Neural Representation of Expected Value , 2005, The Journal of Neuroscience.

[25]  Trevor W Robbins,et al.  Interactions between Serotonin and Dopamine in the Control of Impulsive Choice in Rats: Therapeutic Implications for Impulse Control Disorders , 2005, Neuropsychopharmacology.

[26]  S. Floresco,et al.  Differential effects of dopaminergic manipulations on risky choice , 2010, Psychopharmacology.

[27]  Camelia M. Kuhnen,et al.  The Neural Basis of Financial Risk Taking , 2005, Neuron.

[28]  S. Nicola,et al.  Basolateral Amygdala Neurons Facilitate Reward-Seeking Behavior by Exciting Nucleus Accumbens Neurons , 2008, Neuron.

[29]  T. Robbins,et al.  Effects of lesions to amygdala, ventral subiculum, medial prefrontal cortex, and nucleus accumbens on the reaction to novelty: implication for limbic-striatal interactions. , 1996 .

[30]  Jung Hoon Sul,et al.  Role of Striatum in Updating Values of Chosen Actions , 2009, The Journal of Neuroscience.

[31]  Matthew F. S. Rushworth,et al.  Weighing up the benefits of work: Behavioral and neural analyses of effort-related decision making , 2006, Neural Networks.

[32]  R. Cardinal,et al.  Nucleus accumbens core lesions retard instrumental learning and performance with delayed reinforcement in the rat , 2005, BMC Neuroscience.

[33]  J. Feldon,et al.  Double dissociation of the effects of selective nucleus accumbens core and shell lesions on impulsive‐choice behaviour and salience learning in rats , 2005, The European journal of neuroscience.

[34]  G Elliott Wimmer,et al.  Nucleus accumbens activation mediates the influence of reward cues on financial risk taking , 2008, Neuroreport.

[35]  D. S. Zahm,et al.  The patterns of afferent innervation of the core and shell in the “Accumbens” part of the rat ventral striatum: Immunohistochemical detection of retrogradely transported fluoro‐gold , 1993, The Journal of comparative neurology.

[36]  M. Roesch,et al.  Ventral Striatal Neurons Encode the Value of the Chosen Action in Rats Deciding between Differently Delayed or Sized Rewards , 2009, The Journal of Neuroscience.

[37]  T. Robbins,et al.  Contrasting Roles of Basolateral Amygdala and Orbitofrontal Cortex in Impulsive Choice , 2004, The Journal of Neuroscience.

[38]  M. Walton,et al.  Dissociable cost and benefit encoding of future rewards by mesolimbic dopamine , 2009, Nature Neuroscience.

[39]  G. Rebec,et al.  Dissociation of core and shell single-unit activity in the nucleus accumbens in free-choice novelty , 2003, Behavioural Brain Research.

[40]  S. Mizumori,et al.  Characteristics of basolateral amygdala neuronal firing on a spatial memory task involving differential reward. , 1998, Behavioral neuroscience.

[41]  P. Willner,et al.  The Mesolimbic Dopamine System: From Motivation to Action An International Workshop Malta September 25–29, 1989 , 1989, Psychobiology.

[42]  A. Simmons,et al.  Selective activation of the nucleus accumbens during risk-taking decision making , 2004, Neuroreport.

[43]  Joseph J. Paton,et al.  Moment-to-Moment Tracking of State Value in the Amygdala , 2008, The Journal of Neuroscience.

[44]  Wolfgang Hauber,et al.  Prefrontostriatal circuitry regulates effort-related decision making. , 2009, Cerebral cortex.

[45]  G. Loewenstein,et al.  Neural Predictors of Purchases , 2007, Neuron.

[46]  T. Robbins,et al.  Serotonin Modulates Sensitivity to Reward and Negative Feedback in a Probabilistic Reversal Learning Task in Rats , 2010, Neuropsychopharmacology.

[47]  S. Floresco,et al.  Opposing roles for the nucleus accumbens core and shell in cue-induced reinstatement of food-seeking behavior , 2008, Neuroscience.

[48]  T. Robbins,et al.  Impulsive Choice Induced in Rats by Lesions of the Nucleus Accumbens Core , 2001, Science.

[49]  T. Robbins,et al.  The effects of d-amphetamine, chlordiazepoxide, α-flupenthixol and behavioural manipulations on choice of signalled and unsignalled delayed reinforcement in rats , 2000, Psychopharmacology.

[50]  S. Floresco,et al.  Perturbations in different forms of cost/benefit decision making induced by repeated amphetamine exposure , 2009, Psychopharmacology.

[51]  Brian Knutson,et al.  Dissociation of reward anticipation and outcome with event-related fMRI , 2001, Neuroreport.

[52]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[53]  S. Ikemoto,et al.  The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking , 1999, Brain Research Reviews.

[54]  T. Robbins,et al.  Effects of lesions to amygdala, ventral subiculum, medial prefrontal cortex, and nucleus accumbens on the reaction to novelty: implication for limbic-striatal interactions. , 1996, Behavioral neuroscience.

[55]  S. Floresco,et al.  Differential effects on effort discounting induced by inactivations of the nucleus accumbens core or shell. , 2010, Behavioral neuroscience.

[56]  M. Brandão,et al.  Exploratory behaviour of rats in the elevated plus-maze is differentially sensitive to inactivation of the basolateral and central amygdaloid nuclei , 2007, Brain Research Bulletin.