The Journal of Physiological Sciences

, Volume 69, Issue 6, pp 1085–1096 | Cite as

Inaudible components of the human infant cry influence haemodynamic responses in the breast region of mothers

  • Hirokazu Doi
  • Simone Sulpizio
  • Gianluca Esposito
  • Masahiro Katou
  • Emi Nishina
  • Mayuko Iriguchi
  • Manabu Honda
  • Tsutomu Oohashi
  • Marc H. Bornstein
  • Kazuyuki ShinoharaEmail author
Original Paper


Distress vocalizations are fundamental for survival, and both sonic and ultrasonic components of such vocalizations are preserved phylogenetically among many mammals. On this basis, we hypothesized that ultrasonic inaudible components of the acoustic signal might play a heretofore hidden role in humans as well. By investigating the human distress vocalization (infant cry), here we show that, similar to other species, the human infant cry contains ultrasonic components that modulate haemodynamic responses in mothers, without the mother being consciously aware of those modulations. In two studies, we measured the haemodynamic activity in the breasts of mothers while they were exposed to the ultrasonic components of infant cries. Although mothers were not aware of ultrasounds, the presence of the ultrasounds in combination with the audible components increased oxygenated haemoglobin concentration in the mothers’ breast region. This modulation was observed only when the body surface was exposed to the ultrasonic components. These findings provide the first evidence indicating that the ultrasonic components of the acoustic signal play a role in human mother–infant interaction.


Parenting Cry Mother Infant Ultrasonic 



We thank Wakako Horita and Eriko Yamada for their help in participant recruitment and data collection. Without their help, this study would have been feasible. Yuichiro Kikuno also assisted participant recruitment. We also thank Paola Rigo and Tommaso Sega for their help with editing figures.


This research was supported by the Intramural Research Program of the NIH/NICHD, USA, and an International Research Fellowship at the Institute for Fiscal Studies (IFS), London, UK, funded by the European Research Council (ERC) under the Horizon 2020 research and innovation programme (Grant Agreement No. 695300-HKADeCERC-2015-AdG). This study was partly supported by Grant-in-Aid for Scientific Research on Innovative Areas (Chronogenesis: how the mind generates time; Grant No. 19H05315) to HD.

Compliance with ethical standards

Conflict of interest

We declare no conflict of interest.

Ethical approval

The experimental protocol was approved by the ethical committee of Nagasaki University (No. 08102894-5). The participants were given information about the research and gave written informed consent.


  1. 1.
    Bass A, Gilland E, Baker R (2008) Evolutionary origins for social vocalization in a vertebrate hindbrain spinal compartment. Science 321:417–421CrossRefGoogle Scholar
  2. 2.
    Belin P, Zatorre R, Ahad P (2002) Human temporal-lobe response to vocal sounds. Cognit Brain Res 13(1):17–26CrossRefGoogle Scholar
  3. 3.
    Bornstein MH, Putnick DL, Rigo P, Esposito G, Swain JE, Suwalsky JTD, Su X, Du X, Zhang K, Cote LR, De Pisapia N, Venuti P (2017) Neurobiology of culturally common maternal responses to infant cry. Proc Natl Acad Sci USA 114(45):E9465–E9473CrossRefGoogle Scholar
  4. 4.
    Carruthers IM, Natan RG, Geffen MN (2013) Encoding of ultrasonic vocalizations in the auditory cortex. J Neurophysiol 109(7):1912–1927CrossRefGoogle Scholar
  5. 5.
    Cherry J, Izard M, Simons E (1987) Description of ultrasonic vocalizations of the mouse lemur (Microcebus murinus) and the fat-tailed dwarf lemur (Cheirogaleus medius). Am J Primatol 13:181–185CrossRefGoogle Scholar
  6. 6.
    Crowe HP, Zeskind PS (1992) Psychophysiological and perceptual responses to infant cries varying in pitch: comparison of adults with low and high scores on the Child Abuse Potential Inventory. Child Abuse Negl 16(1):19–29CrossRefGoogle Scholar
  7. 7.
    Doi H, Shinohara K (2012) Event-related potentials elicited in mothers by their own and unfamiliar infants’ faces with crying and smiling expression. Neuropsychologia 50(7):1297–1307CrossRefGoogle Scholar
  8. 8.
    Doi H, Nishitani S, Shinohara K (2013) NIRS as a tool for assaying emotional function in the prefrontal cortex. Front Hum Neurosci 7:770. CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Ehret G (1987) Left hemisphere advantage in the mouse brain for recognizing ultrasonic communication calls. Nature 325:249–251CrossRefGoogle Scholar
  10. 10.
    Eriksson M, Lundeberg T, Uvnäs-Moberg K (1996) Studies on cutaneous blood flow in the mammary gland of lactating rats. Acta Physiol Scand 158(1):1–6CrossRefGoogle Scholar
  11. 11.
    Esposito G, Venuti P (2010) Developmental changes in the fundamental frequency (f0) of infants’ cries: a study of children with autism spectrum disorder. Early Child Dev Care 180(8):1093–1102CrossRefGoogle Scholar
  12. 12.
    Groh AM, Roisman GI (2009) Adults’ autonomic and subjective emotional responses to infant vocalizations: the role of secure base script knowledge. Dev Psychol 45(3):889–893CrossRefGoogle Scholar
  13. 13.
    Janbu T, Koss KS, Thoresen M, Wesche J (1985) Blood velocities to the female breast during lactation and following oxytocin injections. J Dev Physiol 7(6):373–380Google Scholar
  14. 14.
    Japundžić-Žigon N (2013) Vasopressin and oxytocin in control of the cardiovascular system. Curr Neuropharmacol 11(2):218–230CrossRefGoogle Scholar
  15. 15.
    Johnson J, Kellogg D (2010) Local thermal control of the human cutaneous circulation. J Appl Physiol 109(4):1229–1238CrossRefGoogle Scholar
  16. 16.
    Joosen KJ, Mesman J, Bakermans-Kranenburg MJ, Pieper S, Zeskind PS, van IJzendoorn MH (2013) Physiological reactivity to infant crying and observed maternal sensitivity. Infancy 18(3):414–431CrossRefGoogle Scholar
  17. 17.
    Kent R, Murray A (1982) Acoustic features of infant vocalic utterances at 3, 6, and 9 months. J Acoust Soc Am 72:353–365CrossRefGoogle Scholar
  18. 18.
    Kim P, Feldman R, Mayes L, Leckman J, Swain J (2011) Breastfeeding, brain activation to own infant cry, and maternal sensitivity. J Child Psychol Psychiatry 52(8):907–915CrossRefGoogle Scholar
  19. 19.
    Kingston J, Kawahara S, Chambless D, Key M, Mash D, Watsky S (2014) Context effects as auditory contrast. Atten Percept Psychophys 76(5):1437–1464CrossRefGoogle Scholar
  20. 20.
    Kimura C, Matsuoka M (2007) Changes in breast skin temperature during the course of breastfeeding. J Hum Lactat 23(1):60–69CrossRefGoogle Scholar
  21. 21.
    Kuribayashi R, Nittono H (2017) High-resolution audio with inaudible high-frequency components induces a relaxed attentional state without conscious awareness. Front Psychol 8(93):2017. CrossRefGoogle Scholar
  22. 22.
    Kuribayashi R, Yamamoto R, Nittono H (2014) High-resolution music with inaudible high-frequency components produces a lagged effect on human electroencephalographic activities. NeuroReport 25(9):651–655CrossRefGoogle Scholar
  23. 23.
    Laurent H, Stevens A, Ablow J (2011) Neural correlates of hypothalamic-pituitary-adrenal regulation of mothers with their infants. Biol Psychiatry 70(9):826–832CrossRefGoogle Scholar
  24. 24.
    Leon-Carrion J, Damas J, Izzetoglu K, Pourrezai K, Martín-Rodríguez JF, Barroso y Martin JM et al (2006) Differential time course and intensity of PFC activation for men and women in response to emotional stimuli: a functional near-infrared spectroscopy (fNIRS) study. Neurosci Lett 403:90–95. CrossRefGoogle Scholar
  25. 25.
    Lieberman P, Harris K, Wolff P, Russell L (1971) Newborn infant cry and nonhuman primate vocalization. J Speech Lang Hear Res 14:718–727CrossRefGoogle Scholar
  26. 26.
    Lingle S, Wyman M, Kotrba R, Teichroeb L, Romanow C (2012) What makes a cry a cry? A review of infant distress vocalizations. Curr Zool 58:698–725CrossRefGoogle Scholar
  27. 27.
    Marlin B, Mitre M, D’amour J, Chao M, Froemke R (2015) Oxytocin enables maternal behavior by balancing cortical inhibition. Nature 520:499–504CrossRefGoogle Scholar
  28. 28.
    Minagawa-Kawai Y, Naoi N, Kojima S (2009) A new approach to functional neuroimaging: near-infrared spectroscopy (NIRS). Keio University Press, TokyoGoogle Scholar
  29. 29.
    Newman J (2007) Neural circuits underlying crying and cry responding in mammals. Behav Brain Res 182:155–165CrossRefGoogle Scholar
  30. 30.
    Oohashi T, Kawai N, Nishina E, Honda M, Yagi R, Nakamura S, Morimoto M, Maekawa T, Yonekura Y, Shibasaki H (2006) The role of biological system other than auditory air-conduction in the emergence of the hypersonic effect. Brain Res 1073:339–347CrossRefGoogle Scholar
  31. 31.
    Oohashi T, Nishina E, Honda M, Yonekura Y, Fuwamoto Y, Kawai N, Maekawa T, Nakamura S, Fukuyama H, Shibasaki H (2000) Inaudible high-frequency sounds affect brain activity: hypersonic effect. J Neurophysiol 83:3548–3558CrossRefGoogle Scholar
  32. 32.
    Out D, Pieper S, Bakermans-Kranenburg MJ, van Ijzendoorn MH (2010) Physiological reactivity to infant crying: a behavioral genetic study. Genes Brain Behav 9(8):868–876CrossRefGoogle Scholar
  33. 33.
    Portfors CV, Perkel DJ (2015) The role of ultrasonic vocalizations in mouse communication. Curr Opin Neurobiol 25:115–120Google Scholar
  34. 34.
    Riem MM, Bakermans-Kranenburg MJ, Pieper S, Tops M, Boksem MA, Vermeiren RR, van Ijzendoorn MH, Rombouts SA (2011) Oxytocin modulates amygdala, insula, and inferior frontal gyrus responses to infant crying: a randomized controlled trial. Biol Psychiatry 70:291–297CrossRefGoogle Scholar
  35. 35.
    Rilling J, Young L (2014) The biology of mammalian parenting and its effect on offspring social development. Science 345:771–776CrossRefGoogle Scholar
  36. 36.
    Sewell G (1970) Ultrasonic communication in rodents. Nature 227:410CrossRefGoogle Scholar
  37. 37.
    Sales G (2010) Ultrasonic calls of wild and wild-type rodents. In: Brudzynski SM (ed) Handbook of mammalian vocalization. Academic, London, pp 77–88Google Scholar
  38. 38.
    Takahashi T, Okabe S, Broin P, Kikusui T, Hiroi N (2016) Structure and function of neonatal social communication in a genetic mouse model of autism. Mol Psychiatry 21(9):1208–1214CrossRefGoogle Scholar
  39. 39.
    Taylor N, Tipton M, Kenny G (2014) Considerations for the measurement of core, skin and mean body temperatures. J Therm Biol 46:72–101CrossRefGoogle Scholar
  40. 40.
    Tanimoto K, Kusaka T, Nishida T, Ogawa K, Kato I, Ijichi S, Mikami J, Sobue I, Isobe K, Itoh S (2011) Hemodynamic changes in the breast and frontal cortex of mothers during breastfeeding. Pediatr Res 70:400–405CrossRefGoogle Scholar
  41. 41.
    Thaler L, Reich G, Zhan X, Kish D, Antoniou M (2017) Mouth-clicks used by blind expert human echolocators—signal description and model based signal synthesis. PLoS Comput Biol 13(8):e1005670CrossRefGoogle Scholar
  42. 42.
    van der Hoek M, den Haan L, Kaspers A, Steenbergen W, Bosschaart N (2019) Cutaneous perfusion of the human lactating breast: a pilot study with laser Doppler perfusion monitoring. Physiol Meas 40(5):05NT01. CrossRefGoogle Scholar
  43. 43.
    Vuorenkoski V, WaSZ-Hockert O, Koivisto E, Lind J (1969) The effect of cry stimulus on the temperature of the lactating breast of primipara. A thermographic study. Experientia 25(12):1286–1287CrossRefGoogle Scholar
  44. 44.
    Wohr M, Schwarting R (2008) Maternal care, isolation-induced infant ultrasonic calling, and their relations to adult anxiety-related behavior in the rat. Behav Neurosci 122:310–330CrossRefGoogle Scholar
  45. 45.
    Yagi R, Nishina E, Honda M, Oohashi T (2003) Modulatory effect of inaudible high-frequency sounds on human acoustic perception. Neurosci Lett 351(3):191–195CrossRefGoogle Scholar
  46. 46.
    Yagi R, Nishina E, Oohashi T (2003) A method for behavioral evaluation of the “hypersonic effect”. Acoust Sci Technol 24:197–200CrossRefGoogle Scholar
  47. 47.
    Zimmerberg B, Brunelli S, Fluty ACAF (2005) Differences in affective behaviors and hippocampal allopregnanolone levels in adult rats of lines selectively bred for infantile vocalizations. Behav Brain Res 159:301–311CrossRefGoogle Scholar

Copyright information

© The Physiological Society of Japan and Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  • Hirokazu Doi
    • 1
  • Simone Sulpizio
    • 2
    • 3
  • Gianluca Esposito
    • 4
    • 5
  • Masahiro Katou
    • 6
  • Emi Nishina
    • 7
  • Mayuko Iriguchi
    • 1
  • Manabu Honda
    • 8
  • Tsutomu Oohashi
    • 9
  • Marc H. Bornstein
    • 10
    • 11
  • Kazuyuki Shinohara
    • 1
    Email author
  1. 1.Department of Neurobiology and Behavior, Graduate School of Biomedical SciencesNagasaki UniversityNagasakiJapan
  2. 2.Faculty of PsychologyVita-Salute San Raffaele UniversityMilanItaly
  3. 3.Centre for Neurolinguistics and PsycholinguisticsVita-Salute San Raffaele UniversityMilanItaly
  4. 4.Department of Psychology and Cognitive ScienceUniversity of TrentoTrentoItaly
  5. 5.Psychology ProgramNanyang Technological UniversitySingaporeSingapore
  6. 6.Kato Acoustics Consulting OfficeYokohamaJapan
  7. 7.Department of Liberal ArtsThe Open University of JapanChibaJapan
  8. 8.Department of Information MedicineNational Center of Neurology and PsychiatryTokyoJapan
  9. 9.Department of Research and DevelopmentFoundation for Advancement of International ScienceTokyoJapan
  10. 10.Eunice Kennedy Shriver National Institute of Child Health and Human DevelopmentBethesdaUSA
  11. 11.Institute for Fiscal StudiesLondonUK

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