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A Neural Explanation of Fetal Heart Rate Patterns: a Test of the Polyvagal

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A Neural Explanation of Fetal Heart Rate Patterns: a Test of the Polyvagal DEV (WILEJ) LEFT INTERACTIVE Shawn F. Reed University of Maryland College Park, MD 20742 A Neural Explanation of Fetal Gonen Ohel Rahav David Heart Rate Patterns: A Test of Poriya Hospital Tiberias, Israel the Polyvagal Theory Stephen W. Porges University of Maryland College Park, MD 20742 Received 11 March 1998; accepted 5 February 1999 ABSTRACT: The current study applies a neurophysiological model based on the Polyvagal Theory (Porges, 1995) to interpret fetal heart rate patterns. Beat-to-beat heart rate data from 7 fetuses monitored during the ®rst and second stages of labor were analyzed. Transitory heart rate accelerations and reduced beat-to-beat variability reliably preceded heart rate decelera- tions. The data are interpreted within the context of the Polyvagal Theory, which provides a plausible explanation of the neurophysiological mechanisms that mediate fetal heart rate de- celerations. Speci®cally, it is proposed that both the transitory heart rate accelerations and the depression of the respiratory rhythm in the beat-to-beat heart rate pattern re¯ect a withdrawal of the vagal tone determined by myelinated vagal pathways originating in the nucleus ambig- uus. Functionally, withdrawal of vagal tone originating in the nucleus ambiguus results in the cardiac pacemaker becoming vulnerable to sympathetic in¯uences and to the more-primitive unmyelinated vagal pathways originating in the dorsal motor nucleus of the vagus, which may contribute to clinically relevant bradycardia. ᭧ 1999 John Wiley & Sons, Inc. Dev Psychobiol 35: 108±118, 1999 Keywords: electronic fetal heart rate monitoring; heart rate variability; respiratory sinus ar- rhythmia; vagus Based upon clinical observations and limited experi- mechanisms mediating the speci®c features of the mental manipulations, speci®c features of the fetal heart rate patterns used in the clinical assessment of heart rate pattern have been accepted by the clinical the fetus. community as having diagnostic utility. Despite the The primary goal of fetal heart rate monitoring is the widespread acceptance of fetal heart rate monitoring, detection of fetal hypoxia at its earliest stage (Kruse, especially in high-risk pregnancies, there remains a 1982). Speci®c characteristics of the heart rate pattern limited understanding of the neurophysiological (i.e., early decelerations, variable decelerations, late de- celerations, beat-to-beat variability, tachycardia, brady- Correspondence to: Stephen W. Porges, Department of Human cardia, and sinusoidal patterns) have been identi®ed and Development/Institute for Child Study, 3304 Benjamin Bldg., Uni- proposed as re¯ections of the neurophysiological reg- versity of Maryland, College Park, MD 20742±1131. ulation of the heart and thus, as sensitive indices of fetal Contract grant sponsor: National Institute of Child Health and Human Development condition. However, because the features of the fetal Contract grant number: HD 22628 heart rate pattern are often unreliable diagnostic indi- short ᭧ 1999 John Wiley & Sons, Inc. CCC 1012-1630/99/020108-11 standard long DEV (WILEJ) RIGHT INTERACTIVE Fetal Heart Rate Patterns 109 cators, controversy still exists over the use and inter- 1990). This central respiratory rhythm is an emergent pretation of fetal heart rate monitoring. property of the brainstem with signi®cant contribu- Dif®culties in the diagnostic application of fetal tions from the interneuronal communication between heart rate monitoring may be due, in part, to uncertain the nucleus ambiguus and the nucleus of the solitary and contradictory neurophysiological explanations tract. The functional impact of the nucleus ambiguus (Goodlin & Haesslein, 1977; Rosen & Dickinson, vagal pathways on the sinoatrial node is to produce a 1993). For example, beat-to-beat variability is as- respiratory rhythm in the heart rate pattern. The am- sumed to be mediated by the vagus with high levels plitude of these rhythmic increases and decreases in of variability indicating fetal well-being (Kruse, 1982; heart rate (i.e., respiratory sinus arrhythmia, RSA) is, Paul, Suidan, Yeh, Schifrin, & Hon, 1975). However, thus, a valid indicator of vagal out¯ow from the nu- heart rate decelerations, indicators of fetal compro- cleus ambiguus. Even in the absence of actual mise, are assumed also to be mediated by the vagus. breathing, there are reports of beat-to-beat changes in The current article attempts to reconcile this para- fetal heart rate that track a rhythm similar to the spon- dox by interpreting fetal heart rate patterns within the taneous breathing of a neonate (Donchin, Caton, & context of the Polyvagal Theory (Porges, 1995, 1997). Porges, 1984; Groome, Mooney, Bentz, & Wilson, The Polyvagal Theory focuses on the phylogenetic 1994). changes in the functional neuroanatomy of the vagus and how these modi®cations are represented in the neural regulation of heart rate patterns. BRADYCARDIA Across vertebrate species, the control of cardiac func- THE NEUROPHYSIOLOGY OF tion exhibits a phylogenetic trend towards greater neu- MAMMALIAN HEART RATE PATTERNS ral involvement. The Polyvagal Theory (Porges, 1995) focuses on the speci®c phylogenetic changes in the The vagus, the 10th cranial nerve, conveys neural in- vagal efferents and the medullary nuclei from which ¯uences to the cardiac pacemaker (i.e., sinoatrial these pathways originate. Vagal efferent pathways node). The release of acetylcholine on the sinoatrial originate in two medullary nuclei, the nucleus ambig- node of the heart, triggered by vagal activity, not only uus and the dorsal motor nucleus of the vagus. Ac- inhibits cardiac pacemaker activity but also attenuates cording to the theory, because these two vagal systems sympathetic in¯uences on the heart (Levy, 1984; Van- have different phylogenetic and embryologic origins, houtte & Levy, 1979). Therefore, heart rate slows with they have different and potentially contradictory re- increases in vagal tone and heart rate speeds with de- sponse strategies when challenged. The unmyelinated creases in vagal tone. Vagal output to the heart origi- vagal ®bers that originate in the dorsal motor nucleus nates in two brainstem nuclei, the dorsal motor nucleus of the vagus evolved before the myelinated vagal ®- of the vagus and the nucleus ambiguus. Vagal pathways bers of the nucleus ambiguus. The dorsal motor vagal originating in both nuclei are capable of producing heart system evolved as a passive avoidance system and re- rate decelerations (Jones, Wang, & Jordan, 1995). The sponds to environmental challenges by sending inhib- vagal ®bers originating in the dorsal motor nucleus of itory impulses to the heart, which reduces cardiac out- the vagus are unmyelinated. During most states, the un- put in an effort to conserve metabolic resources. In myelinated vagal ®bers have little in¯uence on heart reptiles, the dorsal motor vagal system is the predom- rate levels (Ford, Bennett, Kidd, & McWilliam, 1990; inant vagal system in the regulation of cardiopulmo- Jones et al., 1995) and exhibit little or no spontaneous nary processes. This system promotes apnea and activity or variability (Ford et al., 1990). In contrast, the bradycardia by constricting the bronchi and by inhib- vagal ®bers originating in the nucleus ambiguus are my- iting the cardiac pacemaker. These physiological re- elinated, in¯uence both heart rate level and beat-to-beat sponses are neurophysiologically consistent with the variability (McAllen & Spyer, 1978), and maintain commonly observed reptilian avoidance strategies of tonic in¯uence over the heart. submerging or immobilizing. In mammals, the nucleus ambiguus vagal system is the predominant vagal sys- tem in the regulation of cardiopulmonary processes. RESPIRATORY SINUS ARRHYTHMIA IN This phylogenetically more-recent system has myeli- THE FETUS nated vagal ®bers that enable a rapid and dynamic reg- ulation of cardiac output via transitory increases and The vagal efferent ®bers originating in the nucleus am- decreases in tonic vagal output to the heart. Although short biguus have a respiratory rhythm (Richter & Spyer, both nuclei are capable of slowing heart rate in mam- standard long DEV (WILEJ) LEFT INTERACTIVE 110 Reed et al. mals, stimulation of vagal ®bers originating in the dor- may produce clinically signi®cant bradycardia. Two sal motor nucleus of the vagus has been proven inef- neurophysiological factors contribute to this possibil- fective in producing large bradycardia (Jones et al., ity. First, nucleus ambiguus vagal tone may protect the 1995). pacemaker from the in¯uence of ®bers originating in Research examining the relative in¯uence of dorsal the dorsal motor nucleus. Thus, removal of nucleus motor nucleus vagal ®bers in promoting the clinically ambiguus vagal tone would create a vulnerability of relevant bradycardia observed in fetal distress is not the pacemaker to the cholinergic in¯uences of the va- conclusive at this time (Hopkins, Bieger, de Vente, & gal ®bers originating in the dorsal motor nucleus. Sec- Steinbusch, 1996). However, it is possible that hy- ond, because hypoxia potentiates cholinergic action on poxia itself potentiates the cardioinhibitory actions of the pacemaker, stimulation of only a few vagal ®bers vagal ®bers on the sinoatrial node. Potter and Mc- during hypoxic states might be suf®cient to produce Closkey (1986) report a feedback system between du- massive bradycardia. Potter and McCloskey (1986) ration of hypoxia and vagal efferent discharge, which demonstrated that during progressive asphyxic hy-
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