Biological Psychology 69 (2005) 23–38 www.elsevier.com/locate/biopsycho Maternal psychophysiological change during the second half of gestation Janet A. DiPietroa,*, Kathleen A. Costiganb, Edith D. Gurewitschb a Department of Population and Family Health Sciences, Johns Hopkins University, 615 North Wolfe Street, E4531, Baltimore, MD 21205, USA b Division of Maternal Fetal Medicine, Department of Gynecology and Obstetrics, Johns Hopkins University School of Medicine, 600 North Wolfe Street, Baltimore, MD 21205, USA Available online 4 January 2005 Abstract This study investigated the trajectory of physiological and psychological functioning during the second half of pregnancy and compared responsiveness to a laboratory stressor between pregnant and non-pregnant women. Monitoring of 137 pregnant women at 20, 24, 28, 32, 36, and 38 weeks of pregnancy included measures of heart period (HP), heart period variability (HPV), skin conductance (SCL), respiratory period (RP), respiratory sinus arrhythmia (RSA), and self-report of mood disturbance. HP and RSA declined during this period; SCL and mood disturbance increased. Parity was a significant moderator. HP and SCL responsiveness to the Stroop color-word task was assessed twice in pregnant participants and compared to a sample of 27 non-pregnant women. Physiologic responsiveness was reduced in pregnant women. Pregnant women perceived the Stroop to be more difficult, but performance was unaffected. Despite buffered responsivity to stressful stimuli during pregnancy, advancing gestation is associated with escalating sympathetic tone and declining parasympathetic tone. # 2004 Elsevier B.V. All rights reserved. Keywords: Pregnancy; Pregnancy stress; Respiratory sinus arrhythmia; Heart period; Skin conductance The physical, physiological, and psychological changes that accompany pregnancy are both conspicuous and profound. Much of the knowledge about pregnancy has been generated by obstetric research directed at conditions that jeopardize pregnancy outcome. There is growing recognition that more detailed understanding of the manner through * Corresponding author. Tel.: +1 410 955 8536; fax: +1 410 955 2303. E-mail address: [email protected] (J.A. DiPietro). 0301-0511/$ – see front matter # 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.biopsycho.2004.11.003 24 J.A. DiPietro et al. / Biological Psychology 69 (2005) 23–38 which these processes emerge and interact in uncomplicated pregnancies is necessary to fully characterize the effects of childbearing on women’s lives. A prevailing sentiment regarding the interface between psychological and physiological changes during pregnancy is that pregnancy serves to buffer the physiological response to stress. Evidence enlisted as support for this includes blunted responses to administration of endogenous corticotrophin-releasing hormone (CRH) (Schulte et al., 1990) and dexamethasone (Rees et al., 1975). Compared to non-pregnant women, pregnant women report less pain (Saisto et al., 2001) and fail to mount a cortisol response (Kammerer et al., 2002) to cold pressor stimulation. Blood pressure responsivity to cognitive challenges is attenuated (Matthews and Rodin, 1992). Diminshed heart rate, heart rate variability, and catecholamine responses to postural adjustments, isometric exercise, and controlled breathing conditions have been observed (Barron et al., 1986; Ekholm et al., 1993) as has blunted renin response to thermal stress (Vaha-Eskeli et al., 1992). Within pregnancy, maternal heart rate and electrodermal responses to repeat administration of a cognitive challenge diminish from 24 to 36 weeks of pregnancy (DiPietro et al., 2003). Reports of changes in psychological indicators of distress have been less consistent. Changes observed during gestation include an increase in frequency of daily hassles but a decrease in intensity from first through third trimesters (Thompson et al., 1997), higher hassles and pregnancy-specific stress in the first trimester than in either the second or third (DaCosta et al., 1998), or no changes (DaCosta et al., 1999; DiPietro et al., in press). Mood disturbance, including tension, anger, and confusion have been reported to rise significantly from 28 to 38 weeks gestation, as did a separate fatigue factor (Smith et al., 1990). Some have reported increases in anxiety (DaCosta et al., 1999; Keenan et al., 1998) and depression (Hoffman and Hatch, 2000), while others have not (Heron et al., 2004). Another report suggests that women perceive negative events as more upsetting when they occur during the first trimester as compared to the last trimester of pregnancy (Glynn et al., 2004). Support for a buffering effect on stress during pregnancy has also been provided by either lack of associations between indicators of psychological distress and levels of cortisol, CRH, and catecholamines (Petraglia et al., 2001) or reversal of expected associations (Dorn et al., 1993). However, changes wrought by pregnancy on the HPA axis are complex. Although plasma cortisol levels increase significantly during pregnancy (Goland et al., 1994), the appearance and escalation of placental CRH in plasma during the second half of gestation is far more dramatic (Wadhwa et al., 1997). The lack of correlation between placental CRH and cortisol levels within individuals (Petraglia et al., 2001; Wadhwa et al., 1997) challenges fundamental assumptions about the mediation of the stress response in pregnancy and is the subject of active inquiry. Not all neuroendocrine systems undergo extensive alterations during pregnancy; adrenergic compounds including catecholamines (Katz et al., 1991) and melatonin (Katz et al., 1995) have been reported to remain relatively constant. The numerous structural and functional changes to the cardiac system and vasculature that accompany pregnancy are well known. In general, pregnant women have faster heart rates, reduced heart rate variability in both frequency and time domains, and decreased blood pressure (Ekholm and Erkkola, 1996; Smith et al., 2004; Voss et al., 2000; Yang et al., 2000). Most of these studies rely on a cross-sectional approach or compare the same women before J.A. DiPietro et al. / Biological Psychology 69 (2005) 23–38 25 and during pregnancy. There is limited knowledge about changes in autonomic functioning over the course of pregnancy and minimal information on aspects of autonomic functioning beyond cardiovascular indicators. The primary purpose of this study was to document change and stability of autonomic functioning in pregnant women during the second half of gestation. To this end we measured heart period (HP), heart period variability (HPV), respiratory period (RP), electrodermal activity in terms of skin conductance level (SCL), and respiratory sinus arrhythmia (RSA) as well as psychological state at monthly intervals beginning in the 20th week of pregnancy. Modulation of HP, HPV, and respiration is affected by both sympathetic and parasympathetic influences and other, non-neural determinants. RSA provides an index of vagal control of the heart as modulated through the sinoatrial node and is widely considered to be an indicator of parasympathetic innervation (Berntson et al., 1993). Sympathetic function was evaluated by measurement of electrodermal activity, which reflects changes in conductivity of the skin mediated by eccrine glands, and is singly innervated by the sympathetic branch of the nervous system (Venables, 1991). The study design allowed analysis of the nature and magnitude of change in these parameters over gestation as well as quantification of intraindividual consistency to determine the degree to which each parameter serves as a stable characteristic of individual pregnancies. Maternal parity was examined as a potential moderating influence. First pregnancies are associated with significantly higher cortisol levels (Vleugels et al., 1986) and variation in several cardiovascular parameters, including higher cardiac output (Clapp and Capeless, 1997; van Oppen et al., 1996). Psychological differences have also been observed; nulliparous women feel more uplifted about their pregnancy than parous women, and this discrepancy increases during gestation (DiPietro et al., in press). Our secondary goal was to evaluate the stress-buffering hypothesis by comparing physiological and psychological responses to an experimental stressor in pregnant and nonpregnant women. Based on existing literature, we expected that cardiovascular, electrodermal, and psychological responsiveness of pregnant women would be attenuated at each of two administrations of a cognitive challenge. 1. Methods 1.1. Participants Eligibility was restricted to normotensive, non-smoking women with uncomplicated pregnancies carrying singleton fetuses. Accurate dating of the pregnancy was required and based on early first trimester pregnancy testing or examination and/or confirmed by ultrasound. A total of 185 self-referred pregnant women were enrolled; 48 were either prospectively or retrospectively excluded as follows: preterm labor, preterm delivery, or both (21; 11%); gestational diabetes (6; 3%); congenital malformation (2; 1%); fetal death in utero or non-viable delivery (2; 1%); growth retardation or other condition of antepartum origin detected in the newborn (6; 3%); and lack of completion of protocol due to scheduling difficulties, moving, etc. (12; 6%). The final sample of 137 participants 26 J.A. DiPietro et al. / Biological Psychology 69 (2005) 23–38 represent a population of healthy, relatively well-educated women (M years education = 16.7 years, S.D. = 2.1, range 12–20; M age = 31.3, S.D. = 4.1, range 21–39). Most (85%) women were non-Hispanic white; the remainder were African-American (12%), Hispanic or Asian (3%). Fifty percent of the fetuses were female and this was the first child for 55% (n = 75) of the sample. An additional 27 non-pregnant, healthy women were enrolled as a comparison group for the experimental stress manipulation portion of the study (M years education = 15.3 years, S.D. = 2.8; M age = 33.2, S.D. = 5.2). Most women were non-Hispanic white (63%), the remainder were African-American (22%), Hispanic or Asian (15%). 1.2. Design and procedure Maternal monitoring commenced at 20 weeks gestation and was repeated at 24, 28, 32, 36, and 38 weeks. To control for potential diurnal and post-prandial effects, testing occurred at the same time of day during each visit (either 1:00 or 3:00 p.m.) and women were instructed to eat 1.5 h prior to testing, but not thereafter. Fetal monitoring was also conducted simultaneously with maternal monitoring but is not the subject of this report. Monitoring proceeded for 50 min, with the mother resting comfortably in a semirecumbent, left-lateral position. At 32 weeks, monitoring duration was shortened to 30 min to accommodate an additional protocol. 1.2.1. Physiolological measures Maternal physiological signals were amplified using a multi-channel, electrically isolated, bioamplifier (Model JAD-04; James Long Company, Caroga Lake, NY). Data were digitized on a personal computer at 1000 Hz via an internal analog to digital board using Snapstream data acquisition system (HEM Data Corporation, Southfield, MI). Electrocardiogram was recorded from three carbon fiber disposable electrodes in triangulated placement (right mid-sub-clavicle, left mid-axillary thorax, and upper left thigh for ground lead). Electrodermal activity was monitored from two silver–silver chloride electrodes with a gelled skin contact area placed on the distal phalanxes of the first and index fingers of the non-dominant hand. Electrodes were affixed with adhesive collars to limit gel contact to a 1 cm diameter circle and secured with velcro. Respiration was measured from a bellows apparatus stretched across the ribcage below the breasts. Data quantification proceeded off-line using the PHY General Physiology System and IBI Analysis Systems (James Long Company). ECG data underwent R-wave detection, manual editing for artifact, and interbeat interval computation in ms (HP). Skin conductance level (SCL) was measured by administering a constant 0.5 V root-meansquare 30 Hz ac excitation signal and detecting the current flow. Skin conductance level was scaled from 0 to 25 mS and detrended to remove the mean, thereby amplifying the signal to noise ratio ( 2.5 to +2.5 mS). Respirations were measured by quantifying inspiration to inspiration and expiration to expiration periods based on the detected peaks and troughs of the respiratory waveform. In addition to computation of respiratory period(s), these values were used to quantify respiratory sinus arrhythmia (RSA); units represent peak to valley changes in IBI from inspiration to expiration (ms) (Grossman et al., 1990). All values were averaged over the 50 min monitoring period. J.A. DiPietro et al. / Biological Psychology 69 (2005) 23–38 27 1.2.2. Psychological self-report At each visit, women were asked to rate their current levels of vigor, tension, stress, anger, fatigue, confusion and depression on 5-point scales immediately prior to monitoring. Scores were summed to provide an indicator of mood disturbance. Selection of these items was based on the factor structure of the Profile of Moods States scale (POMS) (McNair et al., 1971). The POMS was administered at 24 and 36 weeks; correlations between the full scale scores and the abbreviated questionnaire were r(135) = .80 and r(133) = .73, respectively. 1.2.3. Experimental manipulation The Stroop Color-Word task, a procedure that has been extensively used to invoke a sympathetic, autonomic response (MacLeod, 1991) was administered at 24 and 36 weeks gestation immediately following the undisturbed, baseline period for pregnant participants. The Stroop task requires disassociating word meaning from printed word color, performed under time pressure. Participants viewed the stimuli on a projector and provided responses orally. Computerized presentation of the Stroop task was not feasible given the positioning of the pregnant women so interference scores are not available. However, the duration of the task, which reflected the speed with which women processed the stimuli, serves as a proxy for cognitive performance. Non-pregnant participants were also administered the procedure twice, separated by a 12-week interval. Testing occurred during the late follicular phase of the menstrual cycle (first visit M = 9.4 days, S.D. = 2.2, second visit M = 9.8, S.D. = 2.0). The Stroop baseline period corresponded to settling the projector into place on an overbed table and providing instructions (M = 2.8 min). An event marker was used to signal the onset of the first Stroop stimulus in the computer file. A series of slides were used that included both traditional color word combinations as well as pregnancy-based emotionally evocative words (e.g., baby, miscarriage, contraction). Women were asked to respond as quickly and accurately as possible; slides were advanced when women reached a predetermined point in each slide to increase urgency. Termination of the procedure, the duration of which was dependent on the amount of time it took each participant to complete all the stimuli, was signaled with the event marker (M = 3.9 min). Monitoring continued for the period of time during which the equipment was dismantled and concluding information was provided (M = 2.7 min). Immediately following administration, women reported the degree to which they experienced the Stroop as stressful and difficult on 5point scales ranging from low (1) to high (5). Women’s behavioral responses indicative of stress were also rated on a similar 5-point scale by an observer. Results detailing the influence of the maternal response to the Stroop on the fetus and change in the maternal response over time have been presented elsewhere (DiPietro et al., 2003). 1.2.4. Data analysis Weighted least squares analysis was used to model the change over the gestational period under observation for each measure. This method estimates the correlation structure generated by the repeated measurements on the same fetus and uses the estimate to weight the observations in the regression analysis. Robustness of the estimated unstructured correlation matrix was assessed using generalized estimating equations methodology (GEE; Zeger and Liang, 1986). This technique produces appropriate estimates of 28 J.A. DiPietro et al. / Biological Psychology 69 (2005) 23–38 regression parameters and their variances (Diggle et al., 1994). Moreover, unlike repeatedmeasures analysis of variance procedures, GEE does not exclude subjects with missing data from the final model. There was only one missed visit (28 weeks) for any participant at any gestational week prior to the final one. However, a substantial number of women (33%) who delivered at term (i.e., 37–41 weeks) delivered before their scheduled 38th week visit. Parity (nulliparous versus all others) was evaluated as a covariate for all variables. Pearson correlations were used to examine intraindividual consistency in variables across gestation and determine relations between physiological measures and the psychological scale. Repeated measure analysis of variance (2 3) was implemented to compare pregnant to non-pregnant responses to the experimental stress manipulation (baseline, Stroop, and post-Stroop periods). HP and SCL were analyzed separately at each of the two sessions, yielding four analyses. Significance levels were based on Greenhouse–Geisser adjusted values. Additional analyses for psychosocial variables were conducted using t-tests (pregnant versus non-pregnant) and repeated measures analysis of variance (session 1– session 2) as appropriate. 2. Results 2.1. Change over gestation Means, standard deviations, and sample size for each measure are presented in Table 1. Note that although respiratory data were collected on all participants, there was significant artifact in a number of cases resulting in missing data. We believe this to be a function of both maternal body habitus during pregnancy and the semi-recumbent, partially lateral positioning during monitoring necessary to alleviate compression of the vena cava. Table 1 also presents the estimate, standard error, and robust Z scores from the GEE analysis. Mood disturbance increased over time from 20 to 38 weeks of pregnancy. However, analysis of individual items indicated that this was largely a result of increased feelings of confusion, stress, fatigue, and less vigor; significant changes in depression, tension or anger over gestation were not detected. Significant linear changes were found for all physiologic measures except respiratory period and HPV. SCL increased over time, while heart period and RSA declined. However, examination of the trend in HPV data and subsequent fitting of a quadratic model revealed a significant decline followed by an increase in slope, with a nadir between 28 and 32 weeks. Parity had a significant influence on mood disturbance and four of the five physiologic measures. Compared to parous women, nulliparous women showed less mood disturbance over time (b = .824, S.E. = .402, Z = 2.05, P < .05), higher HP (b = 35.18, S.E. = 12.74, Z = 2.76, P < .05), greater heart period variability (b = 6.23, S.E. = 2.66, Z = 2.34, P < .05) and elevated SCL (b = 1.11, S.E. = .519, Z = 2.14, P < .05). There was a trend towards higher RSA for nullipara (b = 6.80, S.E. = 3.91, Z = 1.74, P < .10) but no difference in respiratory period. Because nulliparous women were younger than parous women (M difference = 2.4 years; t(135) = 2.49, P < .05) and reported lower prepregnancy weight (M difference = 13 lb; t(135) = 2.49, P < .05) correlations between maternal age and prepregnancy weight were examined. Systematic relations were observed for age and J.A. DiPietro et al. / Biological Psychology 69 (2005) 23–38 29 Table 1 Maternal mood disturbance and physiological measures from 20 to 38 weeks gestation Mean S.D. n S.E. b Z Mood disturbance 20 weeks 24 weeks 28 weeks 32 weeks 36 weeks 38 weeks 5.02 5.86 5.78 6.82 7.13 6.76 2.61 3.51 3.55 3.92 3.57 3.61 137 137 136 137 136 90 .112 .017 6.53*** Heart period (ms)a 20 weeks 24 weeks 28 weeks 32 weeks 36 weeks 38 weeks 747.70 732.38 705.75 693.75 710.09 705.80 89.36 83.98 79.54 92.13 87.91 87.57 137 137 135 137 137 91 3.616 .344 10.51*** Heart period variability 20 weeks 43.54 24 weeks 42.35 28 weeks 39.27 32 weeks 38.29 36 weeks 42.35 38 weeks 43.56 17.90 18.21 26.89 15.62 17.67 18.13 136 137 135 137 137 91 2.849 .759 3.76b,* Skin conductance level (mS)a 20 weeks 7.29 24 weeks 7.39 28 weeks 7.94 32 weeks 7.27 36 weeks 8.75 38 weeks 8.76 3.49 3.59 3.67 3.38 4.17 4.31 137 137 135 133 137 90 .083 .017 4.90** 1.40 1.15 1.24 1.22 1.16 1.24 121 130 125 131 123 75 .001 .007 .20 31.55 23.96 23.61 19.44 27.93 27.93 121 130 125 131 123 75 .821 .209 3.93* a c Respiratory period (s) 20 weeks 24 weeks 28 weeks 32 weeks 36 weeks 38 weeks 4.31 4.17 4.36 4.13 4.29 4.34 c Respiratory sinus arrhythmia (ms) 20 weeks 45.45 24 weeks 40.12 28 weeks 35.72 32 weeks 32.78 36 weeks 38.15 38 weeks 37.68 a With the exception of 1 missed visit at 28 weeks, minor variations in sample size prior to 38 weeks reflect sporadic technical difficulties. b Result for quadratic model. c With the exception of 1 missed visit at 28 weeks, variations in sample size reflect difficulty in obtaining accurate respiration data. * P < .05. ** P < .01. *** P < .001. 30 J.A. DiPietro et al. / Biological Psychology 69 (2005) 23–38 Table 2 Intraindividual consistency in mood disturbance and heart period values during gestation Gestational week 20 20 24 28 32 36 38 24 .32 .81* .80* .77* .71* .63* 28 * .81* .78* .73* .66* 32 * .30 .36* .80* .70* .68* 36 * .38 .31* .45* .77* .67* 38 * .28 .37* .38* .63* .35* .37* .54* .45* .49* .73* Note: Values above the diagonal are within subject correlations for mood disturbance; values below the diagonal are for heart period. * P < .0001. weight with HP only, so two additional analyses were conducted controlling for these two attributes. Parity remained a significant factor for HP. 2.2. Intraindividual stability Tables 2–4 provide within-subject correlations over time. Each table includes intraindividual consistency data for two variables separated along the diagonal. For example, in Table 2 values above the diagonal reflect stability over time for mood disturbance; values below the diagonal reflect stability across the same gestational periods for HP. There was significant stability over time for all measures. Averaged r’s, in order of descending magnitude for the physiological measures, were HPV (r = .80), RSA (r = .78), HP (r = .74), SCL (r = .60), and RP (r = .38). Although average stability for psychological mood disturbance was among the lower values (r = .40), this still reflects a fairly high degree of consistency over time. 2.3. Associations between physiological and psychosocial measures Cross-sectional correlations computed between the mood disturbance measure and the five physiological values at each gestational week revealed no significant (P < .05) Table 3 Intraindividual consistency in heart period variability and skin conductance level values during gestation Gestational week 20 20 24 28 32 36 38 24 .86 .58* .66* .58* .53* .48* 28 * .66* .63* .57* .49* 32 * .83 .83* .74* .69* .55* 36 * .76 .82* .75* .69* .52* 38 * .81 .78* .84* .77* .79* .81* .80* .75* .80* .60* Note: Values above the diagonal are within subject correlations for heart period variability; values below the diagonal are for skin conductance. * P < .0001. J.A. DiPietro et al. / Biological Psychology 69 (2005) 23–38 31 Table 4 Intraindividual consistency in respiratory period and respiratory sinus arrhythmia values during gestation Gestational week 20 20 24 28 32 36 38 24 28 ** .43 .77** .84** .71** .82** .78** .74** .79** .76** .80** 32 ** .33 .41** .66** .84** .76** 36 * .27 .33** .56** .75** .77** 38 ** .34 .24* .53** .35** .38* .33* .36* .47** .36* .84** Note: Values above the diagonal are within subject correlations for respiratory period; values below the diagonal are for respiratory sinus arrhythmia. * P < .01. ** P < .0001. associations with the exception of significant, but small, associations with respiratory period (r = .21, P < .05) and heart period (r = .19, P < .05) at 32 weeks gestation only. Because 30 coefficients were computed, this is roughly the number of significant coefficients that would be expected by chance. 2.4. Effects of pregnancy 2.4.1. Responsiveness to experimental manipulation Maternal heart period and skin conductance values during the baseline, Stroop, and recovery periods are presented in Figs. 1 and 2. Respiratory period and RSA were not used in the analysis because the Stroop task required spoken responses, thereby artificially altering respiratory characteristics. Complete, artifact-free data were available for 135 pregnant women at the 24-week visit and 128 women at 36 weeks. Two non-pregnant women did not return for the second Stroop administration. The Stroop generated significant changes in HP (F(2,320) = 69.39, P < .0001 and F(2,302) = 39.31, P < .0001) and SCL (F(2,320) = 50.86, P < .0001 and F(2,304) = 71.40, P < .0001) at the first and second sessions, respectively. There were significant main effects for pregnancy for both measures, with lower HP (i.e., faster heart rate) during the entire procedure in pregnant women at each gestational period (F(1,160) = 24.47, P < .0001 at 24 weeks and F(1,151) = 7.48, P < .01 at 36 weeks) and higher SCL (F(1,160) = 38.22, P < .0001 at 24 weeks and F(1,152) = 16.38, P < .0001 at 36 weeks). Significant interactions between pregnant/non-pregnant condition and changes during the manipulation were detected for HP at both administrations (F(2,320) = 11.09, P < .0001 and F(2,302) = 9.55, P < .0001). The SCL interaction terms for pregnancy group during the manipulation were also significant at the first (F(2,320) = 7.90, P < .0001) and second (F(2,304) = 54.78, P < .0001) sessions. Examination of Figs. 1 and 2 reveals dampened HP and SCL responsiveness for the pregnant as compared to the non-pregnant group at both sessions. Because the significant interactions alone do not provide specific information on the periods during which differences were manifest, post-hoc 2 2 repeated measures analyses for reactivity (baseline to Stroop) and recovery (Stroop to post-Stroop) segments were conducted for both HP and SCL at each session. Results indicate significant or near 32 J.A. DiPietro et al. / Biological Psychology 69 (2005) 23–38 Fig. 1. Heart period response to the 24-week/first (a) and 36-week/second (b) administrations of the Stroop colorword task by pregnant and non-pregnant women. significant (for two comparisons, P = .06) pregnancy by period interaction terms, indicating both increased reactivity to and recovery from the stressor by the non-pregnant group. Sociodemographic differences were detected between the samples of pregnant and nonpregnant participants. Pregnant participants were younger (t(162) = 2.11, P < .05) and better educated (t(162) = 2.80, P < .01) than their non-pregnant counterparts. These characteristics were subsequently examined as potential covariates in each physiological analysis. Neither was identified as having significant impact on these findings. J.A. DiPietro et al. / Biological Psychology 69 (2005) 23–38 33 Fig. 2. Skin conductance level response to the 24-week/first (a) and 36-week/second (b) administration of the Stroop color-word task by pregnant and non-pregnant women. Pregnant women perceived the Stroop to be more difficult than non-pregnant women at both the first (M = 3.3 versus 2.6, t(158) = 4.03, P < .0001) and second (M = 3.4 versus 2.6, t(158) = 4.90, P < .0001) administrations although the observer did not rate either group of women as appearing to find the task more stressful at either session. There was no difference in performance, as measured by the length of time (s) it took to complete the stimuli at either visit (M = 237 versus 233 and M = 217 versus 210). Both groups of women became more proficient at the second administration (F(1,153) = 85.39, P < .0001) but the degree of improvement did not differ between groups. Maternal 34 J.A. DiPietro et al. / Biological Psychology 69 (2005) 23–38 age and education were unrelated to maternal perception of difficulty; however, more educated women completed the task in less time (r(160) = .20 and r(155) = .21, P’s < .05). Because maternal education was higher in the pregnant group, analysis of covariance was conducted to determine whether this masked detection of a pregnancy effect on performance, but it did not. 2.4.2. Psychological measure Non-pregnant women also rated the seven psychological items that were summed into a mood disturbance variable. There was a trend for pregnant women during the 24th week to indicate greater mood disturbance than non-pregnant women at their first visit (M = 5.9, S.D. = 3.5 versus M = 4.6, S.D. = 1.8, t(162) = 1.88, P = .06) but by 36 weeks this was no longer significant (M = 7.1, S.D. = 3.6 versus M = 6.9, S.D. = 4.8). There was no association between maternal age or education and this measure. 3. Discussion Maternal psychophysiological functioning is affected by circumstances in women’s lives that alter the neuroendocrine milieu, including menstrual cycle phase (Sita and Miller, 1996), oral contraception use (Kirschbaum et al., 1999), and breastfeeding (Mezzacappa et al., 2001). Results of this study confirm that pregnancy and pregnancy stage also affects multiple aspects of functioning. Observed changes in heart period and variability were expected based on the substantial body of literature comparing cardiovascular parameters in pregnant and non-pregnant studies. However, because most of those studies were based on cross-sectional comparisons, the current data provide a more systematic view of the changes to these aspects of cardiac functioning over the course of pregnancy. Similarly, although reductions in the frequency components of heart period variability during pregnancy have been demonstrated previously, to our knowledge this is the first study to quantify RSA during pregnancy and document its decline during the second half of pregnancy. We believe this is also the first report of electrodermal activity during pregnancy. Skin conductance increased linearly from 20 weeks to term, and baseline skin conductance in pregnant women was approximately twice that of non-pregnant women. The extent to which the central mechanism is mediated by peripheral changes of pregnancy, such as increased blood volume or vasodilation within the skin, remains unknown. However, evidence provided by another study that directly measured sympathetic activity by recording post-ganglionic muscle discharge from the peroneal nerve suggests that the change in electrodermal activity is not a function of local effects. Controlling for activity at the level of the skin, single unit nerve activity was twice as high in pregnant women monitored at 35 weeks gestation than in non-pregnant women (Greenwood et al., 2001). We do not have a ready answer for the pervasive effect of parity on physiologic measures given the lack of prior data. Two studies that explicitly tested for parity differences in heart rate failed to detect it (Clapp and Capeless, 1997; van Oppen et al., 1996) although smaller sample sizes may have limited power. The higher degree of J.A. DiPietro et al. / Biological Psychology 69 (2005) 23–38 35 electrodermal activity is consistent with the higher levels of cortisol in nulliparous women (Vleugels et al., 1986); corresponding elevation in RSA may suggest a generalized autonomic activating role of the HPA axis. The observed elevation of maternal mood disturbance in multiparous women may be physiologically mediated; if so, the lack of correlation between this scale and autonomic variables indicate that such mediation is generated by physiological processes other than those measured here. On a psychological level, multiparous women likely experience greater role strain as they juggle demands of work, pregnancy, and existing children. Support for this is provided by a report that nulliparous women decrease physical activity during pregnancy, as measured by pedometers, but multiparous women do not (Ogita et al., 1989). It is also possible that changes resulting from any one pregnancy may not be entirely reversed after delivery, such that some degree of adjustment may be permanent after each pregnancy. The pattern of results observed in this study indicates that pregnancy is marked by greater sympathetic and reduced parasympathetic modulation. These conclusions have been supported by others using different methodologies and measures (Greenwood et al., 2001; Yang et al., 2000). Moreover, we show that these patterns of autonomic activation increase linearly as pregnancy advances, with the exception of HRV, which decreases in the third trimester and then increases through term. Measurement in this study did not commence until midway through gestation, commensurate with our ability to monitor the fetus, thus we are unable to determine the point in pregnancy at which these changes begin. However, three other studies that applied a longitudinal approach to the investigation of hemodynamics from early in pregnancy show that changes in heart rate, blood pressure, and other aspects of cardiovascular function begin early in the first trimester (Clapp and Capeless, 1997; Rang et al., 2004; van Oppen et al., 1996). These changes in hemodynamic parameters likely accommodate the marked increase in blood volume in pregnancy, allowing greater capacitance of the vascular tree and maintenance of blood pressure in the normal or even low range. In addition to changes during gestation, we also showed fairly remarkable levels of intraindividual stability within these measures. The average correlation across the second half of pregnancy for HP, HPV and RSA ranged from r = .74–.80. The values for skin conductance were somewhat lower (r = .60). On a conceptual level, this suggests that these measures reflect a stable characteristic of individual pregnancies. From a methodological perspective, these findings suggest that study results based on measurement of these variables at any point during the second half of gestation may be generalized to the remainder of this period. Thus, when it comes to assessment of maternal HP, HPV, RSA, and to a lesser extent, SCL, once may be enough. Of course, it remains possible that the interaction between these measures and others changes during this period of gestation. Results also support the pregnancy buffering hypothesis. Non-pregnant women showed significantly greater cardiac and electrodermal responses to the Stroop stressor at both administrations. Although pregnant women perceived the Stroop to be more difficult, their performance did not differ from non-pregnant women. Several reports suggest that pregnancy interferes with performance on some, but not all, information processing and memory tasks, particularly during the last trimester (de Groot et al., 2003; Janes et al., 1999; Keenan et al., 1998); however we did not find evidence to support a deleterious effect of pregnancy. The disassociation between pregnant women’s perception of difficulty of the 36 J.A. DiPietro et al. / Biological Psychology 69 (2005) 23–38 task, without a corresponding reduction in performance may suggest that either more effort is required to maintain attention during pregnancy or pregnant women underestimate their mental abilities. The latter is consistent with a report that pregnant women’s perception of their own memory deficits are in excess of any actual performance decrements (Casey et al., 1999). In the current study, of all the items assessed within the mood disturbance scale, women’s report of increasing feelings of confusion as pregnancy advanced showed the strongest trend over time. The functional significance of stress buffering in pregnancy remains unknown. Observations of similar circumstances in other species, including reduced fearfulness to normally distressing situations, are considered to be an adaptive mechanism to protect the fetus and pregnancy from harm (Vierin and Bouissou, 2001). A report of hyporesponsivity in pregnant women in another biological system, audition (Sennaroglu and Belgin, 2001) adds another dimension to this issue and raises the possibility that diminished reactivity during pregnancy may prepare women for the demands of early infant care. Nonetheless, the broader findings from this study indicate that overall sympathetic arousal increases, not decreases, during gestation and that parasympathetic tone lessens. Based on prevailing conceptualization of the orthogonal nature of autonomic control and space (Bernston et al., 1991), we do not conclude that these are merely reciprocal effects, but rather represent dual processes of activation. Heightened baseline sympathetic tone may have a paradoxical effect on the ability of intense environmental stimuli to further arouse while withdrawal of parasympathetic innervation may alter the threshold for responsiveness to threats that are specific to pregnancy. These speculations await confirmation by more targeted investigation into the response capabilities and characteristics that are mediated by pregnancy. Acknowledgements This research was supported by grant R01 HD27592, National Institute of Child Health and Human Development, awarded to the first author. We are grateful for the diligent and generous participation of the women in this study, without which this research would not have been possible. 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