Thus, 3-weeks of prenatal exposure to a specific melodic contour affects infants ‘auditory processing’ or perception, i.e., impacts the autonomic nervous system at least six weeks later, when infants are 1-month old. Our results extend the retention interval over which a prenatally acquired memory of a specific sound stream can be observed from 3–4 days to six weeks. The long-term memory for the descending melody is interpreted in terms of enduring neurophysiological tuning and its significance for the developmental psychobiology of attention and perception, including early speech perception, is discussed.

Here we show that auditory memories can last at least six weeks. Experimental fetuses were given precisely controlled exposure to a descending piano melody twice daily during the 35 th , 36 th , and 37 th weeks of gestation. Six weeks later we assessed the cardiac responses of 25 exposed infants and 25 naive control infants, while in quiet sleep, to the descending melody and to an ascending control piano melody. The melodies had precisely inverse contours, but similar spectra, identical duration, tempo and rhythm, thus, almost identical amplitude envelopes. All infants displayed a significant heart rate change. In exposed infants, the descending melody evoked a cardiac deceleration that was twice larger than the decelerations elicited by the ascending melody and by both melodies in control infants.

Introduction

Human hearing develops progressively during the last trimester of gestation. By 35weeks Gestational Age (GA), cochlear biomechanics and frequency selectivity are mature and absolute auditory thresholds are about 10 dB Hearing Level in the premature infant [e.g., 1]–[4]. Near-term characteristics of fetal cardiac responses to airborne sounds demonstrate that fetuses can discriminate intensity, frequency and spectra [5]–[11] and can also process some fast and slow amplitude temporal variations in auditory streams [12], [13], [14]; see [13], [15] for extended reviews. Fetal MEG studies, using the Mismatch Negativity paradigm with tone bursts, confirmed that detection of frequency changes occurs in utero [e.g., 16]–[19] and shows that it happens very early in development, at 28 weeks GA [17], [19], therefore only 2–3 weeks after the onset of cochlear function [1]. Auditorially evoked cortical activation has been confirmed with fMRI in the near-term fetus [20]–[21], and as early as 33 weeks GA [22]. Learning studies (see below) indicate that fetuses can also perceive temporal variations in the spectra and in amplitude of complex auditory streams such as speech sequences.

For airborne sounds recorded within the amniotic fluid in the gestating ewe [e.g., [23] –[24]] and in women during delivery [25]–[28], power-spectrum analyses show that most components over 60 dB SPL (Sound Pressure level, re: 20 µPa) in the mother's near field environment are transmitted with little distortion into the uterus and, in general, are not masked by internal sounds. Frequencies ≤0.4 kHz are not attenuated; attenuation increases with frequency at a rate of about 6 dB/octave but never exceeds 30 dB above 4 kHz. The transfer functions of complex sounds are themselves more complex and their overall attenuation is lower than that of tones and band noises, e.g., voice attenuation depends on external SPL [29], music is attenuated ≤10 dB SPL in the gestating ewe [30]. In contrast, the maternal voice itself suffers no or little attenuation in the womb [25]–[28].

Near term fetuses and newborns can remember simple and complex sounds that frequently occurred earlier in prenatal life. Here, we will refer to fetal auditory memory when fetuses or infants respond to a sound they had previously and frequently experienced before birth differently than do non-exposed fetuses or infants. It has been examined in three developing psycho-biological domains [31], state or fetal motility, cardiac autonomic responses and associative learning. The state modifications investigated in the fetus were change from a non-active to an active state, habituation rate of gross body movements, changes in behavioral state and state transitions. In the neonate, state changes include the passage into a quiet-alert state, orientation and attention to the stimulus. The cardiac response examined was cardiac deceleration. The associative learning that was studied includes classical conditioning of movements in the fetus, and operant learning in the newborn. These responses differ in their degree of reflexivity, sensory-motor integration, precision of the motor behavior engaged and auditory processing required to resolve the stimulus (stimulus complexity). Memories have been found up to three-four days after birth and prenatal memory effects beyond this period is unknown. Our study assessed memory for a melodic sequence that fetuses repeatedly experienced in utero after a 6-week retention interval, when they were 1-month old infants. A review of the data supporting the phenomena of prenatal auditory memory in three psycho-biological domains follows.

Prenatal studies Habituation of fetal gross body movements and heart rate responses to loud airborne noises and tones [e.g., 32]–[34], or vibro-acoustic stimuli placed against the mother's abdomen [e.g., 35]–[41] have been extensively studied mostly for clinical reasons since the early eighties. Prenatal memory has been mostly investigated by comparing habituation and re-habituation rates of gross movements. Vibro-acoustic studies show a savings in the number of trials to re-habituation after a 10 min delay in fetuses ≥30 weeks GA, independently of GA, after a 24 hours delay [e.g., 42]–[43], a 4-week interval with first habituation at 34 weeks GA [43], or 1–2 days after birth when habituation occurred in the days before birth [44]. It should be noted here that vibro-acoustic stimuli provide tactile and auditory stimulations to the mother and auditory, tactile, proprioceptive and vestibular stimulations to the fetus. Most stimulators have a wide frequency band with fundamental frequencies and first overtones ranging from 75 to 300 Hz. They have a medium-high SPL in air (70–80 dB) but they are highly amplified inside the amniotic fluid, e.g., ≥110 dB intra-uterine level in the gestating ewe [45]–[46]. Abrams et al. found that the ranges of the fetal lamb head accelerations were proportional to the vibrators' SPL inside the amniotic fluid [46]. Therefore, they do not give any clear information about prenatal auditory learning per se. Perhaps, a real-world expression of long term habituation to loud noises is provided in the studies done near Osaka's International Airport: Infants of mothers who lived there before the third trimester of pregnancy did not wake up and had little or no EEG reaction during sleep to a recorded aircraft noise at 80 dB SPL but were awakened by an 80 dB SPL music sequence that had similar spectra [47]. Two experiments indicating classically conditioned movements, with startling noise or a vibro-acoustic stimulus as the unconditioned stimulus and milder vibro-acoustic or tone stimuli as the conditioned stimulus, were reported during the last 2-months of gestation [34], [48]. They suggest that prenatal memory can last several weeks. For example, successful conditioning was reported in 32–39 weeks GA fetuses and successes were independent of GA [34]. Interestingly, such association was shown in a fetal chimpanzee and the conditioned response was observed two months after birth [49]. Fewer studies have examined the effect of repeated exposure to complex auditory streams within the fetal period. Musical stimuli are reported to elicit an increase in movements [34] or in mean Heart Rate (HR) and HR variability in familiarized fetuses compared to control fetuses [50]. Two studies investigated prenatal auditory memories when mothers recited a specific speech passage aloud each day, one between the 35th–38th weeks GA [51] and another from 28–34 weeks GA [52]. When tested with a tape recording of their target stories and a control story, the target stories elicited a brief cardiac deceleration and the control story did not. The stories were emitted at a low SPL that does not usually evoke a HR change. In both cases, differential responding elicited by the target passage was independent of the speakers' voice used during the test. Other studies showed that the heart rate of fetuses exposed to a long recording of their mother's voice or a female stranger's voice saying the same speech passage are different [e.g., 53]–[54].