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Prenatal experience with low-frequency maternal-voice sounds influence neonatal perception of maternal voice samples
INFANT
BEHAVIOR
AND
DEVELOPMENT
10,
13%142
(1987)
Prenatal Experience with Low-Frequency Maternal-Voice Sounds Influence Neonatal Perception of Maternal Voice Samples MELANIE
J. SPENCE
The University of Alabama at Birmingham
ANTHONY
J. DECASPER
University of North Carolina at Greensboro By sucking on a nonnutritive nipple in the presence of one discriminative stimulus, newborns were reinforced with a low-pass filtered tape recording of their mothers’ voices. Sucking in the presence of a different discriminative stimulus was reinforced with unfiltered maternal-voice recordings. Filtered versions simulated maternal-voice sounds that were available before birth and unfiltered versions simulated maternal-voice sounds available after birth. Newborns in the control group could be reinforced with the same stimuli in the same way, but the voices were unfomiliar to them. Infants hearing their mothers’voices had no preference for either version, but infants hearing the unfamiliar voices preferred the unfiltered version. The difference in the between-groups responsiveness to the low-poss voice samples is consistent with the hypothesis that prenatal experience with low-frequency characteristics of maternal voices influences early postnatal perception of maternol voices.
prenatal
sensory experience voice oerceotion
auditory preception maternal voice auditorv
newborn oreference
perception
Human newborns prefer to hear the acoustic properties of a speech passage their mothers had recited when pregnant over those of a passage that their mothers had not recited (DeCasper & Spence, 1986). This preference implies that the newborns had been prenatally exposed to the acoustic properties of the recited material, for example, its pattern of syllabic beats, the voice-onset-time This research is part of a dissertation submitted to the University of North Carolina at Greensboro by Melanie J. Spence and was presented at the International Conference on Infant Studies, Los Angeles, CA, April 1986. The project was supported by a Research Council Grant from the University of North Carolina at Greensboro and a generous equipment loan by Professor Michael D. Zeiler. We wish to thank the medical and administrative staff of Moses H. Cone Hospital, Greensboro, NC, and especially, the mothers and their infants for making this research possible. Thanks also to David Soderquist for the use of his laboratory equipment and his help in preparing stimulus materials, and to Robin Panneton for her assistance in data collection. Correspondence and requests for reprints should be addressed to Melanie J. Spence, Sparks Center for Developmental and Learning Disorders, University of Alabama at Birmingham, P.O. Box 313, University Station, Birmingham, AL 35294. 133
134
SPENCE
AND
DECASPER
of its stop consonants, the harmonic structure of its sustained vowel sounds, and/or the temporal patterns of these sounds. It also implies that the newborns had been exposed to the acoustic cues that specify the mother’s voice per se and her habitual ways of speaking, for example, the spectra of her nasals and vowels, her glottal frequency and spectrum, and/or the temporal characteristics of the pitch and intensity of her stressed and unstressed vowels (Bricker & Pruzansky, 1976). Since prenatal experience with a specific passage can engender a postnatal preference for that passage, it is possible that prenatal experience with specific maternal-voice cues can engender the postnatal preference for the maternal voice (DeCasper & Fifer, 1980; Fifer, 1981). In principle, this hypothesis could be directly tested by manipulating the amount of maternal speech that occurs during pregnancy. In fact, such a manipulation would be unethical and impractical. Thus, only indirect tests of the hypothesis can be achieved. Maternal-voice cues that could subserve newborns’ discrimination of and preference for their mothers’ voices are presently unknown, although there are several likely possibilities (Gottlieb, 1985). However, if the functional significance of the mother-specific voice cues is established before birth, it is highly probable that cues dependent upon maternal speech frequencies below 1 kHz are especially important. Intrauterine recordings indicate that virtually all the acoustic energy available to the fetus is carried by frequencies below 1 kHz, and the intensity of higher frequencies is severely attenuated by maternal tissue (Querleu & Renard, 1981; Vince, Armitage, Baldwin, Toner, & Moore, 1982; Walker, Grimwade, &Wood, 1971). Furthermore, prenatal auditory functioning, which occurs in a fluid environment, may involve mechanisms similar to those used in bone conduction (Rubel, 1985), a process that efficiently transmits the lower frequencies (Aslin, Pisoni, & Jusczyk, 1983; Tonndorf, 1976). Thus, a corollary of the hypothesis is that prenatal experience with low-frequency maternal-voice cues influences neonates’ perception of maternal voices. The corollary can be used to generate a variety of testable predictions. The rationale and procedures of the present test follow. Two groups of newborns performed in a discriminated-operant learning task. When infants in the Maternal group responded during one discriminative stimulus, they were reinforced with the low-pass filtered sounds of their own mother’s voice, whereas when they responded during a second discriminative stimulus, they were reinforced with the normal unfiltered version of her voice. The filtered version simulates the acoustic characteristics of the maternal voice that are available in utero, and the unfiltered version simulates the voice characteristics available after birth. Each infant in the Control group was matched to a Maternal infant and encountered exactly the same task, with the same reinforcers, as his or her counterpart. The groups differed only in that Maternal infants had, and the Control infants did not have, prenatal and postnatal experience with the specific voice sounds that served as reinforcers. The low-pass filtered female voices used as reinforcers in this study have some unknown (positive, neutral, or negative) reinforcing value for newborns.
PRENATAL
AUDITORY
EXPERIENCE
135
Whatever the physical basis of their reinforcing value is, the hypothesis asserts that the filtered voices will have acquired additional positive reinforcing value for the Maternal infants because of their prenatal experience with its specific acoustic characteristics. The basic prediction of the hypothesis is that a between-groups difference in preference for the filtered voice will occur. The relative reinforcing value of, or preference for, the filtered voice will be greater for Maternal infants than for Control infants. That is, of all an infant’s responses, the proportion reinforced by the filtered voice will be greater for Maternal infants than for Control infants. This expected difference in preference can only be attributed to the effects of each group’s previous experience (or lack of experience) with the voice sounds used as reinforcers. (The complementary form of the prediction is that the proportion of responses reinforced by the unfiltered voice will be greater for Control infants than for Maternal infants.) METHOD Subjects
All newborns selected for testing met t1.e following criteria: (a) birthweight between 2500-3940 gm, (b) uncomplicated gestation and delivery, (c) Apgar scores of at least 8 at l- and 5-min after birth, and (d) age at test between 38-60 hours. Males were tested either before or at least 12 hours after circumcision. Infants assigned to the Maternal group (n = 8) were randomly selected from the newborn nursery. Infants in the Control group (n = 8) were selected from the same nursery and matched to a Maternal infant by sex, age at test, and race. Mothers gave informed consent for their infants’ participation and were invited to observe the testing. Apparatus
Experimental sessions were conducted in a quiet, dimly lighted room adjacent to the nursery. The infants lay supine in their bassinets and wore well padded TDH-39 earphones, that were suspended from a supporting bar. A nonnutritive nipple was held loosely in the infant’s mouth. The nipple was connected by 30-cm of surgical tubing to a Statham P-23AA pressure transducer. The transducer was connected to a Grass polygraph, BRS/LVE solid-state programming equipment, and a Marantz PMD 360 stereo-cassette tape recorder. The apparatus automatically controlled all auditory events during the session. Auditory
Stimuli
The reinforcing stimuli were filtered and unfiltered tape recordings of eight women reading the children’s story The Sleeping Princess (Hoxie, 1911). The women, mothers of infants in the Maternal group, were instructed to read as if they were reading to their infants and recorded the story while alone in a quiet room. The low-pass version was obtained by passing the original recording through two Krohn-Hite filters (model 3750) arranged in series with the lower cut-off set at 0 Hz and the upper cut-off set at 1 kHz. Filtering decreased the
136
SPENCE
AND
DECASPER
intensity of the recording by 6 dB at 1 kHz and by 48 dB/octave beyond 1 kHz. The unfiltered version was obtained by passing the original recording through the filters with the lower cut-off set at 0 Hz and the upper cut-off set at 10 kHz. Next, the filtered and unfiltered versions were equated for perceived loudness by two adult observers because adults, and probably newborns as well, perceive wideband signals as being louder than a narrower band signal of the same intensity (Scharf, 1978; Berg & Berg, 1979). Overall intensities of the low-pass signals ranged from 61-64 dB SPL (M = 62 dB) and intensities of the unfiltered signals ranged between 61-62 dB SPL (M = 61.5 dB) measured at the infants’ earphones. Each infant also occasionally heard a 400-Hz sine-wave tone of 4 s duration, at 60 dB SPL. Procedures Sessions began about 2.5 hours after a scheduled feeding in order to maximize the probability of obtaining a cooperative infant (Cairns & Butterfield, 1974). Each infant was required to attain a quiet-alert state and to visually fixate and follow an experimenter’s face, in order for testing to proceed. (If the infant did not attain an alert-state, visually fixate, or follow, he or she was returned to the nursery and another attempt was made after a later feeding.) The infant was then placed in his or her bassinet, the earphones were locked in place, and the nipple was placed in his or her mouth and held by an experimenter who could not hear the auditory stimuli and who was blind to the exact experimental condition. The infant was given two minutes to adjust to this situation and had to emit sucks with negative pressures equivalent to at least 20-mm Hg, a pressure normally exceeded by healthy newborns. Typically, nonnutritive sucking consists of temporally coherent bursts of individual sucks; each burst is several seconds long and is separated from the next burst by several seconds or more without sucks. A sucking burst was defined as a series of sucks separated from each other by less than 2 s. When 2 s elapsed without a suck, the equipment registered the end of the burst (e.g., DeCasper & Spence, 1986, Figure 1). (If the infant failed to suck adequately for any reason, he or she was returned to the nursery and another attempt was made after a later feeding.) The reinforcement phase began immediately after the 2-min. adjustment period. Whenever a burst ended, 2 discriminative stimuli consisting of 4-s periods of the 400-Hz tone alternating with 4-s periods of silence would occur. For half the infants in the Maternal group and for their matched counterparts in the Control group (2 males and 2 females in each group), sucking bursts initiated at any time during a tone period turned off the tone and were reinforced with the unfiltered version of the voice, that remained on until the burst ended. Sucking bursts emitted during the silent period were reinforced with the filtered version. When a burst ended, the alternating sequence of discriminative stimuli began anew. For the remaining infants in each group, sucking begun during the tone was reinforced with the filtered version and sucking during silence was reinforced with the unfiltered version.
PRENATAL
AUDITORY
EXPERIENCE
137
The equipment randomly determined whether each alternating sequence would begin with a tone period or a silent period. Each selection was independent of all the others, so a random half of the sequences would begin with the tone and the other half with the silent period. Thus, if infants responded randomly, the proportion of responses reinforced by the filtered and unfiltered voices would be equal. If, however, one of the reinforcers was more rewarding than the other, then the infants should learn to respond more often in the presence of the stimulus associated with the more potent reinforcer and the proportion of filtered- and unfiltered-voice reinforcements would be unequal. The primary measure of reinforcer potency was the relative frequency of responding during the associated discriminative stimulus; for one reinforcer, the number of tone periods in which sucking began was divided by the total number of tone periods, and for the other reinforcer, the number of no-tone periods in which sucking began was divided by the total number of no-tone periods. The higher the relative frequency of responding, the greater the reinforcing value of the associated voice. Note that this measure is independent of subject factors that could affect how many discriminative stimuli the infant encountered, for example, how long the infant remained in a testable state. An infant’s preference for, or the relative reinforcing value of, the filtered version was defined as the relative frequency of responding during the stimulus associated with the filtered voice divided by the sum of the relative frequency of responding during the stimulus associated with the filtered voice and the relative frequency of responding during the stimulus associated with the unfiltered voice. Filtered-voice preference ratios less than .50 indicate a preference for the unfiltered voice, ratios equal to .50 indicate no preference or indifference, and ratios greater than .50 indicate a preference for the filtered voice. Note that this preference measure is independent of an infant’s overall response rate and that the unfiltered-voice preference ratio equals 1 minus the filteredvoice preference ratio. These procedures and measures have been used to directly demonstrate that infants prefer their own mother’s unfiltered voice over the unfiltered voice of another woman (DeCasper & Fifer, 1980; Fifer, 1981).
RESULTS AND DISCUSSION
A preliminary analysis assessed whether the discriminative stimuli themselves exerted systematic effects on the relative frequency of responding, independent of the associated reinforcer. Wilcoxon matched-pairs signed-ranks tests were used to compare the relative frequency of responding during the tone and no-tone periods for both groups of infants. The relative frequencies did not differ for either the Maternal group, T=9.5, p> .lO, or the Control group, T= 8.5, p> .lO. As predicted, the filtered-voice preference ratio was greater for the Maternal infants (M=.51) than for the matched Control infants (M=.46), T=O, p = .005. The between-groups difference obtained here (M= .05) can only be
Sex
Age
20
55
55 50 38 42 40
51 46
60
55 55 38 44 46
44 42
19 20
20 19 18 19 20
Maternal
Maternal
of responding preference
16 13
18 15 19 16 19
16
Control
Session Length (min)
Control
(hrs)
frequency
filtered-voice
Relative ratio
.63
.62 .63
.73 .67 .76 .44 .51
and Maternal
unfiltered-voice
.66 .56
.55 .43 .77 .51 .63
.72
Unfiltered
Maternal
in the
1
Relative Frequency
infants
TABLE filtered-
Filtered
for
with
reinforcers Control
.45 .48 .53
.57 .61 .50 .47
.47
Preference Ratio
and
.37
.52 .46
.53 .65 .63 33 .49
Relative Frequency
the
Filtered
and groups.
.46 .51 .49 A3 .45 .46 A4
.43 .59 .61 .57
47
Ratio
Preference
.61 .63 .65
.41
Unfiltered
Control
PRENATAL
AUDITORY
EXPERIENCE
139
due to the effects of each group’s previous experience (or lack of experience) with the reinforcing voices used in the study. The Maternal infants’ filtered-voice preference ratio (M= 51) did not differ from .50, T= 16, p> .lO. Indifferent responding would result: (a) if the infants could not discriminate between the filtered and unfiltered versions of the maternal voice, (b) if they could not learn the task, or (c) if the filtered and unfiltered versions of the maternal .voice were equally rewarding. However, Control infants’ preference ratios (M= 46) were consistently less than 50; T= 1.5, p< .05. This indicates that: (a) these infants discriminated the filtered and unfiltered versions, (b) they learned the discrimination task, and (c) the filtered version was less reinforcing than the unfiltered version. The Control infants’ performance indicates that the indifference shown by the Maternal infants probably resulted because the filtered and unfiltered versions of their own mothers’ voices were equally reinforcing. Thus, when infants had previous experience with the filtered and unfiltered reinforcers their reinforcing values did not differ. However, when they lacked specific experience with either reinforcer the unfiltered voice was consistently more reinforcing. The preference difference implies that the reinforcing value of the filtered voice was greater for Maternal infants (M= .62) than for Control infants (M= .50) and/or that the reinforcing value of the unfiltered voice was greater for the Controlinfants (M= .56) than for Maternal infants (M= .60). Wilcoxon tests indicated that the reinforcing value of the filtered voice was greater for Maternal infants, T= 0, p = .005, and that the reinforcing value of the unfiltered voice did not differ for the two groups, T= 12, p> .lO. Note that the absence of a between-groups difference in the reinforcing value of the unfiltered voices is not problematical in the present context. When Fifer (1981) used the same discrimination task to directly contrast the reinforcing values of unfiltered maternal and unfiltered nonmaternal voices, the maternal-voice preference was clear, even for the 8 youngest infants who were comparable in age to the present subjects. Their maternal-voice preference ratio (M= .55) was reliably greater than .50; T=O, p = .005. It seems reasonable that Fifer’s positive finding, and the present null findings, result from procedural differences in how the comparisons between unfiltered maternal and nonmaternal voices were made. The finding that Maternal infants’ filtered-voice preference scores were greater than those of Control infants directly indicates that some previous experience (or lack of experience) with the specific filtered and/or unfiltered reinforcers influenced their relative reinforcing properties. This finding cannot be explained by differential amounts of prenatal experience with various females’ unfiltered voices because independent evidence indicates the acoustic characteristics of unfiltered voices per se are not readily available in utero (Querleu & Renard, 1981). Neither can it be attributed to differential amounts of postnatal experience with various females’ unfiltered voices that occurred within 48 hours of birth, the mean age of infants tested here. This explanation
140
SPENCE
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would require that postnatal experience would have to increase the reinforcing value of unfiltered nonmaternal voices relative to their filtered form, and decrease or leave unchanged the relative reinforcing value of unfiltered maternal voices. Such an account is implausible and inconsistent with existing theories and data about the effects of early perceptual experience on the subsequent reinforcing value of stimuli (Hoffman & Ratner, 1973). Moreover, it cannot account for the fact that filtered maternal voices were more reinforcing than filtered nonmaternal voices. Differential amounts of postnatal experience with the lowerfrequency sounds of various females’ normal unfiltered voices could account for the pattern of results if the effect was to differentially increase the reinforcing value of the lower frequencies of the voices heard most often, for example, the maternal voice. The account seems plausible because it fits with data showing that young infants are more responsive to low frequencies than to high frequencies (Engel & Young, 1969; Hutt, Hutt, Lenard, von Bernuth, & Muntjewerff, 1968; Rubel, 1985) and is consistent with other relevant theories (e.g., Hoffman & Ratner, 1973). This account also requires that differential experience must have its effects within 48 hours after birth. However, two experiments specifically designed to reveal the influence of early postnatal experience on subsequent voice preferences failed to do so. Fifer (1981) tested the maternal-voice preference of breast-fed and bottle-fed newborns less-than 48 hours and older-than 72 hours of age. All infants preferred their own mothers’ voices, but there was no evidence that the magnitude of the preference was influenced by the frequency and/or type of mother-infant contact that occurred before testing. In addition, DeCasper and Prescott (1984) found no evidence that explicitly arranged postnatal experience with the paternal voice induced a paternal-voice preference within 3 days after birth, even though similarly aged infants could discriminate the same male voices without specific prior experience. Furthermore, there are no reports that infants respond differently to paternal and nonpaternal voices before approximately 2 weeks of age (Hulsebus, 1981). Since previous experience with maternal-voice sounds is necessary for the expression of a maternal-voice preference and since there is no evidence that very early voice preferences can be significantly influenced by even earlier postnatal experience, this alternative is less compelling than it would otherwise be. Finally, it is possible that differential amounts of prenatal experience with various females’ low-frequency voice sounds could explain the basic finding if the effect was to increase the reinforcing value of the lower frequency voice sounds heard most often. Since the most prevalent low-frequency voice sounds available in utero are those of the infant’s own mother, the reinforcing value of her low-pass filtered voice would be incremented more than those of other women. This account is consistent with the present results, with the theoretical and empirical considerations presented earlier, and with the results of a study by Querleu et al. (1984). They reported that infants less than 2 hours of age reacted and oriented more to their mothers’ voices than to the voices of other
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AUDITORY
EXPERIENCE
141
women. If the infants’ previous experience with their mothers’ voices was necessary for their differential reactivity, that experience could only have occurred before birth. Note also that the amount of experience with maternal-voice sounds that could occur before birth (hearing becomes functional around 32 weeks gestational age) greatly exceeds what could occur within several days after birth. The preceding logical, theoretical, and empirical considerations favor this last possibility as an explanation of the present pattern of results: The greater filtered-voice preference expressed by Maternal-group infants occurs because of their prenatal experience with mother-specific low-frequency voice sounds.
REFERENCES Aslin,
R.N., Pisoni, D.B., & Jusczyk, P.W. (1983). Auditory development and speech perception in infancy. In M.M. Haith & J.J. Campos (Eds.), Munuol of child psychology Vol.2: Infancy and developmental psychobiology. New York: Wiley. Berg, K.M., & Berg, K. (1979). Psychophysiological development in infancy: State, sensory function, and attention. In J. Osofsky (Ed.), Handbook ofinfanr developmenr. New York: Wiley. Bricker. P.D., & Pruzansky, S. (1976). Speaker recognition. In N.J. Lass (Ed.), Contemporary issues in experimental phonetics. New York: Academic. Cairns.G., & Butterfield, E.C. (1974). Assessing infants’ auditory functioning. In B.Z. Friedlander, G.M. Sterritt, & G.C. Kirk (Eds.), Exceptionolinfanf: Vol. 3. New York: Brunner/ Mazel. DeCasper, A.J., & Fifer, W.P. (1980). Of human bonding: Newborns prefer their mothers’ voices. Science, 208, I 174- I 176. DeCasper. A.J., & Prescott, P.A. (1984). Human newborns’ perception of male voices: Preference, discrimination and reinforcing value. Developmental Psychobiology, 17, 481-491. DeCasper, A.J., & Spence, M.J. (1986). Prenatal maternal speech influences newborns’ perception of speech sounds. Infanr Behavior and Development, 9. 133-150. Engel, R., & Young, N.B. (1969). Calibrated pure tone audiograms in normal neonates based on evoked electroencephalographic responses. Neuropaediafrie, I, 149-160. Fifer, W.P. (1981). Early attachment: Maternal-voicepreference in one- and lhree-day old infants. Unpublished doctoral dissertation, University of North Carolina at Greensboro. Gottlieb, G. (1985). On discovering significant acoustic dimensions of auditory stimulation for infants. In G. Gottlieb & N.A. Krasnegor (Eds.). Measurement of audition and vision in the firsr year of postnatal life. Norwood, NJ: Ablex. Hoffman, H., & Ratner, A. (1973). A reinforcement model of imprinting: Implications for socialization in monkeys and men. Psychological Reviebv, 80, 527-544. Hoxie, J.L. (I91 I). The sleeping princess. In J.L. Hoxie (Ed.), A kindergarrensfory book. Springfield, MA: Milton Bradley Co. Hulsebus, R. (1981, March). Farher discrimination IWO weeks after birth. Paper presented at the meeting of the Southeastern Psychological Association, Atlanta, GA. Hutt, S.. Hutt. C.. Lenard, H.G., von Bernuth, H., & Muntjewerff, W.J. (1968). Auditory responsivity in the human neonate. Nurure, 218, 888-890. Querleu. D., Lefebvre, C., Titran, M., Renard, X.. Morillion, M., & Crepin, G. (1984). ReactivitC du nouveau-ne de moins de deux heures de vie a la voix maternelle [Reactivity of newborns less than two hours old to the maternal voice]. Journal de Gynecologie, Obsrerrique er
Biologie de la Reproduction.
13, 125 134.
142 Querleu, Rubel,
SPENCE AND
DECASPER
D.. & Renard, K. (1981). Les perceptions auditives du foetus ception of the human fetus]. Mhdecine et Hygi&e, 39, 2101-2110. E. (1985). Auditory system development. In G. Gottlieb & N.A.
humain
[Auditory
per-
(Eds.).
Mea-
Krasnegor
suremenl of audition and vision in the first yeor of postnatal life. Norwood, NJ: Ablex. Scharf, B. (1978). Loudness. In E.C. Carterette & M.P. Friedman (Eds.), Handbook of percepfion (Vol. IV). New York: Academic. Tonndorf, J. (1976). Bone conduction. In W.D. Keidel& W.D. Neff (Eds.), Hundbook ofsensory physiology (Vol. 3). Berlin: Springer-Verlag. Vince,
M.A., Armitage, S.E., Baldwin, B., Toner, J.. & Moore, B.C.J. (1982). ronment of the foetal sheep. Behoviour, 81, 296-315. Walker, D., Grimwade, J., &Wood, C. (1971). Intrauterine noise: A component ronment. American Journal of Obstetrics and Gynecology, 109, 9 l-95, 29 July
1985;
Revised
The sound
envi-
of the fetal envi-
4 December
1986
n
BEHAVIOR
AND
DEVELOPMENT
10,
13%142
(1987)
Prenatal Experience with Low-Frequency Maternal-Voice Sounds Influence Neonatal Perception of Maternal Voice Samples MELANIE
J. SPENCE
The University of Alabama at Birmingham
ANTHONY
J. DECASPER
University of North Carolina at Greensboro By sucking on a nonnutritive nipple in the presence of one discriminative stimulus, newborns were reinforced with a low-pass filtered tape recording of their mothers’ voices. Sucking in the presence of a different discriminative stimulus was reinforced with unfiltered maternal-voice recordings. Filtered versions simulated maternal-voice sounds that were available before birth and unfiltered versions simulated maternal-voice sounds available after birth. Newborns in the control group could be reinforced with the same stimuli in the same way, but the voices were unfomiliar to them. Infants hearing their mothers’voices had no preference for either version, but infants hearing the unfamiliar voices preferred the unfiltered version. The difference in the between-groups responsiveness to the low-poss voice samples is consistent with the hypothesis that prenatal experience with low-frequency characteristics of maternal voices influences early postnatal perception of maternol voices.
prenatal
sensory experience voice oerceotion
auditory preception maternal voice auditorv
newborn oreference
perception
Human newborns prefer to hear the acoustic properties of a speech passage their mothers had recited when pregnant over those of a passage that their mothers had not recited (DeCasper & Spence, 1986). This preference implies that the newborns had been prenatally exposed to the acoustic properties of the recited material, for example, its pattern of syllabic beats, the voice-onset-time This research is part of a dissertation submitted to the University of North Carolina at Greensboro by Melanie J. Spence and was presented at the International Conference on Infant Studies, Los Angeles, CA, April 1986. The project was supported by a Research Council Grant from the University of North Carolina at Greensboro and a generous equipment loan by Professor Michael D. Zeiler. We wish to thank the medical and administrative staff of Moses H. Cone Hospital, Greensboro, NC, and especially, the mothers and their infants for making this research possible. Thanks also to David Soderquist for the use of his laboratory equipment and his help in preparing stimulus materials, and to Robin Panneton for her assistance in data collection. Correspondence and requests for reprints should be addressed to Melanie J. Spence, Sparks Center for Developmental and Learning Disorders, University of Alabama at Birmingham, P.O. Box 313, University Station, Birmingham, AL 35294. 133
134
SPENCE
AND
DECASPER
of its stop consonants, the harmonic structure of its sustained vowel sounds, and/or the temporal patterns of these sounds. It also implies that the newborns had been exposed to the acoustic cues that specify the mother’s voice per se and her habitual ways of speaking, for example, the spectra of her nasals and vowels, her glottal frequency and spectrum, and/or the temporal characteristics of the pitch and intensity of her stressed and unstressed vowels (Bricker & Pruzansky, 1976). Since prenatal experience with a specific passage can engender a postnatal preference for that passage, it is possible that prenatal experience with specific maternal-voice cues can engender the postnatal preference for the maternal voice (DeCasper & Fifer, 1980; Fifer, 1981). In principle, this hypothesis could be directly tested by manipulating the amount of maternal speech that occurs during pregnancy. In fact, such a manipulation would be unethical and impractical. Thus, only indirect tests of the hypothesis can be achieved. Maternal-voice cues that could subserve newborns’ discrimination of and preference for their mothers’ voices are presently unknown, although there are several likely possibilities (Gottlieb, 1985). However, if the functional significance of the mother-specific voice cues is established before birth, it is highly probable that cues dependent upon maternal speech frequencies below 1 kHz are especially important. Intrauterine recordings indicate that virtually all the acoustic energy available to the fetus is carried by frequencies below 1 kHz, and the intensity of higher frequencies is severely attenuated by maternal tissue (Querleu & Renard, 1981; Vince, Armitage, Baldwin, Toner, & Moore, 1982; Walker, Grimwade, &Wood, 1971). Furthermore, prenatal auditory functioning, which occurs in a fluid environment, may involve mechanisms similar to those used in bone conduction (Rubel, 1985), a process that efficiently transmits the lower frequencies (Aslin, Pisoni, & Jusczyk, 1983; Tonndorf, 1976). Thus, a corollary of the hypothesis is that prenatal experience with low-frequency maternal-voice cues influences neonates’ perception of maternal voices. The corollary can be used to generate a variety of testable predictions. The rationale and procedures of the present test follow. Two groups of newborns performed in a discriminated-operant learning task. When infants in the Maternal group responded during one discriminative stimulus, they were reinforced with the low-pass filtered sounds of their own mother’s voice, whereas when they responded during a second discriminative stimulus, they were reinforced with the normal unfiltered version of her voice. The filtered version simulates the acoustic characteristics of the maternal voice that are available in utero, and the unfiltered version simulates the voice characteristics available after birth. Each infant in the Control group was matched to a Maternal infant and encountered exactly the same task, with the same reinforcers, as his or her counterpart. The groups differed only in that Maternal infants had, and the Control infants did not have, prenatal and postnatal experience with the specific voice sounds that served as reinforcers. The low-pass filtered female voices used as reinforcers in this study have some unknown (positive, neutral, or negative) reinforcing value for newborns.
PRENATAL
AUDITORY
EXPERIENCE
135
Whatever the physical basis of their reinforcing value is, the hypothesis asserts that the filtered voices will have acquired additional positive reinforcing value for the Maternal infants because of their prenatal experience with its specific acoustic characteristics. The basic prediction of the hypothesis is that a between-groups difference in preference for the filtered voice will occur. The relative reinforcing value of, or preference for, the filtered voice will be greater for Maternal infants than for Control infants. That is, of all an infant’s responses, the proportion reinforced by the filtered voice will be greater for Maternal infants than for Control infants. This expected difference in preference can only be attributed to the effects of each group’s previous experience (or lack of experience) with the voice sounds used as reinforcers. (The complementary form of the prediction is that the proportion of responses reinforced by the unfiltered voice will be greater for Control infants than for Maternal infants.) METHOD Subjects
All newborns selected for testing met t1.e following criteria: (a) birthweight between 2500-3940 gm, (b) uncomplicated gestation and delivery, (c) Apgar scores of at least 8 at l- and 5-min after birth, and (d) age at test between 38-60 hours. Males were tested either before or at least 12 hours after circumcision. Infants assigned to the Maternal group (n = 8) were randomly selected from the newborn nursery. Infants in the Control group (n = 8) were selected from the same nursery and matched to a Maternal infant by sex, age at test, and race. Mothers gave informed consent for their infants’ participation and were invited to observe the testing. Apparatus
Experimental sessions were conducted in a quiet, dimly lighted room adjacent to the nursery. The infants lay supine in their bassinets and wore well padded TDH-39 earphones, that were suspended from a supporting bar. A nonnutritive nipple was held loosely in the infant’s mouth. The nipple was connected by 30-cm of surgical tubing to a Statham P-23AA pressure transducer. The transducer was connected to a Grass polygraph, BRS/LVE solid-state programming equipment, and a Marantz PMD 360 stereo-cassette tape recorder. The apparatus automatically controlled all auditory events during the session. Auditory
Stimuli
The reinforcing stimuli were filtered and unfiltered tape recordings of eight women reading the children’s story The Sleeping Princess (Hoxie, 1911). The women, mothers of infants in the Maternal group, were instructed to read as if they were reading to their infants and recorded the story while alone in a quiet room. The low-pass version was obtained by passing the original recording through two Krohn-Hite filters (model 3750) arranged in series with the lower cut-off set at 0 Hz and the upper cut-off set at 1 kHz. Filtering decreased the
136
SPENCE
AND
DECASPER
intensity of the recording by 6 dB at 1 kHz and by 48 dB/octave beyond 1 kHz. The unfiltered version was obtained by passing the original recording through the filters with the lower cut-off set at 0 Hz and the upper cut-off set at 10 kHz. Next, the filtered and unfiltered versions were equated for perceived loudness by two adult observers because adults, and probably newborns as well, perceive wideband signals as being louder than a narrower band signal of the same intensity (Scharf, 1978; Berg & Berg, 1979). Overall intensities of the low-pass signals ranged from 61-64 dB SPL (M = 62 dB) and intensities of the unfiltered signals ranged between 61-62 dB SPL (M = 61.5 dB) measured at the infants’ earphones. Each infant also occasionally heard a 400-Hz sine-wave tone of 4 s duration, at 60 dB SPL. Procedures Sessions began about 2.5 hours after a scheduled feeding in order to maximize the probability of obtaining a cooperative infant (Cairns & Butterfield, 1974). Each infant was required to attain a quiet-alert state and to visually fixate and follow an experimenter’s face, in order for testing to proceed. (If the infant did not attain an alert-state, visually fixate, or follow, he or she was returned to the nursery and another attempt was made after a later feeding.) The infant was then placed in his or her bassinet, the earphones were locked in place, and the nipple was placed in his or her mouth and held by an experimenter who could not hear the auditory stimuli and who was blind to the exact experimental condition. The infant was given two minutes to adjust to this situation and had to emit sucks with negative pressures equivalent to at least 20-mm Hg, a pressure normally exceeded by healthy newborns. Typically, nonnutritive sucking consists of temporally coherent bursts of individual sucks; each burst is several seconds long and is separated from the next burst by several seconds or more without sucks. A sucking burst was defined as a series of sucks separated from each other by less than 2 s. When 2 s elapsed without a suck, the equipment registered the end of the burst (e.g., DeCasper & Spence, 1986, Figure 1). (If the infant failed to suck adequately for any reason, he or she was returned to the nursery and another attempt was made after a later feeding.) The reinforcement phase began immediately after the 2-min. adjustment period. Whenever a burst ended, 2 discriminative stimuli consisting of 4-s periods of the 400-Hz tone alternating with 4-s periods of silence would occur. For half the infants in the Maternal group and for their matched counterparts in the Control group (2 males and 2 females in each group), sucking bursts initiated at any time during a tone period turned off the tone and were reinforced with the unfiltered version of the voice, that remained on until the burst ended. Sucking bursts emitted during the silent period were reinforced with the filtered version. When a burst ended, the alternating sequence of discriminative stimuli began anew. For the remaining infants in each group, sucking begun during the tone was reinforced with the filtered version and sucking during silence was reinforced with the unfiltered version.
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AUDITORY
EXPERIENCE
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The equipment randomly determined whether each alternating sequence would begin with a tone period or a silent period. Each selection was independent of all the others, so a random half of the sequences would begin with the tone and the other half with the silent period. Thus, if infants responded randomly, the proportion of responses reinforced by the filtered and unfiltered voices would be equal. If, however, one of the reinforcers was more rewarding than the other, then the infants should learn to respond more often in the presence of the stimulus associated with the more potent reinforcer and the proportion of filtered- and unfiltered-voice reinforcements would be unequal. The primary measure of reinforcer potency was the relative frequency of responding during the associated discriminative stimulus; for one reinforcer, the number of tone periods in which sucking began was divided by the total number of tone periods, and for the other reinforcer, the number of no-tone periods in which sucking began was divided by the total number of no-tone periods. The higher the relative frequency of responding, the greater the reinforcing value of the associated voice. Note that this measure is independent of subject factors that could affect how many discriminative stimuli the infant encountered, for example, how long the infant remained in a testable state. An infant’s preference for, or the relative reinforcing value of, the filtered version was defined as the relative frequency of responding during the stimulus associated with the filtered voice divided by the sum of the relative frequency of responding during the stimulus associated with the filtered voice and the relative frequency of responding during the stimulus associated with the unfiltered voice. Filtered-voice preference ratios less than .50 indicate a preference for the unfiltered voice, ratios equal to .50 indicate no preference or indifference, and ratios greater than .50 indicate a preference for the filtered voice. Note that this preference measure is independent of an infant’s overall response rate and that the unfiltered-voice preference ratio equals 1 minus the filteredvoice preference ratio. These procedures and measures have been used to directly demonstrate that infants prefer their own mother’s unfiltered voice over the unfiltered voice of another woman (DeCasper & Fifer, 1980; Fifer, 1981).
RESULTS AND DISCUSSION
A preliminary analysis assessed whether the discriminative stimuli themselves exerted systematic effects on the relative frequency of responding, independent of the associated reinforcer. Wilcoxon matched-pairs signed-ranks tests were used to compare the relative frequency of responding during the tone and no-tone periods for both groups of infants. The relative frequencies did not differ for either the Maternal group, T=9.5, p> .lO, or the Control group, T= 8.5, p> .lO. As predicted, the filtered-voice preference ratio was greater for the Maternal infants (M=.51) than for the matched Control infants (M=.46), T=O, p = .005. The between-groups difference obtained here (M= .05) can only be
Sex
Age
20
55
55 50 38 42 40
51 46
60
55 55 38 44 46
44 42
19 20
20 19 18 19 20
Maternal
Maternal
of responding preference
16 13
18 15 19 16 19
16
Control
Session Length (min)
Control
(hrs)
frequency
filtered-voice
Relative ratio
.63
.62 .63
.73 .67 .76 .44 .51
and Maternal
unfiltered-voice
.66 .56
.55 .43 .77 .51 .63
.72
Unfiltered
Maternal
in the
1
Relative Frequency
infants
TABLE filtered-
Filtered
for
with
reinforcers Control
.45 .48 .53
.57 .61 .50 .47
.47
Preference Ratio
and
.37
.52 .46
.53 .65 .63 33 .49
Relative Frequency
the
Filtered
and groups.
.46 .51 .49 A3 .45 .46 A4
.43 .59 .61 .57
47
Ratio
Preference
.61 .63 .65
.41
Unfiltered
Control
PRENATAL
AUDITORY
EXPERIENCE
139
due to the effects of each group’s previous experience (or lack of experience) with the reinforcing voices used in the study. The Maternal infants’ filtered-voice preference ratio (M= 51) did not differ from .50, T= 16, p> .lO. Indifferent responding would result: (a) if the infants could not discriminate between the filtered and unfiltered versions of the maternal voice, (b) if they could not learn the task, or (c) if the filtered and unfiltered versions of the maternal .voice were equally rewarding. However, Control infants’ preference ratios (M= 46) were consistently less than 50; T= 1.5, p< .05. This indicates that: (a) these infants discriminated the filtered and unfiltered versions, (b) they learned the discrimination task, and (c) the filtered version was less reinforcing than the unfiltered version. The Control infants’ performance indicates that the indifference shown by the Maternal infants probably resulted because the filtered and unfiltered versions of their own mothers’ voices were equally reinforcing. Thus, when infants had previous experience with the filtered and unfiltered reinforcers their reinforcing values did not differ. However, when they lacked specific experience with either reinforcer the unfiltered voice was consistently more reinforcing. The preference difference implies that the reinforcing value of the filtered voice was greater for Maternal infants (M= .62) than for Control infants (M= .50) and/or that the reinforcing value of the unfiltered voice was greater for the Controlinfants (M= .56) than for Maternal infants (M= .60). Wilcoxon tests indicated that the reinforcing value of the filtered voice was greater for Maternal infants, T= 0, p = .005, and that the reinforcing value of the unfiltered voice did not differ for the two groups, T= 12, p> .lO. Note that the absence of a between-groups difference in the reinforcing value of the unfiltered voices is not problematical in the present context. When Fifer (1981) used the same discrimination task to directly contrast the reinforcing values of unfiltered maternal and unfiltered nonmaternal voices, the maternal-voice preference was clear, even for the 8 youngest infants who were comparable in age to the present subjects. Their maternal-voice preference ratio (M= .55) was reliably greater than .50; T=O, p = .005. It seems reasonable that Fifer’s positive finding, and the present null findings, result from procedural differences in how the comparisons between unfiltered maternal and nonmaternal voices were made. The finding that Maternal infants’ filtered-voice preference scores were greater than those of Control infants directly indicates that some previous experience (or lack of experience) with the specific filtered and/or unfiltered reinforcers influenced their relative reinforcing properties. This finding cannot be explained by differential amounts of prenatal experience with various females’ unfiltered voices because independent evidence indicates the acoustic characteristics of unfiltered voices per se are not readily available in utero (Querleu & Renard, 1981). Neither can it be attributed to differential amounts of postnatal experience with various females’ unfiltered voices that occurred within 48 hours of birth, the mean age of infants tested here. This explanation
140
SPENCE
AND
DECASPER
would require that postnatal experience would have to increase the reinforcing value of unfiltered nonmaternal voices relative to their filtered form, and decrease or leave unchanged the relative reinforcing value of unfiltered maternal voices. Such an account is implausible and inconsistent with existing theories and data about the effects of early perceptual experience on the subsequent reinforcing value of stimuli (Hoffman & Ratner, 1973). Moreover, it cannot account for the fact that filtered maternal voices were more reinforcing than filtered nonmaternal voices. Differential amounts of postnatal experience with the lowerfrequency sounds of various females’ normal unfiltered voices could account for the pattern of results if the effect was to differentially increase the reinforcing value of the lower frequencies of the voices heard most often, for example, the maternal voice. The account seems plausible because it fits with data showing that young infants are more responsive to low frequencies than to high frequencies (Engel & Young, 1969; Hutt, Hutt, Lenard, von Bernuth, & Muntjewerff, 1968; Rubel, 1985) and is consistent with other relevant theories (e.g., Hoffman & Ratner, 1973). This account also requires that differential experience must have its effects within 48 hours after birth. However, two experiments specifically designed to reveal the influence of early postnatal experience on subsequent voice preferences failed to do so. Fifer (1981) tested the maternal-voice preference of breast-fed and bottle-fed newborns less-than 48 hours and older-than 72 hours of age. All infants preferred their own mothers’ voices, but there was no evidence that the magnitude of the preference was influenced by the frequency and/or type of mother-infant contact that occurred before testing. In addition, DeCasper and Prescott (1984) found no evidence that explicitly arranged postnatal experience with the paternal voice induced a paternal-voice preference within 3 days after birth, even though similarly aged infants could discriminate the same male voices without specific prior experience. Furthermore, there are no reports that infants respond differently to paternal and nonpaternal voices before approximately 2 weeks of age (Hulsebus, 1981). Since previous experience with maternal-voice sounds is necessary for the expression of a maternal-voice preference and since there is no evidence that very early voice preferences can be significantly influenced by even earlier postnatal experience, this alternative is less compelling than it would otherwise be. Finally, it is possible that differential amounts of prenatal experience with various females’ low-frequency voice sounds could explain the basic finding if the effect was to increase the reinforcing value of the lower frequency voice sounds heard most often. Since the most prevalent low-frequency voice sounds available in utero are those of the infant’s own mother, the reinforcing value of her low-pass filtered voice would be incremented more than those of other women. This account is consistent with the present results, with the theoretical and empirical considerations presented earlier, and with the results of a study by Querleu et al. (1984). They reported that infants less than 2 hours of age reacted and oriented more to their mothers’ voices than to the voices of other
PRENATAL
AUDITORY
EXPERIENCE
141
women. If the infants’ previous experience with their mothers’ voices was necessary for their differential reactivity, that experience could only have occurred before birth. Note also that the amount of experience with maternal-voice sounds that could occur before birth (hearing becomes functional around 32 weeks gestational age) greatly exceeds what could occur within several days after birth. The preceding logical, theoretical, and empirical considerations favor this last possibility as an explanation of the present pattern of results: The greater filtered-voice preference expressed by Maternal-group infants occurs because of their prenatal experience with mother-specific low-frequency voice sounds.
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envi-
of the fetal envi-
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n