Language Lateralization and Cognitive Control Across the Menstrual Cycle PDF

Psychoneuroendocrinology (2012) 37, 1866—1875 Available online at www.sciencedirect.com j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / p s y n e u e n Language lateralization and cog...

Psychoneuroendocrinology (2012) 37, 1866—1875 Available online at www.sciencedirect.com j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / p s y n e u e n Language lateralization and cognitive control across the menstrual cycle assessed with a dichotic-listening paradigm Helene Hjelmervik a,*, René Westerhausen a, Berge Osnes a, Cecilie Byholt Endresen a, Kenneth Hugdahl a,b, Markus Hausmann c, Karsten Specht a,d a Department of Biological and Medical Psychology, University of Bergen, Bergen, Norway b Division for Psychiatry, Haukeland University Hospital, Bergen, Norway c Department of Psychology, Durham University, Durham, United Kingdom d Radiological Department, Haukeland University Hospital, Bergen, Norway Received 22 December 2011; received in revised form 27 February 2012; accepted 26 March 2012 KEYWORDS Summary Lateralization has been shown to vary across the menstrual cycle, however, the Dichotic listening; underlying mechanisms are not fully understood, and results are inconsistent. Additionally, it has Language; been suggested that estradiol enhances cognitive control. By modulating attention in a conso- Lateralization; nant-vowel dichotic listening test, the current study aims to investigate the effects of cycle- Cognitive control; related changes on language lateralization (non-forced condition), as well as the effects of Menstrual cycle; estradiol-modulated cognitive control (forced left condition) on the ear advantage. Fifteen Follicular phase; women and fifteen men tested three times on the dichotic listening test, women once in Estradiol; menstrual, follicular, and luteal phase (verified by hormone assays). Whereas the results from Gonadal hormones the non-forced and forced-right condition remained stable, results from the forced left condition changed across the cycle, where women in the follicular phase compared to both menstrual and luteal phases showed a stronger left ear advantage, i.e. better cognitive control performance. The increase in performance from menstrual to follicular phase correlated negatively with increase in estradiol levels, indicating a shift from a stimulus-driven right ear advantage (indicating a left hemispheric asymmetry for language) when estradiol levels were low toward a cognitively controlled left ear advantage when estradiol levels were high. This finding strongly suggests an active role of estradiol on cognitive control. The study further suggests that the degree of cognitive control demands of a given task is important to consider when investigating lateralization across the menstrual cycle. # 2012 Elsevier Ltd. All rights reserved. * Corresponding author at: Department of Biological and Medical Psychology, University of Bergen, Jonas Lies Vei 91, 5009 Bergen, Norway. Tel.: +47 55 586221; fax: +47 55 589872. E-mail address: [email protected] (H. Hjelmervik). 0306-4530/$ — see front matter # 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.psyneuen.2012.03.021 Language lateralization and cognitive control across the menstrual cycle 1867 1. Introduction hemispheric lateralization was reduced in the luteal phase compared to menstrual phase (Sanders and Wenmoth, 1998). Fluctuating levels of gonadal steroid hormones across the Also, dichotic listening and visual half field tasks often differ menstrual cycle have been suggested to induce a modulating in another important aspect: While the above referred dicho- effect on neuronal activity. Behavioral studies in normally tic listening studies measure a perceptual preference, visual cycling women addressing the effect of gonadal steroid half field studies typically measure differences in perfor- hormones on brain functions fall in either of two categories: mance by accuracy and response times. Additional explana- Studies examining the hormonal effect on cognitive function- tions for the inconsistency can be found in methodological ing per se, or on the underlying functional cerebral organiza- differences across studies. First, studies differ in the selec- tion of these cognitive functions, e.g. lateralization. Positive tion of cycle phases as well as the methods to estimate cycle effects of gonadal steroid hormones on cognition were mainly phases (e.g. day count, hormone essays, etc.). Second, found in research that focused on postmenopausal women studies that did use hormone assays have taken different and hormone therapy which involves estrogen either alone or diagnostic fluids (i.e., blood or saliva) which can largely in combination with gestagen. Although contradictions exist, affect the levels of biologically active steroid hormones, some of these studies report a performance enhancing effect and thus the correlation between hormone levels and degree of hormone therapy on tasks assessing verbal memory (Wolf in lateralization. and Kirschbaum, 2002), working memory (Keenan et al., Dichotic listening is a classical paradigm for investigating 2001), cognitive inhibition (Marinho et al., 2008; Wolf and language lateralization in the auditory domain (Bryden, Kirschbaum, 2002) and other executive functions (Keenan 1988; Kimura, 1961a,b). The Bergen version of the dichotic et al., 2001). Further, an influence of estrogen on working listening paradigm (Hugdahl, 1995; Hugdahl and Andersson, memory in normally cycling women has been shown to be 1986) entails the presentation of two meaningless consonant- especially strong when high level of cognitive control is vowel syllables (e.g., /ba/, /pa/) which are administered required (Jacobs and D’Esposito, 2011). In line with this, simultaneously, one to the left and one to the right ear. The Keenan et al. (2001) suggested that the observed effect of stimuli are presented with three different instructions: the estrogen on cognition is caused by its influence in particular non-forced (NF) condition where the participant is instructed on the prefrontal cortex (PFC) and that this can account for to report the sound heard most clearly, and the forced right the menstrual cycle effects in various types of tasks. (FR) and forced left (FL) conditions, where the participant is One basic organization principal of the human cortex is asked to selectively attend to and report from the respective the hemispheric asymmetry or lateralization of cognitive ears. A right-ear advantage is usually obtained in the NF functions, hereby defined as the differential involvement condition, reflecting a left hemispheric dominance for of the left and right hemisphere when performing a certain speech perception (Kimura, 1967; Pollmann et al., 2002), cognitive task. A widely accepted example of lateralization is since the majority of neuronal fibers from the right ear are the processing of language in the left hemisphere. Gonadal terminating in the left temporal lobe. Further, the FR con- steroid hormones have been suggested to influence this dition typically demonstrates an enhanced right-ear advan- lateralization with respect to both its overall organization, tage while the FL demonstrates — in healthy and young adult primarily studied with testosterone (Geschwind and Gala- participants — a reduction of the right-ear advantage or even burda, 1985), and its activation effect, especially by ovarian a reverse to a left-ear advantage (Hugdahl et al., 2009). hormones. It has been suggested that in particular estradiol Studies that have used the dichotic listening paradigm and and progesterone are influencing the degree of lateraliza- found less pronounced lateralization in the menstrual phase tion, with a reduced lateralization in cycle phases with high compared to the luteal phase, have applied only the NF levels of estradiol and/or progesterone, i.e. the follicular condition (Cowell et al., 2011; Sanders and Wenmoth, and luteal phase, as compared to the menstrual phase where 1998), or have averaged the respective right ear scores level of both estradiol and progesterone is low (Hausmann, and left ear scores from all three conditions (Wadnerkar 2005; Hausmann et al., 2002; Hausmann and Güntürkün, et al., 2008). However, the recent years of dichotic listening 2000; Sanders and Wenmoth, 1998). However, the results research suggest that the three conditions are qualitatively across studies are inconsistent, and some in fact report different from each other, reflecting different cognitive reversed results, with less pronounced lateralization in the processes. Whereas the NF condition targets pure language menstrual phase (Cowell et al., 2011; Hampson, 1990a,b; lateralization, the FR condition is thought to require selec- Sanders and Wenmoth, 1998; Wadnerkar et al., 2008), or tive attention and the FL condition, additionally, cognitive even that no cycle effect was revealed (Compton et al., control processes (Hugdahl, 2003; Hugdahl et al., 2009; 2004). However, most of the studies reporting a reduced Løberg et al., 1999; Oie and Hugdahl, 2008). In these studies, lateralization in the menstrual phase are studies on conso- cognitive control is defined as the ability to override a nant-vowel dichotic listening (Cowell et al., 2011; Sanders stimulus-driven response in the favor of an instruction-driven and Wenmoth, 1998; Wadnerkar et al., 2008), while the one (i.e., top—down process), while selective attention is majority of studies reporting reduced lateralization in high defined as directing attention toward a preferred stimulus hormonal phases have used visual half field tasks (Hausmann, (i.e., bottom—up process). In the FR condition, the partici- 2005; Hausmann and Güntürkün, 2000). Likewise, one study pant is instructed to report syllables from the ear which also suggested the task modality to interact with lateralization without attention instruction is preferably reported in the NF across the cycle. Thus, left hemispheric language lateraliza- condition, thus being supported by the bottom—up effect. In tion, investigated using dichotic listening with speech sounds contrast, in the FL condition the participant is asked to report (e.g. /pee/, /bee/), was reduced in the menstrual compared the task specific non-dominant stimulus and inhibit the to luteal phase, while for music dichotic listening, right dominant one. This requires executive or cognitive control 1868 H. Hjelmervik et al. as the top—down modulation has to overcome the otherwise men (mean 23.13  2.42 years, age range 20—28) completed dominating stimulus driven bottom—up effect (Hugdahl three testing sessions on a dichotic listening paradigm. All et al., 2009). participants were native Norwegian speakers, and right The present study aims to investigate whether fluctua- handed, with an laterality quotient of 93.33 (10.7) in tions in gonadal steroid hormones across the menstrual cycle women and 93.78 (10.23) in men, according to the Edin- affect language lateralization as indicated by the right ear burgh Handedness Inventory (Oldfield, 1971). In addition, an advantage in the NF condition. Additionally, by using two inter-aural hearing difference of 0.5). The multiple regression ana- levels between the follicular and menstrual phase. The lysis did not reveal any significant relationships between an interaction between these two predictors was included as increase in estradiol and/or progesterone from follicular to a third regressor. The second analysis followed the same luteal phase and the corresponding changes in laterality setup except the dependent and independent variables were index in FL condition (all jbj < 0.37, jtj < 1.44, p > 0.18). calculated from the difference between the luteal and folli- cular phase (see Fig. 2). All statistical analyses were per- 4. Discussion formed in Statistica 8 software (Statsoft, Tulsa, OK, USA). The aim of the present study was to investigate language 3. Results lateralization per se, as well as the effects of attention modulation, i.e. selective attention and cognitive control, 3.1. Dichotic listening on the typical right ear advantage in consonant vowel dicho- tic listening across the menstrual cycle. First, the results The repeated measures ANOVA for the dichotic listening task revealed no sex and cycle related change in the right ear revealed a significant Phase  Condition  Sex interaction advantage of the NF condition (see Fig. 1). Thus, these results (F(4,112) = 2.53; p = 0.04, h2 = 0.08) (see Table 4 for addi- are in contrast with previous studies which report menstrual tional main effects and interactions). The interaction was cycle-related changes in the right ear advantage in verbal followed up by three repeated measures ANOVA, i.e. one for dichotic listening (Cowell et al., 2011; Hampson, 1990a,b; each of the three conditions NF, FR, and FL. Neither the Sanders and Wenmoth, 1998; Wadnerkar et al., 2008). ANOVA for NF (F(2,56) = 1.04; p = 0.36, h2 = 0.04, see Fig. 1) Further, the power analysis showed that a medium to large nor FR condition (F(2,56) = 0.19; p = 0.83, h2 = 0.01, see effect in the population could be excluded, indicating that Fig. 1) showed a significant interaction. To determine the the hormonal effects on language lateralization as measured size of effect in the population which is reliably detectable by dichotic listening are rather small. Second, no significant given the present sample, we calculated a sensitivity (power) sex difference or cycle-related change in the right ear analysis (cf. Cohen, 1988) which indicated that for the NF and advantage was found in the FR condition (see Fig. 1). How- the FR conditions effects of 5% explained variance (or larger) ever, for the FL condition a significant left ear advantage was can be excluded with a power of 0.80, which rules out observed in the follicular phase, as compared to the men- medium to large effects in the population. In contrast to strual and luteal phase (see Fig. 1) suggesting that especially the NF and FR ANOVAs, the FL yielded a significant Sex - estradiol is related to the effect. This idea is supported by the  Phase interaction (F(2,56) = 3.95; p = 0.03, h2 = 0.12, see multiple regression analysis (see Fig. 2). Specifically, the Fig. 1). The FL ANOVA was followed up by a Fishers LSD post regression revealed that low estradiol levels result in a hoc analysis, which revealed significant differences between typical right ear advantage, suggesting a stimulus driven left the follicular and menstrual phase ( p < 0.001, d = 0.77) and hemispheric advantage for processing consonant vowel syl- between the follicular and luteal phase ( p < 0.05, d = 0.64), lables. However, a relative increase in estradiol from men- but not between the menstrual phase and the luteal phase strual to follicular phase results in a shift toward a left ear ( p = 0.45, d = 0.24). No significant differences were found advantage suggesting that estradiol enhanced cognitive con- between phase equivalents for men (all p > 0.28, d < 0.24) trol and thereby affected the dichotic listening ear advan- or between men and women in either of the phases (cycle tage significantly. Overall, the results suggest that it is not phases for women and phase equivalents for men) (all necessarily language lateralization per se that is hormonally p > 0.12, d < 0.59). affected, but the modulation of ear advantage by cognitive The multiple regression analysis for addressing the rela- control. tion between increase in hormones from menstrual to folli- In contradiction to the NF condition, the forced attention cular phase and the change in FL laterality index from conditions induce an attention modulation of the ear advan- menstrual to follicular phase was significant (b = 0.69, tage. One would assume that the attention resources SE = 0.22, t = 3.09, p = 0.01, see Fig. 2), indicating a nega- required in the FR and FL conditions, i.e. to focus on the tive relationship between estradiol and the laterality index in right and left ear, would be the same, and throughout Table 4 Statistical analysis. Analysis F p h2 Main effect of sex F(1,28) = 0.04 0.85 0.01 Main effect of phase F(2,56) = 0.3 0.74 0.01 Main effect of condition F(2,56) = 41.05 0.001 0.59 Interaction sex and phase F(2,56) = 1.47 0.24 0.05 Interaction sex and condition F(2,56) = 0.63 0.54 0.02 Interaction phase and condition F(4,112) = 0.76 0.55 0.02 Interaction sex, phase, and condition F(4,112) = 2.53 0.04 0.08 Note: Table shows main and interaction effects of the analysis of variance (ANOVA) listing F-values, p-values, and effect sizes (h2). Language lateralization and cognitive control across the menstrual cycle 1871 Figure 1 Results from the follow-up analyses of variance (ANOVA) conducted for each condition (NF, FR, FL) with the variables sex and phase. The figures show laterality indexes for men and women across phases (cycle phase for women and phase equivalents for men). Solid lines represent women, and dotted lines represent men. Error bars indicate standard error. Laterality index on the y-axis represent degree of ear advantage where positive values means a bias toward right ear, and negative values a bias toward left ear. Note that the values on the y-axis are different for the three conditions. x indicate significant interaction, and * significant at p < 0.05. 1872 H. Hjelmervik et al. Figure 2 Scatterplot of relative difference between menstrual phase and follicular phase in laterality index and estradiol levels. A negative correlation was found, i.e. the higher increase in estradiol level from menstrual to follicular phase the more negative laterality index increase. Positive values on the y-axis indicate an increase in lateralization toward the right ear, and negative values an increase in lateralization toward the left ear. The x-axis indicates the change in estradiol levels from the menstrual to the follicular phase. dichotic listening history this has been the dominant point of influenced by gonadal steroid hormones, but rather that view (see e.g. Bryden et al., 1983; Foundas et al., 2006). cognitive control, or specific PFC regions are more sensitive Resent basic and clinical research suggests (for review see to hormonal effects. Furthermore, the influence of estradiol Hugdahl et al., 2009; Westerhausen and Hugdahl, 2010), on cognitive control can be viewed in relation to the presence however, that FR and FL condition differ in the underlying of estrogen receptors within the PFC (Montague et al., 2008; cognitive processes: whereas the FR condition reflects selec- Wang et al., 2010) and the idea of PFC as a key target of tive attention (reporting from ‘‘dominant ear’’), the FL estrogen (Joffe et al., 2006; Keenan et al., 2001). Two condition additionally requires cognitive control (reporting previous studies have suggested that estradiol affects the from ‘‘non-dominant ear’’) (Hugdahl et al., 2009). Evidence PFC functioning through an increase of spine density in the supporting this argument comes from clinical studies where dorsolateral prefrontal cortex (Hao et al., 2007, 2006), and various clinical groups have difficulties in performing accord- indicating an enhancing effect of estradiol on the PFC. ing to the FL, but not the FR instruction (Gootjes et al., 2006; Another option, however, as underlying mechanism for the Hugdahl et al., 2003; Løberg et al., 1999; Oie and Hugdahl, observed change in the FL condition is a local lateralization 2008). Also, a neuroimaging study indicates that the FL change in the PFC (Hwang et al., 2008, 2009). Stephan et al. condition activates additional areas in the anterior cingulate (2003) have suggested that cognitive control processes are cortex, an area associated with cognitive control, when lateralized and thus are hemispheric specific functions. contrasted with the FR condition, while the reverse contrast Accordingly, van Wageningen et al. (2010) explored the does not reveal an activation pattern (Thomsen et al., 2004). glutamatergic transmission under a dichotic listening task, Following the same interpretation the observed effect of using a pharmacological manipulated level of glutamate, and menstrual cycle on the FL condition in the present study detected a direct relationship between the level of gluta- might be taken to indicate that sex hormones rather affect mate and brain activity during the FL condition in the left PFC cognitive control modulation of the ear advantage than only. This is further supported through a recent fMRI study language lateralization per se. The interpretation would also that found estradiol to interfere with working memory per- explain why the NF and FR conditions do not show a similar formance via left lateral PFC and left inferior parietal lobule reduction in right ear advantage. (Joseph et al., 2012). The authors are suggesting a compen- The interpretation that cognitive control abilities vary sating right hemispheric recruitment for working memory in across the menstrual cycle is in accordance with a range of the follicular phase as compared to the menstrual phase. In hormone therapy studies indicating an enhancing effect of light of the above mentioned studies, a change in recruit- estrogen on a range of executive functions tasks (Keenan ment of left versus right PFC could possibly affect the et al., 2001; Wolf and Kirschbaum, 2002), and more speci- laterality index in the FL condition. However, such a later- fically on tasks involving cognitive control (Marinho et al., alization effect in the PFC appears to be independent of 2008; Wolf and Kirschbaum, 2002). Also the relationship language lateralization, since no cycle effects were observed between increased cognitive control and increased estradiol on the results in the NF condition. Without further evidence levels from menstrual to follicular phase (see Fig. 2) fits this any such interpretation is a matter of speculation. line of interpretation. The finding that selective attention In order to further explore the cycle effect on the FL ear (FR) (see Fig. 1) does not vary through the three cycle phases advantage, we also conducted supplementary analysis to exam- indicates that not all cognitively demanding tasks would be ine the effect of the hormone levels. As already mentioned, the Language lateralization and cognitive control across the menstrual cycle 1873 increase in left ear advantage from menstrual to follicular Heister et al., 1989) and luteal phase (Chiarello et al., 1989; phase was associated with an increase in estradiol levels from Weekes and Zaidel, 1996). Similarly in the visual domain menstrual phase to follicular phase (see Fig. 2). However, figural comparison task (involves updating) has repeatedly although both the follicular phase and the luteal phase are shown reduced left visual field/right hemisphere advantage accompanied by a peak in estradiol, only the follicular phase in the luteal phase compared to the menstrual phase (Haus- positively affected the FL performance. The findings of mann and Güntürkün, 2000; Rode et al., 1995; Weis et al., increased cognitive control in only one of the high-estradiol 2011); In contrast, a line orientation task, which probably phases, lets one speculate about an inverse inhibiting role of requires less cognitive control, failed to show the same cycle progesterone (Smith and Woolley, 2004) or a relationship effect (Chiarello et al., 1989). In sum, the vast majority of between estradiol and performance where moderate levels lateralization studies suggest that tasks involving more cog- enhance while high levels diminish performance on the given nitive control are perhaps more sensitive for menstrual cycle- PFC dependent tasks (Jacobs and D’Esposito, 2011; Wide et al., related effects. 2004). The latter suggestion would be likely since the estradiol In conclusion, in line with previous research, the current level is higher in the luteal phase compared to the follicular study also found variations in lateralization across the men- phase (although not significant) for the current sample. How- strual cycle. However, the present study did not reveal a ever, the multiple regression analysis targeting this showed that general effect of gonadal steroids on language lateralization, neither the increase of progesterone, estradiol, or an interac- but rather a hormone-related change in cognitive control tion of the two, could explain the observed increase in right-ear modulation of the ear advantage (FL condition) where advantage from the follicular phase to the luteal phase. women perform better when tested in the follicular phase Previous studies debate whether women are more later- compared to the menstrual and luteal phase. Further, in the alized during menstruation (Hausmann, 2005; Hausmann and FL condition, the increase in estradiol levels correlate with Güntürkün, 2000), or in the high hormonal follicular or luteal increasing cognitive control abilities from menstrual to folli- phase (Cowell et al., 2011; Hampson, 1990a,b; Wadnerkar cular phase. The study points toward cognitive control as a et al., 2008), and some studies fail to detect a cycle effect at possible confounder in laterality studies, and thereby under- all (Chiarello et al., 1989; Heister et al., 1989). The current lines the importance of controlling for cognitive control when study could not confirm a change in language lateralization investigating lateralization across the menstrual cycle. per se across the cycle, however, the results point toward cognitive control as a possible confounder when investigating Role of funding source lateralization, and one can ask if varying amount of cognitive control across previous laterality studies can explain some of The study was supported by grants from the Bergen research the inconsistencies in the literature. Especially across visual foundation (Bergens forskningsstiftelse; http://www.bfstif- half-field studies a range of different tasks are used, which telse.no/) and by grants STU 263/3—3 and HA 3285/4—1 of most likely vary in the degrees of required cognitive control. the Deutsche Forschungsgemeinschaft to MH. These are inde- Visual half-field studies also often report reduced or reversed pendent research funding sources with no personal interests. visual half-field advantage in menstrual cycle phases high in gonadal steroid hormones (Hausmann and Güntürkün, 2000; Rode et al., 1995; Weis et al., 2008), similar to the finding in Conflict of interest the cognitive control (FL) condition of the present study. When reviewing the literature on menstrual cycle-related There is no conflict of interest for any of the authors involved effects in visual half-field studies, there seems to be a in this research process and manuscript production. pattern in which tasks that partly involve updating of working memory are more likely to show menstrual cycle-related Acknowledgments effects on lateralization than those that involve working memory to a much smaller extent (Chiarello et al., 1989; The authors would like to thank all participants for their Compton and Levine, 1997; Hausmann and Güntürkün, 2000; cooperation, and also the radiographers at Haukeland Uni- Heister et al., 1989; Rode et al., 1995; Weekes and Zaidel, versitetssykehus who assisted the data collection. The study 1996; Weis et al., 2011, 2008). Following Miyake et al. (2000), was supported by grants from the Bergen research foundation updating represents one of three central cognitive control (Bergens forskningsstiftelse; http://www.bfstiftelse.no/) functions (shifting and inhibition being the other two). For and by grants STU 263/3—3 and HA 3285/4—1 of the Deutsche example, two frequently used visual half-field tasks in the Forschungsgemeinschaft to MH. verbal domain are the word matching task and lexical deci- sion task. While the former involves reporting whether two subsequently presented words are the same (i.e. one-back References task relying on updating), the latter involves the discrimina- tion of words and non-words. In word matching tasks, Bryden, M.P., 1988. An overview of the dichotic listening procedure and reduced right visual field advantage has been demonstrated its relation to cerebral organization. In: Hugdahl, K. (Ed.), Hand- book of Dichotic Listening: Theory, Methods, and Research. Wiley & in cycle phases high in gonadal steroids (Hausmann and Sons, Chichester, UK, pp. 1—44. Güntürkün, 2000; Weis et al., 2008), with the exception of Bryden, M.P., Munhall, K., Allard, F., 1983. Attentional biases and the the negative finding of Rode et al. (1995). In contrast, studies right-ear effect in dichotic listening. Brain Lang. 18, 236—248. using lexical decision tasks did not find cycle-related effects Chiarello, C., McMahon, M.A., Schaefer, K., 1989. Visual cerebral on the right visual field/left hemisphere advantage in the lateralization over phases of the menstrual cycle: a preliminary follicular (Chiarello et al., 1989; Compton and Levine, 1997; investigation. Brain Cogn. 11, 18—36. 1874 H. Hjelmervik et al. Cohen, J., 1988. Statistical Power Analysis for the Behavioral Hugdahl, K., Westerhausen, R., Alho, K., Medvedev, S., Laine, M., Sciences, second edn. Lawrence Erlbaum Associates, Hillsdale, HämäIäinen, H., 2009. Attention and cognitive control: unfolding NJ. the dichotic listening story. Scand. J. Psychol. 50, 11—22. Compton, R.J., Levine, S.C., 1997. Menstrual cycle phase and mood Hwang, R.-J., Chen, L.-F., Yeh, T.-C., Tu, P.-C., Tu, C.-H., Hsieh, J.- effects on perceptual asymmetry. Brain Cogn. 35, 168—183. C., 2008. The resting frontal alpha asymmetry across the men- Compton, R.J., Costello, C., Diepold, J., 2004. Interhemispheric strual cycle: a magnetoencephalographic study. Horm. Behav. 54, integration during the menstrual cycle: failure to confirm pro- 28—33. gesterone-mediated interhemispheric decoupling. Neuropsycho- Hwang, R.-J., Wu, C.-H., Chen, L.-F., Yeh, T.-C., Hsieh, J.-C., 2009. logia 42, 1496—1503. Female menstrual phases modulate human prefrontal asymme- Cowell, P.E., Ledger, W.L., Wadnerkar, M.B., Skilling, F.M., White- try: a magnetoencephalographic study. Horm. Behav. 55, 203— side, S.P., 2011. Hormones and dichotic listening: evidence from 209. the study of menstrual cycle effects. Brain Cogn. 76, 256—262. Jacobs, E., D’Esposito, M., 2011. Estrogen shapes dopamine-depen- Foundas, A.L., Corey, D.M., Hurley, M.M., Heilman, K.M., 2006. dent cognitive processes: implications for women’s health. J. Verbal dichotic listening in right and left-handed adults: laterality Neurosci. 31, 5286—5293. effects of directed attention. Cortex 42, 79—86. Joffe, H., Hall, J.E., Gruber, S., Sarmiento, I.A., Cohen, L.S., Geschwind, N., Galaburda, A.M., 1985. Cerebral lateralization bio- Yurgelun-Todd, D., Martin, K.A., 2006. Estrogen therapy selec- logical mechanisms, associations, and pathology. III. A hypothesis tively enhances prefrontal cognitive processes: a randomized, and a program for research. Arch. Neurol. 42, 634—654. double-blind, placebo-controlled study with functional magnetic Gootjes, L., Bouma, A., Van Strien, J.W., Van Schijndel, R., Barkhof, resonance imaging in perimenopausal and recently postmeno- F., Scheltens, P., 2006. Corpus callosum size correlates with pausal women. Menopause 13, 411—422. asymmetric performance on a dichotic listening task in healthy Joseph, J.E., Swearingen, J.E., Corbly, C.R., Curry Jr., T.E., Kelly, aging but not in Alzheimer’s disease. Neuropsychologia 44, 208— T.H., 2012. Influence of estradiol on functional brain organization 217. for working memory. Neuroimage 59, 2923—2931. Hampson, E., 1990a. Estrogen-related variations in human spatial Keenan, P.A., Ezzat, W.H., Ginsburg, K., Moore, G.J., 2001. Prefron- and articulatory-motor skills. Psychoneuroendocrinology 15, 97— tal cortex as the site of estrogen’s effect on cognition. Psycho- 111. neuroendocrinology 26, 577—590. Hampson, E., 1990b. Variations in sex-related cognitive abilities Kimura, D., 1961a. Cerebral dominance and the perception of verbal across the menstrual cycle. Brain Cogn. 14 (1), 26—43. stimuli. Can. J. Psychol. 15, 166—171. Hao, J., Rapp, P.R., Leffler, A.E., Leffler, S.R., Janssen, W.G.M., Lou, Kimura, D., 1961b. Some effects of temporal-lobe damage on audi- W., McKay, H., Roberts, J.A., Wearne, S.L., Hof, P.R., Morrison, tory perception. Can. J. Psychol. 15, 156—165. J.H., 2006. Estrogen alters spine number and morphology in Kimura, D., 1967. Functional asymmetry of the brain in dichotic prefrontal cortex of aged female rhesus monkeys. J. Neurosci. listening. Cortex 3, 163—168. 26, 2571—2578. Løberg, E.-M., Hugdahl, K., Green, M.F., 1999. Hemispheric asym- Hao, J., Rapp, P.R., Janssen, W.G., Lou, W., Lasley, B.L., Hof, P.R., metry in schizophrenia: a ‘‘dual deficits’’ model. Biol. Psychiatry Morrison, J.H., 2007. Interactive effects of age and estrogen on 45, 76—81. cognition and pyramidal neurons in monkey prefrontal cortex. Marinho, R.M., Soares Jr., J.M., Santiago, R.C., Maganhin, C.C., Proc. Natl. Acad. Sci. U.S.A. 104, 11465—11470. Machado, F., de Miranda Cota, A.M., Baracat, E.C., 2008. Effects Hausmann, M., 2005. Hemispheric asymmetry in spatial attention of estradiol on the cognitive function of postmenopausal women. across the menstrual cycle. Neuropsychologia 43, 1559—1567. Maturitas 60, 230—234. Hausmann, M., Güntürkün, O., 2000. Steroid fluctuations modify Miyake, A., Friedman, N.P., Emerson, M.J., Witzki, A.H., Howerter, functional cerebral asymmetries: the hypothesis of progester- A., Wager, T.D., 2000. The unity and diversity of executive one-mediated interhemispheric decoupling. Neuropsychologia functions and their contributions to complex ‘‘Frontal Lobe’’ 38, 1362—1374. tasks: a latent variable analysis. Cogn. Psychol. 41, 49—100. Hausmann, M., Becker, C., Gather, U., Güntürkün, O., 2002. Func- Montague, D., Weickert, C., Tomaskovic-Crook, E., Rothmond, D., tional cerebral asymmetries during the menstrual cycle: a cross- Kleinman, J., Rubinow, D., 2008. Estrogen receptor alpha locali- sectional and longitudinal analysis. Neuropsychologia 40, 808— zation in the prefrontal cortex of three mammalian species. J. 816. Neuroendocrinol. 20, 893—903. Heister, G., Landis, T., Regard, M., Schroeder-Heister, P., 1989. Shift Oie, M., Hugdahl, K., 2008. A 10—13 year follow-up of changes in of functional cerebral asymmetry during the menstrual cycle. perception and executive attention in patients with early-onset Neuropsychologia 27, 871—880. schizophrenia: a dichotic listening study. Schizophr. Res. 106, 29—32. Hugdahl, K., 1995. Dichotic listening: probing temporal lobe func- Oldfield, R.C., 1971. The assessment and analysis of handedness: the tional integrity. In: Davidson, R.J., Hugdahl, K. (Eds.), Brain Edinburgh Inventory. Neuropsychologia 9, 97—113. Asymmetry. MIT Press, Cambidge, pp. 123—156. Pollmann, S., Maertens, M., von Cramon, D.Y., Lepsien, J., Hugdahl, Hugdahl, K., 2003. Dichotic listening in the study of auditory later- K., 2002. Dichotic listening in patients with splenial and non- ality. In: Davidson, R.J., Hugdahl, K. (Eds.), The Asymmetrical splenial callosal lesions. Neuropsychology 16, 56—64. Brain. MIT Press, Cambridge, pp. 441—476. Rode, C., Wagner, M., Güntürkün, O., 1995. Menstrual cycle affects Hugdahl, K., Andersson, L., 1986. The ‘‘forced-attetion paradigm’’ in functional cerebral asymmetries. Neuropsychologia 33, 855—865. dichotic listeing to CV-syllables: a comparison between adults and Ruch, W., Köhler, G., Deckers, L., Carrell, A., 1994. The State-Trait- children. Cortex 22, 417—432. Cheerfulness-Inventory–—STCI International Version (Forms STCI- Hugdahl, K., Carlsson, G., Uvebrant, P., Lundervold, A.J., 1997. T 106i, STCI-T 106i peer, and STCI-S 45i). University of Düsseldorf, Dichotic-listening performance and intracarotid injections of Düsseldorf, Germany. amobarbital in children and adolescents. Preoperative and post- Ruch, W., Köhler, G., van Thriel, C., 1997. To be in a good or bad operative comparisons. Arch. Neurol. 54, 1494—1500. humor: construction of the state form of the State-Trait-Cheer- Hugdahl, K., Rund, B.R., Lund, A., Asbjørnsen, A., Egeland, J., fulness-Inventory-STCI. Pers. Individ. Dif. 22, 477—491. Landrø, N.I., Roness, A., Stordal, K.I., Sundet, K., 2003. Atten- Sanders, G., Wenmoth, D., 1998. Verbal and music dichotic listening tional and executive dysfunctions in schizophrenia and depres- tasks reveal variations in functional cerebral asymmetry across sion: evidence from dichotic listening performance. Biol. the menstrual cycle that are phase and task dependent. Neurop- Psychiatry 53, 609—616. sychologia 36, 869—874. Language lateralization and cognitive control across the menstrual cycle 1875 Smith, S.S., Woolley, C.S., 2004. Cellular and molecular effects of Weekes, N.Y., Zaidel, E., 1996. The influence of menstrual stage on steroid hormones on CNS excitability. Cleve. Clin. J. Med. 71, S4. interhemispheric interactions: converging results from two later- Stephan, K.E., Marshall, J.C., Friston, K.J., Rowe, J.B., Ritzl, A., alized tasks. Brain Cogn. 32, 278—282. Zilles, K., Fink, G.R., 2003. Lateralized cognitive processes and Weis, S., Hausmann, M., Stoffers, B., Vohn, R., Kellermann, T., lateralized task control in the human brain. Science 301, 384— Sturm, W., 2008. Estradiol modulates functional brain organiza- 386. tion during the menstrual cycle: an analysis of interhemispheric Thomsen, T., Rimol, L.M., Ersland, L., Hugdahl, K., 2004. Dichotic inhibition. J. Neurosci. 28, 13401—13410. listening reveals functional specificity in prefrontal cortex: an Weis, S., Hausmann, M., Stoffers, B., Sturm, W., 2011. Dynamic fMRI study. NeuroImage 21, 211—218. changes in functional cerebral connectivity of spatial cognition van Wageningen, H., Jorgensen, H.A., Specht, K., Hugdahl, K., 2010. during the menstrual cycle. Hum. Brain Mapp. 32, 1544—1556. A 1H-MR spectroscopy study of changes in glutamate and gluta- Westerhausen, R., Hugdahl, K., 2010. Cognitive control and auditory mine (Glx) concentrations in frontal spectra after administration laterality. In: Hugdahl, K., Westerhausen, R. (Eds.), The Two of memantine. Cereb Cortex 20, 798—803. Halves of the Brain Information Processing in the Cerebral Hemi- Wadnerkar, M.B., Whiteside, S.P., Cowell, P.E., 2008. Dichotic listen- spheres. MIT Press, Massachusetts, pp. 469—498. ing asymmetry: sex differences and menstrual cycle effects. Wide, J.K., Hanratty, K., Ting, J., Galea, L.A., 2004. High level Laterality 13, 297—309. estradiol impairs and low level estradiol facilitates non-spatial Wang, A.C.J., Hara, Y., Janssen, W.G.M., Rapp, P.R., Morrison, J.H., working memory. Behav. Brain Res. 155, 45—53. 2010. Synaptic estrogen receptor-a levels in prefrontal cortex in Wolf, O.T., Kirschbaum, C., 2002. Endogenous estradiol and testos- female rhesus monkeys and their correlation with cognitive terone levels are associated with cognitive performance in older performance. J. Neurosci. 30, 12770—12776. women and men. Horm. Behav. 41, 259—266.