Performance in a test demanding prefrontal functions is favored by early luteal phase progesterone: An electroencephalographic study

Psychoneuroendocrinology

Volumn 29, Issue 8, 2004, Pages 1047-1057

  Solis Ortiz, S ^a   Guevara, M A ^b   Corsi Cabrera, M ^c  

^a UNIVERSITY OF GUANAJUATO   (Mexico)

^b UNIVERSITY OF GUADALAJARA   (Mexico)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

EEG activity; Estrogen; Frontal lobes; Menstrual cycle; Progesterone; Spectral power

Indexed keywords

PROGESTERONE;

ADULT; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; ELECTROENCEPHALOGRAPHY; EVALUATION; FEMALE; HUMAN; LUTEAL PHASE; MENSTRUAL CYCLE; NORMAL HUMAN; OVULATION; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROGESTERONE BLOOD LEVEL; RECORDING; TASK PERFORMANCE; WISCONSIN CARD SORTING TEST;

ADULT; ATTENTION; BODY TEMPERATURE; ELECTROENCEPHALOGRAPHY; FEMALE; HUMANS; LUTEAL PHASE; MENSTRUATION; NEUROPSYCHOLOGICAL TESTS; OVULATION; PATTERN RECOGNITION, VISUAL; PREFRONTAL CORTEX; PROBLEM SOLVING; PROGESTERONE; PSYCHOMOTOR PERFORMANCE; REFERENCE VALUES; THINKING;

EID: 3042682566     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2003.10.007     Document Type: Article

References (106)

1. Ansseau M., Doumont A., Cerfontaine J.L., Mantanus H., Rousseau J.C., Timist-Berthier M. Self-reports of anxiety level and EEG changes after a single dose of benzodiazepines. Neuropsychopharmacology. 12:1984;255-259
2. Baddley A.D. Working Memory. 1986;Clarendon Press, Oxford
3. 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. 7:1982;75-90
4. Berman K.F., Ostrem J.L., Randolph C., Gold J., Goldberg T.E., Coppola R., Carson R.E., Herscovitch P., Weinberger D.R. Physiological activation of a cortical network during performance of the Wisconsin Card Sorting Test: A positron emission tomography study. Neuropsychologia. 33:1995;1027-1046
5. Berman K.F., Schmidt P.J., Rubinow D.R., Danaceau M.A., Van Horn J.D., Esposito G., Ostrem J.L., Weinberger D.R. Modulation of cognition-specific cortical activity by gonadal steroids: A positron-emission tomography study in women. Proc. Natl. Acad. Sci. USA. 94:1997;8836-8841
6. Bimonte H.A., Denenberg V.H. Estradiol facilitates performance as working memory load increases. Psychoneuroendocrinology. 24:1999;161-173
7. A receptor. Brain Res. 561:1991;157-161
8. Blaustein J.D., Wade G.N. Progestin binding by brain and pituitary cell nuclei and female rat sexual behavior. Brain Res. 140:1978;360-367
9. Blurton-Jones M.M., Roberts J.A., Tuszynski M.H. Estrogen receptor inmunoreactivity in the adult primate brain: neuronal distribution and association with p75, trkA, and choline acetyltransferase. J. Comp. Neurol. 405:1999;529-542
10. Bonnar, J., 1983. Biological approaches to ovulation detection. In: Ovulation: Methods for its Prediction and Detection. John Wiley, New York, pp. 33-47
11. Brinton R.D., Chen S., Montoya M., Hsieh D., Minaya J., Kim J., Chu H.P. The women's health initiative estrogen replacement therapy is neurotrophic and neuroprotective. Neurobiol. Aging. 21:2000;475-496
12. Broverman D.N., Vogel W., Klaiber E.L., Majcher D., Shea D., Paul V. Changes in cognitive task performance across the menstrual cycle. J. Comp. Physiol. Psychol. 95:1981;646-654
13. Brugger P., Milicevic A., Regard M., Cook N.D. Radom-number generation and the premenstrual cycle: Preliminary evidence for a premenstrual alteration of frontal lobe functioning. Percept. Mot. Skills. 77:1993;915-921
14. Chesney M.A., Tasto D.L. The development of the menstrual cycle symptom questionnaire. Behav. Res. Ther. 13:1975;237-244
15. Coppola R., Herrmann W.M. Psychotropic drug profiles: comparison by topographic maps of absolute power. Neuropsychobiology. 18:1987;97-104
16. Cordoba Montoya D.M., Carrer H.F. Estrogen facilitates induction of long term potentiation in the hippocampus of awake rats. Brain Res. 778:1997;430-438
17. Corsi-Cabrera M., Arce C., Ramos J., Guevara M.A. Time course of reaction time and EEG while performing a vigilance task during total sleep deprivation. Sleep. 19:1996;563-569
18. Corsi-Cabrera M., Ugalde E., del Rio-Portilla Y., Fernandez-Guasti A. Organizational and activational effects of gonadal steroids hormones on the EEG of male and female rats. Dev. Psychobiol. 37:2000;194-207
19. Creutzfeldt O.D., Arnold P.M., Becker D., Langenstein S., Tirsch W., Wilhelm H., Wuttke W. EEG changes during spontaneous and controlled menstrual cycle and their correlation with psychological performance. Electroencephalogr. Clin. Neurophysiol. 40:1976;113-131
20. Damasio A.R., Anderson S.W. The Frontal Lobes. Heilman K.M., Valentin E. Clinical Neuropsycology. 1993;409-460 Oxford University Press, New York
21. Damasio A.R. Descartes' Error: Emotion, Reason and the Human Brain. 1994;Putnam Press, New York
22. Del Rio-Portilla Y., Ugalde E., Juarez J., Roldan A., Corsi-Cabrera M. Sex differences in EEG in adult gonadectomized rats before and after hormonal treatment. Psychoneuroendocrinoloy. 22:1997;627-642
23. Eichenbaum H., Otto T. The hippocampus - What does it do? Behav. Neural. Biol. 57:1992;2-36
24. Epting L.K., Overman W.H. Sex-sensitive task in men and women: a search for performance fluctuations across the menstrual cycle. Behav. Neurosci. 112:1998;1304-1317
25. Ferin J., Thomas K., Johansson E.D.B. Ovulation and Detection. Hafez E.S.E., Evans T.N. Human Reproduction Conception and Contraception. 1973;260-283 Harper & Row, New York
26. Fernandez-Guasti A., Picazo O. Sexual differentiation modifies the allopregnanolone anxiolytic actions in rats. Psychoneuroendocrionology. 24:1999;251-267
27. Fernandez-Guasti A., del Rio-Portilla Y., Ugalde E., Corsi-Cabrera M. Diazepam and progesterone produce sexually dimorphic actions on the rat EEG: role of the neonatal sexual differentiation process. Psychoneuroendocrinology. 28:2003;85-100
28. Fernández Th., Harmony Th., Silva-Pereyra J., Fernández- Bouzas A., Gersenowies J., Carbonell F., Marosi E., Otero G., Valdés S.I. Specific EEG frequencies at specific brain areas and performance. Cogn. Neurosci. Neurobiol. 11:2000;2663-2668
29. Frye C.A., Lacey E.H. Progestins influence performance on cognitive tasks independent of changes in affective behavior. Psychobiology. 28:2000;550-563
30. Frye C.A., Duncan J.E. Estradiol benzoate potentiates neuroactive steroids' effects on pain sensitivity. Pharmacol. Biochem. Behav. 53:1995;27-32
31. Friess E., Tagaya H., Trachsel L., Holsboer F., Rupprecht R. Progesterone-induced changes in sleep in male subjects. Am. J. Physiol. 272:1997;E885-E891
32. Fuster J.M. The Prefrontal Cortex. 1989;Raven Press, New York
33. Gerall A.A., Napoli A.M., Cooper V.C. Daily and hourly estrous running in intact spayed and estrone implanted rats. Physiol. Behav. 10:1973;225-229
34. Gibbs R.B. Impairment of basal forebrain cholinergic neurons associated with aging and long-term loss of ovarian function. Exp. Neurol. 151:1998;289-302
35. Goldman-Rakic P.S. Circuitry of primate prefrontal cortex and regulation of the behavior by representational memory. Mountcastle V.B., Plum F. Handbook of Physiology. The Nervous System. Vol. 5, Pt. 1:1987;373-417 American Physiological Society, Bethesda, MD
36. Grant D.A., Berg E.A. A behavioral analysis of degree of reinforcement and ease of shifting to new responses in a Weigl-type card sorting problem. J. Exp. Psychol. 38:1948;404-411
37. Green P.S., Simpkins J.W. Neuroprotective effects of estrogen: potential mechanisms of action. Int. J. Dev. Neurosci. 18:2000;347-358
38. Greenblatt D.J., Ehrenberg B.L., Gunderman J., Locniskar A., Scavone J.M., Harmatz J.S., Shader R.I. Pharmacokinetic and electroencephalographic study of intravenous diazepam, midazolam and placebo. Clin. Pharmac. Ther. 45:1989;356-365
39. Gundlah C., Kohama S.G., Mirkes S.J., Garyfallou V.T., Urbanski H.F., Bethea C.L. Distribution of estrogen receptor beta (ERbeta) mRNA in hypothalamus, midbrain and temporal lobe of spayed macaque: continued expression with hormone replacement. Brain Res. Mol. 76:2000;191-204
40. Gutiérrez S., Corsi-Cabrera M. EEG activity during preformance of cognitive tasks demanding verbal and/or spatial processing. J. Neurosci. Int. 42:1988;149-155
41. Hagihara K., Hirata S., Osada T., Hirai M., Kato J. Distribution of cells containing progesterone receptor mRNA in the female rat di- and telencephalon: an in situ hybridization study. Brain Res. Mol. 14:1992;239-249
42. Hampson E. Estrogen-related variations in human spatial and articulatory-motor skills. Psichoneuroendocrinology. 15:1990;97-111
43. Hampson E. Variation in sex-related cognitive abilities across the menstrual cycle. Brain Cogn. 14:1990;26-43
44. Hampson E., Kimura D. Reciprocal effects of hormonal fluctuations on human motor and perceptual-spatial skills. Neurosci. Behav. 102:1988;456-459
45. Harmony Th., Fernández Th., Silva J., Bosch J., Valdés P., Fernández-Bouzas A., Galán L., Aubert E., Rodríguez D. Do specific EEG frequencies indicate different processes during mental calculation? Neurosci. Lett. 266:1999;25-28
46. Harmony Th., Fernández Th., Fernández-Bouzas A., Silva-Pereyra J., Bosch J., Díaz-Comas L., Galán L. EEG changes during word and figure categorization. Clin. Neurophysiol. 112:2001;1486-1498
47. Hausmann M., Gunturkun O. Steroid fluctuations modify functional cerebral asymmetries: the hypothesis of progesterone-mediated interhemispheric decoupling. Neuropsychologia. 38:2000;1362-1374
48. Heaton R.K. Manual for the Wisconsin Card Sorting Test. 1981;Psychological Assessment Resources. Inc. P.O. Box 998, Odessa, Florida
49. Herrmann W.M., Schaerer E. Pharmaco-EEG: computer EEG analysis to describe the projection to drug effects on a functional cerebral level in humans. Lopes da Silva F.H., Storm van Leewen W., Remond A. Clinical Applications of Computer Analysis of EEG and Other Neurophysiological Signals. 1990;385-445 Elsevier, Amsterdam
50. John E.R., Ahn H., Prichep L., Trepetin M., Bromn D., Kaye H. Developmental equations for the EEG. Science. 210:1980;1255-1258
51. Kennan P.A., Stern R.A., Janowsky D.S., Pedersen C.A. Psychological aspects of the premenstrual syndrome. I: Cognition and Memory. Psychoneuroendocrinology. 17:1992;179-187
52. Komnenich P., Lane D.M., Dickey R.P., Stone S.N. Gonadal hormones and cognitive performance. Physiol. Psychol. 6:1978;115-120
53. A receptor modulators. Am. J. Physiol. 271:1996;E763-E772
54. Lancel M., Faulhaber J., Schiffelholz T., Romeo E., Di Michelle F., Holsboer F., Ruprecht R. Allopregnanolone affects sleep in a benzodiazepine-like fashion. J. Pharmacol. Exp. Ther. 282:1997;1213-1218
55. Landgren S.O. Pregnanolone, a progesterone metabolite, facilitates inhibition of synaptic transmission in the Schaffer collateral pathway of the guinea pig hippocampus in vitro. Epilepsy Res. 10:1991;156-165
56. Lezak M.D. Neuropsychological Assessment. third Ed. 1995;New York, Oxford
57. Little B.C., Zahn T.P. Changes in mood and autonomic functioning during the menstrual cycle. Psychophysiology. 11:1974;579-580
58. Little B.C., Matta R.J., Zahn T.P. Physiological and psychological effects of progesterone in man. J. Nerv. Ment. Dis. 159:1974;256-262
59. Lord T., Taylor K. Monthly fluctuations in task concentration in female students. Percept. Mot. Skills. 72:1991;435-439
60. Lovett M.C., Reder L.M., Lebiere C. Modeling working memory in a unified architecture. Miyake A., Shah P. Models of Working Memory. Mechanisms of Active Maintenance and Executive Control. 1999;135-182 Cambridge University Press
61. Majewska M.D., Harrison N.L., Schwartz R.D., Barker J.L., Paul S.M. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science. 232:1986;1004-1007
62. A receptor. Mechanisms of action and physiological significance. Progr. Neurobiol. 38:1992;379-395
63. McAuley L.D., Gee K.W. Influence of the estrus cycle on the discrimination of apparent neuroactive steroids subtypes on the gamma aminobutyric acid A receptor complex in the rat. J. Pharmacol. Exp. Ther. 175:1995;1412-1417
64. McEwen B.S., Davis P., Gerlach J., Krey L., MacLusky N., McGinnis M., Parsons B., Rainbow T. Progesterone and progestin. Bardin C., Mauvais-Jarvis P., Milgrom G. Progesterone and Progestin. 1983;59-76 Raven Press, New York
65. McEwen B.S., Alves S.E. Estrogen actions in the central nervous system. Endocr. Rev. 20:1999;279-307
66. McEwen B.S., Alves S.E., Bulloch K., Weiland N.G. Ovarian steroids and the brain: implications for cognition and aging. Neurology. 48:1997;S8-S15
67. McEwen B.S., Woolley C.S. Estradiol and progesterone regulate neuronal structure and synaptic connectivity in adult as well as developing brain. Exp. Gerontol. 29:1994;431-436
68. Milner B. Effects of different brain lesions on card sorting. Arch. Neurol. 9:1963;100-110
69. Mocks J., Gasser T. How to select epochs of the EEG for quantitative analysis. Electroencephalogr. Clin. Neurophysiol. 58:1984;89-92
70. Nauta W.J.H. The problem of the frontal lobe: A reinterpretation. J. Psychiat. Res. 8:1971;167-187
71. O'Neal M., Means L., Poole M., Hamm R. Estrogen affects performance of ovariectomized rats in a two-choise water-escape working memory task. Psychoneuroendocrinology. 21:1996;51-65
72. Osterlund M.K., Keller E., Hurd Y.L. The human forebrain has discrete estrogen receptor alpha messenger RNA expression: high levels in the amygdaloid complex. Neuroscience. 95:2000;333-342
73. Petrides M.P. Lateral frontal cortical contribution to memory. Seminars Neurosci. 8:1996;57-63
74. Petrides M. Monitoring of selections of visual stimuli and the primate frontal cortex. Proc. R. Soc. Lond. B. 246:1991;293-298
75. Picazo O., Fernandez-Guasti A. Anti-anxiety effects of progesterone and some of its reduced metabolites: an evaluation using the burying behavior test. Brain Res. 680:1995;135-141
76. Phillips S.M., Sherwin B.B. Variations in memory function and sex steroid hormones across the menstrual cycle. Psychoneuroendocrinology. 17:1992;497-506
77. Phillips K., Silverman I. Differences in the relationships of the menstrual cycle phase to spatial performance on two- and three-dimensional tasks. Horm. Behav. 32:1997;167-175
78. Postma A., Winkel J., Tuiten A., van Honk J. Sex differences and menstrual cycle effects in human spatial memory. Psychoneuroendocrinology. 24:1999;175-192
79. Ramos J., Corsi-Cabrera M., Guevara M.A., Arce C. EEG activity during cognitive performance in women. Int. J. Neurosci. 69:1993;185-195
80. Register T.C., Shively C.A., Lewis C.E. Expression of estrogen receptor alpha and beta transcripts in female monkey hippocampus and hypothalamus. Brain Res. 788:1998;320-322
81. Reitan R.M. Validity of the trailmaking test as an indication of organic brain damage. Percept. Mot. Skills. 8:1983;271-276
82. Rezai K., Andreasen N.C., Alliger R., Cohen G., Swayze V. II, O'Leary D.S. The neuropsychology of the prefrontal cortex. Arch. Neurol. 50:1993;636-642
83. Richardson J.T.E. The menstrual cycle, cognition and paramenstrual symptomatology. Richardson J.T.E. Cognition and the Menstrual Cycle. 1992;1-18 Springer-Verlag, New York
84. Romano-Torres M., Borja-Lascurain E., Chao-Rebolledo C., Del-Rio-Portilla Y., Corsi-Cabrera M. Effects of diazepam on EEG power and coherent activity: sex differences. Psychoneuroendocrinology. 27:2002;821-833
85. Ruprecht R. The neuropsychopharmacological potential of neuroactive steroids. J. Psychiatr. Res. 31:1997;297-314
86. Saucier D.M., Kimura D. Intrapersonal motor but not extrapersonal targeting skill is enhanced during the midluteal phase of the menstrual cycle. Dev. Neuropsychol. 14:1998;385-398
87. Scher D., Pionk M., Purcell D.G. Visual sensitivity fluctuations during the menstrual cycle under dark and light adaptation. Bull. Psychon. Soc. 18:1981;159-160
88. Shallice T., Burgess P. Supervisory control of action and thought selection. Baddeley A., Weiskrantz L. Attention: selection, awareness, and control. 1993;171-187 Clarendon Press, Oxford, UK
89. Shaywitz S.E., Shaywitz B.A., Pugh K.R., Fulbright R.K., Skudlarski P., Mencl W.E., Constable R.T., Naftolin F., Palter S.F., Marchione K.E., Katz L., Shankweiler D.P., Fletcher J.M., Lacadie C., Keltz M., Gore J.C. Effect of estrogen on brain activation patterns in postmenopausal women during working memory tasks. J. A. M. A. 281:1999;1197-1202
90. Silverman I., Phillips K. Effects of estrogen changes during the menstrual cycle on spatial performance. Ethol. Sociobiol. 14:1993;247-270
91. Solis-Ortiz S., Ramos J., Arce C., Guevara M.A., Corsi-Cabrera M. EEG oscillations during the menstrual cycle. Int. J. Neurosci. 76:1994;279-292
92. Solis-Ortiz S., Corsi-Cabrera M. EEG patterns anxiety across the menstrual cycle. Rev. Mex. Psicol. 19:2002;187-195
93. Solis-Ortiz, S., Corsi-Cabrera, M., 2002b. Effects of gonadal hormones on sustained vigilance and their relation with the EEG activity in women. Soc. Neurosci. Abstr. No. 277.3.
94. Sommer B. Cognitive performance and the menstrual cycle. Richardson J.T.E. Cognition and the Menstrual Cycle. 1992;39-56 Springer-Verlag, New York
95. Stroop J.R. Studies of interference in serial verbal reactions. J. Exp. Psychol. 18:1935;643-660
96. Stuss D.T., Benson D.F. The Frontal Lobes. 1986;Raven Press, New York
97. Tanapat P., Hastings N.B., Reeves A.J., Gould E. Estrogen stimulates a transient increase in the number of the new neurons in the dentate gyrus of the adult female rat. J. Neurosci. 19:1999;5792-5801
98. Ugalde E., Del Rio-Portilla Y., Juarez J., Roldan A., Guevara M.A., Corsi-Corsi M. Effects of diazepam and sex hormones on EEG of gonadectomised male and female rats. Psychoneuroendocrinology. 23:1998;701-712
99. Wise P.M., Smith M.J., Dubal D.B., Wilson M.E., Krajnak K.M., Rosewell K.L. Neuroendocrine influences and repercussions of the menopause. Endocr. Rev. 20:1999;243-248
100. Wechsler D. WAIS manual. 1955;The Psychological Corporations, New York
101. Wollnik F., Turek F.W. Estrous correlated modulations of circadian and ultradian wheel-running activity rhythms in LEW/ZM rats. Physiol. Behav. 43:1988;396-398
102. Woolley C.S. Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. Horm. Behav. 34:1998;140-148
103. Woolley C.S. Electrophysiological and cellular effects of estrogen on neuronal function. Clin. Rev. Neurobiol. 13:1999;1-20
104. Woolley C., McEwen B.S. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J. Comp. Neurol. 336:1993;293-306
105. Wu F.S., Gibbs T.T., Farb D.H. Inverse modulation of γ-aminobutiric acid and glicine-induced currents by progesterone. Mol. Pharmacol. 37:1990;597-602
106. Wuttke W., Arnold P., Becker D., Creutzfeldt O., Langenstein S., Tirsch W. Circulating hormones, EEG and performance in psychological tests of women with and without oral contraceptives. Psychoneuroendocrinology. 1:1975;141-151