A Melodic Contour Repeatedly Experienced by Human Near-Term Fetuses Elicits a Profound Cardiac Reaction One Month after Birth

Granier-Deferre, Carolyn; Bassereau, Sophie; Ribeiro, Aurélie; Jacquet, Anne-Yvonne; DeCasper, Anthony J.

doi:10.1371/journal.pone.0017304

Cited by 152 publications

(112 citation statements)

References 80 publications

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“…We have reported that changes in fetal heart rate and motor activity to maternal reading aloud (Cohort VIII) appear to be a response to variation in normal maternal speech patterns which were partially dependent on whether women had been previously speaking naturally (Voegtline, DiPietro, Costigan, & Pater, 2013). Sontag and colleagues noted a fetal response to music that was independent from the maternal response (Sontag, Steele, & Lewis, 1969) and there has been resurgence in fetal response to and retention of musical passages (Granier-Deferre, Bassereau, Ribeiro, Jacquet, & Decasper, 2011; Partanen, Kujala, Tervaniemi, & Huotilainen, 2013). …”

Section: Chapter 12 General Discussionmentioning

confidence: 99%

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DiPietro¹,

Costigan²,

Voegtline³

2015

Monographs Society Res Child

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Among the earliest volumes of this Monograph series was a report by Lester Sontag and colleagues, of the esteemed Fels Institute, on the heart rate of the human fetus as an expression of the developing nervous system. Here, some 75 years later, we commemorate this work and provide historical and contemporary context on knowledge regarding fetal development, as well as results from our own research. These are based on synchronized monitoring of maternal and fetal parameters assessed between 24 and 36 weeks gestation on 740 maternal-fetal pairs compiled from eight separate longitudinal studies, which commenced in the early 1990s. Data include maternal heart rate, respiratory sinus arrhythmia, and electrodermal activity and fetal heart rate, motor activity, and their integration. Hierarchical linear modeling of developmental trajectories reveals that the fetus develops in predictable ways consistent with advancing parasympathetic regulation. Findings also include: within-fetus stability (i.e., preservation of rank ordering over time) for heart rate, motor, and coupling measures; a transitional period of decelerating development near 30 weeks gestation; sex differences in fetal heart rate measures but not in most fetal motor activity measures; modest correspondence in fetal neurodevelopment among siblings as compared to unrelated fetuses; and deviations from normative fetal development in fetuses affected by intrauterine growth restriction and other conditions. Maternal parameters also change during this period of gestation and there is evidence that fetal sex and individual variation in fetal neurobehavior influence maternal physiological processes and the local intrauterine context. Results are discussed within the framework of neuromaturation, the emergence of individual differences, and the bidirectional nature of the maternal-fetal relationship. We pose a number of open questions for future research. Although the human fetus remains just out of reach, new technologies portend an era of accelerated discovery of the earliest period of development.

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Section: Chapter 12 General Discussionmentioning

confidence: 99%

Untitled

DiPietro¹,

Costigan²,

Voegtline³

2015

Monographs Society Res Child

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“…auditory | brain | mother's voice | heartbeat | preterm newborns O ne of the first acoustic stimuli we are exposed to before birth is the voice of the mother and the sounds of her heartbeat. As fetuses, we have substantial capacity for auditory learning and memory already in utero (1)(2)(3)(4)(5), and we are particularly tuned to acoustic cues from our mother (6)(7)(8)(9). Previous research suggests that the innate preference for mother's voice shapes the developmental trajectory of the brain (10,11).…”

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confidence: 99%

Mother’s voice and heartbeat sounds elicit auditory plasticity in the human brain before full gestation

Webb¹,

Heller

Benson

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

195

106

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Brain development is largely shaped by early sensory experience. However, it is currently unknown whether, how early, and to what extent the newborn's brain is shaped by exposure to maternal sounds when the brain is most sensitive to early life programming. The present study examined this question in 40 infants born extremely prematurely (between 25-and 32-wk gestation) in the first month of life. Newborns were randomized to receive auditory enrichment in the form of audio recordings of maternal sounds (including their mother's voice and heartbeat) or routine exposure to hospital environmental noise. The groups were otherwise medically and demographically comparable. Cranial ultrasonography measurements were obtained at 30 ± 3 d of life. Results show that newborns exposed to maternal sounds had a significantly larger auditory cortex (AC) bilaterally compared with control newborns receiving standard care. The magnitude of the right and left AC thickness was significantly correlated with gestational age but not with the duration of sound exposure. Measurements of head circumference and the widths of the frontal horn (FH) and the corpus callosum (CC) were not significantly different between the two groups. This study provides evidence for experience-dependent plasticity in the primary AC before the brain has reached full-term maturation. Our results demonstrate that despite the immaturity of the auditory pathways, the AC is more adaptive to maternal sounds than environmental noise. Further studies are needed to better understand the neural processes underlying this early brain plasticity and its functional implications for future hearing and language development. auditory | brain | mother's voice | heartbeat | preterm newborns

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“…For example, fetuses habituate to the native language of the environment or of the mother (11,12), familiar melodies (13) or fragments of stories heard during pregnancy (14), and even the mother's voice (15). In addition to learning-based habituation involving the laterobasal amygdala only (16), fetuses, for example, react differently to native and nonnative vowels (17) or familiar and unfamiliar melodic contours (18) and discriminate between different vowels of their native language (19). This capability for fine-tuned auditory processing and discrimination suggests that memory traces lasting for several days in the auditory cortex (20) are formed as a result of fetal learning.…”

mentioning

confidence: 99%

Learning-induced neural plasticity of speech processing before birth

Partanen

Kujala

Näätänen

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

200

146

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Learning, the foundation of adaptive and intelligent behavior, is based on plastic changes in neural assemblies, reflected by the modulation of electric brain responses. In infancy, auditory learning implicates the formation and strengthening of neural long-term memory traces, improving discrimination skills, in particular those forming the prerequisites for speech perception and understanding. Although previous behavioral observations show that newborns react differentially to unfamiliar sounds vs. familiar sound material that they were exposed to as fetuses, the neural basis of fetal learning has not thus far been investigated. Here we demonstrate direct neural correlates of human fetal learning of speech-like auditory stimuli. We presented variants of words to fetuses; unlike infants with no exposure to these stimuli, the exposed fetuses showed enhanced brain activity (mismatch responses) in response to pitch changes for the trained variants after birth. Furthermore, a significant correlation existed between the amount of prenatal exposure and brain activity, with greater activity being associated with a higher amount of prenatal speech exposure. Moreover, the learning effect was generalized to other types of similar speech sounds not included in the training material. Consequently, our results indicate neural commitment specifically tuned to the speech features heard before birth and their memory representations. mismatch negativity | event-related potentials D uring the fetal period the brain undergoes extensive developmental changes as new synapses are formed (1) and axonal connections between neurons are myelinated (2), facilitating efficient recognition and analysis of complex information. In audition, the functional maturation of the developing nervous system is driven by external input, which is evidenced by, for instance, the rapid reorganization of the auditory cortex by external stimuli soon after the onset of hearing in rats (3). This was suggested to occur in humans usually by the gestational age of 27 wk (4). Such plastic changes in neural assemblies during early development indicate that humans have some learning capability even before birth (5, 6). However, this learning capability may be based predominantly on the discrimination of low-pitched sounds that can penetrate the intrauterine walls (7-9). This lowpitch information may play an important role in early speech discrimination of newborns (10) by facilitating learning to segment incoming speech into meaningful units.Consistent with this, previous behavioral studies have shown that fetuses become attuned to a variety of features of the surrounding auditory environment. For example, fetuses habituate to the native language of the environment or of the mother (11, 12), familiar melodies (13) or fragments of stories heard during pregnancy (14), and even the mother's voice (15). In addition to learning-based habituation involving the laterobasal amygdala only (16), fetuses, for example, react differently to native and nonnative vowels (17) or f...

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A Melodic Contour Repeatedly Experienced by Human Near-Term Fetuses Elicits a Profound Cardiac Reaction One Month after Birth

Cited by 152 publications

References 80 publications

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Mother’s voice and heartbeat sounds elicit auditory plasticity in the human brain before full gestation

Learning-induced neural plasticity of speech processing before birth

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