Abstract
Aim of this work was to evaluate the reproducibility of hormone driven regional grey matter volume differences in women, and their correlations with premenstrual symptoms, as determined by voxel-based morphometry (VBM). After data quality control, a total of 138 T1-weighted MR images were included in this longitudinal study, and were analyzed as three different subgroups. Women with a natural menstrual cycle were scanned at three time-points: follicular, ovulatory and luteal phase. Two groups of women, using androgenic and anti-androgenic hormonal contraceptives, respectively, were scanned twice: during the pill-free week and during pill intake. Additionally, subjects were asked to complete a “daily rating of severity of problems” questionnaire, to quantify premenstrual symptoms. All data were analyzed using SPM8 and SPM12 with identical parameter settings. In the natural menstrual cycle group, the regional grey matter volume of the insula is larger at ovulation, as compared to the luteal phase. Premenstrual symptoms correlate differently with regional grey matter volumes between women with a natural cycle and hormonal contraceptive users. Changes in hormonal environment can to various extents affect VBM findings in women. We suggest that researchers take these confounding factors into account while applying this technique, to avoid heterogeneity in data acquisition and to safeguard the sensitivity of findings. Additionally, we suggest validating the consistency of results using more than one software package.
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References
Ashburner J (2007) A fast diffeomorphic image registration algorithm. NeuroImage 38(1):95–113 (Epub 2007/09/01)
Ashburner J, Friston KJ (2000) Voxel-based morphometry: the methods. NeuroImage 11(6 Pt 1):805–821 (Epub 2000/06/22)
Ashburner J, Friston KJ (2005) Unified segmentation. NeuroImage 26(3):839–851 (Epub 2005/06/16)
Bayer J, Schultz H, Gamer M, Sommer T (2014) Menstrual-cycle dependent fluctuations in ovarian hormones affect emotional memory. Neurobiol Learn Mem 110:55–63 (Epub 2014/02/05)
Berman SM, London ED, Morgan M, Rapkin AJ (2013) Elevated gray matter volume of the emotional cerebellum in women with premenstrual dysphoric disorder. J Affect Disord 146(2):266–271 (Epub 2012/08/08)
Bitzer J, Simon JA (2011) Current issues and available options in combined hormonal contraception. Contraception 84(4):342–356 (Epub 2011/09/17)
Cahill L (2014) Equal not equal the same: sex differences in the human brain. Cerebrum 2014:5 (Epub 2014/07/11)
Craig AD (2010) The sentient self. Brain Struct Funct 214(5–6):563–577 (Epub 2010/06/01)
Cullberg J (1972) Mood changes and menstrual symptoms with different gestagen/estrogen combinations: a double blind comparison with a placebo. Acta Psychiatr Scand Suppl 236:1–86 (Epub 1972/01/01)
Damasio A, Damasio H, Tranel D (2013) Persistence of feelings and sentience after bilateral damage of the insula. Cereb Cortex 23(4):833–846 (Epub 2012/04/05)
De Bondt T, Jacquemyn Y, Van Hecke W, Sijbers J, Sunaert S, Parizel PM (2013) Regional gray matter volume differences and sex-hormone correlations as a function of menstrual cycle phase and hormonal contraceptives use. Brain Res 1530:22–31 (Epub 2013/07/31)
Derntl B, Hack RL, Kryspin-Exner I, Habel U (2013) Association of menstrual cycle phase with the core components of empathy. Horm Behav 63(1):97–104 (Epub 2012/10/27)
Endicott J, Nee J, Harrison W (2006) Daily record of severity of problems (DRSP): reliability and validity. Arch Womens Ment Health 9(1):41–49 (Epub 2005/09/21)
Epperson CN, Steiner M, Hartlage SA, Eriksson E, Schmidt PJ, Jones I et al (2012) Premenstrual dysphoric disorder: evidence for a new category for DSM-5. Am J Psychiatr 169(5):465–475 (Epub 2012/07/06)
Ertman N, Andreano JM, Cahill L (2011) Progesterone at encoding predicts subsequent emotional memory. Learn Mem 18(12):759–763 (Epub 2011/11/22)
Galea LA, Wainwright SR, Roes MM, Duarte-Guterman P, Chow C, Hamson DK (2013) Sex, hormones, and neurogenesis in the hippocampus: Hormonal modulation of neurogenesis and potential functional implications. J Neuroendocrinol ((Epub 2013/07/05)
Garcia-Segura LM (1997) Estrogen-induced hypothalamic synaptic plasticity. Aging (Milano) 9(4 Suppl):59 (Epub 1997/01/01)
Hagemann G, Ugur T, Schleussner E, Mentzel HJ, Fitzek C, Witte OW, Gaser C (2011) Changes in brain size during the menstrual cycle. PLoS One 6(2):e14655. doi:10.1371/journal.pone.0014655
Hambridge HL, Mumford SL, Mattison DR, Ye A, Pollack AZ, Bloom MS et al (2013) The influence of sporadic anovulation on hormone levels in ovulatory cycles. Hum Reprod 28(6):1687–1694 (Epub 2013/04/17)
Jeong HG, Ham BJ, Yeo HB, Jung IK, Joe SH (2012) Gray matter abnormalities in patients with premenstrual dysphoric disorder: an optimized voxel-based morphometry. J Affect Disord 140(3):260–267 (Epub 2012/03/03)
Jung-Hoffmann C, Kuhl H (1989) Interaction with the pharmacokinetics of ethinylestradiol and progestogens contained in oral contraceptives. Contraception 40(3):299–312 (Epub 1989/09/01)
Klein A, Andersson J, Ardekani BA, Ashburner J, Avants B, Chiang MC et al (2009) Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. NeuroImage 46(3):786–802 (Epub 2009/02/07)
Leranth C, Shanabrough M (2001) Supramammillary area mediates subcortical estrogenic action on hippocampal synaptic plasticity. Exp Neurol 167(2):445–450 (Epub 2001/02/13)
Macrae CN, Alnwick KA, Milne AB, Schloerscheidt AM (2002) Person perception across the menstrual cycle: hormonal influences on social-cognitive functioning. Psychol Sci 13(6):532–536 (Epub 2002/11/15)
McCarthy MM, Arnold AP, Ball GF, Blaustein JD, De Vries GJ (2012) Sex differences in the brain: the not so inconvenient truth. J Neurosci 32(7):2241–2247 (Epub 2012/03/08)
Melcangi RC, Panzica G, Garcia-Segura LM (2011) Neuroactive steroids: focus on human brain. Neuroscience 191:1–5 (Epub 2011/06/28)
Mihm M, Gangooly S, Muttukrishna S (2011) The normal menstrual cycle in women. Anim Reprod Sci 124(3–4):229–236 (Epub 2010/09/28)
Naftolin F, Garcia-Segura LM, Horvath TL, Zsarnovszky A, Demir N, Fadiel A, Leranth C, Vondracek-Klepper S, Lewis C, Chang A, Parducz A (2007) Estrogen-induced hypothalamic synaptic plasticity and pituitary sensitization in the control of the estrogen-induced gonadotrophin surge. Reprod Sci 14(2):101–116. doi:10.1177/1933719107301059
Nielsen SE, Ahmed I, Cahill L (2013) Sex and menstrual cycle phase at encoding influence emotional memory for gist and detail. Neurobiol Learn Mem 106:56–65 (Epub 2013/07/31)
Ortigue S, Grafton ST, Bianchi-Demicheli F (2007) Correlation between insula activation and self-reported quality of orgasm in women. NeuroImage 37(2):551–560 (Epub 2007/07/03)
Osterlund MK, Hurd YL (2001) Estrogen receptors in the human forebrain and the relation to neuropsychiatric disorders. Prog Neurobiol 64(3):251–267 (Epub 2001/03/10)
Phan KL, Wager T, Taylor SF, Liberzon I (2002) Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. NeuroImage 16(2):331–348 (Epub 2002/05/29)
Pletzer BA, Kerschbaum HH (2014) 50 years of hormonal contraception-time to find out, what it does to our brain. Front Neurosci 8:256 (Epub 2014/09/06)
Pletzer B, Kronbichler M, Aichhorn M, Bergmann J, Ladurner G, Kerschbaum HH (2010) Menstrual cycle and hormonal contraceptive use modulate human brain structure. Brain Res 1348:55–62 (Epub 2010/06/17)
Pletzer B, Kronbichler M, Kerschbaum H (2015) Differential effects of androgenic and anti-androgenic progestins on fusiform and frontal gray matter volume and face recognition performance. Brain Res 1596:108–115
Potgieser AR, van der Hoorn A, Meppelink AM, Teune LK, Koerts J, de Jong BM (2014) Anterior temporal atrophy and posterior progression in patients with Parkinson’s disease. Neuro-degener Dis 14(3):125–132 (Epub 2014/08/21)
Protopopescu X, Butler T, Pan H, Root J, Altemus M, Polanecsky M et al (2008) Hippocampal structural changes across the menstrual cycle. Hippocampus 18(10):985–988 (Epub 2008/09/04)
Rosa PG, Zanetti MV, Duran FL, Santos LC, Menezes PR, Scazufca M et al (2014) What determines continuing grey matter changes in first-episode schizophrenia and affective psychosis? Psychol Med 2014:1–12 (Epub 2014/09/03)
Rupp HA, James TW, Ketterson ED, Sengelaub DR, Janssen E, Heiman JR (2009) Neural activation in the orbitofrontal cortex in response to male faces increases during the follicular phase. Horm Behav 56(1):66–72 (Epub 2009/03/25)
Scarpazza C, Tognin S, Frisciata S, Sartori G, Mechelli A (2015) False positive rates in Voxel-based Morphometry studies of the human brain: should we be worried? Neurosci Biobehav Rev 52:49–55. doi:10.1016/j.neubiorev.2015.02.008
Seidman L, Kroll R, Hsieh J (2014) Return to ovulatory capacity with three combined oral contraceptive regimens: a comparative trial. Obstet Gynecol 123(Suppl 1):110S–111S (Epub 2014/04/29)
Shen S, Sterr A (2013) Is DARTEL-based voxel-based morphometry affected by width of smoothing kernel and group size? A study using simulated atrophy. J Magn Reson Imaging 37(6):1468–1475 (Epub 2012/11/23)
Stoodley CJ, Schmahmann JD (2010) Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex 46(7):831–844 (Epub 2010/02/16)
Sulak PJ, Scow RD, Preece C, Riggs MW, Kuehl TJ (2000) Hormone withdrawal symptoms in oral contraceptive users. Obstet Gynecol 95(2):261–266 (Epub 2000/02/16)
Vilares I, Howard JD, Fernandes HL, Gottfried JA, Kording KP (2012) Differential representations of prior and likelihood uncertainty in the human brain. Current Biol 22(18):1641–1648 (Epub 2012/07/31)
Webb R, Ayers S (2014) Cognitive biases in processing infant emotion by women with depression, anxiety and post-traumatic stress disorder in pregnancy or after birth: a systematic review. Cognit Emot 2014:1–17 (Epub 2014/12/05)
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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
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De Bondt, T., Pullens, P., Van Hecke, W. et al. Reproducibility of hormone-driven regional grey matter volume changes in women using SPM8 and SPM12. Brain Struct Funct 221, 4631–4641 (2016). https://doi.org/10.1007/s00429-016-1193-1
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DOI: https://doi.org/10.1007/s00429-016-1193-1