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The Journal of Neuroscience, May 24, 2006, 26(21):5777-5785; doi:10.1523/JNEUROSCI.5223-05.2006

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Behavioral/Systems/Cognitive
Pronociceptive and Antinociceptive Effects of Estradiol through Endogenous Opioid Neurotransmission in Women

Yolanda R. Smith,^1,2 Christian S. Stohler,⁶ Thomas E. Nichols,³ Joshua A. Bueller,⁴ Robert A. Koeppe,⁵ and Jon-Kar Zubieta^4,5

¹Department of Obstetrics and Gynecology, Division of Reproductive Endocrinology, ²Women’s Health Program, ³Department of Biostatistics, ⁴Department of Psychiatry and Molecular and Behavioral Neuroscience Institute, and ⁵Department of Radiology, University of Michigan, Ann Arbor, Michigan 48109, and ⁶Dental School, 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

Prominent interindividual and sex-dependent differences have been described in responses to sustained pain and other stressful stimuli. Variations in µ-opioid receptor-mediated endogenous opioid neurotransmission may underlie some of these processes. We examined both baseline µ-opioid receptor levels and the activation of this neurotransmitter system during sustained pain using positron emission tomography in a sample of young healthy men and women. Women were studied twice, during low and high estrogen states. The high-estrogen state was associated with regional increases in baseline µ-opioid receptor availability in vivo and a greater activation of endogenous opioid neurotransmission during the pain stressor. The latter did not differ from that obtained in males. During the low estrogen condition, however, significant reductions in endogenous opioid tone were observed at the level of thalamus, nucleus accumbens, and amygdala, which were associated with hyperalgesic responses. Estrogen-associated variations in the activity of µ-opioid neurotransmission correlated with individual ratings of the sensory and affective perceptions of the pain and the subsequent recall of that experience. These data demonstrate a significant role of estrogen in modulating endogenous opioid neurotransmission and associated psychophysical responses to a pain stressor in humans.

Key words: µ-opioid receptors; pain; stress; sex differences; PET; human

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Received Dec. 7, 2005; revised March 23, 2006; accepted April 13, 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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