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Brain responses to erotic and other emotional stimuli in breast cancer survivors with and without distress about low sexual desire: a preliminary fMRI study

  • SI: Neuroimaging Studies of Cancer and Cancer Treatment
  • Published:
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Abstract

Many breast cancer survivors report a loss of sexual desire and arousability, consonant with the new DSM-V category of female sexual interest/arousal disorder. The cause of decreased sexual desire and pleasure after treatment for cancer is unknown. One possibility is that cancer, or treatment for cancer, damages brain circuits that are involved in reward-seeking. To test the hypothesis that brain reward systems are involved in decreased sexual desire in breast cancer survivors, we used functional magnetic resonance imaging (fMRI) to compare brain responses to erotica and other emotional stimuli in two groups of women previously treated for breast cancer with chemotherapy: those who were distressed about a perceived loss of sexual desire and those who may have had low desire, but were not distressed about it. Women distressed about their desire had reduced brain responses to erotica in the anterior cingulate and dorsolateral prefrontal cortex, which are part of the brain reward system. This study is the first to demonstrate, in cancer survivors, that problems with sexual desire/arousability are associated with blunted brain responses to erotica in reward systems. Future research is necessary to determine whether brain responses differ as a result of chemotherapy, hormone therapy, and menopausal status. This may contribute to the development of new, evidence-based interventions for one of the most prevalent and enduring side effects of cancer treatment.

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References

  • Abler, B., Kumpfmuller, D., Gron, G., Walter, M., Stingl, J., & Seeringer, A. (2013). Neural correlates of erotic stimulation under different levels of female sexual hormones. PLoS ONE, 8, e54447.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Alder, J., Zanetti, R., Wight, E., Urech, C., Fink, N., & Bitzer, J. (2008). Sexual dysfunction after premenopausal stage I and II breast cancer: do androgens play a role? The Journal of Sexual Medicine, 5, 1898–1906.

    Article  PubMed  Google Scholar 

  • American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders (4th ed.). Washington: American Psychiatric Association.

    Google Scholar 

  • American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th revised ed.). Washington: American Psychiatric Association.

  • American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington: American Psychiatric Association.

    Google Scholar 

  • Arnow, B. A., Millheiser, L., Garrett, A., Lake, P. M., Glover, G. H., Hill, K. R., et al. (2009). Women with hypoactive sexual desire disorder compared to normal females: a functional magnetic resonance imaging study. Neuroscience, 158, 484–502.

    Article  CAS  PubMed  Google Scholar 

  • Avis, N. E., Brockwell, S., Randolph, J. F., Jr., Shen, S., Cain, V. S., Ory, M., et al. (2009). Longitudinal changes in sexual functioning as women transition through menopause: results from the Study of Women’s Health Across the Nation. Menopause, 16, 442–452.

    Article  PubMed Central  PubMed  Google Scholar 

  • Barton, D. L., Wender, D. B., Sloan, J. A., Dalton, R. J., Balcueva, E. P., Atherton, P. J., et al. (2007). Randomized controlled trial to evaluate transdermal testosterone in female cancer survivors with decreased libido; North Central Cancer Treatment Group protocol N02C3. Journal of the National Cancer Institute, 99, 672–679.

    Article  CAS  PubMed  Google Scholar 

  • Berglund, G., Nystedt, M., Bolund, C., Sjoden, P. O., & Rutquist, L. E. (2001). Effect of endocrine treatment on sexuality in premenopausal breast cancer patients: a prospective randomized study. Journal of Clinical Oncology, 19, 2788–2796.

    CAS  PubMed  Google Scholar 

  • Bianchi-Demicheli, F., Cojan, Y., Waber, L., Recordon, N., Vuilleumier, P., & Ortigue, S. (2011). Neural bases of hypoactive sexual desire disorder in women: an event-related FMRI study. The Journal of Sexual Medicine, 8, 2546–2559.

    Article  PubMed  Google Scholar 

  • Bitzer, J., Giraldi, A., & Pfaus, J. (2013). Sexual desire and hypoactive sexual desire disorder in women. Introduction and overview. Standard operating procedure (SOP Part 1). The Journal of Sexual Medicine, 10, 36–49.

    Article  PubMed  Google Scholar 

  • Bober, S. L., Giobbie-Hurder, A., Emmons, K. M., Winer, E., & Partridge, A. (2013). Psychosexual functioning and body image following a diagnosis of ductal carcinoma in situ. The Journal of Sexual Medicine, 10, 370–377.

    Article  PubMed  Google Scholar 

  • Bradford, A. (2013). Listening to placebo in clinical trials for female sexual dysfunction. The Journal of Sexual Medicine, 10, 451–459.

    Article  PubMed  Google Scholar 

  • Bradley, M. M., Sabatinelli, D., Lang, P. J., Fitzsimmons, J. R., King, W., & Desai, P. (2003). Activation of the visual cortex in motivated attention. Behavioral Neuroscience, 117, 369–380.

    Article  PubMed  Google Scholar 

  • Burwell, S. R., Case, L. D., Kaelin, C., & Avis, N. E. (2006). Sexual problems in younger women after breast cancer surgery. Journal of Clinical Oncology, 24, 2815–2821.

    Article  PubMed  Google Scholar 

  • Clayton, A. H., Goldfischer, E. R., Goldstein, I., Derogatis, L., Lewis-D'Agostino, D. J., & Pyke, R. (2009). Validation of the decreased sexual desire screener (DSDS): a brief diagnostic instrument for generalized acquired female hypoactive sexual desire disorder (HSDD). The Journal of Sexual Medicine, 6, 730–738.

    Article  PubMed  Google Scholar 

  • Collins, B., Mackenzie, J., Tasca, G. A., Scherling, C., Smith, A. (2012). Cognitive effects of chemotherapy in breast cancer patients: a dose–response study. Psychooncology.

  • de Ruiter, M. B., Reneman, L., Boogerd, W., Veltman, D. J., van Dam, F. S., Nederveen, A. J., et al. (2011). Cerebral hyporesponsiveness and cognitive impairment 10 years after chemotherapy for breast cancer. Human Brain Mapping, 32, 1206–1219.

    Article  PubMed  Google Scholar 

  • de Ruiter, M. B., Reneman, L., Boogerd, W., Veltman, D. J., Caan, M., Douaud, G., et al. (2012). Late effects of high-dose adjuvant chemotherapy on white and gray matter in breast cancer survivors: converging results from multimodal magnetic resonance imaging. Human Brain Mapping, 33, 2971–2983.

    Article  PubMed  Google Scholar 

  • Derogatis, L. R. (2001). Brief symptom inventory 18: Administration, scoring, and procedures Manuel. Minneapolis: NCS Pearson.

    Google Scholar 

  • Derogatis, L., Clayton, A., Lewis-D'Agostino, D., Wunderlich, G., & Fu, Y. (2008). Validation of the female sexual distress scale-revised for assessing distress in women with hypoactive sexual desire disorder. The Journal of Sexual Medicine, 5, 357–364.

    PubMed  Google Scholar 

  • Dizon, D. S. (2009). Quality of life after breast cancer: survivorship and sexuality. The Breast Journal, 15, 500–504.

    Article  PubMed  Google Scholar 

  • Engelmann, J. M., Versace, F., Robinson, J. D., Minnix, J. A., Lam, C. Y., Cui, Y., et al. (2012). Neural substrates of smoking cue reactivity: a meta-analysis of fMRI studies. NeuroImage, 60, 252–262. doi:10.1016/j.neuroimage.2011.12.024.

    Article  PubMed Central  PubMed  Google Scholar 

  • Finch, A., Metcalfe, K. A., Chiang, J. K., Elit, L., McLaughlin, J., Springate, C., et al. (2011). The impact of prophylactic salpingo-oophorectomy on menopausal symptoms and sexual function in women who carry a BRCA mutation. Gynecologic Oncology, 121, 163–168.

    Article  CAS  PubMed  Google Scholar 

  • Fobair, P., Stewart, S. L., Chang, S., D'Onofrio, C., Banks, P. J., & Bloom, J. R. (2006). Body image and sexual problems in young women with breast cancer. Psycho-Oncology, 15, 579–594.

    Article  PubMed  Google Scholar 

  • Ganz, P. A., Rowland, J. H., Meyerowitz, B. E., & Desmond, K. A. (1998). Impact of different adjuvant therapy strategies on quality of life in breast cancer survivors. Recent Results in Cancer Research, 152, 396–411.

    Article  CAS  PubMed  Google Scholar 

  • Georgiadis, J. R., & Kringelbach, M. L. (2012). The human sexual response cycle: brain imaging evidence linking sex to other pleasures. Progress in Neurobiology, 98, 49–81.

    Article  CAS  PubMed  Google Scholar 

  • Goebel, R., Esposito, F., & Formisano, E. (2006). Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: from single-subject to cortically aligned group general linear model analysis and self-organizing group independent component analysis. Human Brain Mapping, 27, 392–401. doi:10.1002/hbm.20249.

    Article  PubMed  Google Scholar 

  • Greendale, G. A., Petersen, L., Zibecchi, L., & Ganz, P. A. (2001). Factors related to sexual function in postmenopausal women with a history of breast cancer. Menopause, 8, 111–119.

    Article  CAS  PubMed  Google Scholar 

  • Hayes, R. D. (2011). Circular and linear modeling of female sexual desire and arousal. Journal of Sex Research, 48, 130–141.

    Article  PubMed  Google Scholar 

  • Holstege, G., & Huynh, H. K. (2011). Brain circuits for mating behavior in cats and brain activations and de-activations during sexual stimulation and ejaculation and orgasm in humans. Hormones and Behavior, 59, 702–707.

    Article  PubMed  Google Scholar 

  • Kesler, S. R., Kent, J. S., & O'Hara, R. (2011). Prefrontal cortex and executive function impairments in primary breast cancer. Archives of Neurology, 68, 1447–1453.

    Article  PubMed Central  PubMed  Google Scholar 

  • Koppelmans, V., Breteler, M. M., Boogerd, W., Seynaeve, C., Gundy, C., & Schagen, S. B. (2012). Neuropsychological performance in survivors of breast cancer more than 20 years after adjuvant chemotherapy. Journal of Clinical Oncology, 30, 1080–1086.

    Article  PubMed  Google Scholar 

  • Kuhn, S., & Gallinat, J. (2011). Common biology of craving across legal and illegal drugs—a quantitative meta-analysis of cue-reactivity brain response. European Journal of Neuroscience, 33, 1318–1326.

    Article  PubMed  Google Scholar 

  • Lang, P. J. (1980). Behavioral treatment and bio-behavioral assessment: Computer applications. In J. B. Sidowski, J. H. Johnson, & T. A. Williams (Eds.), Technology in mental health care delivery systems (pp. 119–137). Norwood: Ablex.

    Google Scholar 

  • Lang, P. J., & Bradley, M. M. (2009). Emotion and the motivational brain. Biological Psychology, 84, 437–450. doi:10.1016/j.biopsycho.2009.10.007.

    Article  PubMed Central  PubMed  Google Scholar 

  • Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (1997). Motivated attention: Affect, activation, and action. In P. J. Lang, R. F. Simons, & M. Balaban (Eds.), Attention and orienting: Sensory and motivational processes (pp. 97–136). Mahwah: Lawrence Erlbaum.

    Google Scholar 

  • Lang, P. J., Bradley, M. M., Fitzsimmons, J. R., Cuthbert, B. N., Scott, J. D., Moulder, B., et al. (1998). Emotional arousal and activation of the visual cortex: an fMRI analysis. Psychophysiology, 35, 199–210.

    Article  CAS  PubMed  Google Scholar 

  • Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (2008). International affective picture system (IAPS): Affective ratings of pictures and instruction manual. Technical Report A-8. Gainesville: University of Florida.

    Google Scholar 

  • McCrae, R. R., & Costa, P. T. (2004). A contemplated revision of the NEO Five-Factor Inventory. Personality and Individual Differences, 36, 587–596.

    Article  Google Scholar 

  • Morris, J. S., Friston, K. J., Buchel, C., Frith, C. D., Young, A. W., Calder, A. J., et al. (1998). A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain, 121(Pt 1), 47–57.

    Article  PubMed  Google Scholar 

  • Mumford, J. A., & Nichols, T. (2009). Simple group fMRI modeling and inference. NeuroImage, 47, 1469–1475. doi:10.1016/j.neuroimage.2009.05.034.

    Article  PubMed Central  PubMed  Google Scholar 

  • Ochsenkühn, R., Hermelink, K., Clayton, A. H., von Schönfeldt, V., Gallwas, J., Ditsch, N., et al. (2011). Menopausal status in breast cancer patients with past chemotherapy determines long-term hypoactive sexual desire disorder. The Journal of Sexual Medicine, 8, 1486–1494.

    Article  PubMed  Google Scholar 

  • Panjari, M., Bell, R. J., & Davis, S. R. (2011). Sexual function after breast cancer. The Journal of Sexual Medicine, 8, 294–302.

    Article  PubMed  Google Scholar 

  • Pessoa, L. (2008). On the relationship between emotion and cognition. Nature Reviews Neuroscience, 9, 148–158. doi:10.1038/nrn2317.

    Article  CAS  PubMed  Google Scholar 

  • Pessoa, L., McKenna, M., Gutierrez, E., & Ungerleider, L. G. (2002). Neural processing of emotional faces requires attention. Proceedings of the National Academy of Sciences of the United States of America, 99, 11458–11463.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pfaus, J. G. (2009). Pathways of sexual desire. The Journal of Sexual Medicine, 6, 1506–1533.

    Article  CAS  PubMed  Google Scholar 

  • Rosen, R. C., Lobo, R. A., Block, B. A., Yang, H. M., & Zipfel, L. M. (2004). Menopausal Sexual Interest Questionnaire (MSIQ): a unidimensional scale for the assessment of sexual interest in postmenopausal women. Journal of Sex & Marital Therapy, 30, 235–250.

    Article  Google Scholar 

  • Sabatinelli, D., Bradley, M. M., Fitzsimmons, J. R., & Lang, P. J. (2005). Parallel amygdala and inferotemporal activation reflect emotional intensity and fear relevance. NeuroImage, 24, 1265–1270.

    Article  PubMed  Google Scholar 

  • Sabatinelli, D., Bradley, M. M., Lang, P. J., Costa, V. D., & Versace, F. (2007). Pleasure rather than salience activates human nucleus accumbens and medial prefrontal cortex. Journal of Neurophysiology, 98, 1374–1379.

    Article  PubMed  Google Scholar 

  • Sabourin, S., Valois, P., & Lussier, Y. (2005). Development and validation of a brief version of the dyadic adjustment scale with a nonparametric item analysis model. Psychological Assessment, 17, 15–27.

    Article  PubMed  Google Scholar 

  • Sarin, S., Amsel, R. M., Binik, Y. M. (2013). Disentangling desire and arousal: a classificatory conundrum. Archives of Sexual Behavior.

  • Sayakhot, P., Vincent, A., Deeks, A., & Teede, H. (2011). Potential adverse impact of ovariectomy on physical and psychological function of younger women with breast cancer. Menopause, 18, 786–793.

    Article  PubMed  Google Scholar 

  • Schover, L. R. (2008). Premature ovarian failure and its consequences: vasomotor symptoms, sexuality, and fertility. Journal of Clinical Oncology, 26, 753–758.

    Article  PubMed  Google Scholar 

  • Schover, L. R., Yetman, R. J., Tuason, L. J., Meisler, E., Esselstyn, C. B., Hermann, R. E., et al. (1995). Partial mastectomy and breast reconstruction. A comparison of their effects on psychosocial adjustment, body image, and sexuality. Cancer, 75, 54–64.

    Article  CAS  PubMed  Google Scholar 

  • Sescousse, G., Caldu, X., Segura, B., & Dreher, J. C. (2013). Processing of primary and secondary rewards: a quantitative meta-analysis and review of human functional neuroimaging studies. Neuroscience and Biobehavioral Reviews, 37, 681–696.

    Article  PubMed  Google Scholar 

  • Speer, J. J., Hillenberg, B., Sugrue, D. P., Blacker, C., Kresge, C. L., Decker, V. B., et al. (2005). Study of sexual functioning determinants in breast cancer survivors. The Breast Journal, 11, 440–447.

    Article  PubMed  Google Scholar 

  • Stoleru, S., Fonteille, V., Cornelis, C., Joyal, C., & Moulier, V. (2012). Functional neuroimaging studies of sexual arousal and orgasm in healthy men and women: a review and meta-analysis. Neuroscience and Biobehavioral Reviews, 36, 1481–1509.

    Article  PubMed  Google Scholar 

  • Suppli, N. P., Deltour, I., Damkjaer, L. H., Christensen, J., Jensen, A. B., Kroman, N. T., et al. (2011). Factors associated with the prescription of antidepressive medication to breast cancer patients. Acta Oncologica, 50, 243–251.

    Article  PubMed  Google Scholar 

  • Toledano, R., & Pfaus, J. (2006). The Sexual Arousal and Desire Inventory (SADI): a multidimensional scale to assess subjective sexual arousal and desire. The Journal of Sexual Medicine, 3, 853–877.

    Article  PubMed  Google Scholar 

  • Trompeter, S. E., Bettencourt, R., & Barrett-Connor, E. (2012). Sexual activity and satisfaction in healthy community-dwelling older women. American Journal of Medicine, 125, 37–43.

    Article  PubMed Central  PubMed  Google Scholar 

  • Versace, F., Engelmann, J. M., Jackson, E. F., Costa, V. D., Robinson, J. D., Lam, C. Y., et al. (2011). Do brain responses to emotional images and cigarette cues differ? an fMRI study in smokers. European Journal of Neuroscience, 34, 2054–2063.

    Article  PubMed Central  PubMed  Google Scholar 

  • Walter, M., Bermpohl, F., Mouras, H., Schiltz, K., Tempelmann, C., Rotte, M., et al. (2008). Distinguishing specific sexual and general emotional effects in fMRI-subcortical and cortical arousal during erotic picture viewing. NeuroImage, 40, 1482–1494.

    Article  PubMed  Google Scholar 

  • Wefel, J. S., Lenzi, R., Theriault, R. L., Davis, R. N., & Meyers, C. A. (2004). The cognitive sequelae of standard-dose adjuvant chemotherapy in women with breast carcinoma: results of a prospective, randomized, longitudinal trial. Cancer, 100, 2292–2299.

    Article  CAS  PubMed  Google Scholar 

  • Wiegel, M., Meston, C., & Rosen, R. (2005). The female sexual function index (FSFI): cross-validation and development of clinical cutoff scores. Journal of Sex & Marital Therapy, 31, 1–20.

    Article  Google Scholar 

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Acknowledgments

This research was supported by funds from the University Cancer Foundation and the Duncan Family Institute for Cancer Prevention and Risk Assessment via the Cancer Survivorship Research Seed Money Grants at the University of Texas MD Anderson Cancer Center to Francesco Versace.

The University of Texas MD Anderson Cancer Center Breast Cancer Management System Database was consulted to obtain the initial list of potential participants.

The authors wish to thank Lauren Baker, Jerell Jones, Cheryl Mize, and Jennifer Ng for their help in data collection.

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The authors declare that they have no conflict of interest.

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Versace, F., Engelmann, J.M., Jackson, E.F. et al. Brain responses to erotic and other emotional stimuli in breast cancer survivors with and without distress about low sexual desire: a preliminary fMRI study. Brain Imaging and Behavior 7, 533–542 (2013). https://doi.org/10.1007/s11682-013-9252-1

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