Changes in functioning of mesolimbic incentive processing circuits during the premenstrual phase

Social Cognitive and Affective Neuroscience

Volumn 6, Issue 5, 2011, Pages 612-620

  Ossewaarde, Lindsey ^a   Van wingen, Guido A ^a,b   Kooijman, Sabine C ^a   Bäckström, Torbjörn ^c   Fernández, Guillén ^a,b   Hermans, Erno J ^a,b  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UMEÅ UNIVERSITY HOSPITAL   (Sweden)

Author keywords

FMRI; Menstrual cycle; Motivated behavior; Reward anticipation; Ventral striatum

Indexed keywords

ELTANOLONE; OXYGEN;

ADOLESCENT; ADULT; ANALYSIS OF VARIANCE; ARTICLE; BASAL GANGLION; BLOOD; CROSSOVER PROCEDURE; FEMALE; HUMAN; IMAGE PROCESSING; LIMBIC SYSTEM; MENSTRUAL CYCLE; METABOLISM; MOTIVATION; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; QUESTIONNAIRE; REACTION TIME; SALIVA; VASCULARIZATION;

ADOLESCENT; ADULT; ANALYSIS OF VARIANCE; BASAL GANGLIA; CROSS-OVER STUDIES; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LIMBIC SYSTEM; MAGNETIC RESONANCE IMAGING; MENSTRUAL CYCLE; MOTIVATION; OXYGEN; PREGNANOLONE; QUESTIONNAIRES; REACTION TIME; SALIVA; YOUNG ADULT;

EID: 79960856471     PISSN: 17495016     EISSN: 17495024     Source Type: Journal    
DOI: 10.1093/scan/nsq071     Document Type: Article

References (64)

1. Allen, S.S., Hatsukami, D., Christianson, D., Brown, S. (2000). Effects of transdermal nicotine on craving, withdrawal and premenstrual symptomatology in short-term smoking abstinence during different phases of the menstrual cycle. Nicotine Tobacco Research, 2, 231-41.
2. Bazzett, T.J., Becker, J.B. (1994). Sex differences in the rapid and acute effects of estrogen on striatal D2 dopamine receptor binding. Brain Research, 637, 163-72.
3. Bixo, M., Bäckström, T., Winblad, B., Selstam, G., Andersson, A. (1986). Comparison between pre- and postovulatory distributions of oestradiol and progesterone in the brain of the PMSG-treated rat. Acta Physiologica Scandinavica, 128, 241-6.
4. Bjork, J.M., Hommer, D.W. (2007). Anticipating instrumentally obtained and passively-received rewards: a factorial fMRI investigation. Behavioural Brain Research, 177, 165-70.
5. Breiter, H.C., Gollub, R.L., Weisskoff, R.M., et al. (1997). Acute effects of cocaine on human brain activity and emotion. Neuron, 19, 591-611.
6. Chen, S.W., Rodriguez, L., Davies, M.F., Loew, G.H. (1996). The hyperphagic effect of 3 alpha-hydroxylated pregnane steroids in male rats. Pharmacology, Biochemistry and Behavior, 53, 777-82.
7. de Zwart, J.A., van Gelderen, P., Golay, X., Ikonomidou, V.N., Duyn, J.H (2006). Accelerated parallel imaging for functional imaging of the human brain. NMR Biomed, 19, 342-51.
8. Di Paolo, T. (1994). Modulation of brain dopamine transmission by sex steroids. Reviews in the Neurosciences, 5,27-41.
9. Di Paolo, T., Rouillard, C., Bedard, P. (1985). 17 beta-Estradiol at a physiological dose acutely increases dopamine turnover in rat brain. European Journal of Pharmacology, 117, 197-203.
10. Dillon, K.M., Brooks, D. (1992). Unusual cleaning behavior in the luteal phase. Psychological Reports, 70,35-9.
11. Dreher, J.C., Schmidt, P.J., Kohn, P., et al. (2007). Menstrual cycle phase modulates reward-related neural function in women. Proceedings of the National Academy of Sciences of the United States of America, 104, 2465-70.
12. Dye, L., Blundell, J.E. (1997). Menstrual cycle and appetite control: implications for weight regulation. Human Reproduction, 12, 1142-51.
13. Dye, L., Warner, P., Bancroft, J. (1995). Food craving during the menstrual cycle and its relationship to stress, happiness of relationship and depression; a preliminary enquiry. Journal of Affective Disorders, 34, 157-64.
14. Evans, S.M., Haney, M., Foltin, R.W. (2002). The effects of smoked cocaine during the follicular and luteal phases of the menstrual cycle in women. Psychopharmacology, 159, 397-406.
15. Fernández, G., Weis, S., Stoffel-Wagner, B., et al. (2003). Menstrual cycle- dependent neural plasticity in the adult human brain is hormone, task, and region specific. Journal of Neuroscience, 23, 3790-5.
16. Flaisher-Grinberg, S., Albelda, N., Gitter, L., et al. (2009). Ovarian hormones modulate 'compulsive' lever-pressing in female rats. Hormones and Behavior, 55, 356-65.
17. Premenstrual phase and reward SCAN (2011) 619
18. Franklin, T.R., Napier, K., Ehrman, R., et al. (2004). Retrospective study: influence of menstrual cycle on cue-induced cigarette craving. Nicotine Tobacco Research, 6, 171-5.
19. Goldstein, J.M., Jerram, M., Poldrack, R., et al. (2005). Hormonal cycle modulates arousal circuitry in women using functional magnetic resonance imaging. Journal of Neuroscience, 25, 9309-16.
20. Griswold, M.A., Jakob, P., Heidemann, R., et al. (2002). Generalized auto- calibrating partially parallel acquisitions (GRAPPA). Magnetic Resonance in Medicine, 47, 1202-10.
21. Hermans, E.J., Ramsey, N.F., van Honk, J. (2008). Exogenous testosterone enhances responsiveness to social threat in the neural circuitry of social aggression in humans. Biological Psychiatry, 63, 263-70.
22. Hermans, E.J., Bos, P.A., Ossewaarde, L., et al. (2010). Effects of exogenous testosterone on the ventral striatal BOLD response during reward anticipation in healthy women. Neuroimage, 52, 277-83.
23. Kilts, C.D., Gross, R.E., Ely, T.D., Drexler, K.P. (2004). The neural correlates of cue-induced craving in cocaine-dependent women. American Journal of Psychiatry, 161, 233-41.
24. Kilts, C.D., Schweitzer, J.B., Quinn, C.K., et al. (2001). Neural activity related to drug craving in cocaine addiction. Archives of General Psychiatry, 58, 334-41.
25. Knutson, B., Adams, C.M., Fong, G.W., Hommer, D. (2001a). Anticipation of increasing monetary reward selectively recruits nucleus accumbens. Journal of Neuroscience, 21, RC159.
26. Knutson, B., Cooper, J.C. (2005). Functional magnetic resonance imaging of reward prediction. Current Opinion in Neurology, 18, 411-7.
27. Knutson, B., Fong, G.W., Adams, C.M., Varner, J.L., Hommer, D. (2001b). Dissociation of reward anticipation and outcome with event-related fMRI. Neuroreport, 12, 3683-7.
28. Knutson, B., Gibbs, S.E. (2007). Linking nucleus accumbens dopamine and blood oxygenation. Psychopharmacology, 191, 813-22.
29. Kuppers, E., Ivanova, T., Karolczak, M., Beyer, C. (2000). Estrogen: a multi- functional messenger to nigrostriatal dopaminergic neurons. Journal of Neurocytology, 29, 375-85.
30. LaBar, K.S., Gitelman, D.R., Parrish, T.B., et al. (2001). Hunger selectively modulates corticolimbic activation to food stimuli in humans. Behavioral Neuroscience, 115, 493-500.
31. Larson, E.B., Carroll, M.E. (2007). Estrogen receptor beta, but not alpha, mediates estrogen's effect on cocaine-induced reinstatement of extinguished cocaine-seeking behavior in ovariectomized female rats. Neuropsychopharmacology, 32, 1334-45.
32. Le Saux, M., Morissette, M., Di Paolo, T. (2006). ERbeta mediates the estradiol increase of D2 receptors in rat striatum and nucleus accumbens. Neuropharmacology, 50, 451-7.
33. Mani, S. (2008). Progestin receptor subtypes in the brain: the known and the unknown. Endocrinology, 149, 2750-6.
34. Mani, S.K. (2006). Signaling mechanisms in progesterone-neurotransmitter interactions. Neuroscience, 138, 773-81.
35. McBride, D., Barrett, S.P., Kelly, J.T., Aw, A., Dagher, A. (2006). Effects of expectancy and abstinence on the neural response to smoking cues in cigarette smokers: an fMRI study. Neuropsychopharmacology, 31, 2728-38.
36. McEwen, B. (2002). Estrogen actions throughout the brain. Recent Progress in Hormone Research, 57, 357-84.
37. Moos, R.H. (1968). The development of a menstrual distress questionnaire. Psychosomatic Medicine, 30, 853-67.
38. Ossewaarde, L., Hermans, E.J., van Wingen, G.A., et al. (2010). Neural mechanisms underlying changes in stress-sensitivity across the menstrual cycle. Psychoneuroendocrinology, 35,47-55.
39. Petitclerc, M., Bedard, P.J., Di Paolo, T. (1995). Progesterone releases dopamine in male and female rat striatum: a behavioral and microdialysis study. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 19, 491-7.
40. Protopopescu, X., Pan, H., Altemus, M., et al. (2005). Orbitofrontal cortex activity related to emotional processing changes across the menstrual cycle. Proceedings of the National Academy of Sciences of the United States of America, 102, 16060-5.
41. Purdy, R.H., Moore, P.H. Jr, Rao, P.N., et al. (1990). Radioimmunoassay of 3 alpha-hydroxy-5 alpha-pregnan-20-one in rat and human plasma. Steroids, 55, 290-6.
42. Reddy, D.S., Kulkarni, S.K. (1998). The role of GABA-A and mitochondrial diazepam-binding inhibitor receptors on the effects of neurosteroids on food intake in mice. Psychopharmacology, 137, 391-400.
43. Reddy, D.S., Kulkarni, S.K. (1999). Sex and estrous cycle-dependent changes in neurosteroid and benzodiazepine effects on food consumption and plus-maze learning behaviors in rats. Pharmacology, Biochemistry and Behavior, 62,53-60.
44. Reed, S.C., Levin, F.R., Evans, S.M. (2008). Changes in mood, cognitive performance and appetite in the late luteal and follicular phases of the menstrual cycle in women with and without PMDD (premenstrual dysphoric disorder). Hormones and Behavior, 54, 185-93.
45. Robinson, T.E., Berridge, K.C. (1993). The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Research Brain Research Reviews, 18, 247-91.
46. Rolls, E.T., McCabe, C. (2007). Enhanced affective brain representations of chocolate in cravers vs. non-cravers. European Journal of Neuroscience, 26, 1067-76.
47. Roy, E.J., Wilson, M.A., Kelley, D.B. (1986). Estrogen-induced progestin receptors in the brain and pituitary of the South African clawed frog, Xenopus laevis. Neuroendocrinology, 42,51-6.
48. Schott, B.H., Minuzzi, L., Krebs, R.M., et al. (2008). Mesolimbic functional magnetic resonance imaging activations during reward anticipation correlate with reward-related ventral striatal dopamine release. Journal of Neuroscience, 28, 14311-19.
49. Sheehan, D.V., Lecrubier, Y., Sheehan, K.H., et al. (1998). The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry, 59, 22-33.
50. Shughrue, P.J., Scrimo, P.J., Merchenthaler, I. (1998). Evidence for the colocalization of estrogen receptor-beta mRNA and estrogen receptor-alpha immunoreactivity in neurons of the rat forebrain. Endocrinology, 139, 5267-70.
51. Sveindottir, H., Bäckström, T. (2000). Prevalence of menstrual cycle symptom cyclicity and premenstrual dysphoric disorder in a random sample of women using and not using oral contraceptives. Acta Obstetricia et Gynecologica Scandinavica, 79, 405-13.
52. Thompson, T.L., Moss, R.L. (1994). Estrogen regulation of dopamine release in the nucleus accumbens: genomic- and nongenomic-mediated effects. Journal of Neurochemistry, 62, 1750-6.
53. Thompson, T.L., Moss, R.L. (1997). Modulation of mesolimbic dopaminergic activity over the rat estrous cycle. Neuroscience Letters, 229, 145-8.
54. Tomelleri, R., Grunewald, K.K. (1987). Menstrual cycle and food cravings in young college women. Journal of the American Dietetic Association, 87, 311-5.
55. van Hell, H.H., Vink, M., Ossewaarde, L., et al. (2010). Chronic effects of cannabis use on the human reward system: an fMRI study. European Neuropsychopharmacology, 20, 153-63.
56. van Wingen, G.A., van Broekhoven, F., Verkes, R.J., et al. (2008). Progesterone selectively increases amygdala reactivity in women. Molecular Psychiatry, 13, 325-33.
57. van Wingen, G.A., Zylicz, S.A., Pieters, S., et al. (2009). Testosterone increases amygdala reactivity in middle-aged women to a young adulthood level. Neuropsychopharmacology, 34, 539-47.
58. Vollm, B.A., de Araujo, I.E., Cowen, P.J., et al. (2004). Methamphetamine activates reward circuitry in drug naive human subjects. Neuropsychopharmacology, 29, 1715-22.
59. Vulink, N.C., Denys, D., Bus, L., Westenberg, H.G. (2006). Female hormones affect symptom severity in obsessive-compulsive disorder. International Clinical Psychopharmacology, 21, 171-5.
60. Wang, M., Seippel, L., Purdy, R.H., Bäckström, T. (1996). Relationship between symptom severity and steroid variation in women with premenstrual syndrome: study on serum pregnenolone, pregnenolone sulfate, 5 alpha-pregnane-3,20-dione and 3 alpha-hydroxy-5 alpha-pregnan-20-one. Journal of Clinical Endocrinology and Metabolism, 81, 1076-82.
61. Wang, M.D., Wahlström, G., Gee, K.W., Bäckström, T. (1995). Potency of lipid and protein formulation of 5 alpha-pregnanolone at induction of anaesthesia and the corresponding regional brain distribution. British Journal of Anaesthesia, 74, 553-7.
62. Weis, S., Hausmann, M., Stoffers, B., et al. (2008). Estradiol modulates functional brain organization during the menstrual cycle: an analysis of interhemispheric inhibition. Journal of Neuroscience, 28, 13401-10.
63. Wrase, J., Schlagenhauf, F., Kienast, T., et al. (2007). Dysfunction of reward processing correlates with alcohol craving in detoxified alcoholics. Neuroimage, 35, 787-94.
64. York, R., Freeman, E., Lowery, B., Strauss, J.F. (1989). Characteristics of premenstrual syndrome. Obstetrics and Gynecology, 73, 601-5.