Modality Differences in the Habituation and Dishabituation of Cardiac Responsiveness in the Human Newborn TINA MOREAU Department o f Psychology Queens College of The City University o f New York Flushing, New York
The relative efficacy of (1) repeated auditory and somesthetic stimulation for the habituation of cardiac acceleration responses and (2) intramodal and cross-modal stimulation for the dishabituation of cardiac responses was studied in 45 full-term 2-day-old infants. Although the 2 stimuli were equally effective initially, repeated presentation of the somesthetic stimulus had a greater decremental effect than repeated presentation of the auditory stimulus. The stimuli, were equally effective in producing dishabituation when in a different modality from that of the habituating stimulus (cross-modal) but not when in the same modality (intramodd). Changes in the locus of stimulation without a change in modality were ineffective for producing dishabituation. The findings indicate the human newborn discriminates auditory and somesthetic inputs effectively and equally but does not discriminate contralateral from ipsilateral stimulation in either modality.
Over the past 2 decades, considerable effort has been directed to the assessment of the sensory capacities of the newborn infant and, consequently, a large body of evidence regarding the visual, auditory, somesthetic, and olfactory sensitivities of the neonate has been amassed (Kessen, Haith, & Salapatek, 1970; Pick & Pick, 1970; Reese & Lipsitt, 1970). However, because almost all of the investigations have been focused on the infant’s ability to discriminate among stimuli within a given sense modality, little information is available on the functional relationships between and among the various input systems. The importance of ascertaining the nature of dominance relations among afferent systems, of intersensory integrative abilities, and of modality differences in the sensory control of different types of response for elucidating the nature and bases of phylogenetic and ontogenetic differences in neurobehavioral organization has been stressed by both comparative and developmental psychologists (e.g., Birch, 1954, 1962; Held & Hein, 1963; Maier & Schneirla, 1964; Schneirla, 1965;
Received for publication 15 November 1974 Revised for publication 21 April 1975 Developmental Psychobiology, 9(2): 109-1 17 (1976) @ 1976 by John Wiley & Sons, Inc.
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Wohlwill, 1960). Moreover, afferent functional organization is considered prerequisite to the development of higher levels of perceptual, cognitive, and educational functions and skills (Birch & Belmont, 1964, 1965; Bruner, Olver, & Greenfield, 1966; Piaget, 1952, 1964; Werner, 1957). Despite its recognized importance for both comparative and developmental analysis, relatively few investigators have addressed themselves t o the study of afferent system interrelations in the human newborn. In our laboratory we have begun to approach this problem by using the habituation’ model t o compare the decreniental effects of repeated presentations of initially equivalent stimuli in different sense modalities on autonomic and musculoskeletal responses in the full-term neonate (Moreau & Birch, 1974; Moreau, Birch, & Turkewitz, 1970). In the present experiment. the basic habituation paradigm was expanded t o enable assessment of the comparative efficacy of auditory and somesthetic stimuli for the dishabituation of cardiac responsiveness in the healthy, full-term, 2-day-old infant. The specific questions t o which the current investigation was addressed are: (1) Do modalities differ (auditory vs somesthetic) in the efficacy of laterallypresented dishabituation stimuli for the re-elicitation of cardiac responses? (2) What is the relative efficacy of intramodal (i.e., auditory-auditory and somesthetic-somesthetic) and cross-modal (i.e., auditory-somesthetic and s:ornestheticauditory) lateralized stimulation for heart rate dishabituation? (3) Do modalities differ in recovery of cardiac responsiveness (i.e., dishabituation) to contralateral stimulation?
S ii bj ec t s Sixty-eight healthy, human female newborns’ who were resident in the well-baby nurseries of the Bronx Municipal Hospital Center were selected for study in accordance with the following criteria: ( I ) a birth weight of over 2 5 0 0 g, (2) a 1-min Apgar score of 7 or higher (Apgar & James, 1962), (3) a pediatric evaluation as a “wel~lnewborn,” and (4) n o recorded evidence of any abnormality or complication of pregnancy, labor, or delivery. Because of the exclusion of 23 infants who cried or vocalized during testing, the final sample consisted of 4 5 infants whose ages at the time of testing ranged from 22-66 hr = 40.7 hr 11.45 hr). The 45 infants were randomly assigned to 1 of the following experimental groups: Auditory Habituation-Auditory Dishabituation Group (A-A, n = l 2 ) , Somesthetic Habituation-Somesthetic Dishabituation Group (S-S, n = 14), Auditory HabituationSomesthetic Dishabituation Group (A-S, n = lo), and Somesthetic I-labituationAuditory Dishabituation Group (S-A, n = 9). The mothers of 39 of the infants (877Lof the sample) had been administered analgesic and/or anesthetic drugs during labor and/or delivery but the incidence of such medication was approximately equally distributed among the 4 experimental groups (83% in the A-A Group. 86% in thc S-S Group, 90% in the A-S Group, and 89% in the S-A Group).
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Procedure Testing took place 45-60 min prior to the regularly scheduled feeding at 0930 hours. Each infant was individually tested while in her own bassinet in a relatively quiet laboratory. Each infant was swaddled and placed in the supine position to maintain general activity levels as constant as possible. The infant’s head was placed in a (routinely used) head-holding device consisting of 2 heavily padded stainless-steel adjustable cups mounted onto a vertical rod to restrict head movement in the coronal plane. Speakers, mounted on adjustable rods, were positioned 5 cm from each of the infant’s ears. Two small adhesive strips, each having a 1.3-cm diameter cutout, were taped onto the infant’s right and left cheeks midway between the ear and the corner of the mouth to insure consistent placement of the somesthetic stimuli. Surface electrodes were placed precordially and on the abdomen for the polygraphic recording of cardiac activity. A ground electrode was placed above the infant’s left scapula. Each infant was first administered a habituation series of successive stimulations to the left side (ear or cheek) followed by a dishabituation stimulus to the right side (ear or cheek). For the A-A and A-S Groups, the habituation series consisted of 25 successive presentations of a 90-dB white noise to the left ear; for the S-S and S-A Groups, it consisted of 25 successive applications of a Grumbacher No. 12 round camel’s hair brush to the left cheek.3 The dishabituation stimulus for the A-A and S-A Groups was the 90-dB sound presented at the right ear; for the S-S and A-S Groups it was the camel’s hair brush presented to the right cheek. The duration of each stimulus was 1 sec and the interstimulus interval was 8 sec. The dishabituation stimulus was administered 8 sec after the 25th trial of the habituation series. The timing of the auditory stimulus durations and interstimulus intervals was autonated and that for the somesthetic stimulus was controlled by automatically presenting the experimenter with 1-sec auditory indicator signals (via earphones) every 8 sec.
Apparatus The auditory stimulus was produced by a Grason-Stadler noise generator and fed through a Grason-Stadler electronic switch (rise-decay time < .05 msec). The signal was then attenuated by a Hewlitt-Packard attenuator set, amplified by Hewlitt-Packard amplifiers, and presented through Quam 25A07 speakers. The stimulus durations and interstimulus intervals were programmed by a Grason-Stadler interval timer. One channel of an Offner Type R polygraph was used to record cardiac activity and 2 additional channels were used to record the onset and duration of the auditory and somesthetic stimuli. The event marker for the auditory stimuli was electronically activated, whereas that for the somesthetic stimuli was activated by the experimenter who squeezed the bulb end of a pneumograph stimultaneous with the presentation of the somesthetic stimulus to the infant. A Bruel and Kjaer Precision Sound Level Meter was used to measure the sound pressure level of the auditory stimuli at the infant’s ears. The ambient sound pressure level with d l recording apparatus turned on was 60 dB (re .0002 dynes/cm*).
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Response Measure The cardiac response measure was heart-rate (HR) acceleration, defined as an increase of 2 o r more beats per minute during the first 7 poststimulus heart beats over the number of beats per minute during the 7 heart beats immediately preceding stimulus onset. Cardiac responses were independently scored from the polygraph records by 2 raters. The intcrscorer agreement in judging HR accelerations was 95%. In cases of disagreement, decisions were made by a 3rd independent scorer.
In fan t State Two distinct indices of state were obtained t o enable assessment of rlie relationship between the state of the infant and temporal changes in cardiac responsiveness. The 1st was based upon whether her eyes were open (awake) or closed (asleep). The 2nd measure of infant state was the prestimulus HR which was also monitored for each trial in the stimulus series.
FI a bi t u at io n Series The auditory and somesthetic stimuli were equally effective for the initial elicitation of HR responses: 64% of the infants administered the auditory stimulus (A-A & A-S Groups) and 64% of the infants the somesthetic stimulus (S-A Rc S-S Groups) made cardiac accelerations t o the 1 st stimulus presentation. Repeated presentation of the somesthetic stimulus, however, had a greater decreniental effect on HK responsiveness than did repeated presentation of the auditory stimulus. The percentage of liabituation trials (i.e., Trials 2-25) on which inidnts administered the somesthetic stimulus made accelerations (X = 40.2, S.D. = 14.19) was significantly less (f = 1.69, df= 4 3 , 1-tailed p < .0S4) than that on which infants administered the auditory stimulus made such responses = 47.2, S.D. = 13.57). The greater decremental effect o f repeated somesthetic than of repeated auditory stimulation cannot be accounted for in ternis of the Law of Initial Values, i.e., the inverse relationship between prestirnulus IIR level and cardiac acceleration, in that the prestimulus HR over the somesthetic stimulus series = 122.6, S.D. = 9.87) was lower rather than higher than that over the auditory stimulus series (X = 128.4, S.D. = 8.52). By the end of the habituation series, cardiac responsiveness was markcdly rcdiiced in both the auditory and soinesthetic stimulation groups. Significantly fewer infants in the auditory stimulation groups made responses on Trial 25 (26%)) than on Trial I (64%: I-tailed p = .03, McNernar test for significance of change). Similarly, in the somesthetic stirnulation groups, significantly fewer infants responded on Trial 25 (32%) than on Trial 1 (64%); 1-tailed p = .05, McNemar test for significance of change). The decrease in cardiac responsiveness from the 1st t o the last trial of the auditory habituation series was approximately the same as that for the somesthetic habituation series and no evidence existed of a difference between the auditory and somestlietic
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stimulation groups in the percentage of infants making HR accelerations on Trial 25 ( z = .43, n.s.). These findings indicate that although repeated somesthetic stiniulation had a greater overall decremental effect than repeated auditory stimulation, the effect became equalized by the end of the reiterative stimulus series.
Disha bi t ua t ion St irnulus The effectiveness of the auditory and somesthetic disliabituation stin~ulifor the elicitation of HR acceleration was dependent upon whether the stiinulus was in the same or in a different modality from the stimulus used in the habituation series: 65% of the infants for whom the dishabituation stimulus was in a different modality than the habituation stimulus (Groups S-A & A-S) made accelerations to the dishabituation ~ in stimulus, whereas only 3 1% of the infants for whom the dishabituation ~ t i i n u l uwas the same modality as the habituation stimulus (Groups A-A & S-S) made such responses. This difference, which was significant at the .03 level ( z = 2.19), cannot be attributed to differences in prestimulus HR levels in that the prestirnulus HR in the = 127.2, S.D. = I 1.39) was approximately the same as change-of-modality groups the prestimulus HR in the no-change-of-modality groups (X = 128.2, S.D. = 10.1 1 : t = .31, df= 41, n.s.). For neither the no-change-of-modality groups nor the change-of-modality groups did any evidence exist of a differential effect of auditory and somesthetic stimulation: 33% of the infants administered the auditory dishabituation stimulus following auditory stimulus habituation (A-A Group) and 29% of the infants administered the somesthetic dishabituation stimulus following somesthetic stimulus habituation (S-S Group) made cardiac acceleration responses t o the dishabituation stimulus ( z = .26, n.s.). Similarly, approximately the Same number of subjects made accelerations to the auditory dishabituation stimulus following somesthetic stimulus habituation (67%) as made such responses to the somesthetic dishabituation stimulus following auditory stimulus habituation (63%; z = .18, n.s.). Direct comparison of the efficacy of the auditory and somesthetic dishabituation stimuli (i.e., A-S + S-S Groups vs A-A + S-A Groups) for the elicitation of cardiac responses failed to reveal any difference (41% vs 48%, respectively; z = .44, 11.s.). Both the auditory and somesthetic stimuli were effective in reeliciting habituated HR responses when the stimulus was in a different modality from that of the stimulus used in the habituation series but not when the stimulus was in the same modality. For the S-A and A-S Groups, a significant increase existed in the percentage of infants who made accelerations from Trial 25 of the habituation series (25%) to the dishabituation trial (65%; 1-tailed p = .03, McNemar test for significance of change). In contrast, for the A-A and S-S Groups, no change appeared in the percentage of infants making accelerations from habituation Trial 25 (32%) t o the dishabituation trial (31%; n.s., McNernar test for significance of change).
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Infant State and Cardiac Responsiveness To assess the relationship between the state of the infant and changes in HR responsiveness, we examined (1) the distribution of “awake” and “asleep” infants for both the habituation series’ and the dishabituation stimulus, and ( 2 ) the temporal
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course of prestimulus HR over the 25 habituation trials. During the habituation series, 55%)of the infants administered the soinesthetic stimulus (S-S & S-A Groups) and 30V) o f the infants administered the auditory stimulus (A-A & A-S Groups) werc “asleep” ( z = 1.61, p = . I I , 11s.). For the dishabituation stimulus, n o evidence of a difference in the distribution of “awake” and “asleep” infants between the no-change-of-modality groups (Groups A-A & S-S) and the change-of-modality groups (Groups S-A & A-S) appeared: 44% o f the former and 35% of the latter were “asleep” ( z = .45, t1.s.). Analysis of the temporal course o f prestimulus HR over the habituation series also f’:iiled to provide evidence of a systematic change lor either tlie auditory o r tlie somesthetic stimulus; the correlation between trial number and prestiniulus 11R was not significant for either the auditory stimulation groups (r = .24, df= 24, i1.s.) or t h e somestlietic stimulation groups (r =: . I 5 , df= 24, n.s.). Moreover, n o evidence appeared to indicate a relationship between the prestiniulus cardiac rate and the perccntage of infants making HR accelerations across the habituation series for either tlic auditory (r = .18, d f = 24, n s . ) o r the somesthetic stimulation (r = .09. df‘= 24, n.s.) groups. ~
Discussion The results o f the present investigation provide evidence of a differential effecl of cross-modal and intramodal stimulation on the dishabituation o f cardiac rsesponscs in the Iiunian newborn. Because infants for whom the habituation and dishabituation stimuli were in different sense modalities made significantly more HR acceler,‘I t’ions t o the disliabituation stimulus than infants for whom the 2 stimuli were in the same modality, cross-modal input apparently is more effective than intraniodal input f‘or producing disliabituation of cardiac responses. Moreover, whereas presentation of either the auditory stimulus following repeated somesthetic stimulation or tlie somesthetic stimulus following repeated auditory stimulation resulted in a signiticant increase in tlie number of infants who made HR responses, neither stimulus, when adrninistercd following reiterative stimulation in the same modality, resulted in a change in the number o f infants responding. Thus, both the auditory and soniesthetic stimuli were effective for the re-elicitation of habituated cardiac responses when they were in a different modality from that of the habituation stimulus but not when they were in tlie s;inie modality. These findings demonstrate the efficacy of both auditory and somestlietic inputs for cross-modal dishabituation as well as the apparent inefficacy o f either input for intramodal dishabituation. The current results provide important information concerning the discriminative abilities of the young infant. T o the extent that recovery of response t o a change in tlic intensity, the frequency, the locus, the context, or the modality of stimulation is indicative of differentiation and discrimination, the present data suggest that the newborn infant is capable of discriminating inputs to different sense modalities. The finding of cross-modal dishabituation of HR responses to both auditory and somestlietic stimuli reveals that the infant differentiates between the 2 inputs. In addition, tlie failure to obtain evidence of modality differences in the effects 01‘ cross-modal dishabituation suggests that the auditory and somesthetic stimiili are equally discriminable for the infant. Although these results cannot necessarily be
MODALITY DIFFERENCES IN NEONATAL DISHABITUATION
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generalized to other sensory avenues or to other stimuli within the lnodalities examined, they do indicate that the neonate discriminates (these) auditory and somesthetic inputs equally and effectively. In contrast to the obtained recovery of cardiac responses to a change in the modality of stimulation, no evidence existed of an effect of changing the locus of stimulation. Neither right-sided auditory stimulation following repeated left-sided auditory input nor right-sided somesthetic stimulation following repeated left-sided somesthetic input resulted in the re-elicitation of habituated cardiac acceleration responses. Because changes in the locus of stimulation without a change in modality were ineffective for producing dishabituation, 2-day-old infants apparently do not discriminate either right-sided from left-sided stimulation or contralateral from ipsilateral stimulation in either the auditory or somesthetic sense modalities. The failure to obtain evidence of recovery of HR responses to contralateral auditory stimulation in the present study is in apparent disagreement with the findings of Leventhal & Lipsitt (1964) who, utilizing an experimental paradigm similar to that used here, reported recovery of respiratory, stabilimeter, and leg movement responses to a tonal stimulus presented to one ear following habituation of these responses to repeated tonal stimulation of the other ear in normal infants 1-5 days old. Although the absence of evidence of sound localization in the current study limits the intramodal generalizability of auditory localization in the neonate, the discrepant findings of the 2 studies can be accounted for in terms of differences in the type and duration of the stimuli used as well as in the responses measured. One fairly obvious explanation derives from the fact that the present investigation, utilizing HR acceleration as the only response indicator, yielded no evidence of either somesthetic or auditory localization, whereas Leventhal & Lipsitt’s investigation, utilizing 3 different noncardiac responses, did yield evidence of sound localization. The cardiac response for the newborn infant is possibly not as sensitive an indicator of dishabituation to locus change as are the other response measures. The present finding of a greater decremental effect of repeated somesthetic than of repeated auditory stimulation on HR acceleration responses corloborates our earlier finding (Moreau et al., 1970) of faster and more stable cardiac habituation to repeated somesthetic than to repeated auditory stimulation. These results provide evidence of modality differences in the persistance of effect of repeated stimulation and lead to the conclusion that even when inputs to different sense modalities are equally effective for the initial elicitation of response in the newborn, their repeated presentation has different effects on the temporal course of subsequent responsiveness. The results of several experimental studies of the effects of repeated stirnulation on the temporal course of behavioral and physiological responsiveness in young infants reveal a relationship between the state of the infant and the rate and course of response decrement. Campos & Brackbill (1973), for example, demonstrated that state not only predicted prestimulus HR levels in 2-week-old infants but was correlated with the rate and pattern of decrement of cardiac response to repeated white noise stimulation. Hutt, Lenard, and Prechtl (1969) have even suggested that, because they found no evidence of a systematic decline in neonatal responsiveness within a stable state, changes in state may account for much of the response decrement regarded as habituation. Neither the specific results reported nor the inferences made therefrom are supported by the data of the current experiment. We found no evidence of (1) any
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group differences in the distribution of awake and asleep infants during either the habituation series of the dishabituation stimulus, (2) a systematic change in prestimulus HR over either the repeated auditory or the repeated somesthetic stimulus series, ( 3 ) a relationship between prestimulus HR and the number of infants making cardiac responses to either habituation stimulus, and (4) a difference between the change-of-modality and the nochange-of-modality groups in predishabituation stimulus HR. Thus, because neither the rather crude measure of state (i.e., eyes open = awake, eyes closed = asleep) nor the more refined index (i.e., prestimulus HR) was related to cardiac responsiveness, the present findings cannot be attributed to alterations in infant state.
Notes ‘The terms “habituation” and “dishabituation,” as used throughout this paper, refer to response decrement consequent upon repeated stimulation and recovery of response consequent upon a change in stimulation, respectively. *Male infants were excluded because of possible changes in irritability and arousal level resultant from circumcision, routinely performed at this hospital when the infant is 2-3 days old. 3Preselection of the auditory and somesthetic stimuli was based upon our earlier reported finding (hforeau e t al., 1970) of equivalent effectiveness of these stimuli for the initial (elicitation of cardiac acceleration responses. Similarly, a standard number of 25 habituation trials was used because the results of our previous investigation indicated that this number of repeated stimulus prescntations is sufficient t o produce significant decrements in neonatal cardiac responsiveness. 4 A I-tailed test was used here and in those subsequent analyses (indicated in the textj in which thc obtained direction of difference either was predicted/expected o r essentially replicated earlier reported findings (Moreau e t al., 1970). ’Infants who, because of momentary changes in state, could not be clearly designated as “awake” or “asleep” for the entire series were omitted from the analysis, resulting in the exclusion of 3 infants. This investigation was supported by the National lnstitutes of Health, National Institutc of Child Health and Human Development (HD-00719). The author gratefully acknowledges thc help and cooperation of Miriam Winters and the nurses of the Well-Baby Unit of the Bronx Municipal Hospital Center, and the able assistance of Dothlyn Dennis, Maureen Malovany, Dorothy Trifan, and Bertha Williams in the collection and tabulation of data. Send requests for reprints to: Tina Moreau, Department of Psychology, Queens College of The City University of New York, 65-30 Kissena Boulevard, I h s h i n g , New York 11367. U . S . A .
References Apgar, V., and James, L. S. (1962). Further observations on the newborn scoring systcm. Am. J. Dis. Child., 104: 419. Birch, H. (;. (1954). Comparative psychology. In F. L. Marcuse (Ed.), Areas of Psychologj. New York: Harper. Pp. 446-477. Birch, €1. G. (1962). Dyslexia and the maturation of visual function. In J. Money (Ed.), R(>adinp Disability. Baltimore: The Johns Hopkins Press. Pp. 161-169. Birch, H. G., and Belniont, L. (1964). Auditory-visual integration in normal and retarded readers. Am. J. Orthopsychiatry, 34: 852-861. Birch, H. G., and Belmont, L. (1965). Auditory-visual integration, intelligence and reading ability in srhool children. Percept. Mot. Skills, 20: 295-305. Bruner. J. S., Olver, R. R., and Greenfield, P. M. (1966). Studies in Cogtzzitive Growl%. New York: Wilcy.
C m p o s , .I. J., and Hrackbill, Y. (1973). Infant state: Relationship to heart rate, bchavioral r?sponse and response decrement. Dev. Psychohiol., 6: 9-19.
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Held, R., and Hein, A. (1 963). Movement-produced stimulation in the development of visuallyguided behavior. J. Comp. Physiol. Psychol., 56: 872-876. Hutt, S. J., Lenard, H. C., and Prechtl, H. F. R. (1969). Psychophysiological studies in newborn infants. In L. P. Lipsitt and H. W. Reese (Eds.), Advances in Child Development and Behavior, Val. 4. New York: Academic. Pp. 127-172. Kessen, W., IIaith, M. M., and Salapatek, P. H. (1970). Infancy. In P. H. Mussen (Ed.), Carmichael’s Manual of Child Psychology, Vol. I. New York: Wiley. Pp. 287-447. Leventhal, A. S., and Lipsitt, L. P. (1964). Adaptation, pitch discrimination, and sound localization in the neonate. Child Dev., 35: 759-767. Maier, N. R. F., and Schneirla, T. C. (1964). Principles of Animal Psychology. New York: Dover. Moreau, T., and Birch, H. C. (1974). Relationship between obstctrical general anesthesia and rate of neonatal habituation to repeated stimulation. Dev. Med. Child Neurol., 16: 612-619. Moreau, T., Birch, H. G., and Turkewitz, G . (1970). Ease of habituation to repeated auditory and soinesthetic stimulation in the human newborn, J. Exp. Child Psychol., 9: 193-207. Piaget, J. (1952). The Origins of Intelligence in Children. New York: International Universities Press. Piaget, J. (1964). 7’he Construction of Reality in the Child. New York: Basic Books. Pick, H. L., and Pick, A. D. (1970). Sensory and perceptual development. In P. H. Mussen (Ed.), Carmichael’s Manual of Child Psychology, Vol. I. New York: Wiley. Pp. 773-830. Reese, H. W., and Lipsitt, L. P. (1970). Experimental Child Psychology. New York: Academic. Schneirla, T. C. (1965). Aspects of stimulation and organization in approach/withdrawal processes underlying vertebrate behavioral development. In D. L. Lehrman, R. Binde, and E. Shaw (Eds),Advances in the Study of Behavior. New York: Academic. Pp. 2-75. Werner, H. (1957). Comparative Psychology of Mental Development. New York: International Universities Press. Wohlwill, J. F. (1960). Developmental studies of perception. Psychol. Bull., 57: 249-288.
The relative efficacy of (1) repeated auditory and somesthetic stimulation for the habituation of cardiac acceleration responses and (2) intramodal and cross-modal stimulation for the dishabituation of cardiac responses was studied in 45 full-term 2-day-old infants. Although the 2 stimuli were equally effective initially, repeated presentation of the somesthetic stimulus had a greater decremental effect than repeated presentation of the auditory stimulus. The stimuli, were equally effective in producing dishabituation when in a different modality from that of the habituating stimulus (cross-modal) but not when in the same modality (intramodd). Changes in the locus of stimulation without a change in modality were ineffective for producing dishabituation. The findings indicate the human newborn discriminates auditory and somesthetic inputs effectively and equally but does not discriminate contralateral from ipsilateral stimulation in either modality.
Over the past 2 decades, considerable effort has been directed to the assessment of the sensory capacities of the newborn infant and, consequently, a large body of evidence regarding the visual, auditory, somesthetic, and olfactory sensitivities of the neonate has been amassed (Kessen, Haith, & Salapatek, 1970; Pick & Pick, 1970; Reese & Lipsitt, 1970). However, because almost all of the investigations have been focused on the infant’s ability to discriminate among stimuli within a given sense modality, little information is available on the functional relationships between and among the various input systems. The importance of ascertaining the nature of dominance relations among afferent systems, of intersensory integrative abilities, and of modality differences in the sensory control of different types of response for elucidating the nature and bases of phylogenetic and ontogenetic differences in neurobehavioral organization has been stressed by both comparative and developmental psychologists (e.g., Birch, 1954, 1962; Held & Hein, 1963; Maier & Schneirla, 1964; Schneirla, 1965;
Received for publication 15 November 1974 Revised for publication 21 April 1975 Developmental Psychobiology, 9(2): 109-1 17 (1976) @ 1976 by John Wiley & Sons, Inc.
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Wohlwill, 1960). Moreover, afferent functional organization is considered prerequisite to the development of higher levels of perceptual, cognitive, and educational functions and skills (Birch & Belmont, 1964, 1965; Bruner, Olver, & Greenfield, 1966; Piaget, 1952, 1964; Werner, 1957). Despite its recognized importance for both comparative and developmental analysis, relatively few investigators have addressed themselves t o the study of afferent system interrelations in the human newborn. In our laboratory we have begun to approach this problem by using the habituation’ model t o compare the decreniental effects of repeated presentations of initially equivalent stimuli in different sense modalities on autonomic and musculoskeletal responses in the full-term neonate (Moreau & Birch, 1974; Moreau, Birch, & Turkewitz, 1970). In the present experiment. the basic habituation paradigm was expanded t o enable assessment of the comparative efficacy of auditory and somesthetic stimuli for the dishabituation of cardiac responsiveness in the healthy, full-term, 2-day-old infant. The specific questions t o which the current investigation was addressed are: (1) Do modalities differ (auditory vs somesthetic) in the efficacy of laterallypresented dishabituation stimuli for the re-elicitation of cardiac responses? (2) What is the relative efficacy of intramodal (i.e., auditory-auditory and somesthetic-somesthetic) and cross-modal (i.e., auditory-somesthetic and s:ornestheticauditory) lateralized stimulation for heart rate dishabituation? (3) Do modalities differ in recovery of cardiac responsiveness (i.e., dishabituation) to contralateral stimulation?
S ii bj ec t s Sixty-eight healthy, human female newborns’ who were resident in the well-baby nurseries of the Bronx Municipal Hospital Center were selected for study in accordance with the following criteria: ( I ) a birth weight of over 2 5 0 0 g, (2) a 1-min Apgar score of 7 or higher (Apgar & James, 1962), (3) a pediatric evaluation as a “wel~lnewborn,” and (4) n o recorded evidence of any abnormality or complication of pregnancy, labor, or delivery. Because of the exclusion of 23 infants who cried or vocalized during testing, the final sample consisted of 4 5 infants whose ages at the time of testing ranged from 22-66 hr = 40.7 hr 11.45 hr). The 45 infants were randomly assigned to 1 of the following experimental groups: Auditory Habituation-Auditory Dishabituation Group (A-A, n = l 2 ) , Somesthetic Habituation-Somesthetic Dishabituation Group (S-S, n = 14), Auditory HabituationSomesthetic Dishabituation Group (A-S, n = lo), and Somesthetic I-labituationAuditory Dishabituation Group (S-A, n = 9). The mothers of 39 of the infants (877Lof the sample) had been administered analgesic and/or anesthetic drugs during labor and/or delivery but the incidence of such medication was approximately equally distributed among the 4 experimental groups (83% in the A-A Group. 86% in thc S-S Group, 90% in the A-S Group, and 89% in the S-A Group).
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Procedure Testing took place 45-60 min prior to the regularly scheduled feeding at 0930 hours. Each infant was individually tested while in her own bassinet in a relatively quiet laboratory. Each infant was swaddled and placed in the supine position to maintain general activity levels as constant as possible. The infant’s head was placed in a (routinely used) head-holding device consisting of 2 heavily padded stainless-steel adjustable cups mounted onto a vertical rod to restrict head movement in the coronal plane. Speakers, mounted on adjustable rods, were positioned 5 cm from each of the infant’s ears. Two small adhesive strips, each having a 1.3-cm diameter cutout, were taped onto the infant’s right and left cheeks midway between the ear and the corner of the mouth to insure consistent placement of the somesthetic stimuli. Surface electrodes were placed precordially and on the abdomen for the polygraphic recording of cardiac activity. A ground electrode was placed above the infant’s left scapula. Each infant was first administered a habituation series of successive stimulations to the left side (ear or cheek) followed by a dishabituation stimulus to the right side (ear or cheek). For the A-A and A-S Groups, the habituation series consisted of 25 successive presentations of a 90-dB white noise to the left ear; for the S-S and S-A Groups, it consisted of 25 successive applications of a Grumbacher No. 12 round camel’s hair brush to the left cheek.3 The dishabituation stimulus for the A-A and S-A Groups was the 90-dB sound presented at the right ear; for the S-S and A-S Groups it was the camel’s hair brush presented to the right cheek. The duration of each stimulus was 1 sec and the interstimulus interval was 8 sec. The dishabituation stimulus was administered 8 sec after the 25th trial of the habituation series. The timing of the auditory stimulus durations and interstimulus intervals was autonated and that for the somesthetic stimulus was controlled by automatically presenting the experimenter with 1-sec auditory indicator signals (via earphones) every 8 sec.
Apparatus The auditory stimulus was produced by a Grason-Stadler noise generator and fed through a Grason-Stadler electronic switch (rise-decay time < .05 msec). The signal was then attenuated by a Hewlitt-Packard attenuator set, amplified by Hewlitt-Packard amplifiers, and presented through Quam 25A07 speakers. The stimulus durations and interstimulus intervals were programmed by a Grason-Stadler interval timer. One channel of an Offner Type R polygraph was used to record cardiac activity and 2 additional channels were used to record the onset and duration of the auditory and somesthetic stimuli. The event marker for the auditory stimuli was electronically activated, whereas that for the somesthetic stimuli was activated by the experimenter who squeezed the bulb end of a pneumograph stimultaneous with the presentation of the somesthetic stimulus to the infant. A Bruel and Kjaer Precision Sound Level Meter was used to measure the sound pressure level of the auditory stimuli at the infant’s ears. The ambient sound pressure level with d l recording apparatus turned on was 60 dB (re .0002 dynes/cm*).
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Response Measure The cardiac response measure was heart-rate (HR) acceleration, defined as an increase of 2 o r more beats per minute during the first 7 poststimulus heart beats over the number of beats per minute during the 7 heart beats immediately preceding stimulus onset. Cardiac responses were independently scored from the polygraph records by 2 raters. The intcrscorer agreement in judging HR accelerations was 95%. In cases of disagreement, decisions were made by a 3rd independent scorer.
In fan t State Two distinct indices of state were obtained t o enable assessment of rlie relationship between the state of the infant and temporal changes in cardiac responsiveness. The 1st was based upon whether her eyes were open (awake) or closed (asleep). The 2nd measure of infant state was the prestimulus HR which was also monitored for each trial in the stimulus series.
FI a bi t u at io n Series The auditory and somesthetic stimuli were equally effective for the initial elicitation of HR responses: 64% of the infants administered the auditory stimulus (A-A & A-S Groups) and 64% of the infants the somesthetic stimulus (S-A Rc S-S Groups) made cardiac accelerations t o the 1 st stimulus presentation. Repeated presentation of the somesthetic stimulus, however, had a greater decreniental effect on HK responsiveness than did repeated presentation of the auditory stimulus. The percentage of liabituation trials (i.e., Trials 2-25) on which inidnts administered the somesthetic stimulus made accelerations (X = 40.2, S.D. = 14.19) was significantly less (f = 1.69, df= 4 3 , 1-tailed p < .0S4) than that on which infants administered the auditory stimulus made such responses = 47.2, S.D. = 13.57). The greater decremental effect o f repeated somesthetic than of repeated auditory stimulation cannot be accounted for in ternis of the Law of Initial Values, i.e., the inverse relationship between prestirnulus IIR level and cardiac acceleration, in that the prestimulus HR over the somesthetic stimulus series = 122.6, S.D. = 9.87) was lower rather than higher than that over the auditory stimulus series (X = 128.4, S.D. = 8.52). By the end of the habituation series, cardiac responsiveness was markcdly rcdiiced in both the auditory and soinesthetic stimulation groups. Significantly fewer infants in the auditory stimulation groups made responses on Trial 25 (26%)) than on Trial I (64%: I-tailed p = .03, McNernar test for significance of change). Similarly, in the somesthetic stirnulation groups, significantly fewer infants responded on Trial 25 (32%) than on Trial 1 (64%); 1-tailed p = .05, McNemar test for significance of change). The decrease in cardiac responsiveness from the 1st t o the last trial of the auditory habituation series was approximately the same as that for the somesthetic habituation series and no evidence existed of a difference between the auditory and somestlietic
(x
(x
MODALITY DIFFERENCES IN NEONATAL DISIIABITUATION
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stimulation groups in the percentage of infants making HR accelerations on Trial 25 ( z = .43, n.s.). These findings indicate that although repeated somesthetic stiniulation had a greater overall decremental effect than repeated auditory stimulation, the effect became equalized by the end of the reiterative stimulus series.
Disha bi t ua t ion St irnulus The effectiveness of the auditory and somesthetic disliabituation stin~ulifor the elicitation of HR acceleration was dependent upon whether the stiinulus was in the same or in a different modality from the stimulus used in the habituation series: 65% of the infants for whom the dishabituation stimulus was in a different modality than the habituation stimulus (Groups S-A & A-S) made accelerations to the dishabituation ~ in stimulus, whereas only 3 1% of the infants for whom the dishabituation ~ t i i n u l uwas the same modality as the habituation stimulus (Groups A-A & S-S) made such responses. This difference, which was significant at the .03 level ( z = 2.19), cannot be attributed to differences in prestimulus HR levels in that the prestirnulus HR in the = 127.2, S.D. = I 1.39) was approximately the same as change-of-modality groups the prestimulus HR in the no-change-of-modality groups (X = 128.2, S.D. = 10.1 1 : t = .31, df= 41, n.s.). For neither the no-change-of-modality groups nor the change-of-modality groups did any evidence exist of a differential effect of auditory and somesthetic stimulation: 33% of the infants administered the auditory dishabituation stimulus following auditory stimulus habituation (A-A Group) and 29% of the infants administered the somesthetic dishabituation stimulus following somesthetic stimulus habituation (S-S Group) made cardiac acceleration responses t o the dishabituation stimulus ( z = .26, n.s.). Similarly, approximately the Same number of subjects made accelerations to the auditory dishabituation stimulus following somesthetic stimulus habituation (67%) as made such responses to the somesthetic dishabituation stimulus following auditory stimulus habituation (63%; z = .18, n.s.). Direct comparison of the efficacy of the auditory and somesthetic dishabituation stimuli (i.e., A-S + S-S Groups vs A-A + S-A Groups) for the elicitation of cardiac responses failed to reveal any difference (41% vs 48%, respectively; z = .44, 11.s.). Both the auditory and somesthetic stimuli were effective in reeliciting habituated HR responses when the stimulus was in a different modality from that of the stimulus used in the habituation series but not when the stimulus was in the same modality. For the S-A and A-S Groups, a significant increase existed in the percentage of infants who made accelerations from Trial 25 of the habituation series (25%) to the dishabituation trial (65%; 1-tailed p = .03, McNemar test for significance of change). In contrast, for the A-A and S-S Groups, no change appeared in the percentage of infants making accelerations from habituation Trial 25 (32%) t o the dishabituation trial (31%; n.s., McNernar test for significance of change).
(x
Infant State and Cardiac Responsiveness To assess the relationship between the state of the infant and changes in HR responsiveness, we examined (1) the distribution of “awake” and “asleep” infants for both the habituation series’ and the dishabituation stimulus, and ( 2 ) the temporal
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MORl.ALJ
course of prestimulus HR over the 25 habituation trials. During the habituation series, 55%)of the infants administered the soinesthetic stimulus (S-S & S-A Groups) and 30V) o f the infants administered the auditory stimulus (A-A & A-S Groups) werc “asleep” ( z = 1.61, p = . I I , 11s.). For the dishabituation stimulus, n o evidence of a difference in the distribution of “awake” and “asleep” infants between the no-change-of-modality groups (Groups A-A & S-S) and the change-of-modality groups (Groups S-A & A-S) appeared: 44% o f the former and 35% of the latter were “asleep” ( z = .45, t1.s.). Analysis of the temporal course o f prestimulus HR over the habituation series also f’:iiled to provide evidence of a systematic change lor either tlie auditory o r tlie somesthetic stimulus; the correlation between trial number and prestiniulus 11R was not significant for either the auditory stimulation groups (r = .24, df= 24, i1.s.) or t h e somestlietic stimulation groups (r =: . I 5 , df= 24, n.s.). Moreover, n o evidence appeared to indicate a relationship between the prestiniulus cardiac rate and the perccntage of infants making HR accelerations across the habituation series for either tlic auditory (r = .18, d f = 24, n s . ) o r the somesthetic stimulation (r = .09. df‘= 24, n.s.) groups. ~
Discussion The results o f the present investigation provide evidence of a differential effecl of cross-modal and intramodal stimulation on the dishabituation o f cardiac rsesponscs in the Iiunian newborn. Because infants for whom the habituation and dishabituation stimuli were in different sense modalities made significantly more HR acceler,‘I t’ions t o the disliabituation stimulus than infants for whom the 2 stimuli were in the same modality, cross-modal input apparently is more effective than intraniodal input f‘or producing disliabituation of cardiac responses. Moreover, whereas presentation of either the auditory stimulus following repeated somesthetic stimulation or tlie somesthetic stimulus following repeated auditory stimulation resulted in a signiticant increase in tlie number of infants who made HR responses, neither stimulus, when adrninistercd following reiterative stimulation in the same modality, resulted in a change in the number o f infants responding. Thus, both the auditory and soniesthetic stimuli were effective for the re-elicitation of habituated cardiac responses when they were in a different modality from that of the habituation stimulus but not when they were in tlie s;inie modality. These findings demonstrate the efficacy of both auditory and somestlietic inputs for cross-modal dishabituation as well as the apparent inefficacy o f either input for intramodal dishabituation. The current results provide important information concerning the discriminative abilities of the young infant. T o the extent that recovery of response t o a change in tlic intensity, the frequency, the locus, the context, or the modality of stimulation is indicative of differentiation and discrimination, the present data suggest that the newborn infant is capable of discriminating inputs to different sense modalities. The finding of cross-modal dishabituation of HR responses to both auditory and somestlietic stimuli reveals that the infant differentiates between the 2 inputs. In addition, tlie failure to obtain evidence of modality differences in the effects 01‘ cross-modal dishabituation suggests that the auditory and somesthetic stimiili are equally discriminable for the infant. Although these results cannot necessarily be
MODALITY DIFFERENCES IN NEONATAL DISHABITUATION
1 15
generalized to other sensory avenues or to other stimuli within the lnodalities examined, they do indicate that the neonate discriminates (these) auditory and somesthetic inputs equally and effectively. In contrast to the obtained recovery of cardiac responses to a change in the modality of stimulation, no evidence existed of an effect of changing the locus of stimulation. Neither right-sided auditory stimulation following repeated left-sided auditory input nor right-sided somesthetic stimulation following repeated left-sided somesthetic input resulted in the re-elicitation of habituated cardiac acceleration responses. Because changes in the locus of stimulation without a change in modality were ineffective for producing dishabituation, 2-day-old infants apparently do not discriminate either right-sided from left-sided stimulation or contralateral from ipsilateral stimulation in either the auditory or somesthetic sense modalities. The failure to obtain evidence of recovery of HR responses to contralateral auditory stimulation in the present study is in apparent disagreement with the findings of Leventhal & Lipsitt (1964) who, utilizing an experimental paradigm similar to that used here, reported recovery of respiratory, stabilimeter, and leg movement responses to a tonal stimulus presented to one ear following habituation of these responses to repeated tonal stimulation of the other ear in normal infants 1-5 days old. Although the absence of evidence of sound localization in the current study limits the intramodal generalizability of auditory localization in the neonate, the discrepant findings of the 2 studies can be accounted for in terms of differences in the type and duration of the stimuli used as well as in the responses measured. One fairly obvious explanation derives from the fact that the present investigation, utilizing HR acceleration as the only response indicator, yielded no evidence of either somesthetic or auditory localization, whereas Leventhal & Lipsitt’s investigation, utilizing 3 different noncardiac responses, did yield evidence of sound localization. The cardiac response for the newborn infant is possibly not as sensitive an indicator of dishabituation to locus change as are the other response measures. The present finding of a greater decremental effect of repeated somesthetic than of repeated auditory stimulation on HR acceleration responses corloborates our earlier finding (Moreau et al., 1970) of faster and more stable cardiac habituation to repeated somesthetic than to repeated auditory stimulation. These results provide evidence of modality differences in the persistance of effect of repeated stimulation and lead to the conclusion that even when inputs to different sense modalities are equally effective for the initial elicitation of response in the newborn, their repeated presentation has different effects on the temporal course of subsequent responsiveness. The results of several experimental studies of the effects of repeated stirnulation on the temporal course of behavioral and physiological responsiveness in young infants reveal a relationship between the state of the infant and the rate and course of response decrement. Campos & Brackbill (1973), for example, demonstrated that state not only predicted prestimulus HR levels in 2-week-old infants but was correlated with the rate and pattern of decrement of cardiac response to repeated white noise stimulation. Hutt, Lenard, and Prechtl (1969) have even suggested that, because they found no evidence of a systematic decline in neonatal responsiveness within a stable state, changes in state may account for much of the response decrement regarded as habituation. Neither the specific results reported nor the inferences made therefrom are supported by the data of the current experiment. We found no evidence of (1) any
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group differences in the distribution of awake and asleep infants during either the habituation series of the dishabituation stimulus, (2) a systematic change in prestimulus HR over either the repeated auditory or the repeated somesthetic stimulus series, ( 3 ) a relationship between prestimulus HR and the number of infants making cardiac responses to either habituation stimulus, and (4) a difference between the change-of-modality and the nochange-of-modality groups in predishabituation stimulus HR. Thus, because neither the rather crude measure of state (i.e., eyes open = awake, eyes closed = asleep) nor the more refined index (i.e., prestimulus HR) was related to cardiac responsiveness, the present findings cannot be attributed to alterations in infant state.
Notes ‘The terms “habituation” and “dishabituation,” as used throughout this paper, refer to response decrement consequent upon repeated stimulation and recovery of response consequent upon a change in stimulation, respectively. *Male infants were excluded because of possible changes in irritability and arousal level resultant from circumcision, routinely performed at this hospital when the infant is 2-3 days old. 3Preselection of the auditory and somesthetic stimuli was based upon our earlier reported finding (hforeau e t al., 1970) of equivalent effectiveness of these stimuli for the initial (elicitation of cardiac acceleration responses. Similarly, a standard number of 25 habituation trials was used because the results of our previous investigation indicated that this number of repeated stimulus prescntations is sufficient t o produce significant decrements in neonatal cardiac responsiveness. 4 A I-tailed test was used here and in those subsequent analyses (indicated in the textj in which thc obtained direction of difference either was predicted/expected o r essentially replicated earlier reported findings (Moreau e t al., 1970). ’Infants who, because of momentary changes in state, could not be clearly designated as “awake” or “asleep” for the entire series were omitted from the analysis, resulting in the exclusion of 3 infants. This investigation was supported by the National lnstitutes of Health, National Institutc of Child Health and Human Development (HD-00719). The author gratefully acknowledges thc help and cooperation of Miriam Winters and the nurses of the Well-Baby Unit of the Bronx Municipal Hospital Center, and the able assistance of Dothlyn Dennis, Maureen Malovany, Dorothy Trifan, and Bertha Williams in the collection and tabulation of data. Send requests for reprints to: Tina Moreau, Department of Psychology, Queens College of The City University of New York, 65-30 Kissena Boulevard, I h s h i n g , New York 11367. U . S . A .
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C m p o s , .I. J., and Hrackbill, Y. (1973). Infant state: Relationship to heart rate, bchavioral r?sponse and response decrement. Dev. Psychohiol., 6: 9-19.
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Held, R., and Hein, A. (1 963). Movement-produced stimulation in the development of visuallyguided behavior. J. Comp. Physiol. Psychol., 56: 872-876. Hutt, S. J., Lenard, H. C., and Prechtl, H. F. R. (1969). Psychophysiological studies in newborn infants. In L. P. Lipsitt and H. W. Reese (Eds.), Advances in Child Development and Behavior, Val. 4. New York: Academic. Pp. 127-172. Kessen, W., IIaith, M. M., and Salapatek, P. H. (1970). Infancy. In P. H. Mussen (Ed.), Carmichael’s Manual of Child Psychology, Vol. I. New York: Wiley. Pp. 287-447. Leventhal, A. S., and Lipsitt, L. P. (1964). Adaptation, pitch discrimination, and sound localization in the neonate. Child Dev., 35: 759-767. Maier, N. R. F., and Schneirla, T. C. (1964). Principles of Animal Psychology. New York: Dover. Moreau, T., and Birch, H. C. (1974). Relationship between obstctrical general anesthesia and rate of neonatal habituation to repeated stimulation. Dev. Med. Child Neurol., 16: 612-619. Moreau, T., Birch, H. G., and Turkewitz, G . (1970). Ease of habituation to repeated auditory and soinesthetic stimulation in the human newborn, J. Exp. Child Psychol., 9: 193-207. Piaget, J. (1952). The Origins of Intelligence in Children. New York: International Universities Press. Piaget, J. (1964). 7’he Construction of Reality in the Child. New York: Basic Books. Pick, H. L., and Pick, A. D. (1970). Sensory and perceptual development. In P. H. Mussen (Ed.), Carmichael’s Manual of Child Psychology, Vol. I. New York: Wiley. Pp. 773-830. Reese, H. W., and Lipsitt, L. P. (1970). Experimental Child Psychology. New York: Academic. Schneirla, T. C. (1965). Aspects of stimulation and organization in approach/withdrawal processes underlying vertebrate behavioral development. In D. L. Lehrman, R. Binde, and E. Shaw (Eds),Advances in the Study of Behavior. New York: Academic. Pp. 2-75. Werner, H. (1957). Comparative Psychology of Mental Development. New York: International Universities Press. Wohlwill, J. F. (1960). Developmental studies of perception. Psychol. Bull., 57: 249-288.
