Auditory frequency sensitivity in the neonate: A signal detection analysis

JOURNAI.

OF EXPERIMENTAL

CHILD

PSYCHOLOGY

21, 219-225 (1976)

Auditory Frequency Sensitivity in the Neonate: A Signal Detection Analysis

Using signal detectability theory. an analysis was performed on some auditory frequency sensitivity data obtained in I968 by Hutt et al. on human neonates. The d’-values over the frequencies from 70 Hz to 2kHz formed a significant cubic function. No state of arousal effects were found on sensitivity, as had been found in 1968. The p-values did not vary systematically with state. which suggests that levels of arousal should be studied separately. It is also suggested that the complex sensitivity found may provide a mechanism by which neonates may monitor their own vocalizations.

This paper illustrates the usefulness of applying signal detection theory (SDT) to data about auditory frequency sensitivity of the neonate. The data to be analyzed are from an EMG study first published in 1968 by Hutt, Hutt, Lenard, von Bernuth, and Muntjewerff. The authors used a2 x 6 x 3 design: there were two wave forms, square and sine waves; six frequencies between 70 Hz and 2kHz; and three states of arousal (l-regular sleep, 2-irregular sleep, 3-quiet wakefulness). Because there was substantial spontaneous EMG responding (startle), the authors presented an equal number of noise-alone (no-signal) “trials” in each state. The no-signal trials make these data suitable for an SDT analysis. Hutt et al. (1968) found significant differences between spontaneous startles in the three states of arousal. Using corrected auditory scores, they found maximal sensitivity for low frequencies. The square wave group had higher response levels than the sine wave group. Their explanation of these findings was that the neonate responsivity would be greater, the greater the proportion of basilar membrane excitation. Thus, for square waves and low frequencies, more responding would be expected. Hutt et al. (1968) suggest this may be ecologically significant since the neonates are most sensitive to sounds similar to human speech (Licklider & Miller, 1951). In a recent note to this journal (Bench, 1973), Hutt et al. (1968) were criticized for not reporting the spectral analyses of their signals. However, Bench also states that he replicated their findings almost completely. I thank John and Corrine Hutt for providing the data and some help with this analysis, Dr. A. Fourcin for considerable help on its revision. and Dr. Ian Morin and Dr. Saradha Supramaniam for commenting on earlier versions of this paper. Mailing address: Department of Psychology. University College London. Gower Street. London. WCIE 6BT. England. 219 Copyright 0 lY76 by Academic Preb\. Inc. All rights of reproduction in any form reserved.

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Bench disputed the interpretation that there is some ecological value in the potency of square wave, low frequency stimuli. Hutt’s (19731 reply answered the technical criticisms and reasserted the parsimony of the 1968 explanation. Hutt also noted that an ecological interpretation may be helpful in understanding Ashton’s study (19711, where no differential sensitivity to four square wave stimuli between 75 and 135 Hz at 85 dB SPL was found in 3-day-old neonates. He argued that if the baby’s ear is tuned to a range of frequencies representing the fundamentals in human speech, then such differential sensitivity would be unnecessary. The present SDT analysis was undertaken for several reasons. First, since there were variable spontaneous response levels, the SDT measure of sensitivity, d’ (Tanner & Swets, 1954), takes account of this variability both theoretically and empirically. Thus, it may bring to light some new aspect of the frequency data. Second, the effects of the wave form variable may prove interesting. Hutt et al. (1968) simply commented on higher sensitivity to square waves but did no further analysis. Third, an SDT analysis may clarify the role of states of arousal in an auditory situation. Can the states of arousal be considered as different criteria? If so, d’ would be roughly the same for each subject across the states and &values would reflect stricter to more lax criteria as the subject changed from state 1 to 3. This prediction assumes normality and equal variance of the signal-plus-noise and noise-alone distributions. If the states of arousal are not systematically related to fl, then perhaps the situation should be viewed as three separate yes-no experiments, one for each level of arousal, representing three independent states. METHOD

Subjects Twelve male infants from 3 to 8 days old were tested in hospital conditions. They were normal in all respects. Apparatus Stimuli were presented to one ear of the neonate via a loud speaker 40 cm directly above the ear. The ambient noise was 50 ? 2.5 dB SPL, and the signals were played at 75 dB SPL for 2 sec. A sound level meter at the ear of the infant was used to calibrate the average energy of each signaI. The SPL meter, General Radio 155lA, is a full wave amplitude rectifying and averaging device, according to its circuit diagram. For matched signals of the same frequency then, the amplitude of the fundamental of the square wave will be less than the sine wave’s amplitude by about 2 dB since harmonics are absent in sine waves. However, with a loud speaker, the amplitudes of components of the signals at the baby’s ear would be

AUDITORY

FREQUENCY

SENSITIVITY

221

distorted somewhat from any signal generated at the oscillator (see Bench, 1973; Hutt, 1973). The relationship between the sinusoid and square wave fundamental was retained though, as evidenced in the spectral analyses. The EMG was recorded from six surface electrodes on the arms of the infants. These polygraph data, as well as other measures, were analyzed independently by three of the five authors of the 1968 paper, and uniform agreement about startle responses was achieved. Procedure

A 2 x 6 x 3 factorial experiment was performed. The six frequencies investigated were 70, 125, 250, 500, 1000, and 2000 Hz, and there were three arousal states. One group of six subjects was given square waves, and the other, sine waves. The square wave group was also given two speech stimuli, a male and female saying “baby” (on a tape loop). Each infant was laid on his side and presented with a completely randomly ordered series of trials. Each trial lasted for 10 set, and if a subject changed his state of arousal during that time, the trial was eliminated from the record. Interstimulus intervals (ISI) were from 30 to 60 sec. Ten-second epochs of these ISIS were used for no-signal “trials.” There were at least four presentations of each frequency in each state, making 144 trials (at least) for each subject. Further procedural details can be obtained from earlier reports (Hutt et al., 1968; Hutt, Lenard, & Prechtl, 1969; Hutt, 1973). RESULTS

A d’ was obtained for each wave form, frequency, and arousal state combination. The false alarm probabilities used were specific to each combination of variables. These unpooled false alarm values were used because of the significant differences among spontaneous response levels. Although more trials for each probability would be desirable, it was thought that there would be adequate uniformity to calculate d’-values and b-values. d’ d&u. Some interesting results come to light when considering Fig. 1, where mean d’ for each frequency and wave form combination is plotted. The most striking aspect of the figure is that d’-values for the square wave group are always greater than those for the sine wave group. The frequency of the stimulus also affects d’, with signals between 70 and 250 Hz being more detectable than those of higher frequency. Note the low values of d’ for a11sine wave tones and for the three highest square wave stimuli. An analysis of variance confirmed all these generalizations. The linear, quadratic, and cubic components of the frequency variable are all significant (linear: F(l, 50) = I8.81, p c .Ol; quadratic: P’(l, 50) = 4.3, p = .05; cubic: (F(l,50) = 12.6,~ < .Ol; remainder: F(2,50) c l), as was

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C. WEIR

70

125

250 Frequency

FIG. I, The cubic relationship all the signals combined.

between

500

!OOO

2000

(lizI

mean d’ and frequency

for both

wave

forms

and for

the group (wave form) difference (F(1, 10) = 7.24, P < .05). The only significant interaction was between group and frequency [F(5,50) = 2.39, p = .05]. That is, the frequency effects are smaller in the sine wave group. There were no significant state of arousal effects on d’ [F(2,20) = 1.241. This would be predicted if the states of arousal were three criteria yielding estimates of the same LI’ at each frequency. /~-vLz!~~s Median p-values calculated for each condition are in Table 1. There was considerable variability among these values (mean values over subjects ranged from 16.96 to 35.58, whereas standard deviations ranged from 10.61 to 24.02). Even when the two most audible frequencies (square waves, 125 and 250 Hz) were considered alone, there was no statistical corroberation for the predicted trend of smaller ps, the more awake the infant [analysis of variance on log /3’s: F(2, 10) = 2.79, p > . lo]. This lack of significant difference is probably due to the substantial variability. Equuf vuriance ussumprion. Using the slope of the ROC from a double probability plot, an estimate of on/ox can be obtained.l On the average, this ’ uJuS is ratio of standard signal-plus-noise distribution. unity.

deviation of noise-alone distribution to standard deviation If an equal variance assumption holds, then the ratio should

of be

AUDITORY

FREQUENCY TABLE

223

SENSITIVITY I

MEDIAN ~-VALUES FOR EACH STATE OF AROUSAL AND FREQUENCY OF SIGNAL OVER SIX SUBJECTS IN THE SINE WAVE GROUP AND THE SQUARE WAVE

Regular sleep

Irregular sleep

AVERAGED GROUP

Awake

Sine wave group (iv = 6) 70 I25 250 500 1000 2000

Hz Hz Hz Hz Hz Hz

1.0 IO.27 1.0 1.0 I.0 6.64

0.99 I.00 I.15 0.90 I.17 0.94

6.73 I.04 0.95 I.18 I.06 I.27

Square wave group (IV = 6) 70 Hz 125 Hz 250 Hz 500 Hz IO00 Hz 200@ Hz

I .45 5.80 IO.77 1.08 I.00 5.89

5.57 0.98 7.21 0.94 I.15 I.84

I .03 0.33 1.04 0.94 O.% 0.84

ratio was less than unity, which indicated that the variance of the noise-alone distribution was less than the variance of the signal-plus-noise distribution (sine wave group: x = S3, r (5) = 6.25,~ c 41; square wave group: .% = -9, r(5) = .37, NS). Although there is a tendency for low variance ratios to be found in SDT experiments (Markowitz & Swets, 1967), the ratios presented here may be unreliable since the slopes are from curves that had been generated by assuming that the three states represent three criteria. DISCUSSION Frequency

Sensitivity

For stimuli at these intensity levels, both groups of neonates show differential sensitivity to different frequencies. The significant cubic trend (S-shaped) was the highest order function fitting the data, although the results could be described as fitting linear or quadratic curves as well.z If the shape of the neonate curve was like that of adults, then only the quadratic factor would have been significant. If it corresponded to neonate threshold curves (on evoked potentials), it would have been simply linear * That the linear and quadratic components were significant indicates (a) that there is an overall decrement in the S-shaped responsivity curve over frequency and (b) that the two curves in the S were not equal in size.

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c. WEIR

(Taguichi, Picton, Orpin, & Goodman, 1969). The cubic function found here suggests that the frequency sensitivity is complex and further research would be fruitful where frequencies higher than 2000 Hz are used. Worthy of note is that any stimulus of 500 Hz or higher is not responded to unless the subject’s criterion is very low whatever his arousal state. The superiority of 70 Hz in provoking EMG responses (Bench. 1973: Hutt et al., 1968) is only found when spontaneous response levels are not considered. Wuveform

Sensitivity

These S DT data confirm the trend noticed by Hutt et al. (1968) that the groups with square wave stimuli were better. Since the stimuli were matched carefully for average energy, the intensity of the fundamental in the square wave will be less intense than the sine wave. However, the sound reproduction system attenuated low frequencies relative to high frequencies, thus flattening the power spectrum of low-frequency square waves. Since high harmonics were less frequently responsed to, this distortion may have had little effect. The hypothesis of Hutt et al. (1968) predicts that wider band noises will be more effective in provoking startles. and this may explain the superiority of square waves. However, note that alld’-values are less than unity for square waves of 500 Hz or higher, which shows that even these signals of wide bandwidth are less likely to elicit a response. The rise time of signals was rhomboid and similar for square waves and sine waves (between 10 and 25 msec). Any effect of phase of the stimulus was probably averaged over trials for both types of stimuli, Therefore, it is unlikely that these temporal parameters would have been mainly responsible for response differences. This pattern of sensitivity would seem to make the neonate especiahy sensitive to the fundamental frequencies of his own vocalization (Ostwald & Peltzman, 1974) and to adult speech. One aspect of this is that the neonate may be monitoring his own cry. That 3-day-old babies can respond differently to a cry of a j-day-old and a 5-month-old infant was shown by Simner (1971). The complex effects found in his study led to a similar conclusion to one reached by Lenard, Bernuth, and Hutt (1968) in their investigation of evoked potentials: 3-day-old neonates are differentiating features of sound that are complex combinations of bandwidth and frequency. Although proving that this sensitivity pattern is subserving an ecological function is difficult, this hypothesis may provoke further study of the relationship between neonatal crying and auditory sensitivity over the first few weeks of life. Arousal

Effects

There were no arousal effects when d’ was considered. This lack of effect, important initself, (Hutt, Lenard. & Prechtl, pp. l27- 172), suggests that the ad hoc method of correcting for spontaneous reponse levels used

AUDITORY

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SENSITIVITY

225

by Hutt etai. (1968) did not take into account the various differences among false alarm rates. To return to the question posed in the introduction, can the three states be considered as three critical levels in a traditional SDT experiment? No significant trends were found using j3 as the measure. The only finding that was significant was individual differences [F(l 1, 132) = 2.99,~ < .Ol), test on four lowest frequencies], and individual profiles were no more orderly than those of the group. It appears then, in this study at least, that arousal level does not provide a stable criterion continuum. This confirms the notion of Hutt et al. (1969), p. 164) that the states could better be regarded as qualitatively different conditions of the neonate, or perhaps it shows that not enough trials were given to allow for stability in criteria, In conclusion, this reanalysis has given statistical weight to the earlier findings of the superiority of lower frequencies and square waves in provoking startles in neonates. However, the state of arousal effects found originally, were not confirmed here. Thus, the usefulness of SDT in neonate research has been demonstrated since by taking account of spontaneous reponse levels, a new emphasis is given to the results. REFERENCES Ashton, R. State and the auditory reactivity of the human neonate. &l/rho/ of Experimenru/ Child Psychology, 1971, 12, 339-346. Bench, J. “Square wave stimuli” and neonatal auditory behavior: some comments on Ashton (1971). Hutt et 01. (1968) and Lenard, et (11. (1%9). Journal of Experitnentul Child Psychology, 1973, 16, 521-527. Hutt, S. J., Hutt, C,, Lenard. H. G., Bernuth, H. von, & Muntjewerff, W. J. Auditory responsivity in the human neonate. Nufure (London), I%& 218, 888-890. Hutt. S. J., Lenard. H. G., & Prechtl. H. F. R. Psychophysiological studies in newborn infants. In L. P. Lipsett & H. W. Reese (Eds.). Advances in child development and beha\sior (Vol 4). New York: Academic Press. l%9. Hutt, S, J, Square wave stimuli and neonatal auditory behavior: reply to Bench. Journal of Experimeniol Chi/d Psychology, 1973, 16, 530-533. Lenard. H. G., Bemuth, H. von. & Hutt. S. J. Acoustic evoked responses in newborn infants: the influence of pitch and complexity of the stimulus. Ele~rr~~en~eph~l~~r~phy und Clinical Neurophysiology, 1969. 21, I2 1- 127. Licklider, J. C. R.. & Miller, L. P. The perception of speech. In S. Stevens, Handbook of experimental psychology. New York: Wiley, 1951. Markowitz, J.. & Swets. J. A. Factors affecting the slope of empirical ROC curves: comparison of binary and rating responses. Perception and Psychophysics, 1967, 2, 91-100. Ostwald. P. F., & Peltzman. P. The cry of the human infant. Scien@ic American, i974. 230 (3). 84-91. Simner. M. L. Newborn’s response to the cry of another infant. Developmemo Psgholog.v, 5, 1971, 136-150. Taguichi, K.. Picton, T, W., Orpin. J. A., & Goodman. W. S. Evoked response audiometry in newborn infants, Acto Ofo-Lonngologiul, Supplemenfum, 252, 1969. 5- 17. Tanner. W. P.. & Swets. J. A. A decision-making theory of visual detection, P.sycholo,q/~l Re\-ieu,. 61, 1954. 401-409, RECEIVED: August 15, 1974: REVISED: March 27. 1975.