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The Journal of Neuroscience, October 18, 2006, 26(42):10789-10795; doi:10.1523/JNEUROSCI.2577-06.2006

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Behavioral/Systems/Cognitive
Variations in the Human Pain Stress Experience Mediated by Ventral and Dorsal Basal Ganglia Dopamine Activity

David J. Scott,¹ Mary M. Heitzeg,¹ Robert A. Koeppe,² Christian S. Stohler,³ and Jon-Kar Zubieta^1,2

¹Department of Psychiatry and Molecular and Behavioral Neuroscience Institute and ²Department of Radiology, The University of Michigan, Ann Arbor, Michigan 48109-0720, and ³School of Dentistry, University of Maryland, Baltimore, Maryland 21201

Correspondence should be addressed to Dr. Jon-Kar Zubieta, University of Michigan, Molecular and Behavioral Neuroscience Institute, 205 Zina Pitcher Place, Ann Arbor, MI 48109-0720. Email: zubieta{at}umich.edu

In addition to its involvement in motor control and in encoding reward value, increasing evidence also implicates basal ganglia dopaminergic mechanisms in responses to stress and aversive stimuli. Basal ganglia dopamine (DA) neurotransmission may then respond to environmental events depending on their saliency, orienting the subsequent responses of the organism to both positive and negative stimuli. Here we examined the involvement of DA neurotransmission in the human response to pain, a robust physical and emotional stressor across species. Positron emission tomography with the DA D₂ receptor antagonist radiotracer [¹¹C]raclopride detected significant activation of DA release in dorsal and ventral regions of the basal ganglia of healthy volunteers. Activation of nigrostriatal (dorsal nucleus caudate and putamen) DA D₂ receptor-mediated neurotransmission was positively associated with individual variations in subjective ratings of sensory and affective qualities of the pain. In contrast, mesolimbic (nucleus accumbens) DA activation, which may impact on both D₂ and D₃ receptors, was exclusively associated with variations in the emotional responses of the individual during the pain challenge (increases in negative affect and fear ratings). These data demonstrate that basal ganglia dopamine D₂ receptor-mediated neurotransmission is involved in responses to pain and that it contributes to individual variations in the pain experience at the levels of physical and emotional elements, albeit with different neuroanatomical substrates.

Key words: dopamine; saliency; reward; D₂ receptors; nigrostriatal; mesolimbic

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Received June 19, 2006; revised Aug. 22, 2006; accepted Sept. 8, 2006.

Correspondence should be addressed to Dr. Jon-Kar Zubieta, University of Michigan, Molecular and Behavioral Neuroscience Institute, 205 Zina Pitcher Place, Ann Arbor, MI 48109-0720. Email: zubieta{at}umich.edu

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