Dissociable Neural Responses in Human Reward Systems

Abstract

Reward is one of the most important influences shaping behavior. Single-unit recording and lesion studies in experimental animals have implicated a number of regions in response to reinforcing stimuli, in particular regions of the extended limbic system and the ventral striatum. In this experiment, functional neuroimaging was used to assess neural response within human reward systems under different psychological contexts. Nine healthy volunteers were scanned using functional magnetic resonance imaging during the performance of a gambling task with financial rewards and penalties. We demonstrated neural sensitivity of midbrain and ventral striatal regions to financial rewards and hippocampal sensitivity to financial penalties. Furthermore, we show that neural responses in globus pallidus, thalamus, and subgenual cingulate were specific to high reward levels occurring in the context of increasing reward. Responses to both reward level in the context of increasing reward and penalty level in the context of increasing penalty were seen in caudate, insula, and ventral prefrontal cortex. These results demonstrate dissociable neural responses to rewards and penalties that are dependent on the psychological context in which they are experienced.

Activity in human reward-sensitive brain areas is strongly context dependent

“…The scaling of the reward by the range of possible outcomes is consistent with reward prediction error theory, according to which brain areas are sensitive to deviations from expected reward rather than to absolute magnitude of reward (Holroyd and Coles, 2002;Montague and Berns, 2002;Schultz, 2002). Our findings are also consistent with previous research that has identified brain areas showing modulation of reward-sensitive activity by the context of the recent history of monetary rewards and punishments (Akitsuki et al, 2003;Elliott et al, 2000;Nakahara et al, 2004).…”

“…The former possibility would be consistent with theories like reward prediction error theory, according to which brain areas are sensitive to deviations from expected reward rather than to the objective value of reward (Montague and Berns, 2002). The latter possibility would be consistent with previous findings of overlapping but somewhat dissociable systems for processing abstract rewards and punishments (Elliott et al, 2000;O'Doherty et al, 2001;Zalla et al, 1999).…”

“…Neuroimaging studies of reward processing have identified a number of brain areas that are activated by the delivery of primary reinforcers such as appetitive stimuli (Berns et al, 2001;McClure et al, 2003;O'Doherty et al, 2004), and secondary reinforcement such as monetary gains and losses (Breiter et al, 2001;Delgado et al, 2004;Elliott et al, 2000;Holroyd et al, 2004b;Thut et al, 1997). However, it remains to be determined precisely how information about reward and punishment is encoded in these reward-sensitive neural circuits.…”

Predicting events of varying probability: uncertainty investigated by fMRI

“…accumbens), and the dorsal thalamus. These structures belong to a striatal-thalamo-cortical network basically prominent in reward-based learning functions (Graybiel, 2000;Breiter et al, 2001;Delgado et al, 2000;Elliott et al, 2000). As in the currently employed natural sampling approach, such types of learning are typically characterized by a slow delayed acquisition rate of implicit stimulus-response associations.…”

The effect of graded monetary reward on cognitive event-related potentials and behavior in young healthy adults

“…Numerous functional neuroimaging studies in humans have helped to spatially define this neural mesocorticolimbic dopaminergic reward circuitry that encompasses the ventromedial prefrontal cortex, orbitofrontal cortex, anterior cingulate, nucleus accumbens, midbrain (e.g., substantia nigra and ventral tegmentum), amygdala, and the hippocampus (for review, see (Goldstein & Volkow, 2002;Kelley & Berridge, 2002)). Further, neuroimaging studies have contributed to the functional dissociation of these regions based on their specific roles in reward processing (e.g., expectancy and probability, outcome and magnitude, valence) (Breiter, Aharon, Kahneman, Dale, & Shizgal, 2001;Elliott, Friston, & Dolan, 2000;Knutson, Taylor, Kaufman, Peterson, & Glover, 2005). However, current functional neuroimaging studies lack the temporal resolution to provide the precise chronological delineation of such reward-related activity.…”