Journal of Oral and Maxillofacial Surgery
Volume 64, Issue 2 , Pages 158-166 , February 2006

Influence of Estrogen on Brain Activation During Stimulation With Painful Heat

  • Reny de Leeuw, DDS, PhD

      Affiliations

    • Associate Professor, Department of Oral Health Science, University of Kentucky, Lexington, KY.
    • Corresponding Author InformationAddress correspondence and reprint requests to Dr de Leeuw: College of Dentistry, D530, Oral Health Science, Chandler Medical Center, University of Kentucky, 800 Rose Street, Lexington, KY 40536-0297
    • ,
  • Romulo J.C. Albuquerque, DDS

      Affiliations

    • Research Assistant, Department of Oral Health Science, University of Kentucky, Lexington, KY.
    • ,
  • Anders H. Andersen, PhD

      Affiliations

    • Research Associate Professor, Department of Anatomy and Neurobiology, University of Kentucky, Lexington, KY.
    • ,
  • Charles R. Carlson, PhD

      Affiliations

    • Professor, Department of Psychology, University of Kentucky, Lexington, KY.

References 

  1. Lipton RB , Stewart WF , Scher AI . Epidemiology and economic impact of migraine . Curr Med Res Opin . 2001;17(suppl 1):s4
  2. Yunus MB . Gender differences in fibromyalgia and other related syndromes . J Gend Specif Med . 2002;5:42
  3. Taub E , Cuevas JL , Cook EW , et al.   Irritable bowel syndrome defined by factor analysis. Gender and race comparisons . Dig Dis Sci . 1995;40:2647
  4. Dworkin SF , LeResche L , Von Korff MR . Diagnostic studies of temporomandibular disorders (Challenges from an epidemiologic perspective) . Anesth Prog . 1990;37:147
  5. Okeson JP . Management of Temporomandibular Disorders and Occlusion . (ed 5). St Louis, MO: Mosby; 2003;
  6. LeResche L . Epidemiology of temporomandibular disorders (Implications for the investigation of etiologic factors) . Crit Rev Oral Biol Med . 1997;8:291
  7. Bigal ME , Lipton RB , Stewart WF . The epidemiology and impact of migraine . Curr Neurol Neurosci Rep . 2004;4:98
  8. LeResche L , Saunders K , Von Korff MR , et al.   Use of exogenous hormones and risk of temporomandibular disorder pain . Pain . 1997;69:153
  9. Stohler CS . Masticatory myalgias. Emphasis on the nerve growth factor-estrogen link . Pain Forum . 1997;6:176
  10. Fillingim RB , Maixner W , Girdler SS , et al.   Ischemic but not thermal pain sensitivity varies across the menstrual cycle . Psychosom Med . 1997;59:512
  11. Cimino R , Farella M , Michelotti A , et al.   Does the ovarian cycle influence the pressure-pain threshold of the masticatory muscles in symptom-free women? . J Orofac Pain . 2000;14:105
  12. Dao TT , Knight K , Ton-That V . Modulation of myofascial pain by the reproductive hormones (A preliminary report) . J Prosthet Dent . 1998;79:663
  13. Hellstrom B , Anderberg UM . Pain perception across the menstrual cycle phases in women with chronic pain . Percept Mot Skills . 2003;96:201
  14. LeResche L , Mancl L , Sherman JJ , et al.   Changes in temporomandibular pain and other symptoms across the menstrual cycle . Pain . 2003;106:253
  15. Riley JL , Robinson ME , Wise EA , et al.   A meta-analytic review of pain perception across the menstrual cycle . Pain . 1999;81:225
  16. Wise EA , Riley JL , Robinson ME . Clinical pain perception and hormone replacement therapy in postmenopausal women experiencing orofacial pain . Clin J Pain . 2000;16:121
  17. Melzack R . From the gate to the neuromatrix . Pain Suppl . 1999;6:S121
  18. Fillingim RB , Ness TJ . Sex-related hormonal influences on pain and analgesic responses . Neurosci Biobehav Rev . 2000;24:485
  19. Stohler CS . Muscle-related temporomandibular disorders . J Orofac Pain . 1999;13:273
  20. Sessle BJ . Acute and chronic craniofacial pain (Brainstem mechanisms of nociceptive transmission and neuroplasticity, and their clinical correlates) . Crit Rev Oral Biol Med . 2000;11:57
  21. Wise PM , Dubal DB , Wilson ME , et al.   Minireview (Neuroprotective effects of estrogen-new insights into mechanisms of action) . Endocrinology . 2001;142:969
  22. Smith YR , Zubieta JK . Neuroimaging of aging and estrogen effects on central nervous system physiology . Fertil Steril . 2001;76:651
  23. Lee SJ , McEwen BS . Neurotrophic and neuroprotective actions of estrogens and their therapeutic implications . Annu Rev Pharmacol Toxicol . 2001;41:569
  24. McEwen B . Estrogen actions throughout the brain . Recent Prog Horm Res . 2002;57:357
  25. Mogil JS , Sternberg WF , Kest B , et al.   Sex differences in the antagonism of swim stress-induced analgesia (Effects of gonadectomy and estrogen replacement) . Pain . 1993;53:17
  26. D’Amico JF , Greendale GA , Lu JK , et al.   Induction of hypothalamic opioid activity with transdermal estradiol administration in postmenopausal women . Fertil Steril . 1991;55:754
  27. Smith YR , Zubieta JK , del Carmen MG , et al.   Brain opioid receptor measurements by positron emission tomography in normal cycling women (Relationship to luteinizing hormone pulsatility and gonadal steroid hormones) . J Clin Endocrinol Metab . 1998;83:4498
  28. Zubieta JK , Dannals RF , Frost JJ . Gender and age influences on human brain μ-opioid receptor binding measured by PET . Am J Psychiatry . 1999;156:842
  29. Sanders G , Wenmoth D . Verbal and music dichotic listening tasks reveal variations in functional cerebral asymmetry across the menstrual cycle that are phase and task dependent . Neuropsychologia . 1998;36:869
  30. Shaywitz SE , Shaywitz BA , Pugh KR , et al.   Effect of estrogen on brain activation patterns in postmenopausal women during working memory tasks . Jama . 1999;281:1197
  31. Dietrich T , Krings T , Neulen J , et al.   Effects of blood estrogen level on cortical activation patterns during cognitive activation as measured by functional MRI . Neuroimage . 2001;13:425
  32. Quiton RL , Gullapalli RP , Keaser ML , et al.   Repeatability of Pain-Related fMRI Activation in the Human Brain. Program No. 746.7, in Abstract Viewer/Itinerary Planner . Washington, DC: Society for Neuroscience; 2004;
  33. Koyama Y , Koyama T , Kroncke AP , et al.   Effects of stimulus duration on heat induced pain (The relationship between real-time and post-stimulus pain ratings) . Pain . 2004;107:256
  34. Spielberger CD , Gorsuch RL , Lushene R , et al.   Manual for the State-Trait Anxiety Inventory (Form Y) . Palo Alto, CA: Consulting Psychologists Press; 1983;
  35. Talairach J , Tournoux P . Co-planar Stereotaxic Atlas of the Human Brain . New York: Thieme; 1988;
  36. Friston KJ , Ashburner J , Poline JB , et al.   Spatial registration and normalization of images . Hum Brain Mapp . 1995;2:165
  37. Liao CH , Worsley KJ , Poline JB , et al.   Estimating the delay of the fMRI response . Neuroimage . 2002;16:593
  38. Cox RW . AFNI (Software for analysis and visualization of functional magnetic resonance neuroimages) . Comput Biomed Res . 1996;29:162
  39. Smith CD , Andersen AH , Kryscio RJ , et al.   Altered brain activation in cognitively intact individuals at high risk for Alzheimer’s disease . Neurology . 1999;53:1391
  40. Friston KJ , Holmes AP , Poline JB , et al.   Analysis of fMRI time-series revisited . Neuroimage . 1995;2:45
  41. Purdon PL , Weisskoff RM . Effect of temporal autocorrelation due to physiological noise and stimulus paradigm on voxel-level false-positive rates in fMRI . Hum Brain Mapp . 1998;6:239
  42. Burock MA , Dale AM . Estimation and detection of event-related fMRI signals with temporally correlated noise (A statistically efficient and unbiased approach) . Hum Brain Mapp . 2000;11:249
  43. Kesler-West ML , Andersen AH , Smith CD , et al.   Neural substrates of facial emotion processing using fMRI . Brain Res Cogn Brain Res . 2001;11:213
  44. Peyron R , Laurent B , Garcia Larrea L . Functional imaging of brain responses to pain. A review and meta-analysis (2000) . Neurophysiol Clin . 2000;30:263
  45. Vogt BA , Derbyshire S , Jones AK . Pain processing in four regions of human cingulate cortex localized with co-registered PET and MR imaging . Eur J Neurosci . 1996;8:1461
  46. Craig AD , Reiman EM , Evans A . Functional imaging of an illusion of pain . Nature . 1996;384:258
  47. Gelnar PA , Krauss BR , Sheehe PR . A comparative fMRI study of cortical representations for thermal painful, vibrotactile, and motor performance tasks . Neuroimage . 1999;10:460
  48. Treede RD , Kenshalo DR , Gracely RH . The cortical representation of pain . Pain . 1999;79:105
  49. Treede RD , Apkarian AV , Bromm B , et al.   Cortical representation of pain (Functional characterization of nociceptive regions near the lateral sulcus) . Pain . 2000;87:113
  50. Kwan CL , Crawley AP , Mikulis DJ , et al.   An fMRI study of the anterior cingulate cortex and surrounding medial wall activations evoked by noxious cutaneous heat and cold stimuli . Pain . 2000;85:359
  51. Ploghaus A , Tracey I , Gati JS , et al.   Dissociating pain from its anticipation in the human brain . Science . 1999;284:1979
  52. Whalen PJ , Bush G , McNally RJ , et al.   The emotional counting Stroop paradigm (A functional magnetic resonance imaging probe of the anterior cingulate affective division) . Biol Psychiatry . 1998;44:1219
  53. Ploghaus A , Narain C , Beckmann CF , et al.   Exacerbation of pain by anxiety is associated with activity in a hippocampal network . J Neurosci . 2001;21:9896
  54. McEwen BS , Alves SE . Estrogen actions in the central nervous system . Endocr Rev . 1999;20:279
  55. Lisberger SG . The neural basis for learning of simple motor skills . Science . 1988;242:728
  56. Horne MK , Butler EG . The role of the cerebello-thalamo-cortical pathway in skilled movement . Prog Neurobiol . 1995;46:199
  57. Gao JH , Parsons LM , Bower JM , et al.   Cerebellum implicated in sensory acquisition and discrimination rather than motor control . Science . 1996;272:545
  58. Tesche CD , Karhu J . Somatosensory evoked magnetic fields arising from sources in the human cerebellum . Brain Res . 1997;744:23
  59. Coghill RC , Sang CN , Maisog JM , et al.   Pain intensity processing within the human brain (A bilateral, distributed mechanism) . J Neurophysiol . 1999;82:1934
  60. Kupers RC , Svensson P , Jensen TS . Central representation of muscle pain and mechanical hyperesthesia in the orofacial region (A positron emission tomography study) . Pain . 2004;108:284
  61. Svensson P , Minoshima S , Beydoun A , et al.   Cerebral processing of acute skin and muscle pain in humans . J Neurophysiol . 1997;78:450
  62. Casey KL , Morrow TJ , Lorenz J , et al.   Temporal and spatial dynamics of human forebrain activity during heat pain (Analysis by positron emission tomography) . J Neurophysiol . 2001;85:951
  63. Helmchen C , Mohr C , Erdmann C , et al.   Cerebellar neural responses related to actively and passively applied noxious thermal stimulation in human subjects (A parametric fMRI study) . Neurosci Lett . 2004;361:237
  64. Gracely RH , Geisser ME , Giesecke T , et al.   Pain catastrophizing and neural responses to pain among persons with fibromyalgia . Brain . 2004;127:835
  65. Banich MT , Milham MP , Jacobson BL , et al.   Attentional selection and the processing of task-irrelevant information (Insights from fMRI examinations of the Stroop task) . Prog Brain Res . 2001;134:459
  66. Liu X , Banich MT , Jacobson BL , et al.   Common and distinct neural substrates of attentional control in an integrated Simon and spatial Stroop task as assessed by event-related fMRI . Neuroimage . 2004;22:1097
  67. Luna B , Thulborn KR , Strojwas MH , et al.   Dorsal cortical regions subserving visually guided saccades in humans (An fMRI study) . Cereb Cortex . 1998;8:40
  68. Berman RA , Colby CL , Genovese CR , et al.   Cortical networks subserving pursuit and saccadic eye movements in humans (An fMRI study) . Hum Brain Mapp . 1999;8:209
  69. Luo J , Niki K , Ding ZG , et al.   Precuneus contributes to attentive control of finger movement . Acta Pharmacol Sin . 2004;25:637
  70. Resnick SM , Maki PM , Golski S , et al.   Effects of estrogen replacement therapy on PET cerebral blood flow and neuropsychological performance . Horm Behav . 1998;34:171
  71. Liberzon I , Zubieta JK , Fig LM , et al.   μ-Opioid receptors and limbic responses to aversive emotional stimuli . Proc Natl Acad Sci U S A . 2002;99:7084
  72. Zubieta JK , Smith YR , Bueller JA , et al.   μ-opioid receptor-mediated antinociceptive responses differ in men and women . J Neurosci . 2002;22:5100

 This study was supported by National Institutes of Health grant NCRR P20 RR15592.

PII: S0278-2391(05)01585-5

doi: 10.1016/j.joms.2005.10.006

Journal of Oral and Maxillofacial Surgery
Volume 64, Issue 2 , Pages 158-166 , February 2006

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