Infants born with CS delivery following a period of labor have a higher and more developed ANS tone compared to those born with CS without labor (Mulkey et al., 2019). J. Obstet. (2008). (2017). (2017). Gold et al. Neural crest cells also contribute to spleen development (Barlow-Anacker et al., 2017). Once born, newborns have to deal with the extrauterine environment that, especially for preterm babies, is constituted by the incubator. (2016). Assoc. Dev. For this reason, before birth neuroendocrine signaling (e.g., catecholamines, cortisol, thyroid hormones, and renin-angiotensin) surges, and SNS outflow from CAN (e.g., hypothalamus, cortical, and brainstem centers) greatly increases. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Fetal heart rate acceleration in response to light Stimulation s a clinical measure of fetal well-being. J. Anaesth. doi: 10.1111/j.1467-8624.2007.01099.x, DiPietro, J. Circadian variation of heart rate variability. 9:593889. doi: 10.3389/fped.2021.593889, Goldaber, K. G., Gilstrap, L. C., Leveno, K. J., Dax, J. S., and McIntire, D. D. (1991). Hill, M. A. Preterm newborns have an immature ANS, which has great repercussions on cardiac and respiratory functions (Mulkey and du Plessis, 2018). Gynecol. Obstet Gynecol. Assoc. The final exciting element in the mix is the exceptional advance in Machine Learning. Indeed, warm incubators tend to increase SNS tone and reduce PNS activity, whereas the opposite is true for incubators 2C colder than newborns' temperature (Franco et al., 2003; Stphan-Blanchard et al., 2013). Chronobiol. Psychopathol. (2020). Evidence for adverse effect of perinatal glucocorticoid use on the developing brain. 102, F183F187. Prenatal stress and its effects on the fetus and the child: possible underlying biological mechanisms, in Perinatal Programming of Neurodevelopment Advances in Neurobiology, ed M. C. Antonelli (New York, NY: Springer New York), 269283. Lancet Lond. 221, 383.e3392.e3. Fetal monitors are better at separating maternal and fetal heart rate. (2016). Obstet. Moreover, considering the role of the vagus nerve in the CAP, which involves immune cells such as macrophages (Borovikova et al., 2000; Tracey, 2007; Fairchild et al., 2010; Frasch et al., 2016), and the sex-related neurodevelopment impact of microglial functions (Hanamsagar and Bilbo, 2016), the different characteristics of the developmental pattern of vagus nerve between male and female fetuses could predispose for sex-specific susceptibility and outcomes in many neurodevelopmental disorders (Berntson and Cacioppo, 2004). Heart J. Clin. (2009). Some authors but not all have shown that a reduction in long-term variability occurs after sympathetic blockade.19-22 Fetal heart rate variability is more than the simple push-pull interactions between the inhibitory and acceleratory limbs of the autonomic nervous system. Decelerations were present when there was mild hypertension during the compression but they were also present when marked hypotension accompanied the compression. Anatomy and Physiology. Therefore, this hypothesis paper aims to review the development of ANS during fetal and perinatal life, focusing particularly on the vagus nerve, to identify possible critical windows that could impact its maturation. Ann. Computational experiments finally demonstrate that size attenuation results in the paradoxical . Am. Epidemiology 19, 851859. In practice, clinicians must integrate clinical data with electronic fetal monitoring patternsin order to project what is likely to happen and how quickly it might occur. doi: 10.3945/jn.109.116327, Christifano, D. N., Taylor, M. K., Carlson, S. E., Colombo, J., and Gustafson, K. M. (2020). Quantitative aspects. Bistoletti P, Lagercrantz H, Lunell NO. Ther. Care Med. Arch. The Dutch Hunger Winter and the developmental origins of health and disease. 30, 698707. J. Obstet. Maternal metabolic dysfunctions and dysbiosis can affect the systemic inflammatory response of the mother and the fetus (Hasain et al., 2020; Peterson et al., 2020). Gynecol. PLoS ONE 12:e0180167. Front. Obstet. Am J Obstet Gynecol. 2016 Sep 1;594(17):4711-25. Even early prenatal exposure to the virus, indeed, seems to create a chronic hypoxic environment to the fetus, affecting vagus nerve developmental patterns, and imprinting postnatally the ANS cardiac pacemaker activity (Herry et al., 2021). Moreover, preterm birth often involves invasive treatments (e.g., invasive respiratory support) or drugs that can stress even more the immature ANS. doi: 10.1016/j.jri.2018.01.004, Pryor, J. R., Maalouf, F. I., Krans, E. E., Schumacher, R. E., Cooper, W. O., and Patrick, S. W. (2017). Neurosci. Fletcher AJ, Gardner DS, Edwards CM, Fowden AL, Giussani DA. doi: 10.1016/j.jogc.2017.05.029, Jonas, W., Johansson, L. M., Nissen, E., Ejdebck, M., Ransj-Arvidson, A. 12, 354356. Rev. Semin. Gender differences in neurodevelopment and epigenetics. (2014). Moreover, through the production of corticotropin-releasing hormone (CRH), the placenta stimulates adrenocorticotropic hormone release in the anterior pituitary of the fetus, affecting both fetal HPA axis and amygdala development (Seckl and Meaney, 2004). (2021). During labor, especially in cases of prematurity, there are several conditions that can cause NEC: two of these are certainly hypoxia and acidemia (Sharma and Hudak, 2013). Comput. Pediatr. J. Obstet. We have shown how alterations in CAN activity and sensorimotor behaviors can give hints about the developing ANS function. Effects of intrapartum oxytocin administration and epidural analgesia on the concentration of plasma oxytocin and prolactin, in response to suckling during the second day postpartum. During labor, the recommended fetal heart rate assessment interval for auscultation is every A. doi: 10.18632/oncotarget.20110, Gordon, C. (2004). Perinatal hypoxia contributes significantly to the possibility of perinatal brain injury (Gotsch et al., 2007). (2017). 1984 Mar 1; 148(5):490-8. Fetal gut injury due to inflammation in a fetal sheep model of NEC etiology leaves a specific HRV signature and preterm neonates show abnormalities in HRV 13 days before clinical symptoms (Stone et al., 2013; Liu et al., 2016). Gut microbiota: the conductor in the orchestra of immuneneuroendocrine communication. Off. (2010). Alcohol. J. Reprod. Nurs. Although the ANS and vagus nerve activity appear to have an endogenous circadian rhythm (Hilton et al., 2000; Kentish et al., 2013), with a pacemaker system that regulates its behavior regardless of sleep-awake states (Malpas and Purdie, 1990; Hilton et al., 2000), a circadian variation pattern of vagal activity can be recorded via HR variations. Microbiol. Nutr. 63, 649656. Drugs Used to Manage the Timing of Delivery. J. Perinatol. 162, 3541. Human fetal lungs harbor a microbiome signature. Neonatology 112, 187192. doi: 10.1038/s41390-021-01460-3, Ray-Griffith, S. L., Wendel, M. P., Stowe, Z. N., and Magann, E. F. (2018). 84, 433439. 7 Chemoreceptors located in the brainstem are sensitive to low pH and elevated pCO2. Which intrinsic homeostatic response is the fetus demonstrating when abrupt variable decelerations are present? Recently, placenta calcifications samples collected at delivery have been speculated to act as a memory of prenatal maternal stress and diseases exposure, hence highlighting the potential role of placenta in regulating the offspring's future cardiovascular and metabolic health, even through the in utero modulation of the developing ANS (Wallingford et al., 2018). doi: 10.1016/j.semerg.2015.06.005, Gallup, A. C., Church, A. M., and Pelegrino, A. J. ), What do Braxton Hicks contractions feel like? Pulm. Biol. The placental microbiome varies in association with low birth weight in full-term neonates. BJOG Int. The dysregulation of placental functions can induce an insufficient intake of nutrients for the fetus, thus, especially during mid and late gestation, impairing the development of various brain areas, including the hypothalamus that seems to be particularly sensitive to the nutrient deficiency (Nugent and Bale, 2015). Prior studies have catalogued extensive molecular alterations associated with homeostatic scaling. 86: . Fetal growth and maternal exposure to particulate matter during pregnancy. The effect of labor and delivery mode on electrocortical and brainstem autonomic function during neonatal transition. Electromagnetic field coming from the incubator power influences the ANS as revealed by HRV analysis as LF/HF increases, whereas HF decreases (Bellieni et al., 2008). (2020). Am. Frasch, M. G., Baier, C. J., Antonelli, M. C., and Metz, G. A. S. (2018a). 130, 403407. Altered autonomic control of heart rate variability in the chronically (2016). At the beginning of the 2nd trimester, the cerebral cortex creates more and more sulci and gyri to increase its surface area and allow brain development. Res. 68, 173186. doi: 10.14814/phy2.13620, Harrison, N. A., Cooper, E., Voon, V., Miles, K., and Critchley, H. D. (2013). Rochester, NY: Social Science Research Network. Contributions of the maternal oral and gut microbiome to placental microbial colonization in overweight and obese pregnant women. doi: 10.1213/00000539-199012000-00018, Visser, G. H. A., Mulder, E. J. H., and Prechtl, H. F. R. (1992). Pregl. Fetal heart rates decelerated rapidly and well before sustained hypertension developed. 39, 769783. Occupational hazards and pregnancy outcomes. Maternal heart rate variability during the first stage of labor. Front. doi: 10.1002/ajim.4700210312, Zhang, X., Sliwowska, J. H., and Weinberg, J. The fetus is exposed to the lower intervillous oxygen levels only when the uterine contraction forces are sufficient to impede intramyometrial perfusion. 23, 117124. Around 89 WGA, it is possible to clearly record GMs (Prechtl, 1990). (2013). MgSO4, which is often administered between 23 and 27 WGA or intrapartum for its tocolytic effect to delay labor onset in pregnancy at risk for preterm birth (Ramsey and Rouse, 2001; Ingemarsson and Lamont, 2003), does not seem to show a significant change in fHRV (Stallworth et al., 1981; Nensi et al., 2014). Microbiome 4:29. doi: 10.1186/s40168-016-0172-3, Laursen, M. F., Bahl, M. I., Michaelsen, K. F., and Licht, T. R. (2017). Biol. Hormones, pregnancy, and autoimmune diseases. doi: 10.1097/GRF.0b013e31811ebef6, Grandjean, P., Murata, K., Budtz-Jrgensen, E., and Weihe, P. (2004). Curr. doi: 10.1007/s10803-020-04467-7. This increases the flow of deoxygenated blood to your heart and body, including your uterus and placenta. doi: 10.3109/14767058.2011.600370. 1983 Jan; 90(1):11-5. Natl. Am. There is no clarity on its usefulness in decreasing perinatal mortality or cerebral palsy when measured by a CTG which has been explained by the incorrect focus of EFM on prediction of acidemia, a poor correlate to fetal injury, instead of predicting fetal cardiovascular decompensation per se as well as the limitations of CTG technologies in capturing the short-term time scale fluctuations of HRV reflecting vagal modulations (Alfirevic et al., 2017; Frasch et al., 2017; Frasch, 2018; Gold and Frasch, 2021). Physiol. Neurosci. Early Hum. Front. Gynecol. doi: 10.1016/j.smrv.2018.03.004, Weber, A., and Harrison, T. M. (2019). Sci. All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Nevertheless, the presence of many confounding factors and the small sample sizes make unclear the mechanism of action of glucocorticoids on fHRV and consequently the impact on ANS development (Verdurmen et al., 2013). Monitoring fetal maturationobjectives, techniques and indices of autonomic function. Autonomic development in preterm infants is associated with morbidity of prematurity. IGF-1 receptor regulates upward firing rate homeostasis via the Engl. Table 2. Machine learning model on heart rate variability metrics identifies asymptomatic toddlers exposed to Zika virus during pregnancy. Autonomic responses to sighs in healthy infants and in victims of sudden infant death. Figure 1: Schematic outline of heart rate control mechanisms. Autonomic nervous system depression at term in neurologically normal premature infants. Crit. Heart rate variability in neonates of type 1 diabetic pregnancy. Placenta dysbiosis can be related to antepartum infections (Aagaard et al., 2014; Doyle et al., 2017; Pelzer et al., 2017), maternal nutrition (Aagaard et al., 2014), maternal weight gain (Antony et al., 2015; Zheng et al., 2015; Benny et al., 2019), gestational diabetes mellitus (Bassols et al., 2016; Pelzer et al., 2017), use of probiotics/antibiotics (Pelzer et al., 2017), and periodontal pathogens (Fischer et al., 2019), and can lead to several adverse outcomes, such as preeclampsia and chorioamnionitis (Amarasekara et al., 2015; Doyle et al., 2017; Fischer et al., 2019; Olaniyi et al., 2020). Ingemarsson, I., and Lamont, R. F. (2003). 662, 118134. 191, 217224. doi: 10.1515/jpm-2016-0414, Morris, G. S., Zhou, Q., Hegsted, M., and Keenan, M. J. doi: 10.1016/j.ajog.2019.04.029, Flenady, V., Ellwood, D., Bradford, B., Coory, M., Middleton, P., Gardener, G., et al. Therefore, the present paper aims to review the fetal and perinatal development by focusing on the development of the ANS and, in particular, of the vagus nerve to identify possible critical windows that could impact their maturation. Autonomic nervous system impairment, maybe through impaired cardiocirculatory and ventilatory regulation, can increase the risk of apparent life-threatening events or sudden infant death syndrome (SIDS) and, thus, of death in the first 612 months of postnatal life. Med. 36, 441468. doi: 10.1152/ajpregu.00120.2012, Hoyer, D., Schmidt, A., Gustafson, K. M., Lobmaier, S. M., Lakhno, I., van Leeuwen, P., et al. which intrinsic homeostatic response is the fetus demonstrating 10.7: Homeostasis and Feedback - Biology LibreTexts Arterial baroreceptors are sensitive to stretch or distension of a vessel caused by blood pressure changes. doi: 10.1017/S0954579417001730, Garzoni, L., Faure, C., and Frasch, M. G. (2013). Dev. The repetitive movements, with the consequent repetitive sensory afferents induced, produce habituation in the fetus, that is manifested also in fHR changes: the ANS trains to adapt the body systems' response to environmental stimuli, even through the movements (Lecanuet et al., 1992; Kisilevsky and Low, 1998). 37, 954967. Moreover, an impairment in vagal balance, particularly a decreased tone, might be implicated in depression, anxiety, post-traumatic stress disorder, and schizophrenia (Thayer and Brosschot, 2005). 6, 13-15 The parasympathetic component of the chemoreflex causes a rapid decrease in heart rate to lessen cardiac work and its oxygen need. Maternal pathologies influence the onset of altered neurodevelopment patterns during fetal life, which could lead to actual neurologic disorders during childhood (Faa et al., 2016; Vohr et al., 2017). (2017). On the other hand, the hypothalamic-pituitary-adrenals (HPA) axis and vagal activation become more finely tuned (Bystrova, 2009). doi: 10.1097/NNR.0b013e31824b02ad, Tong, L., and Kalish, B. T. (2020). 48, 829842. Exp. doi: 10.1016/B978-0-12-809468-6.00031-0, Prechtl, H. F. (1990). Transient loss of variability usually is associated with benign conditions like fetal sleep or maternal medications. N. Y. Acad. Methods Mol. The isolation of fetal homeostasis or of that of any other group of animals inhabiting a highly specialized environment, for example, desert-swellers, divers, or hibernators from homeostasis in general implies that there is something particular about the circumstances in which it is operating. 11:578898. doi: 10.3389/fphys.2020.578898, Keywords: fetal development, autonomic nervous system, vagus nerve, cholinergic anti-inflammatory pathway, heart rate variability, critical window, maternal health, Citation: Cerritelli F, Frasch MG, Antonelli MC, Viglione C, Vecchi S, Chiera M and Manzotti A (2021) A Review on the Vagus Nerve and Autonomic Nervous System During Fetal Development: Searching for Critical Windows.
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