While previous studies have reported that the dopamine/striatal system is engaged when one unexpectedly encounters salient stimuli in the environment, the present findings explicitly link the level of activity in the striatum with the level of saliency associated with a particular event. Specifically, striatal activations in the bilateral caudate, and to a lesser extent in the left nucleus accumbens, are related to the degree that a stimulus interrupts the current cognitive focus. The novel sounds in the present experiment served as stimuli of interest because they were unexpected events, designed to be associated with varying levels of saliency based on their identifiability and alerting nature—ranging from minimally salient to highly salient. As such, the novel sounds elicited varying delays in reaction times to the subsequent numerical task-stimuli. The deviant tones did not vary in their saliency, and therefore variations in reaction times following deviant tones were attributed to task-unrelated thoughts or fatigue, rather than attributed to an effect of the preceding deviant tone itself.
The saliency manipulation within the novel sound category was confirmed by the SCR and behavioral data. SCRs provide a physiological measure indicating orienting responses or saliency of a particular event (Boucsein, 1992
). The SCRs following novel sounds were significantly greater than SCRs following deviant tones and close to significantly greater than SCRs following unidentifiable novel sounds, confirming that the novel sound category did indeed contain sounds associated with greater saliency compared to the deviant tones. The variance in reaction times following novel sounds and deviant tones was equal, but the reaction times to numerical task-stimuli preceded by identifiable novel sounds were significantly longer than the reaction times to numerical task-stimuli preceded by unidentifiable novel sounds and deviant tones, indicating that the identifiable nature of the novel sounds affected their saliency.
The novel sounds were separated into two groups (identifiable and unidentifiable) for behavioral confirmation of our saliency manipulation, but the saliency of the novel sounds, as reflected in the reaction times to subsequent numerical task-stimuli, lays on a continuum rather than being divided into two discrete groups. Therefore, we opted for a parametric modulation approach to assess the relationship between brain activity and the level of saliency associated with a particular event. The resulting striatal activation in our contrast of interest, ‘‘(NOVEL modulated by RT) > (DEVIANT modulated by RT),’’ was specifically attributed to varying degrees of saliency associated with the novel sounds because ‘‘DEVIANT modulated by RT’’ controlled for variations in reaction times that were not due to the nature of the sound stimuli. Even at an extremely lenient threshold of P < 0.50, striatal activations were not observed for ‘‘DEVIANT modulated by RT,’’ providing strong evidence that the observed striatal response in the contrast, ‘‘(NOVEL modulated by RT) > (DEVIANT modulated by RT),’’ reflected a correlation between striatal activity and the degree of saliency of the novel sounds, rather than task-unrelated thoughts or fatigue.
The sound stimuli in the task design were completely task-irrelevant, which was also important for the interpretation of the results. If a contingency between sound type and number type existed or was perceived by the participants (i.e., the occurrence of a novel sound indicated an upcoming odd or even number), then a prediction error, rather than the saliency of the novel sounds, could have elicited delayed reaction times and the resulting increase in striatal activation. To avoid such a confound, the task was carefully designed so that within each run, the novel sounds were followed by all the numbers, 2–9, twice (16 novel trials total), and the deviant tones were followed by all the numbers once (8 deviant trials total), both in random order. Although no contingency between sounds type and number type existed, to ensure that a contingency was not perceived by the participants, they were explicitly instructed that the sounds were completely task-irrelevant and could be ignored. Furthermore, in post-session interviews, no participants indicated that he/she perceived such a contingency, even when asked.
Although striatal activations follow categorically defined salient events, different interpretations of such data have led to the view that the striatum and its dopaminergic inputs process unexpected rewards or reward prediction error exclusively, rather than saliency in general (Schultz, 1998
; Ungless, 2004
). Furthermore, data that implicate activity in the striatum with reward-related stimuli are more numerous than data that link the dopamine/striatal system with salient, nonrewarding events, which have been studied less frequently in humans. Rewards have been defined as events that elicit approach and consumatory behavior, serve as positive reinforcers of behavior, and induce subjective feelings of pleasure (Schultz, 1998
). In order to be able to attribute the present results to saliency in general, rather than reward, we made sure that the novel sounds were not rewarding to our participants and, perhaps more importantly, that the saliency level of the sounds was not confounded by whatever pleasure they might have conferred. In terms of the pleasantness associated with the novel sounds, participants rated the novel sounds slightly below neutral. Thus, the novel sounds were not considered rewarding and did not elicit hedonic feelings. Furthermore, the reaction times to numbers preceded by novel sounds did not differ across the five levels of pleasantness ratings associated with the novel sounds, indicating that the saliency associated with a particular novel sound was unrelated to its pleasure rating.
The contention that striatal activation reflects the potential importance of a stimulus, and therefore plays a role in the reallocation of resources, is still consistent with decades of research linking the dopamine/striatal system with coding unexpected rewards and reward-related events. Unexpected rewards are highly salient stimuli that are prone to interrupt and redirect the current focus of attention and behavior. In fact, as it has been recently pointed out (Maunsell, 2004
), reward manipulation and attentional effects have not been clearly separated in many previous reward studies. Thus, the so-called ‘‘reward response’’ of the striatum may be more appropriately, and more generally, categorized as a ‘‘saliency response.’’ Recent studies have suggested a link between reward magnitude and level of activity in the striatum of monkeys (Cromwell and Schultz, 2003
) and humans (Delgado et al., 2003
), which, in accordance with the present findings, may be related to higher magnitude rewards receiving higher saliency assignments.
In conclusion, the present findings demonstrate that striatal activity corresponds to the degree to which unexpected stimuli perturb cognitive resources. These results provide strong evidence for the claim postulated by Redgrave et al. (1999b)
that striatal activation drives the reallocation of available resources to process salient events with priority, rather than just providing a reward signal, especially when no obvious reward is present. Beyond their contribution to the interpretation of striatal activation, the present findings have implications regarding a variety of neuropsychiatric disorders that affect the dopamine/striatal system, including schizophrenia, attention deficit hyperactivity disorder, and drug addiction. Current theories that relate these disease states with a breakdown of proper saliency assignments (Kapur, 2003
; Volkow et al., 2004a
) are well supported by our results, and their future clinical development may eventually lead to better preventions and treatments.