Reward processing is complex and involves the contribution from multiple interacting brain regions. 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. This can be attained through the use of event-related potentials (ERPs). Surprisingly, relatively few studies have employed ERPs to investigate intact reward processing; therefore, its temporal correlates remain to be determined.
One well-studied ERP component that seems to play a role in reward processing is the P3 (or P300), a positive wave usually peaking between 300 and 600 msec post-stimulus with largest amplitude at centro-parietal scalp sites (Sutton, Braren, Zubin, & John, 1965
). The major factors affecting P3 amplitude include stimulus probability and task relevance (Squires, Donchin, Herning, & McCarthy, 1977
). Stimuli with high emotional value, informative feedback stimuli, and target stimuli also elicit larger P3s than stimuli that do not have these properties (Johnson, 1988
; Picton, 1992
; Pritchard, 1981
). We therefore expected the P3 to be elicited by monetary feedback manipulation; indeed the P3’s involvement in monetary reward, and specifically in marking reward’s magnitude, has been previously documented (Begleiter, Porjesz, Chou, & Aunon, 1983
; Homberg, Grunewald, & Grunewald-Zuberbier, 1981
; Otten, Gaillard, & Wientjes, 1995
; Ramsey & Finn, 1997
; Yeung & Sanfey, 2004
). For example, Ramsey and Finn (1997)
used a visual discrimination task where subjects were instructed to respond to target stimuli in a neutral condition (no monetary incentive) vs. an incentive condition (monetary gain of 50 cents for correct responses and loss of 50 cents for incorrect responses). Greater amplitude and shorter latency of the P3 was reported in the incentive condition as compared to the neutral condition. In a recent study, Yeung & Sanfey (2004)
revealed a double dissociation between P3 and feedback negativity (a negative component occurring 200 to 300 ms after a feedback stimulus) such that reward magnitude (small: 6–11 cents vs. large: 32–40 cents) was reflected by the P3, but not by feedback negativity, and reward valence (win or loss) was reflected by feedback negativity only.
Unlike most previous studies, the current investigation was designed to induce sustained anticipation of graded monetary reward. This design allowed for comparisons between different amounts of money, which could highlight the role of the P3 in processing of relative reward and not only in processing reward’s absolute value (reward vs. no reward). We were interested in inspecting sustained (blocked) and not event-related (rapidly alternating) anticipation of reward, because of our interest in the examination of relative reward processing in a real-world context, where emotional/motivational information is more likely to occur in a sustained fashion over several minutes, rather than alternating rapidly with information of a different emotional tenor (Compton, et al., 2003
). Our interest in sustained reward was further guided by the prospect of future studies utilizing functional magnetic resonance imaging (fMRI), where signal-to-noise ratio is higher in blocked vs. event-related designs (for a direct comparison see (Mechelli, Price, Henson, & Friston, 2003
)), a concern that is particularly relevant in studies of clinical populations (e.g., with psychopathology that affects reward processing such as drug addiction).
While there have been several studies investigating the role of P3 in reward processing, less attention has been directed to the CNV (contingent negative variation), a slow component typically elicited in Go/No-go paradigms and associated with expectancy in the human brain (Walter, Cooper, Aldridge, McCallum, & Winter, 1964
). In warned S1–S2 Go/No-go paradigms, the CNV develops early in response to the warning stimulus (S1), having a frontal distribution (the orienting, “O”, wave); its later part develops immediately preceding the target stimulus (S2), having a centroparietal distribution (late expectancy, “E”, wave). We were particularly interested in this later CNV component, which is anticipatory in nature, further related to motor response preparation or the readiness potential of the motor potential complex (Rohrbaugh, et al., 1986
) and to motivation (Cant & Bickford, 1967
However, although preparation to and anticipation of reward are core mechanisms in reward processing (Knutson, Fong, Adams, Varner, & Hommer, 2001
; Volkow, et al., 2003
), this slow ERP component has not been frequently targeted in the study of reward processing, and conflicting results abound to date. Thus, while some studies point to a role of the CNV in reward processing (Boyd, Boyd, & Brown, 1979
; Pierson, Ragot, Ripoche, & Lesevre, 1987
), other studies suggest otherwise (Lumsden, Howard, & Fenton, 1986
; Sobotka, Davidson, & Senulis, 1992
). For example, Pierson and colleagues (1987)
conditioned subjects to associate one tone with monetary gain (reward) and another tone with loss of money (punishment); a third tone was not associated with reward or punishment (neutral stimulus). Following the conditioning phase, they found that CNV amplitude differed between rewarding conditioned stimuli and neutral or punishing conditioned stimuli. Other evidence supporting the relationship between the CNV and reward comes from the animal literature; Boyd and colleagues (1979)
examined the CNV in the squirrel monkey and found that it varied as a function of reward (but not consistently in the same direction across all animals). Conversely, Sobotka and colleagues (1992)
manipulated reward and punishment contingencies such that subjects were instructed whether they could potentially win or lose money (25¢) on each trial. To win money (on reward trials) or avoid losing money (on punishment trials), subjects had to press or release a button faster than a specified response time, while responding slower resulted in either no monetary gain or loss of money (respectively). While the CNV was larger for trials on which subjects had faster response times, it did not vary with reward or punishment.
The purpose of this study was to investigate cognitive ERPs, especially the P3 and CNV, evoked by warning (S1) and target (S2) stimuli in a Go/No-go paradigm and their modulation by magnitude of sustained monetary reward (high, low, and none as baseline) in the intact brain. Event-related potential variations were interpreted in conjunction with behavioral measures (including reaction time, accuracy, and self-reported interest and excitement ratings) in 16 healthy young subjects. While we hypothesized the P3 to be modulated by reward magnitude (high > low > none), our analyses of the CNV were more exploratory in nature.