Resting state alpha frequency is associated with menstrual cycle phase, estradiol and use of oral contraceptives

Christina P Brötzner, Wolfgang Klimesch, Michael Doppelmayr, Andrea Zauner, Hubert H Kerschbaum, Christina P Brötzner, Wolfgang Klimesch, Michael Doppelmayr, Andrea Zauner, Hubert H Kerschbaum

Abstract

Ongoing intrinsic brain activity in resting, but awake humans is dominated by alpha oscillations. In human, individual alpha frequency (IAF) is associated with cognitive performance. Noticeable, performance in cognitive and emotional tasks in women is associated with menstrual cycle phase and sex hormone levels, respectively. In the present study, we correlated frequency of alpha oscillation in resting women with menstrual cycle phase, sex hormone level, or use of oral contraceptives. Electroencephalogram (EEG) was recorded from 57 women (aged 24.07 ± 3.67 years) having a natural menstrual cycle as well as from 57 women (aged 22.37 ± 2.20 years) using oral contraceptives while they sat in an armchair with eyes closed. Alpha frequency was related to the menstrual cycle phase. Luteal women showed highest and late follicular women showed lowest IAF or center frequency. Furthermore, IAF as well as center frequency correlated negatively with endogenous estradiol level, but did not reveal an association with endogenous progesterone. Women using oral contraceptives showed an alpha frequency similar to women in the early follicular phase. We suggest that endogenous estradiol modulate resting alpha frequency.

Keywords: Center frequency; Estradiol; Individual alpha frequency; Oral contraceptive.

Copyright © 2014 The Authors. Published by Elsevier B.V. All rights reserved.

Figures

Fig. 1
Fig. 1
Average alpha center frequency (M±SD) in women with a natural menstrual cycle and women using oral contraceptives. Late follicular women show lowest center frequency. EFP: early follicular phase, LFP: late follicular phase, LP: luteal phase; pill intake phase: active phase, pill free week: inactive phase; *p<.05; **p<.01.
Fig. 2
Fig. 2
Average IAF (M±SD) in women with a natural menstrual cycle and women using oral contraceptives. Late follicular women reveal lowest IAF. EFP: early follicular phase, LFP: late follicular phase, LP: luteal phase; pill intake phase: active phase, pill free week: inactive phase; *p<.05; **p<.01.
Fig. 3
Fig. 3
Estradiol level correlates negatively with alpha frequency. (A) The regression line shows a negative correlation between estradiol and center frequency in luteal woman. (B) Alpha oscillation (filtered between 7 and 14 Hz) from late follicular women having either a low estradiol or high estradiol level.

References

    1. Abler B., Kumpfmüller D., Grön G., Walter M., Stingl J., Seeringer A. Neural correlates of erotic stimulation under different levels of female sexual hormones. PLoS One. 2013;8:e54447.
    1. Anokhin A., Vogel F. EEG alpha rhythm frequency and intelligence in normal adults. Intelligence. 1996;23:1–14.
    1. Attwell D., Laughlin S.B. An energy budget for signaling in the grey matter of the brain. J. Cereb. Blood Flow Metab. 2001;21:1133–1145.
    1. Becker D., Creutzfeldt O.D., Schwibbe M., Wuttke W. Changes in physiological, EEG and psychological parameters in women during the spontaneous menstrual cycle and following oral contraceptives. Psychoneuroendocrinology. 1982;7:75–90.
    1. Berger H. Über das Elektrenkephalogramm des Menschen (On the human electroencephalogram) Arch. Psychiatrie Nervenkrankh. 1929;87:527–570.
    1. Braitenberg V., Schüz A. Anatomy of the Cortex. Springer; Berlin: 1991.
    1. Buffenstein R., Poppitt S.D., McDevitt R.M., Prentice A.M. Food intake and the menstrual cycle: a retrospective analysis, with implications for appetite research. Physiol. Behav. 1995;58:1067–1077.
    1. Buzsáki G., Anastassiou C.A., Koch C. The origin of extracellular fields and currents--EEG, ECoG, LFP and spikes. Nat. Rev. Neurosci. 2012;13:407–420.
    1. Creutzfeldt O.D., Arnold P.-M., Becker D., Langenstein S., Tirsch W., Wilhelm H., Wuttke W. EEG changes during spontaneous and controlled menstrual cycles and their correlation with psychological performance. Electroencephalogr. Clin. Neurophysiol. 1976;40:113–131.
    1. De Bondt T., Jacquemyn Y., Van Hecke W., Sijbers J., Sunaert S., Parizel P.M. Regional gray matter volume differences and sex-hormone correlations as a function of menstrual cycle phase and hormonal contraceptives use. Brain Res. 2013;1530:22–31.
    1. Finocchi C., Ferrari M. Female reproductive steroids and neuronal excitability. Neurol. Sci. 2011;32:31–35.
    1. Grandy T.H., Werkle-Bergner M., Chicherio C., Lövdén M., Schmiedek F., Lindenberger U. Individual alpha peak frequency is related to latent factors of general cognitive abilities. NeuroImage. 2013;79:10–18.
    1. Gratton G., Coles M.G., Donchin E. A new method for off-line removal of ocular artifact. Electroencephalogr. Clin. Neurophysiol. 1983;55:468–484.
    1. Gupta S. Weight gain on the combined pill--is it real? Hum. Reprod. Update. 2000;6:427–431.
    1. Hampson E. Variations in sex-related cognitive abilities across the menstrual cycle. Brain Cogn. 1990;14:26–43.
    1. Hampson E., Kimura D. Sex differences and hormonal influences on cognitive function in humans. In: Becker J.B., Breedlove S.M., Crews D., editors. Behavioral Endocrinology. MIT Press/Bradford Books; Cambridge, MA: 1992. pp. 357–398.
    1. Hausmann M., Slabbekoorn D., Van Goozen S.H., Cohen-Kettenis P.T., Güntürkün O. Sex hormones affect spatial abilities during the menstrual cycle. Behav. Neurosci. 2000;114:1245–1250.
    1. Hudgens E.D., Ji L., Carpenter C.D., Petersen S.L. The gad2 promoter is a transcriptional target of estrogen receptor (ER)alpha and ER beta: a unifying hypothesis to explain diverse effects of estradiol. J. Neurosci. 2009;29:8790–8797.
    1. Jasper H.H. The ten-twenty electrode system of the International Federation. Electroencephalogr. Clin. Neurophysiol. 1958;10:371–375.
    1. Klimesch W. EEG-alpha rhythms and memory processes. Int. J. Psychophysiol. 1997;26:319–340.
    1. Klimesch W. EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res. Rev. 1999;29:169–195.
    1. Lindh I., Ellström A.A., Milsom I. The long-term influence of combined oral contraceptives on body weight. Hum. Reprod. 2011;26:1917–1924.
    1. Lyons P.M., Truswell A.S., Mira M., Vizzard J., Abraham S.F. Reduction of food intake in the ovulatory phase of the menstrual cycle. Am. J. Clin. Nutr. 1989;49:1164–1168.
    1. Maki P.M., Rich J.B., Rosenbaum R.S. Implicit memory varies across the menstrual cycle: estrogen effects in young women. Neuropsychologia. 2002;40:518–529.
    1. Marecková K., Perrin J.S., Nawaz Khan I., Lawrence C., Dickie E., McQuiggan D.A., Paus T. Hormonal contraceptives, menstrual cycle and brain response to faces. Soc. Cogn. Affect. Neurosci. 2014;9:191–200.
    1. McEwen B.S. Stress, sex, and neural adaptation to a changing environment: mechanisms of neuronal remodeling. Ann. N.Y. Acad. Sci. 2010;1204:38–59.
    1. McEwen B.S., Akama K.T., Spencer-Segal J.L., Milner T.A., Waters E.M. Estrogen effects on the brain: actions beyond the hypothalamus via novel mechanisms. Behav. Neurosci. 2012;126:4–16.
    1. Petersen N., Kilpatrick L.A., Goharzad A., Cahill L. Oral contraceptive pill use and menstrual cycle phase are associated with altered resting state functional connectivity. Neuroimage. 2014;90:24–32.
    1. Phillips S.M., Sherwin B.B. Variations in memory function and sex steroid hormones across the menstrual cycle. Psychoneuroendocrinology. 1992;17:497–506.
    1. Pletzer B., Kronbichler M., Aichhorn M., Bergmann J., Ladurner G., Kerschbaum H.H. Menstrual cycle and hormonal contraceptive use modulate human brain structure. Brain Res. 2010;1348:55–62.
    1. Pletzer B., Kronbichler M., Nuerk H.C., Kerschbaum H. Hormonal contraceptives masculinize brain activation patterns in the absence of behavioral changes in two numerical tasks. Brain Res. 2014;1543:128–142.
    1. Protopopescu X., Butler T., Pan H., Root J., Altemus M., Polanecsky M., McEwen B., Silbersweig D., Stern E. Hippocampal structural changes across the menstrual cycle. Hippocampus. 2008;18:985–988.
    1. Puri J., Bellinger L.L., Kramer P.R. Estrogen in cycling rats alters gene expression in the temporomandibular joint, trigeminal ganglia and trigeminal subnucleus caudalis/upper cervical cord junction. J. Cell. Physiol. 2011;226:3169–3180.
    1. Raichle M.E. Two views of brain function. Trends Cogn. Sci. 2010;14:180–190.
    1. Raichle M.E., MacLeod A.M., Snyder A.Z., Powers W.J., Gusnard D.A., Shulman G.L. A default mode of brain function. Proc. Natl. Acad. Sci. U. S. A. 2001;98:676–682.
    1. Rosenberg L., Park S. Verbal and spatial functions across the menstrual cycle in healthy young women. Psychoneuroendocrinology. 2002;27:835–841.

Source: PubMed

Sponsorit ja yhteistyökumppanit

Sairaudet

Huumeiden interventiot

3
Tilaa