Verbal and visuospatial working memory during pregnancy: EEG correlation between the prefrontal and parietal cortices

Neurobiology of Learning and Memory 148 (2018) 1–7

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Verbal and visuospatial working memory during pregnancy: EEG correlation between the prefrontal and parietal cortices

T

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Mayra Linné Almanza-Sepúlvedaa,b, , Marisela Hernández-Gonzáleza, Jorge Carlos Hevia-Orozcoa,c, Claudia Amezcua-Gutiérreza, Miguel Angel Guevaraa a

Instituto de Neurociencias, Universidad de Guadalajara, Francisco de Quevedo 180, Col. Arcos Vallarta, C.P. 44130 Guadalajara, Jalisco, Mexico Department of Psychology, Neuroscience and Behaviour (PNB), McMaster University, 1280 Main Street West, Hamilton, Ontario L8S 4K1, Canada1 c Instituto de Neurobiología, UNAM, campus Juriquilla, 76230 Querétaro, Querétaro, Mexico1 b

A R T I C L E I N F O

A B S T R A C T

Keywords: Pregnancy Verbal working memory Visuospatial working memory Prefrontal cortex Parietal cortex EEG correlation

Pregnancy is a dynamic process during which significant cognitive changes take place. It has been suggested that working memory (WM) is affected during gestation as a result of functional changes among cortical areas, such as the prefrontal and parietal cortices. This study examined cortical electroencephalographic correlations (rEEG) during performance of WM tasks in each trimester of pregnancy. Forty women were divided into 4 groups: first (T1), second (T2), and third (T3) trimester of pregnancy, and a control group of non-pregnant women. Electroencephalographic activity (EEG) was recorded from the frontopolar, dorsolateral and parietal cortices during performance of one verbal and one visuospatial working memory task. Only groups T2 and T3 showed increased onset latency in the visuospatial WM. During the verbal WM task, the T1 group showed a higher correlation between dorsolateral areas in the theta and alpha bands, as well as a lower left prefrontal-parietal correlation in the gamma band. During the visuospatial WM task, the T1 and T3 groups showed a higher left EEG correlation in the delta and alpha1 bands, whereas T2 presented a higher right prefrontal-parietal correlation in the gamma band. Although pregnancy had only a subtle effect on the visuospatial WM task, these different patterns of cortical synchronization in each trimester of pregnancy could represent adaptive mechanisms that enabled the pregnant women to focus their attention and use more cognitive resources and so adequately solve the WM tasks.

1. Introduction Pregnancy is one of the most important phases of a woman’s reproductive cycle; a period characterized by a series of physiological, neurological, metabolic and endocrinological changes that support fetal growth and development in the future mother, while maintaining maternal homeostasis and preparing for lactation (King, 2000). A substantial number of pregnant women report various cognitive changes during pregnancy and the postpartum period, with memory deficits being the most common complaint (Brett & Baxendale, 2001). Various studies have evaluated whether these subjective appraisals of memory difficulties reflect objective impairment, but have failed to yield consistent results. In particular, the literature related to the executive component of working memory (WM) has demonstrated inconsistences, as some studies failed to detect any deficits of this kind (Casey, 2000; Henry & Rendell, 2007), while others report significant impairment (Casey, Huntsdale, Angus, & Janes, 1999). For example, Henry and ⁎

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Rendell (2007) found evidence of the impact of pregnancy on WM by showing that: (1) pregnant women rated their WM significantly worse than non-pregnant women; and (2) these differences persisted postpartum. Onyper, Searleman, Thacher, Maine, and Johnson (2010) in contrast, found no significant differences between pregnant women and non-pregnant controls on tests of short-term and working memory. Some of the discrepancies in these findings may arise from methodological differences and/or the period of pregnancy in which the evaluations of WM were conducted, as these are two potential determinants of the magnitude of the effects of pregnancy on WM. As is well-known, significant changes occur in the levels of several hormones during pregnancy, highlighted by the gradual increase of progesterone, estradiol and other hormones that reach maximum levels just before birth (Russell, Douglas, & Ingram, 2001). Both cerebral functionality and cognition are affected by these hormones as, for example, studies have demonstrated that significant changes occur in the degree of cortical synchronization in relation to the phase of the

Corresponding author at: Instituto de Neurociencias, Universidad de Guadalajara, Francisco de Quevedo # 180, Colonia Arcos Vallarta, C.P. 44130, Mexico. E-mail address: [email protected] (M.L. Almanza-Sepúlveda). Present address.

https://doi.org/10.1016/j.nlm.2017.12.003 Received 7 July 2017; Received in revised form 8 December 2017; Accepted 18 December 2017 Available online 23 December 2017 1074-7427/ © 2017 Elsevier Inc. All rights reserved.

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Considering the pivotal role that the prefrontal and parietal cortices play in modulating memory processes, we hypothesized that distinct degrees of inter- and intrahemispheric synchronization between the prefrontal-parietal regions would be detected on the different WM tasks. Because the most marked hormonal changes occur in the first and third trimesters of pregnancy, we expected, in accordance with the literature, higher rEEG in the theta and gamma bands in the hemisphere specialized for each task (verbal-left; visuospatial-right). Finally, we hypothesized that pregnant women in these periods will present poorer performance on both verbal and visuospatial WM tasks than nonpregnant controls. Analyzing the possible behavioral and electroencephalographic differences while performing verbal and visuospatial WM tasks during the three trimesters of pregnancy could help clarify contradictory results in the literature regarding the impact that pregnancy may exert on cognitive processes.

menstrual cycle (Solis-Ortiz et al., 2009; Solís-ortíz, Ramos-Loyo, Arce, Guevara, & Corsi-Cabrera, 1994). Similarly, it has been shown that the hormonal changes characteristic of pregnancy are also related to women’s performance on various cognitive tasks (Buckwalter et al., 1999). Studies with rats, mean while, have shown that several brain structures, including the preoptic area, amygdala, prefrontal cortex, and nucleus accumbens, manifest important changes in neuroplasticity during gestation, associated with the secretion of sex steroid hormones and peptides unique to the condition of pregnancy (Afonso, Sison, Lovic, & Fleming, 2007; Kinsley et al., 1999; Pawluski, Lambert, & Kinsley, 2016; Russell et al., 2001). Although the neural system responsible for WM is known to involve a large number of brain regions, evidence from neurophysiological and lesion studies shows that the prefrontal cortex is a critical component (Fuster, 2000; Goldman-Rakic, 1990); especially the dorsolateral region and its functional connections with the posterior parietal cortex in relation to both verbal and visuospatial WM processes (Fuster, 2001). One method used to measure brain functionality consists in recording electroencephalographic activity (EEG). Several changes in specific EEG bands have been associated with specific cognitive and physiological states. For example, the slow waves of the delta band are often found during attention in relation to internal processing during performance of mental tasks (Fernández et al., 1995; Harmony, 2013; Harmony et al., 1996; Vogel, Broverman, & Klaiber, 1968), while the theta band is detected during relaxation, meditation (Buzsáki, 2002) and memory processes (Klimesch, Doppelmayr, Russegger, & Pachinger, 1996; Klimesch et al., 2001; Sarnthein, Petsche, Rappelsberger, Shaw, & Von Stein, 1998; Sauseng, Klimesch, Schabus, & Doppelmayr, 2005). The Alpha band, mean while, has been associated with attentional processes (Cooper, Croft, Dominey, Burgess, & Gruzelier, 2003; Foxe & Snyder, 2011; Payne, Guillory, & Sekuler, 2013), whereas the fast frequencies of the beta and gamma band have been related to wakefulness (Basar, Basar-Eroglu, Karakas, & Schürmann, 2000) and activities that require consciousness and perception (Basar et al., 2000; Blinowska & Durka, 2006). In particular the gamma band is involved in both the perception and maintenance of information during a delay (Tallon-Baudry, Bertrand, Delpuech, & Pernier, 1996), which is indicative of its crucial participation in WM. Electroencephalographic correlation (rEEG) is a mathematical index that makes it possible to determine the degree of similarity between two EEG signals and, hence, the possible functional relation among different brain regions (Guevara & Corsi-Cabrera, 1996). This correlation method has been used by several researchers to determine whether the functional connectivity between brain regions changes in relation to different emotional and cognitive states (Corsi-Cabrera, Arce, Ramos, & Guevara, 1997; Corsi-Cabrera, Meneses, & Molina, 1987; Costa, Rognoni, & Galati, 2006). In fact, a low correlation between frontal regions in the alpha band and an increased fronto-parietal correlation in the theta band have been associated with executive functions, such as visuospatial WM (Sauseng et al., 2004, 2005). Other studies have provided clear evidence of a functional hemispheric specialization of WM in adulthood. Adults exhibit brain lateralization when responding and, possibly, further refinement of the left hemisphere in verbal processes, while the right hemisphere specializes in visuospatial processes (Ojemann & Dodrill, 1985; Scherf, Sweeney, & Luna, 2006; Smith & Jonides, 1997; Smith & Milner, 1981). Although cortical EEG bands have been related to cognitive processes, and several studies have shown that these processes are affected during pregnancy, it is still not known whether EEG correlations between the prefrontal and parietal cortices change during pregnancy while performing WM tasks. Therefore, the purpose of this study was to compare, on the one hand, the behavioral parameters of verbal and visuospatial WM tasks and, on the other, to compare the degree of cortical synchronization between the prefrontal and parietal cortices while performing both WM tasks during the three trimesters of pregnancy.

2. Materials and methods 2.1. Participants A total of 40 women, divided into 4 groups of 10 participants each, took part in the study. Three groups included women in different trimesters of pregnancy, as follows: trimester one (T1), 1–12 weeks of gestation; trimester two (T2), 13–28 weeks of gestation; and trimester three (T3), 29–42 weeks of gestation. The fourth group consisted of non-pregnant women as controls (CO). None of the control women had ever been pregnant. The pregnant women were all primigravid and their medical histories reported uncomplicated pregnancies, defined as a single pregnancy with no known fetal abnormalities or poor fetal growth. All groups were recruited via flyers posted in public places. Participation was voluntary. All the women were right-handed, healthy, and had no known medical or psychiatric conditions that might affect their cognitive functioning. Subjects were matched by demographic characteristics, as all participants completed a preliminary procedure that included a demographic questionnaire on their age, education, health, and other details. They also completed the Beck Anxiety Inventory (Beck, Epstein, Brown, & Steer, 1988), the Beck Depression Inventory (Beck, Steer, & Brown, 1996), and the brief version of WAISIII (Wechsler, 2010) to measure IQ. All procedures involved in this experiment were approved by the Institutional Ethics Committee in accordance with the ethical standards laid down in the 1964 Helsinki Declaration. All participants gave their informed consent prior to their inclusion in the study. 2.2. Behavioral measures All participants completed the Digit Span sub-test of the WAIS-III (Wechsler, 2010). Digit sequences were presented backwards (two trials per item, 2–8 digits) as a measure of verbal WM. For the Digit span backward task (DSB), the examiner read a sequence of numbers and the examinee had to repeat the numbers in reverse order, following the procedure described in Wechsler (2010). The parameters measured were: number of correct trials (CT), and the longest sequence or span (LSS). After completing the DSB, the Corsi Block-tapping task (CBT) was applied to measure visuospatial WM. A computerized version of the CBT (CubmemPC.exe) was used (Guevara, Sanz-Martin, HernándezGonzález, & Sandoval-Carrillo, 2014), in which 10 blue cubes are shown on a computer screen against a rectangular gray background. The task begins when the participant touches the computer’s touch screen to automatically initiate a sequence of cubes. To emulate the sequence of cubes that the examiner taps, the program changes the color of the tapped cubes from blue-to-yellow (1-s duration), one-byone and sequentially, to form a series of bins, whose length increases progressively up to a series of 7 cubes (4 trials for each length). 2

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Table 1 Mean ± SE of demographic characteristics: age, education level, anxiety, depression levels and IQ for the pregnant (T1, T2, T3) and non-pregnant (CO) groups. Group n = 10

Age (years)

Education (years)

Anxiety level

Depression level

IQ

CO T1 T2 T3

24.1 25.5 27.5 26.0

14.5 15.2 15.2 13.8

7.5 ± 3.28 10.6 ± 5.14 11.3 ± 5.30 11.4 ± 4.64

7.60 ± 5.14 10.20 ± 3.89 11.20 ± 3.00 8.80 ± 2.76

100.3 ± 4.51 99.0 ± 5.72 99.72 ± 5.96 97.7 ± 8.46

± ± ± ±

1.53 2.36 3.44 2.74

± ± ± ±

1.61 1.06 1.06 1.90

2.4. Statistical analyses

Immediately after the last cube of the sequence lights up, the participant had to reproduce the sequence presented before by touching the cubes on the screen, but in backwards order. The total number of trials was 24, and the following parameters were measured: onset latency (OL) in milliseconds (ms), total execution time (TET) in seconds (s), number of correct trials (CT), and the longest sequence or span (LSS) reproduced correctly. The Corsi Block-tapping and Digit span tasks were counterbalanced with an interval of 3 min between them.

The EEG analyses included three phases: (1) 3 min of the baseline condition; (2) 5 min that corresponded to the DSB; and, (3) 5 min of the CBT condition. Thus, 60 filtered, artifact-free EEG epochs (approx. 2 s each) were representative of the entire duration of the EEG recordings in each one of the three phases. In the EEG analysis, a one-way ANOVA was performed for each parameter (inter- and intrahemispheric rEEG) and for each EEG band to compare the 4 groups in each recording condition (DBS or CBT), from which the baseline values were subtracted. All analyses were performed with the EEGmagic program (Guevara & Hernández-González, 2009). All demographic data from the four study groups –CO, T1, T2, T3– were compared using one-way ANOVAs for participants’ age, education, anxiety, depression level, and IQ; followed by a post hoc Duncan 1% test. One-way ANOVAs were also used to analyze the behavioral parameters; i.e., for DSB: number of correct trials (CT) and longest sequence or span reproduced correctly (LSS); and, for CBT: onset latency (OL), total execution time (TET), number of correct trials (CT), and the longest sequence or span reproduced correctly (LSS). In all analyses, differences were considered significant when p ≤ .05 values were attained.

2.3. EEG recordings and procedure Electrode placement followed the international 10–20 system (Jasper, 1958). The recording sites were the frontopolar (Fp1-Fp2), dorsolateral (F3-F4) and parietal (P3-P4) areas. EEG from these cortices were recorded while the participants were sitting quietly with eyes open in front of a 13-inch Mac laptop in three conditions: (1) baseline (3 min), when they were asked to look at a red dot against a white background on the PC screen; (2) during performance of the DSB as a test of verbal WM (5 min); and (3) while performing the CBT to test visuospatial WM (5 min). Therewas a 3-min interval between conditions. All EEG were recorded in a single session of approximately 1 h, and all testing was done in a shielded, dimly-lit, soundproof room with natural lighting. Each participant performed the tasks individually on the laptop. Recordings were made with subjects awake in a sitting position with their heads supported by the headrest of a comfortable chair. All derivations were referred to linked ears with the ground electrode placed on the forehead. Linked ears were chosen as the reference in order to avoid, insofar as possible, the reference electrode and volume conduction. EEG were amplified using a Grass model P7 polygraph with EEG filters set at 1 and 30 Hz. Impedance for the EEG electrodes was maintained below 10 k Ohms. Specially-designed software (Guevara, Ramos-Loyo, Hernández-González, Madera-Carrillo, & Corsi-Cabrera, 2000) was used to sample (1024 points at a sample rate of 512 Hz) and store the EEG data for processing offline. Also, electrooculograms were recorded to detect eye-movement artifacts using a bipolar montage with electrodes placed at the outer end of both eye sockets. Epoch rejection was based on both visual and computer assessment. The EEG signals were examined offline to identify saturated epochs or those that showed noise due to muscle activity, eye-movement, or heartbeat. All EEG epochs that were visually identified as being contaminated by noise were removed automatically by means of a computer program (CHECASEN), (Guevara, Sanz-Martín, Corsi-Cabrera, Amezcua-Gutiérrez, & Hernández-González, 2010) so that the background noise in the EEG did not differ among groups. The filtered, artifact-free EEG data were then reduced to 150 EEG epochs (approx. 2 s each) representative of the entire duration of EEG recording. EEG were analyzed using the EEGmagic computer program (Guevara & Hernández-González, 2009) to calculate the interhemispheric (rINTER, between areas of the two hemispheres) and intrahemispheric (rINTRA, between different areas in the same hemisphere) EEG correlations of 7 broad EEG bands: delta (δ, 1.5–3.5 Hz), theta (θ, 3.5–7.5 Hz), alpha1 (α1, 7.5–10.5 Hz), alpha2 (α2, 10.5–13.5 Hz), beta1 (β1, 13.5–19.5 Hz), beta2 (β2, 19.5–30 Hz), and gamma (γ, 31–50 Hz).

3. Results 3.1. Behavioral results As Table 1 shows, no significant differences were found among the groups for any of the demographic characteristics measured. To evaluate the hypothesis that pregnancy confers a specific disadvantage to WM processes, we first examined performance on the verbal and visuospatial WM tasks. No significant between-group differences were found on verbal WM, but with respect to behavioral performance on the visuospatial WM task, T2 ( ± 2SE = 1585.1 ± 468.14) and T3 ( ± 2 SE = 1539.7 s ± 285) had significantly higher scores for OL than CO (±2 SE = 921.8 s ± 134.1), F (3, 36) = 3.48; p < .02 (Fig. 1). 3.2. EEG results 3.2.1. Verbal working memory/Digit span backward T1 showed higher rINTER between the dorsolateral cortices (F3-F4) in the theta (4–7.5 Hz) (F (3, 36) = 4.14; p < .01) band than CO and T3, as well as in alpha1 (8–10.5 Hz) (F (3, 36) = 4.12; p < .01) compared to T3 during the DSB task (Fig. 2A). Likewise, T1 showed lower left rINTRA between the frontopolar and parietal cortices (Fp1-P3) in the gamma band (31–50 Hz) (F (3, 36) = 2.71; p < .05) compared to CO during the DSB task (Fig. 2B). The T1 group was also characterized by a higher left rINTRA between the frontopolar and dorsolateral areas of the prefrontal cortex (Fp1-F3) in the delta band (0.5–3.5 Hz) (F (3, 36) = 4.71; p < .007) compared to T2 and T3 during this verbal WM task (Fig. 2C). 3.2.2. Visuospatial working memory/Corsi Block-tapping task No significant between-group differences were found in the rINTER between frontopolar (Fp1-Fp2) or dorsolateral (F3-F4) areas during the 3

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Fig. 1. Mean ± 2 SE of onset latency (ms) in all groups: CO, T1, T2 and T3 during performance of the Corsi Block-Tapping Task (CBT, visuospatial WM). *p < .05 with regard to CO, **p < .02 with regard to CO.

Fig. 3. Mean ± 2 SE of the correlation (r) in z values. (A) rINTRA between left frontopolar and dorsolateral areas (Fp1-F3); (B) rINTRA between right dorsolateral and parietal areas (F4-P4), in all EEG bands of the groups: CO, T1, T2 and T3 during performance of the Corsi Block-Tapping Task (CBT, visuospatial WM). *p < .05 with regard to CO.

CBT task. T3 showed higher rINTRA in the delta band (0.5–3.5 Hz) (F (3, 36) = 3.63; p < .02), while T1 showed higher rINTRA in the alpha1 band (8–10.5 Hz) (F (3, 36) = 3.60; p < .02) between the left frontopolar-dorsolateral areas of the prefrontal cortex (Fp1-F3) compared to CO during the CBT task (Fig. 3A). For the right rINTRA between frontopolar-dorsolateral regions (Fp2F4), no significant differences between groups were found during this visuospatial task, while in another comparison, T2 showed higher rINTRA between right dorsolateral and parietal areas (F4-P4) in the gamma band (31–50 Hz) (F (3, 36) = 2.38; p < .05) than CO (Fig. 3B).

4. Discussion The present study compared performance on verbal and visuospatial WM tasks during the three trimesters of pregnancy, and then characterized the degree of EEG coupling between prefrontal and parietal cortices during performance of both WM tasks. Our behavioral results show that pregnancy did not affect performance on the DSB (verbal WM task), which concurs with earlier studies that found no differences in WM between pregnant and non-pregnant women (Casey, 2000; Casey et al., 1999; Onyper et al., 2010). However, while no performance differences were obtained on the verbal WM, clear differences in the degree of coupling between cortices were observed, mainly in the first trimester of pregnancy. In fact, during performance of the verbal WM task, the women in T1 required higher synchronization between dorsolateral areas of the prefrontal cortex in the range of the theta and alpha1bands. The dorsolateral region of the prefrontal cortex plays a pivotal role in modulating cognitive processes (Braver & Bongiolatti, 2002; D'Esposito, Postle, Ballard & Lease, 1999; Fletcher & Henson, 2001; Petrides, 2005). Moreover, oscillations in the prefrontal theta band are involved especially in verbal WM, for they increase parametrically with the number of items presented, but decrease during information retrieval (Jensen & Tesche, 2002; Roux &

Fig. 2. Mean ± 2 SE of the correlation (r) in z values. (A) rINTER between leftand right dorsolateral cortices (F3,F4); (B) left rINTRA between frontopolar and parietal cortices (Fp1-P3), and (C) left rINTRA between frontopolar and dorsolateral areas (Fp1-F3), in all EEG bands of the groups: CO, T1, T2 and T3 during performance of the Digit span backward (DSB, verbal WM). *p < .05 with regard to CO, ○p < .05 with regard to T3, and ▾p < .05 with regard toT2.

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finally, those required to induce labor (Russell et al., 2001). Thus, it is possible that a higher correlation between left hemisphere structures is required in these periods as an adaptive mechanism that enables proper processing of visuospatial working memory in order to achieve the same behavioral outcomes as in CO and T2, At this point, it is important to emphasize that on both the verbal andvisuospatial WM tasks, gamma band activity was found in the specialized hemisphere in relation to each kind of working memory, and that this oscillation was found in the frontal-parietal correlation during both tasks. However, T1 showed a lower rEEG on the verbal task, while T2 showed a higher rEEG on the visuospatial task, both in comparison to CO. These contrasting results might be explained by the notion that brain functionality is affected in periods of pronounced hormonal changes (Geier, Garver, Terwilliger, & Luna, 2009; Klingberg, Forssberg, & Westerberg, 2002; Schweinsburg, Nagel, & Tapert, 2005). However, more studies will be required to elucidate how the hormonal changes in these stages of pregnancy could affect EEG correlations. In conclusion, our EEG results provide evidence that although pregnancy had only a subtle effect on the visuospatial WM, at the level of brain functionality the women presented characteristic patterns of EEG synchronization between the prefrontal and parietal cortices during performance of both WM tasks in each trimester of pregnancy. It is probable that these different patterns of cortical synchronization in each trimester of pregnancy could represent adaptive mechanisms that enable pregnant women to focus their attention and use more cognitive resources to adequately solve the WM tasks and achieve the same behavioral outcomes as non-pregnant women. It is important to recognize that there are some limitations associated with the present study. First, as an exploratory analysis, our sample is relatively small. Perhaps because of this, the behavioral results showed only subtle differences that were not statistically associated with EEG outcomes. Second, the WM tasks used in this study are relatively simple ones for healthy women, and it has been reported that during laboratory tests pregnant women focus their cognitive resources and, therefore, achieve results within normal ranges (Crawley, Grant, & Hinshaw, 2008). As a result, future studies are necessary to explore these aspects in greater depth. Despite these limitations, and although additional studies are required to clarify the degree of EEG coupling between cortices and how this correlates to behavioral outcomes, ours is the first study to characterize EEG correlations during verbal and visuospatial WM tasks through the three trimesters of gestation, which could reflect the cerebral adaptive mechanisms that future mothers require to adequately perform the multiple tasks involved in their everyday lives.

Uhlhaas, 2014), while alpha has been related to attentional demands as a mechanism that underlies selective attention and inhibition of irrelevant information (Cooper et al., 2003; Foxe & Snyder, 2011; Payne et al., 2013; Sauseng et al., 2005). Hence, it is probable that in this first trimester, the women required greater attention and inhibition processes to perform the verbal WM in a similar way to those in the second and third trimesters. Together with the higher dorsolateral rEEG of the theta and alpha bands, the women in T1 showed a higher rEEG between prefrontal areas in the delta band, as well as a lower prefrontal-parietal rEEG in the gamma band during the verbal WM only in the left hemisphere, which is involved primarily in verbal processes (Ojemann & Dodrill, 1985). Moreover, participation of the delta and gamma bands in cognitive processes has been reported in various studies. For example, delta bands appear during cognitive processes and attention in relation to internal processing during performance of mental tasks (Fernández et al., 1995; Harmony, 2013; Harmony et al., 1996; Vogel et al., 1968), while frequencies in the ranges of the gamma band have been associated with higher cognitive processes (Haig, Gordon, Wright, Meares, & Bahramali, 2000; Jefferys, Traub, & Whittington, 1996; Paul et al., 2005; Sauvé, 1999). In addition, the simultaneous occurrence of gamma and other frequency bands, such as alpha or theta, could underlie distinct WM information (Roux & Uhlhaas, 2014). The first trimester of pregnancy is considered the most critical stage due to the marked hormonal changes that take place in this period (Fleming, Ruble, Krieger, & Wong, 1997; Russell et al., 2001; Sitteri & Stites, 1982), Thus, these particular patterns of synchronization between the left prefrontal and parietal cortices in T1 could be an adaptive mechanism that enables proper processing of verbal working memory in order to achieve similar behavioral outcomes that women in other trimesters of the pregnancy. The women in T2 and T3 had higher onset latencies than CO only during performance of the CBT (visuospatial WM). Total execution time and onset latency are parameters considered indicators of efficiency in working memory, which is understood as the ability to minimize the amount of resources used (time) to reach a goal (Hale, 1990; Mokate, 2002). Although groups T2 and T3 required more time to begin the task, once they began, they presented adequate performance during all three trimesters of gestation. Thus, these findings could explain why a higher percentage of women in the second and third trimesters of pregnancy perceive memory deficits (Brett & Baxendale, 2001). During the visuospatial WM task, the women in T1 and T3 showed higher EEG correlations (rEEG) in the delta and alpha1 bands between the prefrontal cortices of the non-specialized hemisphere (left), while only the women in T2showed a higher prefrontal-parietal rEEG of the gamma band in the specialized hemisphere (right). Oscillations in the delta band have been considered an indicator of attention during mental tasks, such thatwhen attentional demand increases and the individual is able to respond adequately, activity in delta increases (Harmony et al., 1996). Other studies have suggested that delta is associated with loading during working memory (Zarjam, Epps, & Chen, 2015); hence, it is probable that T3 required more attention in order to perform the task correctly, which could explain why T3 presented greater OL than CO. T2 required higher right prefronto-parietal rEEG in the gamma band, one that is involved in both the perception and maintenance of information during a delay (Tallon-Baudry et al., 1996). Gamma band oscillations prevail during increased alertness or optimal processing of sensory stimuli (Steriade, Dossi, Paré, & Oakson, 1991). Therefore, the synchronization in the gamma band observed between the prefrontal and parietal cortices in group T2 may be associated with a state of alertness generated by expectation at the time of the sequence in CBT, and this could explain why this group manifests differences in efficiency, but not in performance, compared to CO. Trimesters 1 and 3 are the most critical stages of pregnancy due to the marked hormonal changes required, first, for implantation and,

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