Fetuses show various facial expressions, such as blinking, yawning, sucking, mouthing, tongue expulsion, scowling, and smiling, assessed by four-dimensional ultrasound from the early second trimester of pregnancy. Moreover, some fetuses demonstrate emotion-like behaviors as noted in infants, children, and adults. Selective fetal responses to stimuli indicate a high degree of brain development, which is reflected in the facial reactions. The fetal face with its movements and expressions can mirror the fetal brain function and development during different stages of the fetus in utero. The fetal face might represent the key to opening the box containing the secrets of fetal brain function and development. Four-dimensional ultrasound may be an important modality in current and future research on fetal facial expressions and assist in the evaluation of the fetal brain function.
The work reported in this paper was supported by a Grant-in-Aid for scientific Research on Innovative Areas “Constructive Developmental Science” (No.24119004) from The Ministry of Education, Culture, Sports, Science and Technology, Japan.
Conflict of interest: Authors state no conflict of interest.
Materials and methods: Informed consent: Informed consent has been obtained from all individuals included in this study.
Ethical approval: The research related to human subject use has complied with all the relevant national regulations, and institutional policies, and is in accordance with the tenets of the Helsinki Declaration, and has been approved by the authors’ institutional review board or equivalent committee.
 Prechtl HF. Qualitative changes of spontaneous movements in fetus and preterm infant are a marker of neurological dysfunction. Early Hum Dev. 1990;23:151–8.10.1016/0378-3782(90)90011-7Search in Google Scholar
 Prechtl HF. State of the art of a new functional assessment of the young nervous system: an early predictor of cerebral palsy. Early Hum Dev. 1997;50:1–11.10.1016/S0378-3782(97)00088-1Search in Google Scholar
 Kuno A, Akiyama M, Yamashiro C, Tanaka H, Yanagihara T, Hata T. Three-dimensional sonographic assessment of fetal behavior in the early second trimester of pregnancy. J Ultrasound Med. 2001;20:1271–5.10.7863/jum.2001.20.12.1271Search in Google Scholar PubMed
 Hata T, Kanenishi K, Hanaoka U, Marumo G. HDlive and 4D ultrasound in the assessment of fetal facial expressions. Donald School J Ultrasound Obstet Gynecol. 2015;9:44–50.10.5005/jp-journals-10009-1388Search in Google Scholar
 Kurjak A, Miskovic B, Stanojevic M, Amiel-Tison C, Ahmed B, Azumendi G, et al. New scoring system for fetal neurobehavior assessed by three- and four-dimensional sonography. J Perinat Med. 2008;36:73–81.10.1515/JPM.2008.007Search in Google Scholar PubMed
 Stanojević M, Talic A, Miskovic B, Vasilj O, Shaddad AN, Ahmed B, et al. An attempt to standardize Kurjak’s antenatal neurodevelopmental test: osaka consensus statement. Donald School J Ultrasound Obstet Gynecol. 2011;5:317–29.10.5005/jp-journals-10009-1209Search in Google Scholar
 Hata T, Kanenishi K, AboEllail MAM, Marumo G, Kurjak A. Fetal consciousness 4D ultrasound study. Donald School J Ultrasound Obstet Gynecol. 2015;9:471–4.10.5005/jp-journals-10009-1434Search in Google Scholar
 Kurjak A, Stanojević M, Andonotopo W, Scazzocchio-Duenas E, Azumendi G, Carrera JM. Fetal behavior assessed in all three trimesters of normal pregnancy by four-dimensional ultrasonography. Croat Med J. 2005;46:772–80.Search in Google Scholar
 Yigiter AB, Kavak ZN. Normal standards of fetal behavior assessed by four-dimensional sonography. J Matern Fetal Neonatal Med. 2006;19:707–21.10.1080/14767050600924129Search in Google Scholar PubMed
 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 Gynecol Obstet. 2006;94:108–13.10.1016/j.ijgo.2006.05.004Search in Google Scholar PubMed
 Kanenishi K, Hanaoka U, Noguchi J, Marumo G, Hata T. 4D ultrasound evaluation of fetal facial expressions during the latter stages of the second trimester. Int J Gynecol Obstet. 2013;121:257–60.10.1016/j.ijgo.2013.01.018Search in Google Scholar PubMed
 Sato M, Kanenishi K, Hanaoka U, Noguchi J, Marumo G, Hata T. 4D ultrasound study of fetal facial expressions at 20–24 weeks of gestation. Int J Gynaecol Obstet. 2014;126:275–9.10.1016/j.ijgo.2014.03.036Search in Google Scholar PubMed
 Lebit DF, Vladareanu PD. The role of 4D ultrasound in the assessment of fetal behaviour. Maedica (Buchar). 2011;6: 120–7.Search in Google Scholar
 Kurjak A, Azumendi G, Andonotopo W, Salihagic-Kadic A. Three- and four-dimensional ultrasonography for the structural and functional evaluation of the fetal face. Am J Obstet Gynecol. 2007;196:16–28.10.1016/j.ajog.2006.06.090Search in Google Scholar PubMed
 Bosma JF. Anatomic and physiologic development of the speech apparatus. In: Towers DB, editor. Human Communication and its Disorder. New York: Raven; 1975. p. 469–81.Search in Google Scholar
 Bodfish J, Powell S, Golden R, Lewis M. Blink rate as an index of dopamine function in adults with mental retardation and repetitive movement disorders. Am J Ment Retard. 1995;99:335–44.Search in Google Scholar
 Fukuda K, Stem JA, Brown TB, Russo MB. Cognition, blinks, eye movements, and pupillary movements during performance of a running memory task. Aviat Space Envir MD. 2005;76:C75–85.Search in Google Scholar
 Siegle GJ, Ichikawa N, Steinhauer S. Blink before and after you thibk: blinks occur prior to and following cognitive load indexed by pupillary responses. Psychophysiology. 2008;45:679–87.10.1111/j.1469-8986.2008.00681.xSearch in Google Scholar PubMed
 Kleven MS, Koek W. Diffetential effects of direct and indirect dopamine agonists on eye blink rate in cynomolgus monkeys. J Pharmacol Exp Ther. 1996;279:1211–9.Search in Google Scholar
 Driebach G, Muller J, Goschke T, Strobel A, Schulze K, Lesch K, et al. Dopamine and cognitive control: the influence of spontaneous eyeblink rate and dopamine gene polymorphism on perseveration and distractibility. Behav Neurosci. 2005;119:483–49.10.1037/0735-7044.119.2.483Search in Google Scholar
 Colzato LS, van den Wildenberg WPM, van Wouwe NC, Pannebakker MM, Hommel B. Dopamine and inhibitory action control: evidence from spontaneous eye blink rates. Exp Brain Res. 2009;196:467–74.10.1007/s00221-009-1862-xSearch in Google Scholar
 Giganti F, Hayes MJ, Cioni G, Salzarulo P. Yawning frequency and distribution in preterm and near term infants assessed throughout 24-h recordings. Infant Behav Dev. 2007;30:641–7.10.1016/j.infbeh.2007.03.005Search in Google Scholar
 Reissland N, Francis B, Manson J. Development of fetal yawn compared with non-yawn mouth openings from 24–36 weeks gestation. PLoS One. 2012;7:e50569.10.1371/journal.pone.0050569Search in Google Scholar
 Reissland N, Mason C, Schaal B, Lincoln K. Prenatal mouth movements: can we identify co-ordinated fetal mouth and lip actions necessary for feeding? Int J Pediatr. 2012;2012:848596.10.1155/2012/848596Search in Google Scholar
 Horimoto N, Koyanagi T, Nagata S, Nakahara H, Nakano H. Concurrence of mouthing movement and rapid eye movement/non-rapid eye movement phases with advance in gestation of the human fetus. Am J Obstet Gynecol. 1989;161:344–51.10.1016/0002-9378(89)90517-6Search in Google Scholar
 Reissland N, Francis B, Aydin E, Mason J, Exley K. Development of prenatal lateralization: evidence from fetal mouth movements. Physiol Behav. 2014;131:160–3.10.1016/j.physbeh.2014.04.035Search in Google Scholar PubMed
 Reissland N, Francis B, Mason J. Can healthy fetuses show facial expressions of “pain” or “distress”? PLoS One. 2013;8:e65530.10.1371/journal.pone.0065530Search in Google Scholar PubMed PubMed Central
 Hata T, Hanaoka U, Tenkumo C, Sato M, Tanaka H, Ishimura M. Three- and four-dimensional HDlive rendering images of normal and abnormal fetuses: pictorial essay. Arch Gynecol Obstet. 2012;286:1431–5.10.1007/s00404-012-2505-1Search in Google Scholar PubMed
 Lopez-Teijon M, Garcia-Faura A, Prats-Galino A. Fetal facial expression in response to intravaginal music emission. Ultrasound. 2015;23:216–23.10.1177/1742271X15609367Search in Google Scholar PubMed PubMed Central
 Reissland N, Francis B, Kumarendran K, Mason J. Ultrasound observations of subtle movements: a pilot study comparing foetuses of smoking and nonsmoking mothers. Acta Paediatr. 2015;104:596–603.10.1111/apa.13001Search in Google Scholar PubMed PubMed Central
 Nakamura Y, Takeishi Y, Ito N, Ito M, Atogami F, Yoshizawa T. Comfort with motherhood in late pregnancy facilitates maternal role attainment in early postpartum. Tohoku J Exp Med. 2015;235:53–9.10.1620/tjem.235.53Search in Google Scholar PubMed
 Hata T, Hanaoka U, AboEllail MAM, Uematsu R, Noguchi J, Kusaka T, et al. Does parity have an effect on fetal behavior? A comparison between primi- and multiparas. Donald School J Ultrasound Obstet Gynecol. 2016;10:99–102.10.5005/jp-journals-10009-1448Search in Google Scholar
 Ferrari GA, Nicolini Y, Demuru E, Tosato C, Hussain M, Scesa E, et al. Ultrasonographic investigation of human fetus responses to maternal communicative and non-communicative stimuli. Front Psychol. 2016;7:354.10.3389/fpsyg.2016.00354Search in Google Scholar PubMed PubMed Central
©2017 Walter de Gruyter GmbH, Berlin/Boston