Lateral Differences and HeadTurning Responses to Somesthetic Stimulation in Premature Human Infants DAVID LEWKOWICZ JUDITH GARDNER Biopsy chology Program Hunter College City University of New York New York. New York GERALD TURKEWITZ Department of Pediatrics Rose F. Kennedy Center Albert Einstein College o f Medicine Bronx, New York and Department o f Psychology Hunter College City University of New York New York, New York Head-turning responses t o somesthetic stimulation of the perioral region were studied at weekly intervals in 25 prematurely born infants. No regular changes associated with age were evident. The premature infants were more likely to turn towards than away from a stimulus; however, they were less so than are full-term infants. The infants were as likely to turn towards the stimulus when it was on the left as when it was on the right; however, they were more likely to turn away from a stimulus on the left than on the right. Comparisons with full-term infants indicated reduced lateral differences in responding. Such a reduction is in sharp contrast with the previous finding of marked postural asymmetry in a comparable sample of prematurely born infants. These data indicate a possible sequence in the development of head-turning responses to somesthetic stimulation and the assumption and maintenance of an asymmetrical head posture which consists of (1) a right-turning postural bias, (2) contralateral responding to somesthetic stimulation, (3) lateral differentiation of contralateral responding, (4) ispilateral responding, and (5) lateral differentiation of ipsilateral responding.

During the 1st week of life human infants are more responsive to auditory, visual, and tactile stimulation of their right than of their left sides (Turkewitz, 1977). Such Reprint requests should be sent to Gerald Turkewitz, Department of Pediatrics, Albert Einstein College of Medicine, Bronx, New York 10461, U S A . Received for publication 9 March 1978 Revised for publication 30 June 1978 Developmental Psychobiology, 12(6):607-614 (1979) 0 1 9 7 9 by John Wiley & Sons, Inc.

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lateral differences in responsiveness are related to asymmetries of input and muscle tonus associated with the infant’s asymmetrical head posture (Turkewitz, Moreau, Davis, & Birch, 1969). Elimination of this asymmetry by holding the infant’s head in a midline position for 15 min prior to stimulation reduces or eliminates the characteristic lateral differences in the infant’s eye-turning response to auditory stimulation (Turkewitz, Moreau, & Birch, 1966) and head-turning response to somesthetic stimulation of the perioral region (Turkewitz, Moreau, Birch, & Crystal, 1967). With this evidence that lateral differences are, in part, attributable to the infant’s head posture, we have suggested that a reciprocal relationship exists between posture and responsiveness with lateral differences in responsiveness strengthening the head-position bias (Turkewitz & Creighton, 1974). To examine the factors contributing to the marked postural asymmetry present as early as 12 hr after birth (Turkewitz & Creighton, 1974), Gardner, Lewkowicz, and Turkewitz (1977) examined the head positions of prematurely born infants and found a systematic increase in the consistency of the head position bias as a function of conceptional age. Given this finding, we now feel that premature infants represent a potentially useful group in which to examine either early phases of normal development or the effects of altered congenital or environmental conditions (intra- or extrauterine) on subsequent patterns of lateral differences in responsiveness. The present investigation is a step in such an examination and aims at determining the nature of the effects of prematurity on lateral differences in head-turning responses to somesthetic stimulation of the perioral region.

Methods The human infants for the study were residents in the Intensive Care Unit (ICU) of Jacobi Hospital of the Bronx Municipal Hospital Center. The group included 12 males and 13 females all classified as premature because they were born at or below 37 weeks estimated gestational age (EGA). (Gestational age of the infants was determined by the Dubowitz method [Dubowitz, Dubowitz, & Goldberg, 19701 based on the assessment of 10 neurological and 11 bodily characteristics.) The infants varied with regard to the basis for their prematurity and included 5 infants who were small for gestational age (SGA). Although our aim was to test each infant on a weekly basis from birth until 39 weeks, we were unable to achieve this objective for the following reasons: (1) the infant’s medical status changed during its stay on the unit; (2) infants were discharged from the unit at variable ages; and (3) infants who were connected to respirators, heart monitors, or any other form of apparatus were not tested. Consequently, the schedule of testing was quite irregular and different infants were tested at different ages and received different numbers of tests: 9 of the infants were tested once, 12 were tested twice, 2 were tested 3 times, and 2 were tested 4 times. (The number of infants born at each EGA, their mean birthweights, and the number of times they were tested are presented in Table 1.) As circumcision was performed only shortly before discharge none of the boys was tested following circumcision. Infants were tested while in the supine position in their own basinettes or isolettes. Because responsiveness differs with feeding condition (Prechtl, 1958;

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TABLE 1. Characteristics of the Infants Studied. EGA at birth (weeks)

28 31 32 33 34 3s 36 31

Number of Males Females 1 0

2 3 0 4 1 1

0 1 0 3 4 4 1 0

Mean birthweight (g)

Conceptional age of testing

1020 1250 1265 1587 1958 1745 2040 1910

34 35 36 37 38 39

No. of infants tested

3 7 12 12 9 4

Turkewitz, Gordon, & Birch, 1965), a l l infants were tested approximately 1% hr after feeding, generally during the late morning and early afternoon hours. An attempt was made t o test responsiveness in only those infants who were awake. To meet this objective we had t o waken some infants prior to the start of testing. Because we were not always successful, we noted the state of the infant, using a modification of the criteria set forth in the Prechtl scale (Prechtl, 1965), prior to each trial. These criteria are: State 1-eyes closed, no limb or body movements; State 2-eyes closed, some movement; State 3-eyes open, no movement; State 4-eyes open, movement; and State 5-eyes open or closed, movement, crying and/or flailing. Before and during each application of the stimulus, the infant’s head was positioned in the midline by holding it between a thumb and finger at the bitemporal regions. This was done to minimize differences in responsiveness due to the preceding head position. The stimulus was applied only after the head was balanced in the midline without any detectable tendency to turn in either direction at the time the head was released and the stimulus applied. Stimulus application consisted of touching the angle of the mouth for 1 sec. The response measure was the direction of the 1st lateral head movement within 1 sec following the application of the stimulus. We stimulated the 1st 14 infants with a standard round camel’s hair brush (Grumbacher No. 12). To examine the relationship between stimulus intensity and head turning we stimulated the remaining 11 infants with No. 1 and 6 brushes as well. Each stimulus used was applied 5 times to the right and 5 times to the left. In addition, 5 sham trials, which were identical to the stimulus presentations except that no contact between the brush and the infant was made, were interspersed in the test sequence. The same experimenter who administered the stimulus also judged the response. (Given the nature of the stimulation we had no practical way of preventing the experimenter from knowing the direction or character of the stimulus.) The order of stimulus presentation was random and each infant received the same sequence. The interstimulus interval was a minimum of 10 sec but sometimes exceeded this if additional time was required to balance the head in the midline.

Results Analysis of the data with regard to differences as a function of brush failed to reveal a clear pattern so the data from the different brushes were combined to yield a

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single score for each test. Inspection of the data from the SGA babies failed to indicate any differences between them and the rest of the infants so no such distinctions were considered in subsequent analyses. Although the data offered some suggestions of associations between conceptional age and responsiveness, we found no systematic age trends. Therefore, we combined the scores for all infants regardless of conceptional age for subsequent analyses. The scores of those infants who were tested at more than 1 age were combined to yield a single mean score for each infant. To determine whether the infants were responsive to the stimulus, we compared head-turning responses on stimulus trials with those on sham stimulus trials. Head turning occurred on 39.6% of the true trials and on only 18.3% of the sham trials. This difference was highly significant (t = 4.56, df= 24, p < .001; 1-tailed). (Different analyses included data from different numbers of infants because only those babies who made at least 1 response appropriate to a particular analysis were considered in that analysis.) As is the case for full-term infants, the characteristic response of the infants was a turn toward the stimulus: 61% of the responses were ipsilateral and 39% were contralateral. This difference approached but did not reach significance (t = 1.96, df= 23, p < .lo).

Lateral Differences in Response To determine whether the infants were similar to full-term infants in being more responsive to stimulation of the right than of the left, we compared the percentages of responses to the 2 loci of stimulation. Differences in responsiveness were not found as 48% of the infants’ responses were made to stimulation of the right and 52% to stirnulation of the left. This difference was not significant (p > .05). The only suggestion of any lateral differences in responsiveness was with regard to contralateral responses. When contralateral responses to left stimulation were compared with those to stimulation of the right, we found that 62% of the infants’ responses were to left stimulation and 38% were to right stimulation. This difference approached significance (t = 1.9 1, df = 19, p < .lo). Despite the limited evidence for relationships to conceptional age, differing amounts of intra- and extrauterine experience may still have an effect on responsiveness. To examine this possibility, we grouped the data according to the infant’s age at birth. The scores of the 9 infants born at 33 weeks and younger and those of the 15 born at 34-37 weeks were compared. Comparison of the older- and younger-born infants with regard to ipsilateral responsiveness indicated that the older-born infants made significantly more responses in the direction of the stimulus than the youngerborn (t = 2.94, df= 22, p < .Ol). However, no differences existed between older- and younger-born infants with regard to lateral differences in response to stimulation when ipsilateral and contralateral responses were considered separately or in combination.

Comparison with Full-Term Infants Prior investigations have indicated that full-term infants: (1) make head-turning responses to somesthetic stimulation of the perioral region (Prechtl, 1958; Turkewitz P t al., 1965); (2) make nearly all responses toward the stimulus (Prechtl, 1958; Turkewitr

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et al., 1965); (3) exhibit a marked lateral difference in their ipsilateral responding such that they make more ipsilateral turns to stimulation of the right than of the left (Turkewitz et al., 1965); and (4) make more contralateral responses to stimulation of the left than to stimulation of the right (Turkewitz et al., 1967; Turkewitz, Moreau, & Birch, 1968). The current data indicate that premature infants are similar to full-term infants in that they are responsive to somesthetic stimulation, tend to make more ipsilateral responses, and tend to make more contralateral responses to stimulation of the left than of the right. However, some of these patterns of response are relatively weak and inconsistent in the premature infants. In view of these apparent differences between full-term and premature infants, a direct comparison was made between the data obtained in the present study and those previously obtained from comparable testing of a group of 71 full-term infants (“high Apgar group” from Turkewitz et al., 1968). Infants who were 36 weeks and older gave the strongest indication of being more likely to make ipsilateral than contralateral responses; therefore all comparisons with the full-term infants were based on tests conducted when the premature infants were at these older ages. A comparison of the proportion of responses made toward the stimulus by these infants with that observed in full-term infants revealed that 93% of the full-term infants’ responses were towards the stimulus as compared to 63% of the prematures’. This difference was highly significant (t = 4.73, df= 92, p < .OOl). In addition, lateral differences in ipsilateral responding in premature infants were compared with those observed in the full-term infants. Because of marked differences in the responsiveness of the 2 groups of infants, we had to adjust the raw lateral difference score and compute an ipsilateral difference index, Ipsi R - Ipsi L I.D.I. = Ipsi R + Ipsi L t 1 ‘ To reduce the effect of those infants making few responses, we added 1 to the denominator and discarded the data from any infant making fewer than 4 ipsilateral responses. On this basis, the data from 5 premature and 3 full-term infants were discarded. The mean I.D.I. of the premature infants was -.02 whereas that of the full-term was .15, a difference which was significant (t = 2.12, df= 81, p < .05). In comparing the lateral differences in contralateral responses of the full-term and premature infants, we did not compute an index as both groups made roughly comparable numbers of contralateral responses; 71% of the away-turning responses of the full-tern and 65% of the away-turning responses of the premature were to stimulation of the left. This difference was not significant.

Gender Differences Because a number of developmental differences have been found between males and females, especially with regard to laterality (Witelson, 1976; Witelson & Pallie, 1973), responding in boys and girls was compared. The ages at which the males and females were tested were similar, the mean age at testing being 36.8 weeks for the girls and 36.4 for the boys. The ages at birth for the boys and girls were also similar with the mean age at birth being 33.8 weeks for the girls and 33.7 for the boys.

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The boys and girls were similar with regard to responsiveness to stimulation, head-turning on sham trials, and lateral differences in both ipsilateral and contralateral responses. They did differ, however, with regard to the differentiation of ipsilateral from contralateral responses, with the girls making a higher proportion of turns toward the stimulus than the boys: 75% of the head-turning responses of the girls were toward the stimulus whereas only 46% of the responses of the boys were similarly oriented, a significant difference (t = 2.67, df= 22, p < .02). This difference resulted from the females making significantly more ipsilateral than contralateral responses (t = 3.91, df= 12, p < .005) whereas the males were no more likely to turn toward than away from the stimulus. The preponderance of ipsilateral responding in the girls was primarily due to the contribution of the older-born girls who turned toward the stimulus on 85% of their responses. The younger-born girls turned towards the stimulus on 53% of their responses. This difference was significant (t = 2.65, df= 11, p < .05) as was the difference between older-born girls and older-born boys who turned toward the stimulus on 54% of their responses (t = 2.08, df = 13, p < .05).

Discussion The data indicate that premature infants are responsive to soinesthetic stimulation of the perioral region but that their responsiveness is relatively undifferentiated. Such infants are more likely to turn toward than away from the stimulus and turn away from stimulation of the left more frequently than from stimulation of the right. However, comparison with healthy full-term infants indicates reduced differentiation with regard to both the differences between towards- and away-turning and the lateral differences in responsiveness. This reduced differentiation is in contrast to the marked lateral difference in head posture observed in another sample of premature infants (Gardner etal., 1977). In view of previously obtained findings that the full-term infant’s asymmetrical head posture results in lateral differences in response to somesthetic stimulation of the perioral region (Turkewitz et al., 1969), the present data suggest a disturbance or a delay in the development of the mechanisms underlying this effect. However, the absence of any marked association between any of the measures examined and conceptional or postnatal ages may reflect the confounding effects of illness and duration of stay on the Intensive Care Unit, with better-functioning infants leaving the unit at earlier ages. The possibility also exists that features of life in the Intensive Care Unit, including the use of drugs and mechanical respiration as well as general environmental conditions, disrupt differential responding. Such disruption, whether by itself or in conjunction with the medical reasons for differential durations of stay on the Unit, might combine to obscure systematic relationships with conceptional or postnatal age. Despite the potential multiple determinants for the absence or reduction of differential responding, analysis of the pattern of reduction suggests a sequence for the development of lateral differentiation of head-turning. The presence of an atypical relationship between head posture and responsiveness, in conjunction with Hughling Jackson’s (1 884) dicta that neurologically earlier behaviors are less vulnerable and more likely to be reinstated following trauma than are developmentally later behavior patterns, suggests the possibility of identifying a developmental sequence with those features of head posture and turning which are

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developmentally later being more readily disturbed than others. Viewed in this light, the data of the current investigation, when taken in conjunction with prior studies, suggest an ordered pattern in the development of lateral differences. The asymmetrical head position appears to be both the earliest laterally differentiated behavior to appear and the most difficult to disrupt. Thus, by 35 weeks, infants exhibit a tendency to lie with their heads turned to the right, and this position bias increases with age whether development is occurring within or outside the uterus (Gardner efal., 1977). The assumption of an assymetrical posture is more vulnerable to disruption than is the maintenance of an asymmetrical posture. The assumption of the head-right posture exhibits a clear-cut developmental sequence with healthy full-term infants who are over 12-hr old turning to the right even following maintenance of the head in a midline position for 15 min. Full-term infants who are younger than this are as likely to turn left as right following such a procedure, although when their heads are restrained in the midline only momentarily, they consistently turn to the right following head release (Turkewitz & Creighton, 1974). Premature infants, even when they have reached the typical age for birth, exhibit a further disruption in that they do not show an excess of right turns following even a momentary maintenance of the head in a midline position (Gardner et d.,1977). With regard to head-turning in response to somesthetic stimulation, full-term infants predominantly turn toward a touch and only rarely (on less than 10% of the responses [Turkewitz et al., 19681 do they turn away. Although premature infants also tend to make more ipsilateral than contralateral turns, they do so to a much lesser extent than do the full-term infants. The relatively high level of contralateral responses by premature infants is consistent with findings that during the embryonic development of a number of vertebrate species, movements away from stimulation appear before those toward it (Cogh~ll, 1929; White, 1915). The same has been found specifically with regard to head-turning during human embryogenesis (Humphrey, 1969). The developmentally earlier status of away-turning is probably further reflected in the finding that at 2 days of age babies born at term but in poor physiologic condition are more likely to turn away from the stimulus than are full-term infants who were in good condition at birth (Turkewitz etal., 1968). The fact that away-turning develops earlier, and therefore is likely to become differentiated earlier, also helps to account for the finding that prematurely born infants exhibit a lateral difference with regard to this behavior but n o clear lateral difference in towardsturning. This line of reasoning suggests further refinements in the sequence of development of head-turning responses. Thus, the finding that older-born premature infants show a greater differentiation of towards- from away-turning than do younger born infants and no increased lateral difference in away-turning responses suggests that lateral differences in away-turning become established before towards-turning becomes the dominant mode of functioning. The fact that the increased differentiation of towards- from away-turning differs between males and females, with only older-born girls exhibiting a clear preponderance of toward-turning, is consistent with the widespread view that girls are precocial in their development when compared with boys. It is also consistent with the general finding of greater vulnerability to stress in boys than in girls. Despite the consistency with which the data fit an interpretation in terms of a retrograde dissolution of functioning, the postulated sequence of development is to a

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large extent post hoc and therefore requires independent verification. In addition, this interpretation clearly suggests that more severe sequelae should attach to certain manifestations of disturbance than to others. Thus, we would expect that infants with disturbances of lateral differences in away-turning would be at considerably greater risk for subsequent dysfunction than would infants who were atypical with regard to lateral differences in towards-turning responses. Such differential outcomes remain to be examined.

Notes This investigation was supported in part by the National Institute of Child Health and Human Development of the National Institutes of Health (HD 01799). We thank Dr. Lawrence Gartner, Director of Neonatology, Anita Garcia, Jean Gonzalez, and the medical and nursery staff of the Neonatal Intensive Care Unit of the Bronx Municipal Hospital Center for their cooperation. We also thank Louisa Katz for her able assistance in the data collection.

References Coghill, G. E. (1929). A n a f o m y and the Problem of Behavior. New York: Macmillan. Dubowitz, L. M. S., Dubowitz, V., and Goldberg, C. (1970). Clinical assessment of gestational age in the newborn infant. J. Pediatr., 77:l-10. Gardner, J., Lewkowicz, D., and Turkewitz, G. (1977). Development of postural asymmetry in premature human infants, Dev. Pychobiol., I0:471480. Humphrey, T. (1969). Postnatal repetition of human prenatal activity sequences with some suggestions for their neuroanatomical basis. In R. J. Robinson (ed.), Brain and EarZy Behavior. New York: Academic Press. Pp. 43-71. Jackson, H. (1884). Evolution and dissolution of the nervous system. Lancet, 1:408412. Prechtl, H. F. R. (1958). The directed head turning response and allied movements of the human baby. Behaviour, 13:212-242. Prechtl, H. F. R. (1965). Problems of behavior studies in the newborn infant. In D. S. Lehrman, R. A. Hinde, & E. Shaw (eds.), Advances in the Study of Behavior. Volume 1 , New York: Academic Press. Pp. 75-98. Turkewitz, G. (1977). The development of lateral differentiation in the human infant. Ann. N.Y. Acad. Sci., 299:309-318. Turkewitz, G., and Creighton, S. (1974). Changes in lateral differentiation of head posture in the human neonate. Dev. Psychobiol., 8:85-89. Turkewitz, G., Gordon, E. W., and Birch, H. G. (1965). Head turning in the human neonate: Effect of prandial condition and lateral preference. J. Cornp. Physiol. Psychol., 59: 189-1!32. Turkewitz, G., Moreau, T., and Birch, H. G. (1966). Head position and receptor organization in the human neonate. J. Exp. Child Psychol., 4:169-177. Turkewitz, G., Moreau, T., and Birch, H. G. (1968). Relation between birth condition and neurobehavioral organization in the neonate. Pediatr. Res., 2:243-249. Turkewitz, G., Moreau, T., Birch, H. G., and Crystal, D. (1967). Relationship between prior head position and lateral differences in responsiveness to somesthetic stimulation in the human neonate. J. Exp. Child Psychol., 5:548-561. Turkewitz, G., Moreau, T., Davis, L. A., and Birch, H. G. (1969). Factors affecting lateral differentiation in the human newborn. J. Exp. Child Psychol., 8:483493. White, G.M. (1915). The behavior of brook trout embryos from the time of hatching to the absorption of the yolk sac. J. Anim. Behav., 5:44-60. Witelson, S. F. (1976). Sex and the single hemisphere: Specialization of the right hemisphere for spatial processing. Science, 193:425427. Witelson, S. F., and Pallie, W. (1973). Left hemisphere specialization for language in the newborn: Neuroanatomical evidence of asymmetry. Brain, 96:641-647.

Lateral differences and head-turning responses to somesthetic stimulation in premature human infants.

Lateral Differences and HeadTurning Responses to Somesthetic Stimulation in Premature Human Infants DAVID LEWKOWICZ JUDITH GARDNER Biopsy chology Prog...
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