Cochlear microphonics recorded from fetal and newborn sheep

doi:10.1016/0196-0709(92)90026-P

American Journal of Otolaryngology

Volume 13, Issue 4, July–August 1992, Pages 226-233

https://doi.org/10.1016/0196-0709(92)90026-P Get rights and content

Abstract

Purpose: Sounds present within the uterus stimulate the fetal inner ear and central auditory pathway. This study was undertaken to determine the efficiency of transmission of exogenous airborne stimuli to the fetal inner ear. In this way, we may quantify the extent to which the fetal auditory system is isolated from sounds produced outside the mother.

Materials and Methods: Cochlear microphonics were recorded from fetal and newborn sheep to evaluate the extent to which the fetus is isolated from sounds exogenous to the ewe. Electrodes were surgically placed in contact with the round window membrane in nine near-term fetal sheep. Cochlear microphonics were recorded in response to $13$ octave-band noises (0.125 to 2.0 kHz) delivered through a loudspeaker 1.8 m from one side of the pregnant ewe. Sound pressure levels generated by the noises were simultaneously recorded ex utero with a microphone and in utero with a hydrophone previously sutured to the fetal neck. After cochlear microphonic amplitudes were recorded, the fetus was delivered through an abdominal incision. Recordings were repeated from the newborn lamb. Fetal sound isolation was calculated as the difference between the sound pressure levels that were necessary to evoke equal cochlear microphonic amplitudes from the fetus and from the newborn lamb.

Results: The sound attenuation observed was variable for all frequencies. The fetus was isolated from external sounds by 11.1 dB for 0.125 kHz, 19.8 dB for 0.25 kHz, 35.3 dB for 0.5 kHz, 38.2 dB for 1.0 kHz, and 45.0 dB for 2.0 kHz.

Conclusions: Other investigators have demonstrated that the immature auditory system is more susceptible to damage produced by noise exposure than is the mature auditory system. Low-frequency noise produces damaged cells that later in life code higher frequencies. A possibility of fetal hearing loss produced by intense noise exposure needs more careful evaluation.

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Such a hypothesis predicts that adults and children can adapt to time-compressed speech, as has been observed, but that newborns, who only have experience with speech as heard in utero, which is very different from regular speech transmitted through the air, would fail. Third, it may be the case that little or no experience is needed for the adaptation ability to occur, so the degraded, low-pass filtered speech signal experienced prenatally, which only preserves the prosodic properties of the native language (Gerhardt et al., 1992; Querleu et al., 1988), may be sufficient. In this case, newborns may adapt to time-compressed speech successfully.
Humans can adapt to a wide range of variations in the speech signal, maintaining an invariant representation of the linguistic information it contains. Among them, adaptation to rapid or time-compressed speech has been well studied in adults, but the developmental origin of this capacity remains unknown. Does this ability depend on experience with speech (if yes, as heard in utero or as heard postnatally), with sounds in general or is it experience-independent? Using near-infrared spectroscopy, we show that the newborn brain can discriminate between three different compression rates: normal, i.e. 100% of the original duration, moderately compressed, i.e. 60% of original duration and highly compressed, i.e. 30% of original duration. Even more interestingly, responses to normal and moderately compressed speech are similar, showing a canonical hemodynamic response in the left temporoparietal, right frontal and right temporal cortex, while responses to highly compressed speech are inverted, showing a decrease in oxyhemoglobin concentration. These results mirror those found in adults, who readily adapt to moderately compressed, but not to highly compressed speech, showing that adaptation to time-compressed speech requires little or no experience with speech, and happens at an auditory, and not at a more abstract linguistic level.
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Speech experienced in utero, however, is different from broadcast speech transmitted through the air. Maternal tissues act as a low-pass filter, mainly transmitting sounds below 300–400 Hz (Gerhardt et al., 1992; Querleu, Renard, Versyp, Paris-Delrue, & Crèpin, 1988). As a consequence, prosody, the global melody and rhythm of speech, is relatively well preserved and transmitted to the fetal inner ear, whereas more detailed, phonetic aspects are disrupted (Querleu et al., 1988).
Experience with spoken language starts prenatally, as hearing becomes operational during the second half of gestation. While maternal tissues filter out many aspects of speech, they readily transmit speech prosody and rhythm. These properties of the speech signal then play a central role in early language acquisition. In this study, we ask how the newborn brain uses variation in duration, pitch and intensity (the three acoustic cues that carry prosodic information in speech) to group sounds. In four near-infrared spectroscopy studies (NIRS), we demonstrate that perceptual biases governing how sound sequences are perceived and organized are present in newborns from monolingual and bilingual language backgrounds. Importantly, however, these prosodic biases are present only for acoustic patterns found in the prosody of their native languages. These findings advance our understanding of how prenatal language experience lays the foundations for language development.
Neuromagnetic signatures of syllable processing in fetuses and infants provide no evidence for habituation
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Animal studies with hydrophones implanted into ewe's uteri indicate that our chosen stimuli are still discernible for fetuses in utero [35,36]. However, the level of sound attenuation was associated with fetal position and status of development [37]. On the basis of the findings of AERs to the different syllables, we can safely assume that acoustic features of the syllables were transmitted to the fetus and stimulated the fetal auditory system.
Habituation, as a basic form of learning, is characterized by decreasing amplitudes of neuronal reaction following repeated stimuli. Recent studies indicate that habituation to pure tones of different frequencies occurs in fetuses and infants.
Neural processing of different syllables in fetuses and infants was investigated.
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Magnetic brain signals of N = 30 fetuses (age: 28–39 weeks of gestation) and N = 28 infants (age: 0–3 months) were recorded. Forty-two of the 60 fetal recordings and 29 of the 58 infant recordings were included in the final analysis.
AERs were recorded and amplitudes were normalized to the amplitude of the first stimulus.
In both fetuses and infants, the amplitudes of AERs were found not to decrease with repeated stimulation. In infants, however, amplitude of syllable 6 (dishabituator) was significantly increased compared to syllable 5 (p = 0.026).
Fetuses and infants showed AERs to syllables. Unlike fetuses, infants showed a discriminative neural response to syllables. Habituation was not observed in either fetuses or infants. These findings could be important for the investigation of early cognitive competencies and may help to gain a better understanding of language acquisition during child development.
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However, hearing is operational from about the 24th to 28th week of gestation [37,38••,39], so experience with spoken language starts in the womb. What spoken language sounds like in the womb is not fully known, but existing intrauterine recordings in humans and in animal models suggest that maternal tissues act as a low-pass filter at around 300–400 Hz [40–42], transmitting most of the prosody and rhythm of spoken language, but much less of the individual phonemes (possibly some aspects of the vowels, but not the consonants). It has been known that fetuses can learn from this prenatal language experience [42,43], as newborns show a preference for their mother's voice [44] and for the language heard in utero [45].
Early experience with speech and language, starting in the womb, has been shown to shape perceptual and learning abilities, paving the way for language development. Indeed, recent studies suggest that prenatal experience with speech, which consists mainly of prosodic information, already impacts how newborns perceive speech and produce communicative sounds. Similarly, the newborn brain already shows specialization for speech processing, resembling that of the adult brain. Yet, newborns’ early preparedness for speech is broad, comprising many universal perceptual abilities. During the first years of life, experience narrows down speech perception, allowing the child to become a native listener and speaker. Concomitantly, the neural correlates of speech and language processing become increasingly specialized.
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A sustained heart rate (HR) deceleration, elicited by low-intensity stimulation, is considered part of Sokolov’s generalized orienting reflex and is a useful measure of information processing in nonverbal subjects. This study was undertaken to investigate developmental changes in the perinatal period in information processing during quiet sleep (QS). Twenty-six infants were tested as fetuses at 36–40 weeks and again as neonates at a postnatal age of 2 weeks. Quiet sleep was defined in the same way for fetuses and neonates, and the same airborne sound was used for fetal and neonatal testing. We found that stimulation elicited a sustained, monophasic HR deceleration in the majority of fetuses. However, the response was more heterogenous when these infants were tested after birth, with approximately half the 2-week-old infants exhibiting a prolonged HR deceleration and half exhibiting a HR acceleration. These data provide evidence that a developmental change may occur, between the prenatal and postnatal periods, in information processing during QS.
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Supported by National Institutes of Health Grant No. HD20084.

Presented at the American Speech-Language-Hearing Association in St Louis, MO, November 1989.

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Original contributionCochlear microphonics recorded from fetal and newborn sheep☆

Abstract

Eur J Obstet Gynecol Reprod Biol

Am J Obstet Gynecol

Early Hum Dev

Brain Res

Dev Brain Res

Hear Res

Am J Obstet Gynecol

Am J Obstet Gynecol

Am J Obstet Gynecol

Am J Obstet Gynecol

EEG Neurophysiol

Lancet

Perception auditive et reactivite foetale aux stimulations sonores

J Gynecol Obstet Biol Reprod (Paris)

The fetal sound environment of sheep

Science

The sound environment of the foetal sheep

Behavior

Recording the fetal lamb's sound environment using an implantable radio hydrophone

Physiol Soc

Characteristics of the fetal sheep sound environment

Semin Perinatol

Original contribution
Cochlear microphonics recorded from fetal and newborn sheep☆