Anticipation of Increasing Monetary Reward Selectively Recruits
Brian Knutson, Charles M. Adams, Grace W. Fong, and Daniel Hommer
National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Bethesda, Maryland 20892-1610
Comparative studies have implicated the nucleus accumbens
(NAcc) in the anticipation of incentives, but the relative responsiveness of this neural substrate during anticipation of rewards versus punishments remains unclear. Using event-related functional magnetic resonance imaging, we investigated whether the anticipation of increasing monetary rewards and punishments would increase NAcc blood oxygen level-dependent contrast (hereafter, “activation”) in eight healthy volunteers.
Whereas anticipation of increasing rewards elicited both increasing self-reported happiness and NAcc activation, antici-
pation of increasing punishment elicited neither. However, anticipation of both rewards and punishments activated a different striatal region (the medial caudate). At the highest reward level
($5.00), NAcc activation was correlated with individual differences in self-reported happiness elicited by the reward cues.
These ﬁndings suggest that whereas other striatal areas may code for expected incentive magnitude, a region in the NAcc codes for expected positive incentive value.
Key words: nucleus accumbens; caudate; reward; anticipation; FMRI; human
The ventral striatum has been implicated as a critical neuroanatomical substrate for the anticipation of rewards in mammals
(Ikemoto and Panksepp, 1999). For example, electrophysiological studies of monkeys indicate that dopamine projections from the ventral tegmental area of the midbrain to the nucleus accumbens
(NAcc) of the ventral striatum ﬁre selectively in response to presentation of reward cues (Schultz et al., 1992). However, theorists have questioned the selectivity of NAcc dopamine release for anticipation of rewards versus punishments, because rat studies indicate that stressors can also increase dopamine release in the NAcc and that NAcc lesions can impair active avoidance as well as approach behaviors (Salomone et al., 1997).
Comparative research also suggests that dopamine release occurs more robustly in the NAcc during reward anticipation than during reward consumption (Berridge and Robinson, 1998; Ikemoto and Panksepp, 1999). However, no human brain-imaging studies that have examined ventral striatal activity during incentive tasks have explicitly focused on the anticipation of rewards versus punishments (Thut et al., 1997; Koepp et al., 1998; Delgado et al., 2000; Elliott et al., 2000; Knutson et al., 2000;
O’Doherty et al., 2001). In the present study, we were able to visualize brain activity during anticipatory intervals because of the enhanced temporal resolution afforded by event-related functional magnetic resonance imaging (FMRI) (ϳ2 sec for multislice volumes) relative to other brain imaging modalities such as positron emission tomography (PET). In addition, we were able to focus on neural responses in small regions of the ventral striatum (e.g., the NAcc) because of the relatively ﬁne spatial resolution of FMRI (ϳ4 mm).
Based on primate work (Schultz et al., 1997), we have adapted a paradigm for FMRI that elicits anticipation of monetary reward or punishment, called the monetary incentive delay (MID) task
(Knutson et al., 2000). During the MID task, participants see cues that indicate that they may win or lose money, then wait for a variable anticipatory delay period, and ﬁnally respond to a rapidly presented target with a single button press to try to either win or avoid losing money. In this study, we used a parametric version of the MID task to examine whether the NAcc would respond during anticipation of varying amounts of potential reward versus punishment in a graded manner and whether this