Estradiol levels during the menstrual cycle differentially affect latencies to right and left hemispheres during dichotic listening: An ERP study

doi:10.1016/j.psyneuen.2009.06.018

Psychoneuroendocrinology

Volume 35, Issue 2, February 2010, Pages 249-261

https://doi.org/10.1016/j.psyneuen.2009.06.018 Get rights and content

Summary

Many behavioral studies have found high-estrogen phases of the menstrual cycle to be associated with enhanced left-hemisphere processing and low-estrogen phases to be associated with better right-hemisphere processing. This study examined the changing of hemispheric asymmetry during the menstrual cycle by analyzing event-related potential (ERP) data from midline and both hemispheres of 23 women during their performance of a dichotic tasks shown to elicit a left-hemisphere response (semantic categorization) and a right-hemisphere response (complex tones). Each woman was tested during her high-estrogen follicular phase and low-estrogen menstrual phase. Salivary assays of estradiol and progesterone were used to confirm cycle phase. Analyses of the ERP data revealed that latency for each hemisphere was differentially affected by phase and target side, such that latencies to the left hemisphere and from the right ear were shorter during the high-estrogen phase, and latencies to the right hemisphere and from the left ear were shorter during the low-estrogen phase. These findings supply electrophysiological correlates of the cyclically based interhemispheric differences evinced by behavioral studies.

Section snippets

Participants

Twenty-three females between the ages of 18 and 35 who experienced spontaneous, regularly recurring menstrual cycle and who did not use hormonal contraceptives were recruited for this study. They were native speakers of English, had no history of otological or neurological disease based on self-report, and were right-handed as assessed by a handedness questionnaire (Annett, 1970). Since musical training has been shown to improve performance (Musiek, 1994) and elicit a greater right-ear

Salivary samples

Salivary samples collected from each participant during both the follicular and the menstrual sessions were assayed for estradiol and progesterone by an independent laboratory. Data from only the participants whose estradiol was higher during the late preovulatory phase than during the menstrual phase were included in the ERP analysis. Thus, a one-way analysis of variance showed that estradiol was significantly higher during the late preovulatory phase (M = 11.87 pg/ml, SD = 8.23) than in the

Discussion

The present study found electrophysiological correlates to the strong trends seen in the behavioral literature (e.g., Altemus et al., 1989, Hampson, 1990a, Hampson, 1990b, Mead and Hampson, 1996, Sanders and Wenmoth, 1998, Alexander et al., 2002), which have indicated better performance on tasks attributed to left-hemisphere processing when estrogen is high and better performance on tasks attributed to right-hemisphere processing when estrogen is low in spontaneously cycling women. Evoked

Conclusions

The electrophysiological data from this study provide physiological correlates of the behavioral evidence for cyclically based interhemispheric differences. Whereas previous electrophysiological studies examining menstrual cycle effects have been able to detect latency differences but not hemispheric differences by using only midline electrodes, and imaging studies have been able to detect global changes but not latency or hemispheric changes, ERP data from both hemispheres revealed

Role of funding source

Funds for the salivary assays were provided by a grant from the Jesuit Fathers of Albuquerque, who had no further role in the study.

Conflict of interest

There are no conflicts of interest.

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The functional cerebral asymmetry (FCA) in processing targets within rapid serial visual presentation (RSVP) streams has been reported to fluctuate across the menstrual cycle, with identification of the second of two closely spaced targets being impaired when both targets occur in the left or the right hemifield stream during the luteal phase, while during the menstrual phase identification of the second target is only impaired for target pairs presented in the right hemifield stream. This fluctuation has been proposed to result from variations in estradiol levels. The current study used EEG to investigated whether the cycle-related fluctuation in RSVP target identification FCA relates to changes in early, stimulus-driven, bottom-up or in later, top down-driven aspects of FCA. While the former would be expected to become evident in the early visual evoked potentials (VEPs) P1 or N1, the latter would be evident in later event-related potentials (ERPs) such as N2pc or P3. Women performed a dual-stream RSVP task once during the menstrual phase and once during the follicular phase. Estradiol levels were determined from saliva samples. In contrast to previous findings, FCA in RSVP target identification was not affected by cycle phase. However, the impairment in second-target identification when targets where closely spaced was generally smaller during the menstrual phase than during the follicular phase. This effect was matched by shorter peak latencies of P1 VEPs for the menstrual phase, and by a reduction in the latency of the second-target P3 ERP for closely spaced relative to widely spaced target pairs, again for the menstrual phase. Results suggest that in a dual-stream RSVP setup, target identification, early stage stimulus processing, and target consolidation are affected by cycle phase, but that the asymmetry of these effects does not differ between menstrual and follicular phase. The observed cycle-related modulations in neurophysiology and behavior could relate to the effects of estradiol on the locus ceruleus norepinephrine (LC-NE) system, which is known to play a major role in arousal, attention and stress response.
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Natural fluctuations of sex hormones during the menstrual cycle have been shown to modulate language lateralisation. Using the dichotic listening (DL) paradigm, a well-established measurement of language lateralisation, several studies revealed that the left hemispheric language dominance was stronger when levels of estradiol were high. A recent study (Hjelmervik et al., 2012) showed, however, that high levels of follicular estradiol increased lateralisation only in a condition that required participants to cognitively control (top-down) the stimulus-driven (bottom-up) response. This finding suggested that sex hormones modulate lateralisation only if cognitive control demands are high. The present study investigated language lateralisation in 73 normally cycling women under three attention conditions that differed in cognitive control demands. Saliva estradiol and progesterone levels were determined by luminescence immunoassays. Women were allocated to a high or low estradiol group. The results showed a reduced language lateralisation when estradiol and progesterone levels were high. The effect was independent of the attention condition indicating that estradiol marginally affected cognitive control. The findings might suggest that high levels of estradiol especially reduce the stimulus-driven (bottom-up) aspect of lateralisation rather than top-down cognitive control.
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An exaggerated response to emotional stimuli is one of the several symptoms widely reported by veterans of the 1991 Persian Gulf War. Many have attributed these symptoms to post-war stress; others have attributed the symptoms to deployment-related exposures and associated damage to cholinergic, dopaminergic, and white matter systems. We collected event-related potential (ERP) data from 20 veterans meeting Haley criteria for Gulf War Syndromes 1–3 and from 8 matched Gulf War veteran controls, who were deployed but not symptomatic, while they performed an auditory three-condition oddball task with gunshot and lion roar sounds as the distractor stimuli. Reports of hyperarousal from the ill veterans were significantly greater than those from the control veterans; different ERP profiles emerged to account for their hyperarousability. Syndromes 2 and 3, who have previously shown brainstem abnormalities, show significantly stronger auditory P1 amplitudes, purported to indicate compromised cholinergic inhibitory gating in the reticular activating system. Syndromes 1 and 2, who have previously shown basal ganglia dysfunction, show significantly weaker P3a response to distractor stimuli, purported to indicate dysfunction of the dopaminergic contribution to their ability to inhibit distraction by irrelevant stimuli. All three syndrome groups showed an attenuated P3b to target stimuli, which could be secondary to both cholinergic and dopaminergic contributions or disruption of white matter integrity.
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Estradiol levels during the menstrual cycle differentially affect latencies to right and left hemispheres during dichotic listening: An ERP study

Summary

Section snippets

Participants

Salivary samples

Discussion

Conclusions

Role of funding source

Conflict of interest

Neuropsychologia

Neuropsychologia

Brain Res.

Psychiatry Res.

Brain Cogn.

Neuropsychologia

Physiol. Behav.

Brain Res. Rev.

NeuroImage

Hear. Res.

Electroencephalogr. Clin. Neurophysiol.

Neurosci. Lett.

Brain Cogn.

Psychoneuroendocrinology

NeuroImage

Neuropsychologia

Clin. Neurophysiol.

Neuropsychologia

Brain Lang.

Neuropsychologia

Hear. Res.

Neuropsychologia

Cogn. Brain Res.

Brain Lang.

Neuropsychologia

Neuropsychologia

Psychoneuroendocrinology

Neuropsychologia

Horm. Behav.

Electroencephalogr. Clin. Neurophysiol.

Cogn. Brain Res.

Clin. Neurophysiol.

Biol. Psychiat.

Brain Res. Rev.

Neuropsychologia

Prog. Brain Res.

Neurosci. Lett.

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Speech perception and brain laterality: the effect of ear advantage on auditory event-related potentials

Brain Lang.

Classification of hand preference by association analysis

Br. J. Psychol.