Music during pregnancy

Ultrasound Obstet Gynecol 2002; 20: 425– 430

Opinion

Blackwell Science, Ltd

Opinion

Music during pregnancy

‘Music was my first love, it will be my last, music of the future, music of the past’. This text of the song of John Miles1 holds true for many of us independent of our cultural background.

Music exists in the passage of time and cross-culturally. It is thought that musicality is structured by an ensemble of protorhythms of biological inheritance2. The hypothesis that music has prenatal origins, does not necessarily explain its survival value3 but possibly some of its cross-cultural features comparable to rhythmic elements in utero. Nevertheless, there is a complete absence of cross-cultural studies on the effect of music on the fetus and infant. In many cultures, lullabies have been sung for centuries to soothe babies. Thereby different elements might be effective such as the pure effect of music but also the combination of a musical experience expressed by the mother’s voice—the voice that represents a salient stimulus throughout the perinatal period with continuity from prenatal to postnatal life—and thus forms a sensory bridge into postnatal life that is hardly available from other prenatal sensations. The mother’s voice has been proven to have an impact on the developing brain4. At birth, newborns react to musical rhythms of speech5 and thus orient to the social world. It is even hypothesized that this relationship is essentially ‘musical’ because babies do not yet understand the meaning of words. By listening to the mother the fetus obviously stores her musical speech-features (‘prosody’).

Hearing has a close relation to the ‘auditory–vocal–kinetic channel’6, consequently spectrography of the first cries has proved that even newborns born at 28 weeks had similar rhythmic voice performance features to their mothers7.

Since the prenatal experience of music cannot be completely separated from that of the maternal voice, both sound stimuli will be considered in this article.

Throughout childhood and adulthood music has been used therapeutically to reduce stress and pain, in children with developmental disease or in the elderly with cerebral disease whose verbal communication (just like in the fetus) is limited. The physiology of the auditory pathway and its interconnections with nuclei known to be involved with pain inhibition suggests that auditory stimuli may contribute to pain relief. ‘Baby-go-to-sleep-tapes’ timed to an adult heartbeat were used to determine the modulating effect of music on pain experience. After procedures to obtain blood samples babies exposed to music had lower pain ratings detected from videotapes and higher oxygen saturations9.

Music therapy has been used in the treatment of children who are mentally, physically or multiply handicapped to encourage them to use non-verbal communication and to foster the use of coordinated movements, which occur in a context of rhythmical music. In a crossover study in children with developmental delay, music therapy improved their development in comparison with a control group without

OPINION

music therapy (patients on a waiting list). The significant parameters were hand–eye coordination, personal–social interaction and improvement in hearing and speech10.

Investigations of the immediate effects of sound can elucidate the development of the auditory system, autonomic reactivity and processing of sensory information. Research into the enduring effects is much more complex but may shed light on the development of memory, attention, as well as language and cognitive development4. To differentiate the role of sound, most studies have up to now concentrated on the time after birth primarily for methodological reasons. However, it is realized that in human development there is continuity from prenatal to postnatal life. Parents nowadays may be overwhelmed by conflicting information relating to ‘the prenatal origin of later capabilities or disease’. Basic questions, which I would like to comment on in this article, are summarized as follows:

HO W E A R L Y C A N W E DE T E R M INE A N INFL UE NC E O F S O UND A ND M U S I C O N T HE F E T US ?

For a long time it was a philosophical rather than a scientific question how early sensory abilities are acquired. Aristotle anticipated that sensory development is a quiet process of the prenate gradually responding to an extrauterine world.

However, until the 19th century negative thinking was more common: Rousseau referred to the fetus as a ‘witless tadpole’.

First scientific approaches to detect fetal hearing capacities were performed by Preyer in 188511. Paradoxically, studies on the onset of fetal responses to sound have used a variety of unphysiological stimuli, not always with rationale, such as a car horn12, a metal stick while mothers are lying in a water bath13, smacking of boards14, electric tooth brushes15 or vibroacoustic stimulation devices (VAS)16. There are hundreds of studies on VAS as a test of fetal well-being from 1980 onwards. The differentiation between airborne sound and vibration possibly stimulating the skin was a source of discussion. However, in lambs with bilateral cochlear ablation no reactions towards VAS could be registered, indicating that the auditory apparatus is necessary for responses17. Similarly, no reactions were found when VAS was used in deaf fetuses (Hepper, personal communication). This seems to prove that hearing abilities depend on cochlear function.

All described experiments were performed after 26 gestational weeks. However, the start of hearing does not seem to be an all or nothing phenomenon. Fetuses from 19 weeks onwards were presented with tone frequencies of 100– 3000 Hz. First responsiveness was detected at 23 weeks at 500 Hz, at 27 weeks to 100–500 Hz and at 31 weeks responses were observed to 1000–3000 Hz18. Responsiveness to sound

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Opinion before that age has even been described19. Developmental origins were systematically examined using 80–2000-Hz broadband stimuli between 15 and 25 gestational weeks.

When changing the stimulus from a single sound to a series of ten 2-second pulses, an increased number of fetal movements (FM) was found even at 20 weeks20.

Knowledge of embryology is a prerequisite for understanding the onset of hearing abilities (as we have summarized21).

From 10 weeks onwards, the external ear is visualized by ultrasound. The outer ear collects sound energy shaping it towards the tympanic membrane. The ossicles of the middle ear reach full size by 18 weeks. Only then do they become ossified and are of adult size by 36 weeks. At 7 weeks, the eustachian tube and the tympanic cavity are formed where acoustic energy is transduced into mechanical energy. The inner ear consists of membranous tissue within a bony labyrinth. Ossification does not occur until each portion has attained adult size. Hair cell differentiation, synaptogenesis and ciliogenesis are completed at around 24 weeks and form the basis of the frequency-related displacement of the cochlear partition revealed by the Nobel laureate von Bekesy22.

With the entry of the acoustic nerve into the brainstem, auditory neurons multiply and project the information to the auditory cortex. Many auditory abilities are attributable to subcortical processing. This explains why decorticated animals are capable of detecting intensity and frequency of sounds and even anencephalic fetuses demonstrate reactions to external stimuli23.

WHI C H K I N D OF SOUND STIMULI ARE O F INFL U E N CE THROUGHOU T DEV E L O P ME N T ?

Fetal acoustic challenges may derive from two environments: the ‘intrauterine world’ includes stimuli caused by maternal circulation, digestion and finally the mother’s voice and singing.

As birth approaches, sound stimuli from the ‘extrauterine world’ are increasingly responded to.

Some basics about acoustics are a prerequisite to understand the specific fetal situation21: sound is created by a vibratory source, causing molecules to be displaced. The amplitude is measured in Pascals (Pa). Sound pressure level (SPL) and frequency are given in decibels (dB) and Hertz (Hz). The SPL required to evoke a fetal response is 20–30 dB less at 35 than at 23 weeks, indicating that the fetal auditory system becomes more sensitive with prenatal age18. However, changes in attenuation, behavior and senso-motor neural connections might also have an impact. The range of 20–20 000 Hz is the bandwidth of human hearing.

Information about prenatal hearing has been mainly obtained from sheep experiments since prenatal auditory sensitivity and sound attenuation are similar in sheep and humans24–26. The bone conduction route implies that sound energy is diminished by 10–20 dB for frequencies < 250 Hz and by 40–50 dB for frequencies > 500 Hz. A reason for fetal ‘sound isolation’ is the sound pressure attenuation. Thereby, transmission losses range from 39 dB at 500 Hz to 85 dB at 5000 Hz. Sound attenuation decreases during late gestation. In humans, sound of at least 65–70 dB

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Arabin is transmitted with attenuation of 30 dB in SPL for tones up to 12 kHz. Frequencies of 200 Hz are even enhanced. Sound environment in utero is dominated by frequencies < 500 Hz and mean SPLs of 90 dB caused by vessel pulsations, intervillous injections, maternal digestion or breathing. This might have an ‘imprinting’ effect. Intelligibility is the ability to distinguish complex sounds. Music and voices are distinguishable from the basal noise by 8–12 dB. The male voice or music with a mean frequency of 125 Hz is better transmitted but its frequencies resemble the frequencies of the internal noise in utero (and are thus more difficult to distinguish). Female voices or music with an average of 220 Hz receive greater attenuation, but the higher sound frequencies are outside the range of the main noise frequencies in utero (and are thus easier to distinguish).

Even intelligibility has developmental aspects27. Using a habituation–dishabituation technique fetuses aged 35 weeks could discriminate between frequencies of 250 and 500 Hz and between speech sounds, whereas fetuses of 27 weeks were unable to make this differentiation, though they differentiated between a 250-Hz pure tone and 80–2000-Hz broadband sounds.

W HA T A R E T HE IM M E DIA T E P R E NA T A L R E S P O NS E S A ND W HA T M E T HO DS A R E A V A IL A BL E T O DE T E R M INE T HE M ?

To demonstrate the existence of prenatal acoustic perception, one can empirically study immediate electrophysiological and behavioral (motor and cardiovascular) responsiveness.

Prenatal electrophysiological responsiveness is obtained by recordings of electric potentials from levels of the auditory system by means of non-invasive techniques based on compound potentials. They represent the activity of many cells by stimulus-related electroencephalographic (EEG) and magnetoencephalographic (MEG) methods. Fetal EEG responses towards acoustic signals have been performed after ruptured membranes using scalp electrodes28,29. In MEG recordings, sensitive magnetic field detectors are used to measure prenatal neuromagnetic auditory responses to clicks of 1 kHz up to 100 dB with intact membranes. Stimulus-related auditory evoked neuromagnetic fields were recorded at 34 weeks30,31 comparable with postnatal recordings. In a more recent study, the earliest recording of evoked neuromagnetic fields was made at 29 gestational weeks. The latencies of the auditory evoked responses declined during the third trimester from 300 ms to nearly 150 ms at term32. Prenatal behavioral responsiveness has been used because an association of neonatally evoked potentials with heart beat and motor responses implies the reception of the auditory signals up to subcortical levels33. Due to the present lack of routine technology to record neural activity in the womb, fetal sensory abilities are examined by observing behavioral reactions.

Appropriate methodology has to be used to ensure that stimulus and response are correlated. Problems arise when the fetus does not react, since we cannot say that the stimulus is not sensed.

Ultrasound observations allow defining motor responses such as ‘twinkling’ of the eyelids and body, head, arm and leg movements34. The methodology can be simplified by using Doppler devices for detection of FM quantifying all FM

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Opinion responses with a high sensitivity and specificity35. Using this method we observed first fetal reactions towards acoustic stimulation at 25 weeks. With increasing gestational age, an increasing number of FM combined with fetal heart rate (FHR) accelerations and reactions with a change of FHR baseline of longer duration up to several minutes is observed.

Some factors influence fetal responsiveness, such as the behavioral state before or during the stimulus36 or gender15.

Fetal responses to speech stimuli were studied between 26 and 34 weeks gestation. During periods of low FHR variability, a decrease in baseline and an increase in the deviation of FHR were found37. This is a demonstration of prenatal responses to speech stimuli, whereby the response depends on a kind of fetal state38. Female fetuses seem to respond earlier than males to acoustic stimuli15.

W H A T A R E T HE ENDURING EFFECTS A N D W H AT ME THOD S ARE AVAI LAB LE F O R DETE RMIN ING THEM? Considerable attention is given to the possibility that the fetus forms memories of speech and music that may influence postnatal development. In the past, most studies have used behavioral responsiveness of the fetus and the newborn. Short-term memory is reflected by habituation, which had been described by Peiper in 1885 reporting a decrease in FM after repeated stimulation12. Since then a number of studies have demonstrated a decrease in response to repeated stimulation using FHR/FM or ultrasound documentation. Habituation may be distinguished from fatigue by the recovery of response on presentation of a new stimulus (‘dishabituation’) and faster habituation upon re-presentation of the stimulus39.

The intensity influences habituation time (faster habituation to more intense stimuli). Refractory time of habituation processes were studied40 and responses to sound were observed as one major focus for fetal conditioning41,42. Habituation experiments in the fetus or newborn typically take place over a period of minutes and demonstrate that the infant retains sound characteristics long enough (up to 24 h)16 to compare them with a new signal.

There is also proof of long-term memory from pre to postnatal life43, whereby the term ‘fetal learning’ or ‘fetal enrichment’ should still be used with caution. Prenatal sound experience might influence postnatal sound preference and fine-tune the developing auditory system44. Neonates have been taught that, if they produce a specific sucking pattern altering the duration of their pauses between sucking bursts and/or the duration of their sucking bursts, they may listen to their mother’s voice via headphones. Using this non-nutritive ‘high-amplitude sucking procedure’, newborns prefer the voice of their mother to other voices and even a lullaby, which had been presented by the mother during the last weeks of pregnancy45 suggesting elementary prenatal sound acquisition and discrimination Prenatal exposure to sound may also have an effect on neonatal performance. Sound stimulations recalling intrauterine noise serve as a reinforcer during sucking and can lull the newborn to sleep46. Similarly, postnatal feeding may be enhanced by background music47. Settings of talking and

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Arabin music were performed during pregnancy48: within the talking group, only 58% of newborn behavioral variables were identified as positive (e.g. the child being easily comforted), 16% as ambiguous and 26% as negative (e.g. crying for obscure reasons, needing constant supervision). However, within the group exposed to music, 90% of the newborns presented with positive attitudes. It is speculated, whether variations of timbre expressing care, anger or anxiety or maternal hormonal changes associated with speech and music evoke associations in the infant. Pilot studies have demonstrated a simultaneous reduction of fetal breathing and an increase of FM, when only mothers listened to a preferred type of music via earphones49 proving certain forms of conditioning (‘music, mother relaxed’). Time to listen separated from surrounding influences may itself be an important intervention. Whether the unborn is more affected by the mother’s emotions during listening or singing than by the pure sound is still uncertain.

In China, children who had been exposed to music stimulation during pregnancy and the neonatal period were followed by the ‘Gesell Infant Scale’. After 5 and 12 months postpartum, some abilities such as sitting, staying and walking were observed earlier compared with a control group50. In Venezuela, weekly lectures to pregnant mothers about nutrition were combined with music stimulation. Significant improvement was found postnatally in orientation and autonomic stability of the infants in the experimental compared with a control group51. In England, Lamont has demonstrated that prenatal stimuli with music induce memory tracings that can still be detected after 1 year independent of the intelligence of the mother or the kind of music (BBC program ‘Child of our Time’, 2000). Preferred types of music were characterized by fast rhythmic patterns52.

Studies investigating an influence of music and sound on later development (‘prenatal learning’) have used developmental tests such as the ‘Early Language Milestones’ (ELM) test, the Brazelton and the Denver Developmental screening test, the Gesell Infant and the Bayley Scale of Infant Development53. However, these tests are sensitive for subjective interpretations and may even lead to ambiguous interpretations when the investigator relies too much on information of the parents54.

Hypothesizing that behavioral research can produce no standardized evidence on sound feature discrimination, some groups have used electrophysiological methods in newborns.

Sensory processes underlying sound perception have been studied using the mismatch negativity (MMN) component of auditory event-related potentials (ERPs), which is not contingent on conscious perception. Thus, MMN may be suitable for studying newborns, from which it is difficult to obtain behavioral responses. Recent studies have investigated newborns’ preattentive analysis of sound duration and frequency changes. The majority of neonates appear to possess effective discrimination mechanisms, which is facilitated by rich sound content55. The temporal dynamics of auditory sensory memory has been studied in newborns that were either awake or asleep with stimuli of 1000 Hz tones that were occasionally replaced by 1100 Hz tones. The results imply that the time span of auditory memory is considerably shorter in neonates than in adults56.

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Opinion Event-related brain potentials (ERPs) elicited by music have not yet been investigated in newborns or children. In adults, however, how music processing is influenced by a preceding musical context has been investigated. The amplitudes of both early and late negativities were found to be sensitive to the degree of musical expectancy and to the probability for deviant acoustic events. The results strengthen the hypothesis of an implicit musical ability of the human brain57.

Impure chords, presented among perfect major chords elicited a distinct MMN in professional musicians, but not in non-musicians58. The results demonstrate that musicians are superior in extracting information out of musical stimuli and that training might modulate sensory memory. Whether this holds true for the fetus or newborn is not yet known.

CAN WE E X P E CT ANY EDUCATI ONAL , PRE VE N TIVE OR THERAPEU TI C EFFEC T FRO M CU RRE NT D ATA, ARE THERE SPEC IF IC SE N SITI VE PERI OD S AND HO W SHO U L D W E D IRECT FUTURE RESEAR C H ?

One of the goals of this article is to report on information that could assist in critiquing the findings of former studies on prenatal hearing and ‘learning’, helping in decision-making for what might have a positive effect on both mother and child and in directing further research.

The short history of research relating to prenatal perception and its implications for further life highlight that physiological stimuli combined with modern technology should be applied in order to understand the physiology of the sensory developmental process, to create stimulative interventions and understand or even prevent pathological development.

In order to fulfill any criteria of transnatal retention of auditory experience—what is called in the paper in this issue of James et al. ‘fetal learning’59—some key conditions must be satisfied: the fetus must be able to hear, the sound must be detectable within the acoustically rich amniotic environment and the fetus must be capable to form memories. Our ability to learn, retain information, recognize individuals or recall previous events all depend on memory. Newborns have shown via a variety of learning paradigms to possess a functioning memory60. The term ‘fetal learning’ as used in the article of James et al.59 includes more than just habituation (the authors might underestimate their work) relating to remaining memorization and thus to associative learning. Repeated experience over longer periods of time than those afforded by the usual laboratory habituation setting was applied and is demanded when terms such as ‘learning’ are used. If the results of the here-described studies including that of James et al.59 are evaluated, there is evidence for prenatal learning although more research is certainly warranted. An important source of information about fetal learning capabilities is still the neonate. The strength of the study of James et al.59 is not only their strictly designed concept (Table 5), but also that they try to reproduce the effects of music stimulation before and after birth. Thus they stress the fact that it is unlikely that birth makes an abrupt change in the prenate’s ability to learn.

In most experiments dealing with the prominence of the maternal voice to other voices45 it is difficult to rule out some

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Arabin effect of postnatal experience. However, there are some studies in which postnatal experience was excluded. Hepper et al. studied the effect of prenatal music exposure of a television soap opera on infants of 2– 4 days, which their mothers had watched during pregnancy61. The ‘TV learning group’ experienced a decrease in heart rate and movements and a change to a more alert state while listening to the same melody 2– 4 days after birth. No reaction was observed in the control group of mothers who had not observed the program or in newborns of the study group exposed to other melodies.

Since none of the infants had heard the melody after birth it was suggested that the fetus can learn not only from the maternal voice but also from deliberate ex utero environmental sounds throughout the perinatal period. However, neonates also seem to have the ability to forget in the absence of repetitive exposure: by day 21, recognition of the melody seemed to be lost61. The prenatal response to the TV theme had been investigated using real-time ultrasound. It was concluded that the ability to recognize familiar stimuli starts between 30 and 37 weeks.

Nowadays, ‘instruction programs’ for mothers on how to stimulate their unborn children have emerged even before basic research has proven that the stimuli might enhance postnatal cognitive functioning and neuromotor development. However, it has been established that a great number of functions of the central nervous system depend on its maturational status62,63 so that it might be doubted that sensual stimulation may enhance physiological ripening at such an early stage. From all studies cited in this article on the fetal exposure to sound experience, such as talking, singing or listening to music, it seems that the influence on postnatal behavior such as presenting with more stable rhythms or being more easily comforted is not so much based on the pure sound effect but more on creating an environment for the start of a caring relationship64.

Given the fact that the fetus is exposed to ongoing sound in utero, to the voice of the mother whenever she speaks or sings and to the ambient sound level of the maternal environment, it seems that exaggerated acoustic stimulation with unphysiological frequencies and intensities by audio speakers or megaphones—just in order to get any reaction—might even be risky for hearing development and behavioral state regulation in the unborn child and reminds me of the uncritical use of VAS to evoke some FHR changes65,66. Promoting these instruments in order to enhance neuronal ripening except within defined research trials seems therefore illogical. Conversely, several commercial products are recommended such as little bells to wear on chains throughout pregnancy, which have been proven to be without any effect on the fetus since the sound cannot even reach intrauterine hearing thresholds.

Recent investigations have been directed towards fetal– maternal heart rate coordination by magnetocardiograms. It was demonstrated that the coordination of a maternal–child pair is higher than between incidentally chosen mothers and fetuses67. It would be interesting to know whether this has an acoustic origin and whether the coordination might be enhanced by rhythmic music.

A new area of research is summarized as the ‘fetal origin of adult disease’ whereby neural programming is a completely

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Opinion new field. Data show, in model species, that antenatal exposure to glucocorticoids produces hypertension, hyperglycemia or hyperinsulinemia, but also alters behavior and neuroendocrine responses throughout the lifespan68. Analogous stress axis hyperreactivity may indicate approaches to manipulation or prevention of the phenotype. The extent to which early music stimulation in obstetric risk patients with preeclampsia and/or intrauterine growth restriction or the continuation of music therapy during childhood would help to reduce some of these risks is speculative and difficult to evaluate since many other factors have an impact on the development between early interventions and adult age.

Nevertheless, it has been proven in randomized trials that music therapy is effective in reducing stress and relieving fear and anxiety in patients admitted to an intensive care unit69.

Magnetic resonance findings and spectroscopy might be a future tool for evaluating brain function in the high-risk newborn and even possibly for detecting anatomical and functional differences between various interventions70.

Based on the articles cited here, of James et al. in this issue59 and my personal opinion of the general importance of creative arts and research to our development involving natural curiosity, I would like to make some proposals on the design of trials addressing the influence of music on the prenate. Thereby the concept of a caring relationship (‘dare to care’) should be the primary goal instead of just enhancing cardiovascular and behavioral reactions of doubtful importance for the infant.

1 Pregnancies included in studies should be a homogeneous group consisting of women with normal singleton pregnancies. In such a group, the difference of various types of speech and music as well as maternal preferences could be investigated. Furthermore, the influence of the maternal reactions on music (headphones with music) might be further differentiated from the influence of sound on the fetus (microphones to the abdomen but mother with headphones without sound).

In addition, the influence of maternal or paternal singing (various rhythms) to the child might be investigated. Thereby the specific acoustic conditions for the fetus should be considered. Cross-cultural studies would possibly bring further insights regarding anthropological perspectives.

2 Pregnancies included in the described design could also be twin pregnancies in order to investigate the effect on both twins (homogeneous? different?) and the correlation with gender, zygosity or intrauterine weight (supposing different neuronal ripening).

3 Pathological pregnancies might be used to investigate whether music might be of positive influence on the mother (stress reduction), fetus or both in controlled trials.

4 Ultrasound methodology such as ‘four-dimensional (4D)’, computerized FHR and FM detection will be improved which will make antenatal behavioral evaluation including state changes easier. Outcome has to be determined by behavioral and follow-up developmental tests and by electrophysiological and new imaging methods, which might contribute to more standardized and reproducible data exploring neurodevelopmental aspects.

Health is understood as the physical, mental and social wellbeing that goes further than just the absence of suffering. As important as it is to teach children abilities at certain times,

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Arabin we cannot exclude that integrated physiological musical stimulations for the unborn, the neonate and the infant might favor development or prevent sensory retardation. This might be a matter of concern of public health projects.

Encouragement and avoidance of stimuli have to be balanced in observational or interventional projects according to critical developmental phases striving to understand the early physiology and pathophysiology of our sensory system and to create designs suitable to induce a comprehensive expression of our genetic potential.

Addendum: This article was written while the author was exposed to music stimulation recalling prenatal and infant environment.

B. Arabin*† *Clara Angela Foundation, A. Herrhausen Str. 44/58455, Witten, Germany †Isala-Clinics (Sophia) 8025 AB Zwolle, Netherlands (e-mail: clara-angela@wxs.nl or clara-angela@t-online.de)

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Opinion 18 Hepper PG, Shahidullah S. Development of fetal hearing. Arch Dis Childh 1994; 71: 81–7 19 Hepper PG, White R, Shahidullah S. The development of fetal responsiveness to external auditory stimulation. Presented at the Br Psychol Soc, London, 1991: 30 20 Shahidullah S, Hepper PG. The developmental origins of fetal responsiveness to an acoustic stimulus. J Reprod Infant Psychol 1993; 11: 135–41 21 Arabin B, van Straaten I, van Eyck J. Fetal hearing. In: Kurjak A, ed.

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