The Fetus &&&&&&&&&&&&&& Evidence of Transnatal Auditory Learning Christine M. Moon, PhD hurdles to surmount in asking newborn infants whether they William P. Fifer, PhD have learned about specific sounds before birth. In order for transnatal retention of auditory experience to be possible, three key conditions must be satisfied. The fetus must There is converging evidence for fetal retention of auditory experience into be able to hear, there must be sound to detect, and the fetus early postnatal life, but critical tests with appropriate controls are rare due must have the ability to learn. There is much evidence that the to methodological hurdles. Research has been conducted on newborn intrauterine environment is acoustically rich (see Gerhardt and response to naturally occurring stimuli such as heartbeats, intrauterine Abrams, this volume), that the human fetus is capable of recordings, pre-and postnatal versions of the maternal voice, father's hearing (see Hall, this volume), and does respond to sound in voice, and unfamiliar voices. Postnatal experience cannot be ruled out as a the womb (see Abrams and Gerhardt, this volume). Bearing on possible explanation for many results. Only one critical prenatal exposure the learning question, there is growing evidence from non- experiment with postnatal testing has been carried out and published in a human animals and from humans that learning occurs prior to peer-reviewed scientific journal. Interpretation of acoustic and linguistic birth. Birds, e.g., learn about the calls of conspecifics while still information on intrauterine recordings suggests that the prosodic features in the egg, and the birds' own post-hatching vocalizations are of speech (pitch contours, rhythm, and stress) are available to the fetus. affected by this experience (see Lickliter, this volume). In This is compatible with newborn responses and may contribute to language addition to birds, non-human mammals have provided evidence acquisition during the first year. There is no sound evidence that providing of prenatal learning. For example, elegant experiments with rat extra prenatal auditory stimulation benefits the developing child, and there fetuses have demonstrated that it is possible to classically are potential risks. condition aversion to a specific odor prior to birth that affects Journal of Perinatology 2000; 20:S36±S43. the rat's behavior after birth.1 Empirical investigation into whether human learning can be LEARNING BY THE FETUS demonstrated during the fetal period has a long, if not replete, history. In 1932, Ray2 described a single subject classical Many, if not most, people believe that we can learn before we conditioning experiment. The CS was the clapper of an electric bell are born and that some of the things we have learned are gong, and it was placed so that it vibrated on the mother's abdomen. retained after birth. It is not difficult to find someone who can It was paired with the UCS that was fashioned out of two wood relate a personal or family story about a baby who seemed, blocks made to snap together by a spring from a rat trap, thus shortly after birth, to respond in a special way to a familiar making a loud sound. Problems with timing of stimulus voice or sound. Examples of such accounts are the 1-day-old presentation and fetal response interval prevented Ray from who turns to look in the direction of a family member visiting reporting the data. In 1948, Spelt,3 using the same methodology in the hospital room for the first time after the birth, or a an experiment with 13 pregnant women, measured four types of newborn who seems to reliably become quiet when a familiar fetal movement and concluded that classical conditioning of the piece of music is played. From this perspective, it is surprising human fetus had occurred, although incomplete information in the that although there is much converging evidence for human report renders independent interpretation of the results difficult. transnatal auditory learning, there are few carefully controlled More recently, Hepper4 referred to his replication of Spelt, but did not human studies on the topic. From the researcher's perspective, describe the experiment. If the literature on human fetal classical the paucity of published empirical studies in peer-reviewed conditioning is sparse, the literature on instrumental learning is journals that directly address transnatal learning is under- non-existent. standable. There are daunting methodological and practical Despite the paucity of research on fetal associative learning, several studies of fetal habituation learning do exist. Habituation Pacific Lutheran University(C.M.M.), Tacoma, WA 98447;Department of Developmental occurs when there is a reduction in fetal responding to a repeated Psychobiology(W.P.F.), New York State Psychiatric Institute;Columbia University, Box 40, 722 N. 168th St., New York, NY 10032. auditory stimulus, and the decrement cannot be attributed to sensory or response system fatigue.5,6 Demonstrations of habituation learning Address correspondence and reprint requests to Christine M. Moon, PhD, Department of Psychology, Pacific Lutheran University, Tacoma, WA 98447. are especially convincing when, after a decrease in responding to a Journal of Perinatology 2000; 20:S36 ± S43 # 2000 Nature America Inc. All rights reserved. 0743-8346/00 $15 S36 www.nature.com/jp Transnatal Auditory Learning Moon and Fifer repeated stimulus, the fetus begins responding anew when a that they are capable of retaining information about specific auditory discriminately different stimulus is presented. Recovery of both stimuli for at least 24 hours,23 including differentiating two words motor7,8 and cardiac9,10 responding to a change in auditory spoken by the same female speaker.24 These latter results bear stimulation has been reported for late-term fetuses (see Lecanuet strongly on transnatal learning because it is unlikely that the and Schaal11 for a review). demonstrated capacity for neonates to retain auditory information Repeated experience over longer periods of time than those over a longer period had its onset only once the infant has been born. afforded by the laboratory habituation or classical conditioning In addition to learning in habituation procedures, newborns have setting may result in learning by the fetus. This has been described as also shown that they can be classically conditioned, although it has exposure learning12 and may result in a preference formed by been difficult to do so.25 Results with instrumental conditioning are familiarity.13 ± 15 In one study of response to the mother's voice, which much more prevalent. For example, infants less than 4 days old can is presumably a familiar sound, 36-week-old fetuses did not learn in less than an hour that headturning26 or sucking on a tube 27 demonstrate a difference in numbers of movements (visualized via is rewarded with a sweet taste. Non-nutritive sucking has proven to ultrasound images) to a tape recording of the mother's versus a be a relatively malleable behavior in instrumental conditioning stranger woman's voice played through speakers placed directly on procedures with newborns. Butterfield and Siperstein28 described the mother's abdomen. But in a separate condition, fetuses of the changes in sucking by 24- to 48-hour-old infants as a result of same gestational age did respond with fewer movements when the hearing music that was either contingent or non-contingent on mother was actually speaking versus when presented with a tape sucking. DeCasper et al. have developed an instrumental recording of her voice.16 This may mean that 36-week-old fetuses conditioning procedure using non-nutritive sucking to assess cannot discriminate between the mother's and another female's newborn infant perceptual and learning capacities. In this procedure, voice, but can discriminate characteristics of the maternal voice that 1- to 4-day-old infants learn to activate and maintain different result from different means of transmission. Alternatively, the sounds presented through headphones by altering the duration of methods used in the study may not have been sufficiently sensitive to their pauses between sucking bursts (interburst intervals) and/or detect fetal ability to discriminate between the externally presented the duration of their sucking bursts.13,29 ± 34 In a variant of this non- voices. A more recent study using fetal heart rate suggests that it may nutritive sucking preference procedure, 2-day-olds can learn within have been the latter. Pregnant women recited one of two different 15 minutes to initiate sucking bursts during auditory signals for the children's rhymes daily between weeks 33 and 37 of their availability of preferred sounds.29,32,34 ± 36 The parameters of neonatal pregnancies. Fetal heart rate was monitored in week 37 during learning have been the focus of some recent studies using non- presentation of a tape recording of each rhyme separately. Heart rates nutritive sucking and auditory stimulation with investigators finding declined significantly during the rhyme that had been recited by the evidence for cognitive processes in newborns beyond simple mother, but not during the other rhyme.17 association learning.37,38 As with habituation learning, it seems If the results from all fetal learning studies are taken together, it unlikely that such capacities emerge only during the first day after appears that there is some evidence for human prenatal learning birth. although more research is certainly warranted. Another potential source of information about fetal learning is the neonate. It seems unlikely that birth marks an abrupt change in the perinate's ability NATURALLY OCCURRING SOUNDS to learn. Indeed, learning by the premature infant supports this, If we accept that fetuses can learn about sounds that they hear in although it is difficult to study the learning capacities of these infants utero, then it becomes reasonable to ask whether there is any due to their fragility 18 plus their range of medical conditions and indication that newborns respond differentially to sounds that state lability.