On one hand, fetal
neurobehavioral patterns have been considered
indicators of nervous system development. On
the other hand, the capacity of
four-dimensional sonography to evaluate
complex facial expressions allows recognition
of common behaviors with which one can
appreciate the prenatal functionnal
development of the central nervous system.
Using yawning as an example, we review this
interpretation on the basis of knowledge
derived from phylogeny and ontogeny.
As a flip-flop switch,
the reciprocal interactions between sleep-
and wake-promoting brain regions allow the
emergence of distinct states of arousal. By
its ontogenical links with REM sleep, yawning
appears as a behavior which causes an arousal
reinforcement through the powerful stretch
and the neuromuscular connections induced.
Yawning indicates a harmonious progress in
the development of both the brainstem and the
peripheral neuromuscular function, testifying
to the induction of an ultradian rhythm of
vigilance. The lack of fetal yawn, frequently
associated with lack of swallowing,
associated or not with retrognathia, may be a
key to predict a brainstem's dysfunction
Medical sonography is a medical
imaging modality used across many medical
disciplines. Its use is growing, probably due
to its relative low cost and easy
accessibility. There are now many high
quality ultrasound imaging systems available
that are easily transportable, making it a
diagnostic tool amenable for bedside and
office scanning. This book includes
applications of sonography that can be used
across a number of medical disciplines
including radiology, thoracic medicine,
urology, rheumatology, obstetrics and fetal
medicine and neurology. The book revisits
established applications in medical
sonography such as biliary, testicular and
breast sonography and sonography in early
pregnancy, and also outlines some interesting
new and advanced applications of
General movements are
part of the spontaneous movement repertoire
and are present from early fetal life. Prior
to the seventies, self-perception by the
mothers was the only testimony of this fetal
motor activity. The advent of ultrasound
technology in the 1970s enabled live,
unobtrusive observations of fetal behaviors
in humans, vastly increasing our knowledge of
many others more subtle motor activity
(swallowing, respiratory movements, smiling,
hiccup) and thus of the human fetal
development. Our understanding of the orderly
and sequential fetal behavioral's development
increased substantly, leading to a greater
appreciation of the embryologic and
developmental anatomy. The introduction of
four-dimensional ultrasound (4D-US) has led
to very important conclusions concerning
fetal behavior milestones (Kurjak and
Azumendi, 2007). The development of oral
sensorimotor function and swallowing
(essential for the survival) from the fetal
period through early infancy assess normal or
abnormal neurobehavioral development. While
the appreciation of theses functions takes a
long time, another daily behavior will can be
detected: yawning (Yan et al., 2006).
Curiously, little data has been published for
25 years and since the following was written
: "yawning is a universally well known, but
poorly understood"(Sepulveda and
Mangiamarchi, 1995) or "a rudimentary reflex,
appears to have at best an obscure purpose,
if any"(Egerman and Emerson, 1996). Although
remarkably little interest has been paid to
yawning in research, even though it is an
everyday phenomenon, we will discuss the
meaning of this behavior and how its
characterization can enhance neuro-behavioral
A popular belief
states that yawning is a response to elevated
CO2 or depressed O2 levels in the blood.
Provine and Tate (1987) found no support for
this hypothesis. Fetal yawning in amniotic
fluid (like a fish's yawn in water) also
speak data against any association between
oxygenation capacity and yawning.
With the significant
advances in the image quality, and resolution
of ultrasound, and now 3D and 4D technology,
the practice of ultrasound examination during
pregnancy steps forward from anatomical
examination to functional evaluation.
Recognition of fetal yawning helps to verify
the harmonious progress of brainstem
maturation, and on the other hand, to
appreciate the neural underpinnings of sleep
and arousal systems. An abnormality of yawn's
occurrence fosters an intensive research of
anemic fetuses (frequency amplified) or
brainstem dysfunction with or without
mandibular hypoplasia (frequency sparse or
null) (Prechtl, 1990). We hope and expect
that upcoming researchs complete the datas
Morisseau-Durand M. Brainstem dysfunction: a
possible neuroembryological pathogenesis of
isolated Pierre Robin sequence. Eur J Ped.
Society. Idiopathic congenital central
hypoventilation syndrome: diagnosis and
management. Am J Respir Crit Care Med
Almli CR, Ball RH,
Wheeler ME. Human fetal and neonatal
movements patterns: gender differences ans
fetal-to-neonatal continuity. Dev
Argiolas A, Melis MR.
The neuropharmacology of yawning. Eur J
Baenninger R. On
yawning and its functions. Psychonomic Bul
Blumberg MS, Luca DE.
A developmental and component analysis of
active sleep. Develop Psychobiol.
Briscoe J, Wilkinson
DG. Establishing neuronal circuitry: hox
genes make the connection. Genes Dev.
Cattaneo L, Chierici
E, Bianchi B et al. The localization of
facial moto impairment in sporadic
Möbius syndrom. Neurology.
Davis FC, Frank MG,
Heller HC. Ontogeny of Sleep and Circadian
Rhythms. In. Regulation of Sleep and
Circadian Rhythms. Turek, Fred. W. and Zee,
Phyllis C. eds. Marcel Dekker Inc. New York,
de Vries JI, Visser
GH, Prechtl HF. The emergence of fetal
behaviour. Early hum Dev. 1982;7(4):301-322
Dobzhansky T. Nothing
in biology makes sense except in the light of
evolution. The American Biology Teacher.
Egerman RS, Emerson
DS. Images in clinical medicine. A fetal
yawn. N Engl J Med.
Ezure K, Tanaka I.
Convergence of central respiratory and
locomotor rhythms onto single neurons of the
lateral reticular nucleus. Exp Brain Res.
Giganti F, Hayes MJ,
Akilesh MR et al. Yawning and behavioral
states in premature infants. Development
Graham A. The
development and evolution of the pharyngeal
arches. J Anat. 2001;199(Pt
Hata T, Kanemshi K,
Akiyama M et al. Real-time 3-D sonographic
observation of fetal facial expression. J
Obstet Gynecol Res
Jacob J, Guthrie S.
Facial visceromotor neurons display specific
rhombomere origin and axon pathfinding
behavior in the chick. J Neurosci.
Joseph R. Fetal Brain
Behavior and Cognitive Development.
Kinney HC, Brody BA,
Kloman As etal. Sequence of central nervous
system myelination in human infancy. J
Neuropathol Exp Neurol.
Kobayashi T, Good C,
Mamiya K, et al. Development of REM sleep
drive and clinicals implications. J Appl
Lumsden A. Rhombencephalic neural crest
segmentation is preserved throughout
craniofacial ontogeny. Development.
Kumar R, Macey PM, Woo
MA, et al. Diffusion tensor imaging
demonstrates brainstem and cerebellar
abnormalities in congenital central
hypoventilation syndrome. Pediatr Res.
Kurjak A, Stanojevic
M, Azumendi G et al. The potential of four
dimensional (4D) ultrasonography in the
assessment of fetal awareness. J Perinat Med.
Kurjak A, Azumendi G.
The fetus in three dimensions. Imaging,
Embryology and fetoscopy. Informa healthcare.
London 2007. 520p.
Marder E, Rehm KJ.
Development of central pattern generating
circuits. Curr Opin Neurobiol.
Masuzaki H, Masuzaki
M. Color Doppler imaging of fetal yawning.
Ultrasound Obstet Gynecol.
Yanagihara T et al. Antenatal
three-dimensional sonographic features of
Pierre Robin Syndrome. Case report. Gynecol
May M, Schaitkin B,
Shapiro A: Facial nerve disorders in newborns
and children. In The Facial Nerve. Thieme
Medical Publishers 2000; 2nd
Pace-Schott EF, Hobson
A. The neurobiology of sleep: genetics,
cellular physiology and subcortcal networks.
Nature Rev Neurosci.
Petrikovsky BM, Kaplan
GP, Holsten N. Fetal yawning activity in
normal and high-risk fetuses: a preliminary
observation. Ultrasound Obstet Gynecol.
Qualitative changes of spontaneous movements
in fetus and preterm infant are a marker of
neurological dysfunction. Early Hum
Provine RR, Tate BC,
Geldmacher LL. Yawning: No effect of 3-5%
C02. 100% 02, and exercise. Behav Neural
Robinson SR, Blumberg
MS, Lane MS et al. Spontaneous motor activity
in fetal and infant rats is organized into
discrete multilimb boots. Behav Neurosci.
Wladimiroff JW, van Es A et al.
Classification and quantitative aspects of
fetal movements during the second half of
normal pregnancy. Early Hum Develop.
Rose RJ. Prenatal
programming of behavior: a twin study
perspective. Neurosci Biobehav Rev.
Santagati F, Rijli F.
Cranial neural crest and the building of the
vertebrate head. Nature Rev Neurosci.
Saper CB, Chou TC,
Scammell TE. The sleep switch: hypothalamic
control of sleep and wakefulness. Trends
Sarnat HB. Watershed
infarcts in the fetal and neonatal brainstem:
an aetiology of central hypoventilation,
dysphagia, micrognatia. Europ J Ped Neurol.
Mangiamarchi M. Fetal yawning. Ultrasound
Obstet Gynecol. 1995;5:(1):57-59.
Siegel JM. Sleep
phylogeny : clues to the evolution and
function of sleep. In Luppi PH ed. Sleep :
circuits and functions. Boca Raton CRC Press.
Valatx JL. The
ontogeny and physiology confirms the dual
nature of sleep states. Arch Ital Biol.
van Woerden EE, van
Geijin HP, Caron FJ et al. Fetal mouth
movements during behavioural states 1F and
2F. Europ J Obstet Gynecol Reprod Biol.
Volpe P, Gentile M.
Three dimensional diagnosis of Goldenhar
syndrome. Ultrasound Obstet Gyncol.
von Haeckel E.
Anthropogenie oder, Entwickelungs-geschichte
des menschen, Keimes und stammesgeschichte.
Leipzig : W. Engelmann ed. 1877:
Walusinski O, Deputte
B. The phylogeny, ethology and nosogeny of
yawning. Rev Neurol (Paris).
Walusinski O. Yawning:
from birth to senescence Psychol
Neuropsychiatr Vieil. 2006;4(1):39-46.
Wan H, Xu Y, Ikegami
M, et al. Foxa2 is required for transition to
air breathing at birth. Proc Natl Acad Sci U
S A. 2004;101(40):14449-14454.
Wragg LE, Smith JA,
Borden CS. Myoneural maturation and function
of the fetal rat tongue at the time of
secondary plate closure. Arch Oral Biol.
Yachnis AT. Cerebellar
and Brainstem Development: An Overview in
Relation to Joubert Syndrome. J Child Neurol.
Yan F, Dai SY, Akther
N, Kuno A, Yanagihara T, Hata T.
Four-dimensional sonographic assessment of
fetal facial expression early in the third
trimester. Int J Gynaecol Obstet.
Yigiter AB, Kavak ZN.
Normal standards of fetal behavior assessed
by four-dimensional sonography. J Matern
Fetal Neonatal Med.