Human striatal activation reflects degree of stimulus saliency
Introduction
Due to the limitations of our cognitive resources, it is impossible to process every stimulus in the environment at a given moment. Although much of our surroundings are predictable, we constantly encounter unexpected changes of potential behavioral significance. Consequently, our available cognitive resources preferentially shift toward salient events at the expense of less salient stimuli. Saliency, in this context, refers to the capability of important or arousing stimuli to interrupt the current cognitive focus and cause the reallocation of available resources, i.e., elicit an attentional or behavioral switch. The exact mechanisms underlying this prioritized processing of unexpected, potentially important stimuli remain unclear, but it has been proposed that the striatum and its major dopaminergic inputs may play a role by providing a signal that facilitates the reallocation of resources toward unexpected, salient events (Redgrave et al., 1999a, Redgrave et al., 1999b).
Activity in the striatum has long been associated with reward exclusively, but there is considerable evidence supporting the hypothesis that activity in the striatum signals saliency in general. Midbrain dopamine neurons that project to the striatum respond to a large category of arousing events, including novel stimuli (Schultz and Romo, 1990, Legault and Wise, 2001), aversive stimuli (Young, 2004), and high intensity visual and auditory events (Steinfels et al., 1983, Strecker and Jacobs, 1985, Horvitz, 2000, Horvitz et al., 1997), in addition to unexpected rewards (Mirenowicz and Schultz, 1994, Schultz, 1998). Similarly, human neuroimaging studies have demonstrated that striatal activations follow unexpected rewards and reward-related stimuli (Delgado et al., 2000, Knutson et al., 2000, Berns et al., 2001), but also follow aversive stimuli (Becerra et al., 2001, Jensen et al., 2003), and neutral arousing visual stimuli (Zink et al., 2003).
Although the striatum responds to a variety of stimuli that can be categorically defined as salient, saliency is not a discrete quality (not “either/or”). It lies instead on a continuum, so that the higher the saliency, the greater the likelihood of perturbing the current focus of attention or behavior. It follows that brain regions that drive the reallocation of resources should signal the degree of saliency associated with a stimulus, such that the strength of the signal determines the likelihood of an attentional or behavioral switch. A precise relationship between striatal activity and the degree to which events perturb limited cognitive resources has not yet been established, which is essential to determine a striatal role in prompting the reallocation of resources to unexpected potentially important stimuli in our environment.
We used functional magnetic resonance imaging (fMRI) to investigate human neuronal responses to unexpected stimuli that were associated with varying levels of saliency, in the absence of reward. We hypothesized that if the striatum provides a signal to switch resources to important events, then its activity following a stimulus should increase with the level of saliency associated with the stimulus.
Section snippets
Participants
Twenty right-handed, healthy adults (ten males; ten females), ages 18–30, participated in the fMRI experiment. Participants had no history of neurological or psychiatric disorder and gave written, informed consent for a protocol approved by the Emory University Institutional Review Board.
Experimental task
The software package, Cogent 2000 (FIL, University College London), was used for stimulus presentation and response acquisition.
While in the scanner, participants performed four runs of a modified version of a
Behavioral and physiological results
On average, participants made less than 3 errors per run. The SCR and reaction time data were used to confirm that the novel sound category did contain sounds associated with different levels of saliency, as intended. The novel sounds were designed to vary in their saliency based on their identifiability, and therefore, to confirm the saliency manipulation, we divided the novel sounds into two categories for the behavioral and physiological data analysis: identifiable (“high salience”) and
Discussion
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
Acknowledgments
We thank the Biomedical Imaging Technology Center at Emory University, especially Keith Heberlein and Robert Smith for their technical assistance during scanning sessions. We also thank Rosa Aurora Chavez-Eakle for helpful comments and Carles Escera for providing sound stimuli. Novel sounds were also selected from various websites:a1freesoundeffects.com, soundamerica.com, simplythebest.com, andcepl.nyspi.org. This work was gratefully supported by grants from the National Institutes of Health,
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2022, Biological PsychiatryCitation Excerpt :Taken together, these findings indicate that the GPi and STN could exhibit distinct bottom-up and top-down roles in reward processing, respectively (Figure S6). Specifically, during stimulus evaluation, the GPi likely contains information on reward expectation salience, which is distributed widely through the thalamo-cortical-basal ganglia loop and to broad limbic circuitry (38,39). The STN, in contrast, exerts strong inhibitory action control until evidence driving a final behavioral decision is accrued and passes a threshold (17).