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Neonatal Feeding Behavior As A Complex Dynamical System
Neonatal Feeding Behavior As A Complex Dynamical System
Dynamical System
Eugene C. Goldfield, Ph.D.,1 Jennifer Perez, M.S., CCC-SLP,2 and
Katherine Engstler, M.A., CCC-SLP2
ABSTRACT
Learning Outcomes: As a result of this activity, the reader will be able to (1) describe how a dynamical
systems perspective may be used to assess when to initiate oral feeding in preterm neonates; (2) define a
synergy, and describe how it informs sucking and respiration behavior; and (3) describe the role of the
caregiver as part of a complex system.
1
Department of Psychiatry, Harvard Medical School, Bos- Pediatric Dysphagia; Guest Editor, Gilson J. Capilouto,
ton, Massachusetts; 2Feeding and Swallowing Program, Ph.D., CCC-SLP, ASHA Fellow.
Boston Children’s Hospital, Boston, Massachusetts. Semin Speech Lang 2017;38:77–86. Copyright # 2017
Address for correspondence: Eugene C. Goldfield, Ph. by Thieme Medical Publishers, Inc., 333 Seventh Avenue,
D., Boston Children’s Hospital, 300 Longwood Avenue, New York, NY 10001, USA. Tel: +1(212) 584-4662.
Pavilion 159, Boston, MA 02115 DOI: http://dx.doi.org/10.1055/s-0037-1599105.
(e-mail: eugene.goldfield@childrens.harvard.edu). ISSN 0734-0478.
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78 SEMINARS IN SPEECH AND LANGUAGE/VOLUME 38, NUMBER 2 2017
new theoretical foundations and methodologi- bestiary of underlying “attractors,” each with
cal tools for characterizing not only the anatomy a unique signature dynamics revealed in
and physiology of oropharyngeal structures, but measurements of neonatal behavior during
also how they are organized for the swallowing sucking, breathing, and swallowing.
function.1 The elegant architecture of the hun- 2. The nervous system controls the oropharyn-
dreds of muscles of the hydrostatic tongue and geal and respiratory anatomy not simply by
the muscles of the pharynx, lungs, and inter- activating individual muscles, but rather by
costals constitute hundreds of controllable de- collecting muscles and elastic tissue into
grees of freedom. Moreover, the ability of the functional groupings, or synergies, so that
pharyngeal anatomy to change its shape for adjustments in one part of the system are
different functions presents the newborn with automatically compensated in other parts.
the remarkable challenge of using the same The same parts of the system may be used in
anatomy in different ways for breathing, swal- different ways for different functions and so
lowing, and vocalizing. To do so requires rapid must rapidly assemble for one function (say,
transitions in the organization of these muscles vegetative breathing), dissolve that organi-
newborn’s behavior. At the breast, nature pro- bation.19 This kind of experiment reveals the
vides newborns with an exquisitely tuned organ signature characteristic of a synergy: it is a
for feeding. Newborns actively look, touch, and cooperative organization of weakly coupled
taste breast milk during breast-feeding. The parts. What does the nervous system contribute
context of breast-feeding makes information to the formation and dissolution of synergies?
available for the guided discovery of how to A dramatic demonstration that muscle
regulate sucking and swallowing milk while synergies are encoded in the nervous system
maintaining vegetative breathing. Indeed, dur- comes from a series of studies by Overduin et
ing bottle-feeding, the challenge for a caregiver al,20,21 who applied long-duration electrical
is to try to emulate nature by observing the intracortical microstimulation (ICMS) to mo-
neonate to make some of the same kinds of tor areas in two awake monkeys and simulta-
postural and timing adjustments apparent dur- neously recorded muscle electromyography
ing breast-feeding. Clinicians and engineers (EMG) and finger movements. Overduin et
have sought to use computer-controlled devices al found that ICMS drives the hand and digits
to emulate the breast, but the realization of such toward particular postures at each stimulation
organization of the tongue and pharynx may pharynx on its journey to the upper esophageal
also serve the function of a positive displace- sphincter. Deglutition proper involves muscles
ment pump. However, unlike the heart, a pump controlling retrusion and protrusion of the
dedicated to circulating blood, a pump for tongue, contraction of palatal muscles, vocal
ingesting liquid and solid nutrients must be cord adduction, and contraction of the pharyn-
rapidly assembled and dissolved to allow the geal constrictors.27 Neonatal feeding, then, may
pharynx to switch between the multiple func- be made possible by the weak coupling of
tions of deglutition, vegetative breathing, and respiratory and suck-swallowing attractors,
speaking. How do the tongue and pharynx act and dysphagia may be a disorder of synergy
together to become a pumper during neonatal formation and dissolution.
feeding? The familiar pattern of neonatal suck-
ling may be thought of as the formation and
dissolution of a pumper for deglutition: the Consortia
coordination between oral, labial, mandibular, A dynamical systems approach places particular
and lingual-pharyngeal muscles draws milk into emphasis on the newborn as part of a consor-
introduce thickened liquids. In each case, the process that mature convergently, but not nec-
concepts from a dynamical systems perspective essarily synchronously.40 Sucking and swallow-
place individual behaviors in a broader context. ing are a highly linked and softly assembled
synergy. Modifications to the kinematics of
sucking enable greater stability within the
When to Initiate Oral Feeds physiology of the pharyngeal swallow, facilitat-
In the decades since the 1997 articles on ing safe bolus passage.41 Providing small
neonatal feeding that appeared in this journal, amounts of breast milk or formula on a pacifier
the controversy over when to initiate oral feeds or finger promotes exploration of milk or
has been informed by a greater appreciation for formula taste, a means for establishing infor-
feeding complexity (i.e., an expanding of the mational coupling to guide sucking.42
range of variables that may be used to make Consistent with a dynamical systems
diagnostic judgments). Rather than simply fo- view, there are now subjective diagnostic
cusing on gestational age or on the expected age assessment tools that describe physiological
at which coordination between sucking and and behavioral parameters of “infant-driven,”
oral feedings while newborns are being sup- line respiratory disease, considering that flow
ported by CPAP or HFNC. rate required may serve as a proxy for severity of
The robustness of a complex system is an illness. Second is the manner by which in-
indication of its ability to maintain functionality creased pressure force from nCPAP or
despite internal and external perturbations. As HFO2-NC may impact (1) swallow function,
one illustration, neural circuits are robust be- (2) airway protection from above, and (3) risk of
cause they maintain target performance despite bolus misdirection resulting in aspiration.51
ongoing neuron channel and receptor turn- Because the majority of newborns who aspirate
over.47 In the context of attractor dynamics, during the swallow do so silently,52 to reliably
robustness refers to the way that a system may assess the impact of HFO2-NC or nCPAP on
either return to its current attractor or move to a swallow function, instrumental assessment
new one that maintains a system’s functions. would be indicated. Conversely, it is also worth
Consider the respiratory pattern of a newborn considering if the neonate’s lung capacity may
during quiet sleep, apparently governed by a be improved on HFO2-NC or nCPAP, may
limit-cycle attractor with a characteristic signa- make the newborn better able to tolerate respi-
Oral Feedings and Consortia dynamical system. In the near future, we can
If a newborn exhibits oropharyngeal dysphagia expect vast amounts of new data on interactions
on videofluoroscopy that does not improve with between developing neonate, microbiome,
the use of therapeutic feeding interventions such caregiver, and environment to guide evidence-
as slow flow nipples, side-lying position, and based practice. But unless practitioners are able
pacing, then thickened liquids may be consid- to integrate these “big data” into their daily
ered a treatment option. The use of thickened decision making, progress in therapeutic inter-
liquids in pediatrics to treat dysphagia, and ventions will not be effectively translated to the
particularly with neonates, remains controver- clinic.
sial. A new direction for evaluating the potential
negative effects of thickening agents is to iden-
DISCLOSURES
tify their effects on the community structure of
Eugene C. Goldfield receives salary from
the neonatal gut microbiome.57 In this approach,
Boston Children’s Hospital and from the
deviations from normal microbiota development
Wyss Institute.
may be used as a measure of risk assessment for
40. Thoyre S. Developmental transition from gavage to feeding. National Association of Neonatal
oral feeding in the preterm infant. In: Miles M, Therapists; 2014
Holditch-Davis D, eds. Annual Review of Nursing 51. Dodrill P, Gosa M, Thoyre S, et al. First do no
Research. New York, NY: Springer; 2003:61–92 harm: a response to “Oral alimentation in neona-
41. McGrattan KE, Sivalingam M, Hasenstab KA, tal and adult populations requiring high-flow
Wei L, Jadcherla SR. The physiologic coupling oxygen via nasal cannula.”. Dysphagia 2016;
of sucking and swallowing coordination provides a 31(6):781–782
unique process for neonatal survival. Acta Paediatr 52. Uhm KE, Yi SH, Chang HJ, Cheon HJ, Kwon JY.
2016;105(7):790–797 Videofluoroscopic swallowing study findings in
42. Ross ES, Browne JV. Developmental progression full-term and preterm infants with dysphagia.
of feeding skills: an approach to supporting feeding Ann Rehabil Med 2013;37(2):175–182
in preterm infants. Semin Neonatol 2002;7(6): 53. Arvedson J, Lefton-Greif M. Instrumental assess-
469–475 ment of pediatric dysphagia. Semin Speech Lang
43. Thoyre SM, Shaker CS, Pridham KF. The early 2017;38(2):135–146
feeding skills assessment for preterm infants. Neo- 54. Cichero J, Nicholson T, Dodrill P. Liquid barium
natal Netw 2005;24(3):7–16 is not representative of infant formula: characteri-
44. Ross ES, Philbin MK. Supporting oral feeding in sation of rheological and material properties. Dys-