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The Journal of Neuroscience, September 3, 2003, 23(22):8092-8097
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Human Striatal Response to Salient Nonrewarding Stimuli
Caroline F. Zink,1 Giuseppe Pagnoni,1 Megan E. Martin,1 Mukeshwar Dhamala,1,2 andGregory S. Berns1,3 1Department of Psychiatry and Behavioral Sciences, Emory University School of Medicine, Atlanta, Georgia 30322, and 2School of Physics and 3Department of Biomedical Engineering, Georgia Institute of Technology, Atlanta, Georgia 30332
Although one proposed function of both the striatum and its major dopamine inputs is related to coding rewards and reward-related stimuli, an alternative view suggests a more general role of the striatum in processing salient events, regardless of their reward value. Here we define saliency as an event that both is unexpected and elicits an attentional-behavioral switch (i.e., arousing). In the present study, human striatal responses to nonrewarding salient stimuli were investigated. Using functional magnetic resonance imaging (fMRI), the blood oxygenation level-dependent signal was measured in response to flickering visual distractors presented in the background of an ongoing task. Distractor salience was manipulated by altering the frequency of distractor occurrence. Infrequently presented distractors were considered more salient than frequently presented distractors. We also investigated whether behavioral relevance of the distractors was a necessary component of saliency for eliciting striatal responses. In the first experiment (19 subjects), the distractors were made behaviorally relevant by defining a subset of them as targets requiring a button press. In the second experiment (17 subjects), the distractors were not behaviorally relevant (i.e., they did not require any response). The fMRI results revealed increased activation in the nucleus accumbens after infrequent (high salience) relative to frequent (low salience) presentation of distractors in both experiments. Caudate activity increased only when the distractors were behaviorally relevant. These results demonstrate a role of the striatum in coding nonrewarding salient events. In addition, a functional subdivision of the striatum according to the behavioral relevance of the stimuli is suggested.
Key words: fMRI; striatum; predictability; salience; reward; behavioral relevance
Received May 5, 2003; revised July 10, 2003; accepted July 16, 2003.
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