واکنش پذیری های فیزیولوژیکی زنان باردار به وحشت زدگی برانگیخته جنین

Abstract Objective The bidirectional nature of mother–child interaction is widely acknowledged during infancy and childhood. Prevailing models during pregnancy focus on unidirectional influences exerted by the pregnant woman on the developing fetus. Prior work has indicated that the fetus also affects the pregnant woman. Our objective was to determine whether a maternal psychophysiological response to stimulation of the fetus could be isolated. Methods Using a longitudinal design, an airborne auditory stimulus was used to elicit a fetal heart rate and motor response at 24 (n = 47) and 36 weeks (n = 45) of gestation. Women were blind to condition (stimulus versus sham). Maternal parameters included cardiac (heart rate) and electrodermal (skin conductance) responses. Multilevel modeling of repeated measures with 5 data points per second was used to examine fetal and maternal responses. Results As expected, compared to a sham condition, the stimulus generated a fetal motor response at both gestational ages, consistent with a mild fetal startle. Fetal stimulation was associated with significant, transient slowing of maternal heart rate coupled with increased skin conductance within 10 s of the stimulus at both gestational ages. Nulliparous women showed greater electrodermal responsiveness. The magnitude of the fetal motor response significantly corresponded to the maternal skin conductance response at 5, 10, 15, and 30 s following stimulation. Conclusion Elicited fetal movement exerts an independent influence on the maternal autonomic nervous system. This finding contributes to current models of the dyadic relationship during pregnancy between fetus and pregnant woman.

Introduction Initial developmental research into the maternal–child relationship was guided by the historical philosophical view of the child as a tabula rasa and children were primarily regarded as vessels upon which the environment, and most notably their parents, acted. A seminal paper by Bell [1] challenged the existing view of parent–child interaction as a unidirectional phenomenon leading to the now accepted view of the maternal–child relationship as dynamic and transactional. Temporally based associations between parent and offspring have been variously termed synchrony, mutual responsiveness, or attunement [2], [3], [4] and [5], and are core to understanding the development of regulatory processes within each partner. This research has identified such relations in behavioral domains that include affective and attentional processes, and have also been identified at the psychophysiological level. There is currently great interest in the manner in which the prenatal period sets the stage for later life [6], [7], [8] and [9]. Prevailing models focus on the downstream effects of psychological, environmental, and physiological influences that flow from the pregnant woman to the developing fetus [9], [10], [11] and [12]. Baseline levels of maternal psychological characteristics related to stress and anxiety [13], [14], [15] and [16] and products of the hypothalamic–pituitary–adrenal axis [17], [18] and [19] have been associated with fetal neurobehavior. Perhaps the most convincing evidence of a link between maternal psychological functioning and fetal neurobehavior has been generated from experimental designs in which maternal state is experimentally manipulated and effects on the fetus are observed. Both induced maternal stress [20], [21], [22], [23], [24] and [25] and relaxation [26] and [27] have been shown to affect fetal heart rate patterns and/or motor activity. While such findings are supportive of the role of the maternal context in affecting prenatal development, generally unacknowledged are the potential upstream effects, from fetus to pregnant woman, which may serve as potential regulators of subsequent maternal adaptation to pregnancy and child-rearing. The same neurobehavioral constructs that are central to infant and early childhood have been traditionally applied to fetal development [28] and [29], although measurement methodology is necessarily different. The prenatal and postnatal environments share little similarity, but the underlying capacities and neurological organization of the developing organism are essentially the same as the fetus adapts from intrauterine function to extrauterine life. It is also clear that the fetus, through its own behavior, plays an active role in epigenesis and ontogeny [30] and [31] as it interfaces with the characteristics of the intrauterine environment. Previously, in a sample of 137 maternal–fetal pairs assessed longitudinally during the second half of pregnancy, we demonstrated that spontaneous fetal motor activity transiently stimulates maternal sympathetic arousal [32] even though women perceive only a small proportion of fetal movements [33]. This association, which showed little change between the 20th and 38th weeks of gestation, was replicated in an additional sample of women (n = 195) from different sociodemographic and ethnic backgrounds [34]. These findings were based on second by second time series analyses of contemporaneous maternal–fetal recordings during undisturbed, baseline periods that were 50 min long. In both reports, spontaneous fetal movements were observed to generate an increase in maternal heart rate and electrodermal activity within 2–3 s at each of the six gestational periods studied. Initially, these analyses were not focused on detecting an effect from fetus to mother. Rather, dual data streams were empirically analyzed ± 100 s of origin without respect to the originating axis thereby allowing effects to emerge in either direction. From this process, we identified change in the fetus (i.e., in motor activity) to be the impetus for change in the pregnant woman. However, measurement under baseline conditions does not control for potential joint stimulation of both members of the dyad by uncontrolled sources. Here we use an experimental model in an effort to isolate a maternal response to an elicited fetal movement. Fetuses can detect and respond to sounds external to the uterine environment [35] and [36], thereby affording us the chance to stimulate the fetus independently of the woman and record any maternal response. The fetal response to the brief application of vibroacoustic or auditory stimulation has been well documented in academic literature as early as the 1930's [37]. Examples of vibroacoustic stimuli applied directly to the maternal abdomen have included those designed for obstetric purposes to stimulate a dormant fetus [38], [39], [40] and [41], an electronic artificial larynx [42] and [43], and other devices that emit vibrations [44] and [45]. In general, fetuses respond to initial applications of vibroacoustic stimuli with transient increases in fetal motor activity and heart rate, consistent with a startle response. The magnitude of the fetal response tends to be commensurate with the intensity of the stimulus. Thus, airborne auditory signals delivered above and not touching the maternal abdomen tend to elicit a less intense response, but are necessary to a design in which pregnant women must be blind to stimulus presentation. Airborne stimuli shown to elicit a fetal response include electronically generated signals of varying intensity and frequency [46], [47], [48] and [49], speech sounds [50], [51] and [52], and music [37] and [53]. We hypothesized that, as observed with spontaneous movements, elicited fetal movements would generate a transient maternal autonomic response as measured by heart rate, which includes both parasympathetic and sympathetic influences, and electrodermal activity, which is singly innervated by sympathetic processes [54]. Fetal sex and maternal parity were evaluated as potential moderators of either the fetal or maternal response based on the existing data indicating differential responsiveness of male fetuses to stimulation [40] and higher background electrodermal activity in nulliparous as compared to multiparous women [55].

Results Per design protocol, presentation of the stimulus/sham condition had to be delayed for an additional 3 minute period in 8 instances due to excessive fetal movement at 36 weeks; no cases required delayed protocol onset at 24 weeks. Fetal response to stimulation Mean pre-condition baseline values for fetal measures at each gestational age are presented in Table 1. Although mean values were not used in the data analyses, these are included to provide information on level and variation over gestation. No order effects (i.e., stimulus or sham first) were detected for either fetal motor activity (24 weeks: t = − 1.61, p = .11; 36 weeks: t = − 0.48, p = .64) or fetal heart rate response to stimulation (24 weeks: t = − 0.64, p = .53; 36 weeks: t = − 0.23, p = .82). Similarly, there were no differences in fetal motor activity (24 weeks: t = − 1.23, p = .23; 36 weeks: t = − 0.71, p = .48) or heart rate response (24 weeks: t = − 0.36, p = .72; 36 weeks: t = 0.82, p = .42) as a result of fetal sex. Order and fetal sex were not included in further analytic models. Table 1. Mean fetal and maternal 3-minute pre-condition baseline values by gestational age. 24 weeks (n = 47) 36 weeks (n = 45) Mean (sd) n a Mean (sd) n a t Fetal measures Heart rate (bpm) 146.68 (5.33) 47 140.01 (8.76) 45 − 4.63⁎ Motor activity (aus) 4.46 (1.11) 47 4.75 (2.01) 44 1.36 Maternal measures Heart rate (bpm) 78.19 (9.11) 45 81.07 (9.74) 44 3.47⁎ Skin conductance (μS) 5.46 (2.29) 44 6.47 (3.14) 42 0.93 Skin conductance response (μS) − 0.045 (0.04) 44 − 0.049 (0.05) 42 0.49 ⁎ p < .01. a Note. Minor variation in ns reflects variable-specific deletion of outliers or problematic signal. Table options The airborne stimulus was effective at generating the requisite fetal response. Fetuses reacted to the stimulus within 5 s after application, evidenced by a significant interaction effect for time by condition (i.e., stimulus v sham) predicting fetal motor activity. As a group, fetuses exhibited a transient increase in movement at both 24 weeks (β = .10, SE = .03, t = 3.02, p < .01) and 36 weeks of gestation (β = .12, SE = .03, t = 4.19, p < .01) to the stimulus but not to the sham. Fetuses also reacted with an acceleratory heart rate response to the stimulus in comparison to sham (β = .21, SE = .06, t = 3.54, p < .01) at 36 weeks but not at 24 weeks (β = − .04, SE = .04, t = − 1.05, p = .29). Maternal response to fetal stimulation Mean pre-condition baseline values for maternal measures at each visit are presented in Table 1. Note that skin conductance level is provided for contextual information; the de-trended skin conductance response variable was used for the remaining analyses. There were no order effects for presentation at either gestational age for either maternal heart rate (24 weeks: t = − 0.50, p = .63; 36 weeks: t = − 0.76, p = .45) or skin conductance response (24 weeks: t = 0.76, p = .45; 36 weeks: t = − 1.21, p = .23) to the stimulus condition. Fetal sex was also unrelated to maternal heart rate (24 weeks: t = 1.03, p = .31; 36 weeks: t = 0.02, p = .98) and skin conductance (24 weeks: t = 0.23, p = .82; 36 weeks: t = − 1.30, p = .20). Order and fetal sex were not included in further analytic models. The maternal cardiac and electrodermal responses following fetal stimulus and sham conditions are presented in Fig. 2a–d. Note that the figures provide data in seconds for clarity of viewing; analyses are based on 5 points per second. Maternal data were optimally modeled by quadratic change over time which captures the maternal reaction and recovery response. In contrast to the sham condition, the fetal stimulus condition induced significant suppression of maternal heart rate within 5 s after onset at 24 weeks of gestation (Fig. 2a, β = .24, SE = .12, t = 2.01, p < .05) and 36 weeks of gestation ( Fig. 2b, β = .27, SE = .12, t = 2.34, p < .05). This was accompanied by a significant increase in maternal skin conductance response within 10 s at 24 weeks ( Fig. 2c, β = − 0.001, SE = .001, t = − 2.17, p < .05) and 36 weeks ( Fig. 2d, β = − 0.002, SE = .001, t = − 2.07, p < .05) compared to the sham. Mean maternal heart rate and maternal skin conductance response 30s before and ... Fig. 2. Mean maternal heart rate and maternal skin conductance response 30 s before and 30 s following stimulus and sham conditions at 24 weeks (a, c) and 36 (b, d) weeks. Figure options Correlation coefficients computed on mean delta values for each maternal and fetal parameter did not detect any significant maternal–fetal associations at 24 weeks. At 36 weeks, greater fetal motor responses were associated with larger maternal skin conductance responses at 5, 10, 15, and 30 s after the stimulus (rs (42) = 0.48, 0.39, 0.36, and 0.42, respectively; ps range from p < .05 to p < .001). Significant or trend correlations were detected between the magnitude of the heart rate change in both mothers and fetuses (rs (44) = 0.29, 0.31, 0.31, and 0.26, respectively; ps range from p < .10 to p < .05). No significant associations between fetal movement and maternal heart rate responses, or fetal heart rate and maternal skin conductance responses were detected. Parity (1st child vs all others) was related to maternal responsiveness. Nulliparous women exhibited greater skin conductance responsiveness than multiparous women in response to the fetal stimulation compared to sham condition at both gestational ages, indicated by a significant interaction between parity and condition (24 weeks, β = .04, SE = .01, t = 4.32, p < .05, 25 nullipara, 22 multipara; 36 weeks, β = .16, SE = .01, t = 11.23, p < .05, 24 nullipara, 21 multipara). At 24 weeks, nulliparous women also showed greater heart rate suppression to fetal stimulation (β = − 1.33, SE = .31, t = − 4.27, p < .05). In contrast, at 36 weeks, multipara showed greater heart rate suppression to fetal stimulation (β = 1.53, SE = .30, t = 5.08, p < .05). Comparisons across gestational age Table 1 presents t-values that evaluate change in pre-condition baseline levels from 24 to 36 weeks. As expected, baseline fetal heart rate declined and maternal heart rate increased; the remaining measures did not change significantly. Modeling of delta values to the stimulation was used to ascertain whether the fetal and maternal responses were different over time. As expected, since there was a significant fetal heart rate response at 36 but not 24 weeks, the interaction between gestational age and fetal heart rate was significant (β = − 0.049, SE = .013, t = − 3.80, p < .01). Although a fetal motor response was observed at both gestational ages, interaction results indicated that the responses were somewhat different (β = 0.045, SE = .008, t = 5.39, p < .01). Specifically, the elevation in motor activity to the stimulus persisted for a longer duration at 24 weeks than at 36 weeks. Fig. 3a shows the maternal heart rate delta values to the fetal stimulus condition by gestational age. The suppression pattern observed for maternal heart rate did not change in magnitude over time (β = − 0.0008, SE = .001, t = − 0.79, p = .43). The maternal skin conductance response ( Fig. 3b) was greater at 36 weeks than at 24 weeks (β = 0.002, SE = .0001, t = 5.68, p < .01). Mean change (delta) in maternal heart rate (a) and skin conductance response (b) ... Fig. 3. Mean change (delta) in maternal heart rate (a) and skin conductance response (b) to fetal stimulus at each gestational age.