Human striatal activation reflects degree of stimulus saliency

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.

[1]  Andrew M. J. Young,et al.  Increased extracellular dopamine in nucleus accumbens in response to unconditioned and conditioned aversive stimuli: studies using 1 min microdialysis in rats , 2004, Journal of Neuroscience Methods.

[2]  J. Maunsell Neuronal representations of cognitive state: reward or attention? , 2004, Trends in Cognitive Sciences.

[3]  S. Kapur,et al.  Direct Activation of the Ventral Striatum in Anticipation of Aversive Stimuli , 2003, Neuron.

[4]  W. Schultz,et al.  Importance of unpredictability for reward responses in primate dopamine neurons. , 1994, Journal of neurophysiology.

[5]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[6]  R. Knight,et al.  Neural Mechanisms of Involuntary Attention to Acoustic Novelty and Change , 1998, Journal of Cognitive Neuroscience.

[7]  L. Nystrom,et al.  Tracking the hemodynamic responses to reward and punishment in the striatum. , 2000, Journal of neurophysiology.

[8]  S. Kapur Psychosis as a state of aberrant salience: a framework linking biology, phenomenology, and pharmacology in schizophrenia. , 2003, The American journal of psychiatry.

[10]  Samuel M. McClure,et al.  Predictability Modulates Human Brain Response to Reward , 2001, The Journal of Neuroscience.

[11]  R. Wise,et al.  Novelty‐evoked elevations of nucleus accumbens dopamine: dependence on impulse flow from the ventral subiculum and glutamatergic neurotransmission in the ventral tegmental area , 2001, The European journal of neuroscience.

[12]  J. Swanson,et al.  Evidence that methylphenidate enhances the saliency of a mathematical task by increasing dopamine in the human brain. , 2004, The American journal of psychiatry.

[13]  Carles Escera,et al.  Attention capture by auditory significant stimuli: semantic analysis follows attention switching , 2003, The European journal of neuroscience.

[14]  H. Breiter,et al.  Reward Circuitry Activation by Noxious Thermal Stimuli , 2001, Neuron.

[15]  P. Redgrave,et al.  The basal ganglia: a vertebrate solution to the selection problem? , 1999, Neuroscience.

[16]  Brian Knutson,et al.  FMRI Visualization of Brain Activity during a Monetary Incentive Delay Task , 2000, NeuroImage.

[17]  B. Jacobs,et al.  Behavioral correlates of dopaminergic unit activity in freely moving cats , 1983, Brain Research.

[18]  Wolfram Schultz,et al.  Effects of expectations for different reward magnitudes on neuronal activity in primate striatum. , 2003, Journal of neurophysiology.

[19]  Karl J. Friston Imaging cognitive anatomy , 1997, Trends in Cognitive Sciences.

[20]  B. Jacobs,et al.  Substantia nigra dopaminergic unit activity in behaving cats: Effect of arousal on spontaneous discharge and sensory evoked activity , 1985, Brain Research.

[21]  P. Redgrave,et al.  Is the short-latency dopamine response too short to signal reward error? , 1999, Trends in Neurosciences.

[22]  G. Pagnoni,et al.  Human Striatal Response to Salient Nonrewarding Stimuli , 2003, The Journal of Neuroscience.

[23]  J. Ashburner,et al.  Nonlinear spatial normalization using basis functions , 1999, Human brain mapping.

[24]  J. Swanson,et al.  Dopamine in drug abuse and addiction: results from imaging studies and treatment implications , 2004, Molecular Psychiatry.

[25]  W. Schultz,et al.  Dopamine neurons of the monkey midbrain: contingencies of responses to stimuli eliciting immediate behavioral reactions. , 1990, Journal of neurophysiology.

[26]  J. Horvitz Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events , 2000, Neuroscience.

[27]  M. Delgado,et al.  Dorsal striatum responses to reward and punishment: Effects of valence and magnitude manipulations , 2003, Cognitive, affective & behavioral neuroscience.

[28]  J. Horvitz,et al.  Burst activity of ventral tegmental dopamine neurons is elicited by sensory stimuli in the awake cat , 1997, Brain Research.

[29]  R. Turner,et al.  Characterizing Dynamic Brain Responses with fMRI: A Multivariate Approach , 1995, NeuroImage.

[30]  Karl J. Friston,et al.  How Many Subjects Constitute a Study? , 1999, NeuroImage.

[31]  M. Ungless Dopamine: the salient issue , 2004, Trends in Neurosciences.