Human striatal activation reflects degree of stimulus saliency

Abstract

Salient stimuli are characterized by their capability to perturb and seize available cognitive resources. Although the striatum and its dopaminergic inputs respond to a variety of stimuli categorically defined as salient, including rewards, the relationship between striatal activity and saliency is not well understood. Specifically, it is unclear if the striatum responds in an all-or-none fashion to salient events or instead responds in a graded fashion to the degree of saliency associated with an event. Using functional magnetic resonance imaging, we measured activity in the brains of 20 participants performing a visual classification task in which they identified single digits as odd or even numbers. An auditory tone preceded each number, which was occasionally, and unexpectedly, substituted by a novel sound. The novel sounds varied in their ability to interrupt and reallocate cognitive resources (i.e., their saliency) as measured by a delay in reaction time to immediately subsequent numerical task-stimuli. The present findings demonstrate that striatal activity increases proportionally to the degree to which an unexpected novel sound interferes with the current cognitive focus, even in the absence of reward. These results suggest that activity in the human striatum reflects the level of saliency associated with a stimulus, perhaps providing a signal to reallocate limited resources to important events.

Fig. 1

Schematic diagram of the experimental task. A single digit number appeared on the screen for 200 ms followed by a blank screen for 2500 ms. Participants were required to classify the number as either odd or even with a button press (shown here with button #1 corresponding to odd numbers and button #2 corresponding to even numbers). 600 ms preceding the appearance of the number, the outline of a circle appeared and remained on the screen for the duration of the trial, such that the number was presented in the center of the circle outline. Concurrent with the circle outline appearance, a 500 ms sound was played for the participants via headphones. The sound was a 600 Hz ‘‘standard’’ tone for 85% of trials, a 700 Hz ‘‘deviant’’ tone for 5% of trials, and a ‘‘novel’’ sound (e.g., a siren or a burst of noise) for 10% of the trials. The standard and deviant tones were considered minimally salient. The novel sounds were designed to be associated with varying degrees of saliency.

Fig. 2

Brain regions where a correlation between BOLD activity and reaction times (to subsequent numerical task-stimuli) was significantly greater for the novel sounds compared to deviant tones. The only significant activations (P < 0.001 uncorrected; voxel extent = 10) were in the bilateral caudate (A) shown overlaid on a glass brain in three orthogonal planes and (B) shown overlaid on a coronal section (y = 3) of a structural template brain. (C) Graphical representations of the results in the left and right caudate are also shown. The plots demonstrate the fitted relationship between the effect sizes (parameter estimates) and the normalized reaction times to subsequent task-related stimuli for the novel sounds (red) and the deviant tones (blue). The effect size is expressed as percentage of the global mean intensity of the scans. The reaction times were normalized using a Euclidean Normalization method as implemented by SPM2. The dotted lines are 95% confidence intervals.

Fig. 3

Brain activations to the (A) novel sounds and (B) deviant tones, each modulated by reaction times to subsequent task-related stimuli (RT), overlaid on coronal sections of a structural template brain ( y = 3). The significance threshold was leniently set to P < 0.50 uncorrected, confirming lack of striatal activity to the deviant tones modulated by RT (B). The striatal region is outlined by the blue rectangle.