A melodic contour repeatedly experienced by human near-term fetuses elicits a profound cardiac reaction one month after birth

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  Granier Deferre, Carolyn ^a   Bassereau, Sophie ^a   Ribeiro, Aurélie ^a   Jacquet, Anne Yvonne ^b   DeCasper, Anthony J ^c  

^a CNRS   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; AUDITORY DISCRIMINATION; AUDITORY MEMORY; AUTONOMIC NERVOUS SYSTEM FUNCTION; CONTROLLED STUDY; DECELERATION; EVOKED AUDITORY RESPONSE; FEMALE; FETUS; GESTATIONAL AGE; HEART FUNCTION; HEART RATE VARIABILITY; HUMAN; HUMAN EXPERIMENT; LONG TERM MEMORY; MALE; MEMORY CONSOLIDATION; NEUROPHYSIOLOGY; NEWBORN; PRENATAL DEVELOPMENT; PRENATAL EXPOSURE; SOUND DETECTION; SPEECH PERCEPTION; STIMULUS RESPONSE; ADULT; BIRTH; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; FETUS HEART RATE; HEARING; HEART RATE; MEMORY; MUSIC; PERIODICITY; PHYSIOLOGY; PREGNANCY; PSYCHOLOGICAL ASPECT; RANDOMIZED CONTROLLED TRIAL; THIRD TRIMESTER PREGNANCY; TIME;

ADULT; FEMALE; FETUS; GESTATIONAL AGE; HEARING; HEART RATE; HEART RATE, FETAL; HUMANS; INFANT, NEWBORN; MEMORY; MUSIC; PARTURITION; PERIODICITY; PREGNANCY; PREGNANCY TRIMESTER, THIRD; RETENTION (PSYCHOLOGY); TIME FACTORS;

EID: 79952034561     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017304     Document Type: Article

References (95)

1. Pujol R, Laville-Rebillard M, Lenoir M, (1998) Development of sensory neural structures in the Mammalian cochlea. In: Rubel EW, Popper AN, Fay RR, editors. Development of the auditory system New York Springer Handbook of Auditory Research, Springer-Verlag pp. 146-193.
2. Morlet T, Collet L, Salle B, Morgon A, (1993) Functional maturation of cochlear active mechanisms of the medial olivocochlear system in humans. Acta Otolaryngol (Stock) 113: 271-277.
3. Rotteveel JJ, de Graaf R, Stegeman DF, Colon EJ, Visco YM, (1987) The maturation of the central auditory conduction in preterm infants until three months post term V: The auditory cortical response (ACR). Hear Res 27: 95-110.
4. Eldredge L, Salamy A, (1996) Functional auditory development in preterm and full term infants. Early Hum Dev 45: 215-228.
5. Lecanuet J-P, Granier-Deferre C, Busnel M-C, (1988) Fetal cardiac motor responses to octave-band noises as a function of central frequency, intensity and heart rate variability. Early Human Dev 18: 81-93.
6. Lecanuet J-P, Granier-Deferre C, DeCasper AJ, Maugeais R, Andrieu AJ, et al. (1987) Perception et discrimination foetales de stimuli langagiers: mise en évidence à partir de la réactivité cardiaque, résultats préliminaires. C R Acad Sci Paris Ser III 305: 161-164.
7. Lecanuet J-P, Granier-Deferre C, Busnel M-C, (1989) Differential fetal auditory reactiveness as a function of stimulus characteristics and state. Sem in Perinat 13: 421-429.
8. Lecanuet J-P, Granier-Deferre C, Jacquet A-Y, Busnel M-C, (1992) Decelerative cardiac responsiveness to acoustical stimulation in the near term foetus. Quart J of Exp Psychol 44b: 279-303.
9. Lecanuet J-P, Granier-Deferre C, Jacquet A-Y, Capponi I, Ledru L, (1993) Prenatal discrimination of a male and a female voice uttering the same sentence. Early Dev Parenting 2: 217-228.
10. Lecanuet J-P, Granier-Deferre C, Jacquet A-Y, DeCasper AJ, (2000) Fetal discrimination of low-pitched musical notes. Dev Psychobiol 36: 29-39.
11. Shahidullah S, Hepper PG, (1994) Frequency discrimination by the fetus. Early Human Dev 36: 13-26.
12. Groome LJ, Mooney DM, Holland SB, Smith LA, Atterbury JL, et al. (1999) Behavioral state affects heart rate response to low-intensity sound in human fetuses. Early Human Dev 54: 39-54.
13. Granier-Deferre C, Ribeiro A, Jacquet A-Y, Bassereau S, (2010) Near-term fetuses process temporal features of speech. Dev Sci DOI:101111/j1467-7687201000978X.
14. Lecanuet J-P, Jacquet A-Y, (2002) Our dear friend and colleague Jean-Pierre Lecanuet completed a study on tempo discrimination which showed that near term fetus could detect several temporal changes, for example, a 10% increase or decrease in the 600 ms inter-onset-interval of an isochronous sequence of a musical note. Sadly, he had not completed the manuscript before he passed away.
15. Lecanuet J-P, Granier-Deferre C, Busnel M-C, (1995) Human fetal auditory perception. In: Lecanuet J-P, Fifer WP, Krasnegor NA, Smotherman WP, editors. Fetal development: a psychobiological perspective Hillsdale Lawrence Erlbaum Associates pp. 239-262.
16. Schleussner E, Schneider U, (2004) Developmental changes of auditory-evoked fields in fetuses. Exp Neurol 190: 59-64.
17. Holst M, Eswaran H, Lowery C, Murphy P, Norton J, et al. (2005) Development of auditory evoked fields in human fetuses newborns: a longitudinal MEG study. Clin Neurophysiol 116: 1949-1955.
18. Huotilainen M, Kujala A, Hotakainen M, Parkkonen L, Taulu S, et al. (2005) Short-term memory functions of the human fetus recorded with magnetoencephalography. Neuroreport 16: 81-84.
19. Draganova R, Eswaran H, Murphy P, Lowery C, Preissl H, (2007) Serial magnetoencephalographic study of fetal newborn auditory discriminative evoked responses. Early Hum Dev 83: 199-207.
20. Moore RJ, Vadeyar S, Fulford J, Tyler DJ, Gribben C, et al. (2001) Antenatal determination of fetal brain activity in response to an acoustic stimulus using functional magnetic resonance imaging. HBM 12: 94-99.
21. Fulford J, Vadeyar SH, Dodampahala SH, Ong S, Moore RJ, et al. (2004) Fetal brain activity and hemodynamic response to a vibroacoustic stimulus. HBM 22: 116-121.
22. Jardri R, Pins D, Houfflin-Debarge V, Chaffiotte C, Rocourt N, et al. (2008) Fetal cortical activation to sound at 33 weeks of gestation: a functional MRI study. NeuroImage 42: 10-18.
23. Armitage SE, Baldwin BA, Vince MA, (1980) The fetal sound environment of sheep. Science 208: 1173-1174.
24. Peters AJ, Abrams RM, Gerhardt KJ, Griffiths SK, (1993) Transmission of airborne sounds from 50-20,000 Hz into the abdomen of sheep. J Low Freq Noise Vib 12: 16-24.
25. Querleu D, Renard X, Versyp F, Paris-Delrue L, Vervoot P, (1988) La transmission intra-amniotique des voix humaines. Rev Gynecol Obstet 83: 43-50.
26. Querleu D, Renard X, Boutteville C, Crépin G, (1989) Hearing by the human fetus? Semin Perinatol 13: 409-420.
27. Benzaquen S, Gagnon R, Hunse C, Foreman J, (1990) The intrauterine sound environment of the human fetus during labor. Am J Obstet Gynecol 163: 484-490.
28. Richards DS, Frentzen B, Gerhardt KJ, McCann ME, Abrams RM, (1992) Sound levels in the human uterus. Obstet Gynecol 80: 186-190.
29. Griffiths SJ, Brown WS Jr, Gerhardt KJ, Abrams RM, Morris RJ, (1994) The perception of speech sounds recorded within the uterus of a pregnant sheep. JASA 96: 2055-2063.
30. Abrams RM, Griffiths SK, Huang X, Sain J, Langford G, et al. (1998) Fetal music perception: The role of sound transmission. Music Percept 15: 307-317.
31. Rovee-Collier C, Cueva SK, (2009) Multiple memory systems are unnecessary to account for infant memory development: an ecological model. Dev Psy 45: 160-174.
32. Granier-Deferre C, Lecanuet J-P, Cohen H, Busnel M-C, (1985) Feasibility of prenatal hearing test. Acta-Otolaryngol (Stockh) 421: 93-101.
33. Lecanuet J-P, Granier-Deferre C, Cohen H, Le Houezec R, Busnel M-C, (1986) Fetal responses to acoustic stimulation depend on HR variability pattern, stimulus intensity and repetition Early Human Dev 13: 269-283.
34. Hepper PG, (1996) Fetal memory: Does it exist? What does it do? Acta Paediatr 416 (Suppl): 16-20.
35. Leader LR, Baillie P, Martin B, Vermeulen E, (1982) The assessment and significance of habituation to a repeated stimulus by the human fetus. Early Human Dev 7: 211-283.
36. Madison LS, Adubato SA, Madison JK, Nelson RM, Anderson JC, et al. (1986) Fetal response decrement: True habituation? J Dev Behav Pediat 7: 14-20.
37. Kisilevsky BS, Muir DW, Low JA, (1992) Maturation of human fetal responses to vibroacoustic stimulation. Child Dev 63: 1497-1508.
38. Visser GH, Mulder EJ, (1993) The effect of vibro-acoustic stimulation on fetal behavioral state organization. Am J Ind Med 23: 531-539.
39. Smith CV, (1995) Vibroacoustic stimulation. Clin Obstet Gynecol 38: 68-77.
40. Sandman CA, Wadhwa PD, Hetrick WP, Porto M, Peeke HVS, (1997) Human fetal heart rate dishabituation between 30-32 weeks gestation. Child Dev 68: 1031-1040.
41. Sandman CA, Glynn L, Wadhwa PD, Chicz-DeMet A, Porto M, et al. (2003) Maternal HPA deregulation during the third trimester influences human fetal responses. Dev Neurosci 25: 41-49.
42. van Heteren CF, Boekkooi P, Jongsma HW, Nijhuis JG, (2000) Fetal learning memory Lancet 356: 1169-1170.
43. Dirix CE, Nijhuis JG, Jongsma HW, Hornstra G, (2009) Aspects of fetal learning memory. Child Dev 80: 1251-1258.
44. Gonzalez-Gonzalez NL, Suarez MN, Perez-Pinero B, Armas H, Domenech E, et al. (2006) Persistence of fetal memory into neonatal life. Acta Obstet Gynecol Scand 85: 1160-1164.
45. Graham EM, Peters AJ, Abrams RM, Gerhardt KJ, Burchfield DJ, (1991) Intraabdominal sound levels during vibroacoustic stimulation. Am J Obstet Gynecol 164: 1140-1144.
46. Abrams RM, Peters AJ, Gerhardt KJ, (1997) Effect of abdominal vibroacoustic stimulation on sound acceleration levels at the head of the fetal sheep. Obstet Gynecol 90: 216-20.
47. Ando Y, Hattori H, (1977) Effects of noise on sleep of babies. JASA 62: 199-204.
48. Spelt DK, (1948) The conditioning of the fetus in utero. J Exp Psychol 38: 338-46.
49. Kawai N, Morokuma S, Tomonaga M, Horimoto N, Tanaka M, (2004) Associative learning memory in a chimpanzee fetus: learning long-lasting memory before birth. Dev Psychobio 44: 116-122.
50. James DK, Spencer CJ, Stepsis BW, (2002) Fetal learning: a prospective randomized controlled study. Ultrasound Obstet Gynecol 20: 431-438.
51. DeCasper AJ, Lecanuet J-P, Maugeais R, Granier-Deferre C, Busnel M-C, (1994) Fetal reactions to recurrent maternal speech. Inf Behav Dev 17: 159-164.
52. Krueger C, Holditch-Davis D, Quint S, DeCasper AJ, (2004) Recurring auditory experience in the 28- to 34-week old fetus. Inf Behav Dev 27: 537-543.
53. Kisilevsky BS, Hains SM, Lee K, Xie X, Huang H, et al. (2003) Effects of experience on fetal voice recognition. Psychol Sci 4: 220-224.
54. Smith LS, Dmochowski PA, Muir DW, Kisilevsky BS, (2007) Estimated cardiac vagal tone predicts fetal responses to mother's stranger's voices. Dev Psychobio 49: 543-47.
55. DeCasper AJ, Spence MJ, (1991) Auditorially mediated behavior during the perinatal period: A cognitive view. In: Weiss MJ, Zelazo PR, editors. Infant Attention Norwood N.J. Ablex pp. 142-176.
56. DeCasper AJ, Fifer WP, (1980) Of human bonding: newborns prefer their mother's voice. Science 208: 1174-1176.
57. Spence MJ, DeCasper AJ, (1987) Prenatal experience with low frequency maternal voice sounds influences neonatal perception of maternal voice samples. Infant Behav Dev 10: 133-142.
58. Spence MJ, Freeman MS, (1996) Newborn infants prefer the maternal low-pass filtered voice, but not the maternal whispered voice. Inf Behav Dev 19: 199-212.
59. Fifer WP, Moon CM, (1995) Effects of fetal experience with sound. In: Lecanuet J-P, Fifer WP, Krasnegor NA, Smotherman WP, editors. Fetal development: a psychobiological perspective Hillsdale Lawrence Erlbaum Associates pp. 351-366.
60. DeCasper AJ, Spence MJ, (1986) Prenatal maternal speech influences newborn's perception of speech sounds. Infant Behav Dev 9: 133-150.
61. Cooper RP, Aslin RN, (1989) The language environment of the young infant: Implications for early perceptual development. Canad J Psychol 43: 247-265.
62. Moon CM, Cooper R, Fifer WP, (1993) Two-Days-olds prefer their native language Infant. Behav Dev 16: 495-500.
63. DeCasper AJ, Prescott P, (2009) Lateralized processes constrain auditory reinforcement in human newborns. Hear Res 255: 135-141.
64. Byers-Heinlein K, Burns TC, Werker JF, (2010) The roots of bilingualism in newborns. Psychol Sci 21: 343-348.
65. Mastropieri D, Turkewitz G, (1999) Prenatal experience and neonatal responsiveness to vocal expressions of emotion. Dev Psychobio 35: 204-214.
66. Hepper PG, (1988) Fetal "soap"addiction. Lancet 11: 1347-1348.
67. Trehub ST, (2001) Musical predispositions in infancy. Ann NY Acad Sci 930: 1-16.
68. Fernald A, Kuhl P, (1997) Acoustic determinants of infant preference for motherese. Inf Behav Dev 10: 279-293.
69. Porges SW, (1974) Heart rate indices of newborn attentional responsiveness. Merrill-Palmer Quarterly 20: 231-253.
70. Graham FK, (1992) Attention: The heart beat, the blink, the brain. In: Campbell BA, Hayne H, Richardson R, editors. Attention: information processing in infants adults; perspective from human and animal research Hillsdale Erlbaum pp. 3-29.
71. Guyomarc'h J-C, (1974) L'empreinte auditive prénatale. Rev Comp Anim 8: 3-6.
72. Gottlieb G, (1982) Development of species identification in ducklings: IX The necessity of experiencing normal variations in embryonic auditory stimulation. Dev Psychobio 15: 507-517.
73. Granier-Deferre C, Lecanuet J-P, (1987) Influence de stimulations auditives précoces sur la maturation anatomique et fonctionnelle du système auditif. Prog Neonatol 7: 236-249.
74. Lickliter R, Stoumbos J, (1992) Modification of prenatal auditory experience alters postnatal auditory preferences of bobwhite quail chicks. Quart J Exp Psychol 44B: 199-214.
75. Dmitrieva LP, Gottlieb G, (1994) Influence of auditory experience on the development of brain stem auditory-evoked potentials in mallard duck embryos hatchlings. Behav Neural Biol 61: 19-28.
76. Vince MA, (1979) Postnatal effects of prenatal sound stimulation in the guinea pig. Anim Behav 27: 908-918.
77. Keuroghlian AS, Knudsen EI, (2007) Adaptive auditory plasticity in developing adult animals. Prog Neurobiol 82: 109-121.
78. Sanes DH, Bao S, (2009) Tuning up the developing auditory CNS. Curr Opin Neurobiol 19: 188-199.
79. de Villers-Sidani E, Chang EF, Bao S, Merzenich MM, (2007) Critical period window for spectral tuning defined in the primary auditory cortex (A1) in the rat. J Neurosci 27: 180-189.
80. Xu J, Yu L, Cai R, Zhang J, Sun X, (2009) Early auditory enrichment with music enhances auditory discrimination learning and alters NR2B protein expression in rat auditory cortex. Behav Brain Res 196: 49-54.
81. Insanally MN, Kover H, Kim H, Bao S, (2009) Feature-dependent sensitive periods in the development of complex sound representation. J Neurosci 29: 5456-5462.
82. Weinberger NM, (1998) Physiological memory in primary auditory cortex: characteristics mechanisms. Neurobiol Learn Mem 70: 226-251.
83. Rayson P, Leech G, Hodges M, (1997) Social differentiation in the use of English vocabulary: some analyses of the conversational component of the British National Corpus. Int J Corpus Ling 2: 133-152.
84. Mehl MR, Vazire S, Ramírez-Esparza N, Slatcher RB, Pennebaker JW, (2007) Are women really more talkative than men? Science 31: 82.
85. Seebach BS, Intrator N, Lieberman P, Cooper LN, (1994) A model of prenatal acquisition of speech parameters. Proc Natl Acad Sci USA 91: 7473-7476.
86. Teinonen T, Fellman V, Näätänen R, Alku P, Huotilainen M, (2009) Statistical language learning in neonates revealed by event-related brain potentials. BMC Neurosci 13: 10:21.
87. Lecanuet J-P, Granier-Deferre C, (1993) Speech stimuli in the fetal environment. In: de Boysson-Bardies B, de Schoenen S, Jusczyck P, McNeilag P, Morton EJ, editors. Developmental neurocognition: speech face processing in the first year of life Dordrecht, Boston, London Klüver Academic Publisher pp. 237-248 NATO, ASI Series (Series D) 69.
88. Moore JK, (2002) Maturation of human auditory cortex: Implications for speech perception. Ann Otol Rhinol Laryngol 189: 7-10.
89. Nazzi T, Bertoncini J, Mehler J, (1998) Language discrimination by newborns: towards an understanding of the role of rhythm. J Exp Psychol: Hum Percep Perf 24: 756-766.
90. Mampe B, Friederici AD, Christophe A, Wermke K, (2009) Newborns' cry melody is shaped by their native language. Current Biol 19: 1-4.
91. Smotherman WP, (1982) In utero chemosensory experience alters taste preference and corticosteroid responsiveness. Behav Neural Biol 36: 61-68.
92. Leon M, Coopersmith R, Lee S, Sullivan RM, Wilson DA, et al. (1987) Neural and behavioral plasticity induced by early olfactory learning. In: Krasnegor N, Blass E, Hofer M, Smotherman W, editors. Perinatal development: a psychobiological perspective New York Academic Press pp. 145-168.
93. Schaal B, Marlier l, Soussignan R, (2000) Human fetuses learn odors from their pregnant mother's diet. Chem Senses 25: 729-737.
94. Marlier L, Schaal B, (2005) Human newborns prefer human milk: conspecific milk odor is attractive without postnatal exposure. Child Dev 76: 155-168.
95. Prechtl HF, (1974) The behavioral states of the newborn infant (a review). Brain Res 76: 185-212.