Developmental Psychology 1996, Vol. 32, No.

6, 1090-1099

Copyright 1996 by the American Psychological Association, Inc. 0012-1649/96/S3.00

Sweet Taste, Looking, and Calm in 2- and 4-Week-Old Infants: The Eyes Have It
Debra Zeifman, Sarah Delaney, and Elliott M. Blass
Cornell University
This study investigated the effectiveness of orally delivered sucrose in calming agitated 2- and 4week-old infants. Sucrose arrested crying and reduced heart rate and gross activity in 2-week-olds but was ineffective in calming 4-week-olds unless accompanied by eye contact. These results were confirmed in a second study in which the experimenter deliberately either held or avoided the infants' gaze. For infants who received sucrose in the absence of eye contact, or water along with eye contact, crying was only modestly reduced, and this effect was not sustained. The emergent necessity of conjoint visual and gustatory stimulation at 4 weeks of age may mark a transition from calming by nonsocial proximate stimulation, such as sweet taste, to calming by specific, distal social interactions. Implications of thefindingsfor the formation of infant-caregiver affectional ties are discussed.

Recent studies on the ability of different substances to calm newborn humans and rats and to protect them against pain have revealed the following: (a) Microliter volumes of milk, fat (corn oil), and the sugars sucrose, glucose, and fructose (but not lactose, the milk sugar) arrest crying in infant rats (Blass & Fitzgerald, 1988; Blass, Fitzgerald, & Kehoe, 1987; Blass & Shide, 1993; Shide & Blass, 1991) and human newborns (Barr et al., 1994; Blass & Ciaramitaro, 1994; Blass, Fillion, Rochat, Hoffmeyer, & Metzger, 1989; Blass & Shah, 1995; Blass & Smith, 1992; Smith, Fillion, & Blass, 1990); (b) quieting lasts for minutes beyond the last administration of an effective fluid (Blass & Ciaramitaro, 1994; Shide & Blass, 1991; Smith et al., 1990); (c) for sugars, quieting appears to be mediated by gustatory factors, because calm is achieved with very small volumes (as little as 250 fd; Barr et al., 1994) well before possible postabsorptive factors can come into play. Moreover, the nonnutritive sweetener aspartame also quiets (Barr, Pantel, Wright,

Debra Zeifman, Department of Human Development and Family Studies, Cornell University; Sarah Delaney and Elliott M. Blass, Department of Psychology, Cornell University. Experiment 1 is based on a master of arts thesis by Debra Zeifman. Thanks are extended to Cindy Hazan, chair of the masters committee, and the other members, Daryl Bern and Henry Ricciuti. Experiment 2 was conducted by Sarah Delaney in fulfillment of the requirement for a bachelor of arts degree with Honors. This research was supported by a grant from the New York State College of Human Ecology, Cornell University, and by National Institute of Mental Health Grant MH 51705 and Research Scientist Award MH00524. We thank Kathleen Henry for valuable assistance, Richard Darlington and Ed Frongillo for statistical consultation, and Todd Alan Sauers for his assistance with statistical analyses. We also thank Nathan Fox for his helpful feedback on earlier versions of this article. Correspondence concerning this article should be addressed to Debra Zeifman, who is now at the Psychology Department, Vassar College, Box 44, Poughkeepsie, New York 12601, or to Elliott M. Blass, who is now at the Department of Psychology, Tobin Hall, University of Massachusetts, Amherst, Massachusetts 01003. Electronic mail may be sent to Debra Zeifman via Internet to dezeifman@vassar.edu.

Gravel, & Young, 1995); and (d) sweet taste causes the release of endogenous opioids: quieting can be blocked in rats by pretreatment with opioid antagonists such as naloxone or naltrexone that prevent endogenous opioids from reaching their receptors (Blass & Fitzgerald, 1988; Shide & Blass, 1989). Furthermore, human newborns, whose endogenous opioids were depleted because their mothers were maintained on methadone during pregnancy, were not quieted by sucrose (Blass & Ciaramitaro, 1994). Sucrose taste induces other major changes in newborns as well. Heart rate (HR) is markedly lowered (Blass & Ciaramitaro, 1994), activity is reduced (Blass & Ciaramitaro, 1994), the infant brings its hand(s) to its mouth (Blass et al., 1989; Rochat, Blass, & Hoffmeyer, 1988), pain threshold is elevated (Blass & Hoffmeyer, 1991; Blass & Shah, 1995), and metabolic rate is lowered (by 10%) in crying infants (Rao, Blass, Brignol, Marino, & Glass, 1993). Taken together, this orchestrated complex of behavioral, physiological, and metabolic changes suggests that the taste of certain sugars and, perhaps under normal circumstances, milk flavor, release central endogenous opioids to mobilize effector systems that induce energy conservation. This complements, of course, the well-known energy repletion function of milk ingestion. A similar profile of energy-conserving changes is induced by sucking a pacifier. These changes differ from ones induced by gustatory afferents, however. They do not persist beyond pacifier removal (Blass & Ciaramitaro, 1994; Smith et al., 1990) and are not opioid mediated (Blass, Fillion, Weller, & Brunson, 1990; Blass, Shide, Zaw-Mon, & Sorrentino, 1995; Blass & Ciaramitaro, 1994). The above represent first steps toward understanding how mothers may influence their newborns' behavior and physiology and how these induced changes may allow infants to learn about the features of their own mothers (Blass, Ganchrow, & Steiner, 1984; Bushnell, Sai, & Mullin, 1983; Pascalis, de Schonen, Morton, Deruelle, & Fabre-Grenet, 1995). It builds on the pioneering work of Lipsitt and others demonstrating that infants could discriminate among sugars and preferred the taste of

1090

SWEET TASTE

1091

sweeter solutions (Ashmead, Reilly, & Lipsitt, 1980; Crook & Lipsitt, 1976; Desor, Mailer, & Turner, 1973; Engen, Lipsitt, & Peck, 1974). The present studies were undertaken to determine whether there are developmental changes in the ability of sucrose to affect infant physiology and behavior. Given that a constant stimulus, sucrose, was delivered under constant experimental circumstances, any differences in the infants' reactions to this stimulus had to reflect maturational or experiential changes in the infants themselves. Because development is so accelerated during the initial postnatal month, we have confined the present analysis to 2- and 4week-olds. We now report that sucrose continued to quiet infants of these ages and reduced heart rate as well. There were two noteworthy developmental changes, however. First, whereas as little as 0.1 ml sucrose calmed crying newborns, a minimum of 0.5 ml had to be tasted each time by the 2-week-old infant to achieve calm and bradycardia; 4-week-old infants required at least a 1.0 ml volume. Second, in order for sucrose to markedly calm 4-week-old infants, it had to be delivered while the infant was visually engaged by the person delivering the solution.

General Method Participants

A total of 63 infants were studied in their homes at either 2 or 4 weeks of age. The infants were drawn from a larger population of normal healthy newborns who were delivered at the Tompkins Community Hospital in Ithaca, New York. Infants were recruited for the study as follows: Mothers were originally contacted during their hospital stay and allowed us to evaluate their and their infant's current medical records and to contact them at a future date for participation in the home study. The purpose and the nature of the study were explained to the mothers who then read and signed the permission letter. It was made explicit to them that participation in the study was not obligatory and that participation, or lack of same, did not in any way affect their or their infants' hospital care. The experiments were approved by the Cornell University Board of Human Subjects Research and the Tompkins Community Hospital Institutional Review Board. All infants who participated in the study met the following criteria: (a) unremarkable prepartum history, labor, and delivery; (b) 5-min Apgar(Apgar, 1953) scores of 9 or 10; (c)gestational age of between 38 and 42 weeks; (d) birth weight of between 3,000 and 4,000 g; (e) no chronic or infectious diseases during pregnancy or after birth; and (e) good health at the time of study, according to parental report.

riods of time (5-10 min in the present studies). The measure does not provide information concerning underlying mechanisms; more sensitive measures and different experimental paradigms are required. The experimenter was stationed on one side of the crib (or sofa), and a mirror was placed on the other side in a position that allowed the video camera to simultaneously capture both infant and experimenter faces. This arrangement was used at first to ensure that the experimenter maintained a neutral, normal facial expression that was not masklike. As is stated below, this also allowed us to evaluate whether and when eye contact occurred between the infant and experimenter. Solutions. Solutions were mixed on the day of the experiment by a research assistant and placed in 5-cc sterile plastic syringes. The experimenter was never aware of syringe content. One of twofluidswas delivered to each infant: sterile water or a 12% wt/vol solution of sucrose. This was prepared by adding sterile water to 12 gm of sucrose until 100 cc of solution was achieved. Infants were assigned randomly to a treatment condition. Data collection. The experiment proper began after the infant cried for 40 s or more for 1 min, or for 24 s or more for each of 2 successive minutes. These criteria provided a stable baseline against which the effects of treatment could be evaluated. This level of crying was almost always achieved within 10 min. Once criterion had been reached, the infant received four tastes, one per minute, of either sucrose or water in volumes that are specified below. Delivery time was 30 s and was monitored through a hand-held stopwatch. A maximum of 4 min were allowed to elapse after the last delivery before the experiment was terminated. If vigorous crying ensued or if the mother so desired, the experiment was terminated at any time.

Measures
Four measures were used in Experiment 1 to capture changes in infant state and interactions with the experimenter. The measures were crying, HR, activity, and hand-mouth coordination. Two additional measures, visual engagement and gaze, were scored post hoc because of our impression that they were relevant to the observed phenomenon. With the exception of HR and activity, all behaviors were scored on a continuous basis and are reported in seconds per minute. Behaviors were scored from the videotape by Cornell undergraduates who were extensively trained in the scoring procedures and who were uninformed as to syringe content. In order to further guard against scoring bias through familiarity with the infants' reactions to the test substance, a scorer evaluated only two measures for a particular infant. The measures for every fourth baby were scored independently by two observers. Interobserver reliability for all dependent measures was .95 or greater according to Pearson's product-moment correlations. Crying was scored when the infant emitted a cry sound with a cry face. We did not distinguish among the different types of cries that infants made because sucrose was an effective calming agent, regardless of crying intensity. We also determined the latency to resume crying during the poststimutation period from inspection of the crying records. The latency was defined as the time that had elapsed until the start of the first crying bout of 15 sec or greater. HR was determined once per 10 s from the audio portion of the tape with the video portion blacked out. Hand-to-mouth behavior was scored when any portion of the hand made contact with the mouth or with the perioral zone as demarcated by an imaginary mustache that extended downward to the jaw. Activity was scored every 10 s on a 6-point scale (0-5). A 0 was given when the infant lay still, except for brief twitches, during a 10-s interval. One point was awarded for each of the following limb movements, if they occurred for 1 s or more during a 10-s interval: head, left arm, right arm, torso, and either or both legs. Each movement could be scored only once per interval regardless of how frequently it occurred during the interval. Visual engagement was determined by inspection from the

Procedure
Studies were conducted in the infants' home between 2 p.m. and 4 p.m., generally after they had awakened from their afternoon nap and were likely to cry. The infants were placed supine in their cribs OF on a soft couch (if the child's room did not allow filming), and their heads were elevated using either a firm pillow or a rolled-up blanket. To provide additional support, blankets were also placed on either side of the infant, in such a way that permitted unrestrained limb movement. HR was recorded through electrodes that were embedded in a Velcro belt that was gently secured about the infant's chest. The infant was immediately dressed to maintain warmth. For purposes of data collection, HR was called off of the monitor (Air-Shield Vickers Systems; Model V, Burnsville, MN) by the research assistant once every 10 s for the duration of the study. The HR value was that of the moment and not an average for a time interval. This means of obtaining HR data is suitable for capturing large, systematic changes over relatively long pe-

1092

ZEIFMAN, DELANEY, AND BLASS

mirror in which the line of regard of the infants and experimenter was assessed. The infant was considered visually engaged when the infant's eyes were directed toward the face of the experimenter. Gaze was indicated when the infant had its eyes opened and was not looking at the experimenter.

Method
Participants. A total of twenty 2-week-old and sixteen 4-week-old infants participated in this study. Nine of the 20 younger infants were boys. Infants in the younger group averaged 3,644 g at the time of testing. Eight of these infants were bottle-fed; 11 were breast-fed and I was combination-fed. The 4-week-old infants included 6 boys and 10 girls, with a mean weight of 4,170 g at testing. Three infants were fed by bottle, 7 by breast, and 6 by the combination. The small number of bottle-fed infants and their distribution in the different groups precluded statistical evaluation of breast- versus bottle-feeding. Informal evaluation of the data did not reveal any apparent differences between feeding styles. Procedure. The procedures described in the General Method section were used.

Statistical Evaluation
A multivariate analysis of variance (MANOVA) was used to test the composite hypothesis that the independent variable condition (sucrose vs. water) did not affect any of the dependent variables. Independent, one-tailed / tests then evaluated statistical reliability between sucrose and water for 9 dependent variables (cry, HR, activity, and hand-mouth interactions during treatment and posttreatment phases of the study and the latency with which crying was reinitiated). The one-tailed t tests were justified by the expectations of directionality from our previous studies on newborns (Blass & Ciaramitaro, 1994; Smith et al., 1990). A two-factor (Solution X Age) analysis of variance (ANOVA) was used to compare the crying and cardiac responses to sucrose of 2- and 4week-olds.

Results and Discussion

Two-week-old infants. Sucrose (12% wt/vol), when delivered in a volume of 0.5 ml, continued to exert a profound effect on infant behavior and HR. (In pilot studies onfive2-week-old infants, 0.1 ml aliquots of sucrose, did not affect either infant behavior or physiology in any of our measures.) As shown in Figure 1, the incidence of crying was reduced by over 50% during the first minute of treatment, fell essentially to zero during the rest of the treatment phase, and showed a modest rebound during the posttreatment period. The differences were confirmed statistically. The MANOV\ assessment of the main effect of solution (sucrose vs. water) on the dependent

Experiment 1
The purpose of Experiment 1 was to determine whether there was a developmental change regarding sucrose's ability to quiet crying infants, reduce their HR and activity, and induce handto-mouth contact. Accordingly, infants were studied at 2 and 4 weeks of age as described above.

Time (in minutes) Figure 1. Mean (SE) time spent crying by 2-week-old infants before, during, and after receiving water (filled columns) or 12% sucrose solution (0.5 ml/min). B = baseline; P = posttreatment.

SWEET TASTE

1093

variables (crying, HR, activity, and hand-mouth contact) during treatment and posttreatment phases of the study, and latency to resume crying, yielded a significant Wilks's X F statistic, F( 9, 10) = 15.34, p < 0.001. Infants receiving sucrose cried an average of 6.55 s/min (SD = 6.11) during treatment and 14.02 s /min (SD = 19.15) following treatment, compared with 32.95 s/min (SD = 22.89) and 41.48 s/min (SD = 17.66) for those receiving water. One-tailed t tests revealed that differences between the treatment conditions in crying were statistically significant both during, t( 18) = 3.44, p < .01, and following treatment, t( 18) = 3.24, p < .01. In fact, seven of the eight infants who received sucrose simply did not cry during the 4 min that followed sucrose administration. This was also reflected in a significant difference in latency to resume crying (188.5 s vs. 41.0 s for sucrose and water infants, respectively), t( 18) = 3.62, p<.01. Sucrose also markedly reduced HR. In particular, HR dropped 17 beats per minute (BPM) during sucrose treatment and this decline extended into the posttreatment phase when there was a further 11 BPM reduction. Infants in the sucrose condition averaged 165.18 BPM (SD = 8.54) during and 152.69 BPM (SD = 12.41) following treatment, compared with 196.58 BPM (SD = 14.99) during and 189.94 BPM (SD = 25.84) following treatment for those in the water condition. Both treatment and posttreatment differences between water and sucrose were statistically significant; rs(18) = 5.99 and t( 18) = 4.34, respectively; ps < .01 for both t values. It is not likely that the decline in HR can be attributed exclusively to crying reduction because crying stopped within the first 2 min of treatment, whereas HR continued to decline even after sucrose administration terminated. Sucrose only modestly affected activity levels relative to water treatment. The mean activity score on a 6-point scale was 1.48 (SD = .72) for the sucrose condition, compared with 2.07 (SD = .43) for water, t( 18) = 2.11, p < .03. An even smaller effect of sucrose during the posttreatment period was not statistically significant, and sucrose did not induce infants to bring their hands to their mouths (t = 0.36, p > .3). This failure suggests that hand-mouth integration becomes more intrinsically organized during the first 2 postnatal weeks and disassociated from stress and motivational states as defined by crying and cardiac rate. Specifically, central changes that accrue from tasting sucrose wane in their influence over hand-mouth integration even though sucrose reduced crying and HR. In short, the reactions of 2-week-old infants to sucrose taste were essentially like those observed in newborns in our earlier studies. Most significantly, sucrose continued to markedly diminish crying and HR. A larger volume of sucrose was necessary to instantiate these changes than in the newborn, however, indicating a quantitative difference. It may be necessary to stimulate a certain proportion of the functional gustatory neurology in order to induce the affective and cardiac changes under study. The 0.1 ml aliquot of 12% sucrose used in our previous studies of newborns may not have been either sufficiently large or sweet to quiet 2-week-old infants. Four-week-old infants. Behavioral and cardiac adjustments of 4-week-old infants differed markedly from those of 2-weekolds. Indeed, according to MANOVA, there was no main effect of solution (sucrose vs. water) on any of the dependent variables

(crying, HR, activity, and hand-mouth contact) during treatment and posttreatment phases of the study, Wilks's X F(9, 4) = 2.561, p= .19. One-tailed/tests of each dependent variable revealed that, of the dependent variables, only crying during treatment, t( 14) = 2.17, p < .02, and posttreatment, /(14) = 2J6,p< .01, as well as latency to resume crying, t( 14) = 3.62, p < .01, were significantly different for sucrose and water conditions. Infants receiving sucrose cried an average of 17.43 s/min during treatment and 25.54 s/min following treatment compared with infants receiving water who cried an average of 36.92 s/min during treatment and 53.34 s/min following treatment. The latency to resume crying was 109.59 s for infants in the sucrose condition, compared with 8.45 s for those in the water condition. Relative to newborn and 2-week-old infants, sucrose did not substantially reduce crying either in the first minute or thereafter, even in a volume of 1.0 ml/min (Figure 2). Four-week-old reactions were considerably more variable, and the rebound was substantially greater after sucrose termination. In fact, only one of the eight infants remained calm for the entire poststimulation period and three infants had to be removed from the study at the end of the first minute following sucrose termination because of excessive crying. The latter infants were extremely informative because they were 3 of the 5 infants in the sucrose group who did not establish visual contact with the experimenter. Sucrose did not affect either activity levels or hand-inmouth behavior, and HR was not reduced during sucrose treatment or during the posttreatment interval. The following comparison between the behavior of 2- and 4week-old infants during the poststimulation period who were either visually engaged (i.e., maintained visual contact for at least 15 s/min) or not engaged during sucrose administration suggested that at 4 weeks of age, sucrose might be effective only when paired with visual engagement. During the postsucrose phase, the engaged 2-week-old infants (n = 5) cried for a mean of 11.5 s/min, whereas the nonengaged infants (n = 7) cried for 15.8 s/min. In contrast, the 5 nonengaged 4-week-olds cried for a mean of 38.7 s/min during the postsucrose phase, whereas the 3 engaged infants cried for a mean of 3.6 s. To evaluate whether the apparent transition between 2 and 4 weeks of age in crying and cardiac responses to sucrose taste was statistically reliable, the crying and HR data sets were subjected to an ANOVA with age and solution as factors. For HR, the effect of solution, F( 1, 37) = 16.30, p < .0001, and the interaction between solution and age, F( 1, 37) = 6.92, p < .01, were statistically significant. The difference between sucrose effects at 2 and 4 weeks of age were also statistically significant, F( 1, 37) = 7.16, p < .01. Crying outcomes were significant as well, with a main effect of solution, F( 1,41) = 24.89, p < .0001. For age, F( 1,41) = 3.08 approached conventional levels of statistical reliability (p < .08). We are impressed by this outcome because three of the eight infants were under the stimulus control of both visual and gustatory afferents and were the only three infants for whom the treatment was extremely effective. Thus, despite the larger volume of sucrose, 4-week-old infants reacted differently than the younger infants. On the bases of thefindingsof Experiment 2, we claim that the differences are qualitative. In short, Experiment 1 has revealed developmental changes

1094

ZEIFMAN, DELANEY, AND BLASS

Time (in minutes) Figure 2. Mean time (SE) spent crying by 4-week-old infants before, (luring, and after receiving water (filled columns) or 12% sucrose solution (1.0 ml/min). B = baseline; P = posttreatment.

in both 2- and 4-week-old infants. Quantitatively, larger volumes of sucrose were necessary to induce calm and lower HR in 2-week-old infants. The qualitative change in 2-week-olds was related to hand-mouth coordination; in 4-week-old infants, sucrose alone, in a volume of 1.0 ml/min, did not exert the calming effect that it had in newborns or even in 2-week-old infants. This indicates a fundamental reorganization in motivational systems between 2 and 4 weeks of age such that the putative neurochemical changes caused by sweet taste are themselves no longer able to gain control over infant crying and (possibly secondarily) HR. Videotape evaluation suggested that sucrose effectively calmed older infants, when delivered during infant-experimenter eye contact. Experiment 2 evaluated this proposition. Experiment 2 The marked contrast between 4-week-old infants who were visually engaged by the experimenter during sucrose delivery and those who were not demanded experimental verification. Accordingly, in the present study, an infant was randomly designated to receive (a) water, or (b) sucrose while the experimenter attempted to maintain visual contact with the infant, or (c) sucrose while the experimenter deliberately avoided eye contact by focusing her gaze on the infant's forehead. The success or failure of a particular maneuver was determined by evaluating eye contact during sucrose administration.

Method
Participants. A total of 27 infants participated in this study. They were randomly assigned to engaged-water, engaged-sucrose, or non-engaged-sucrose groups. During the course of data collection, however, three infants who were assigned to the engaged-sucrose group were subsequently removed from the sample because their eyes remained closed during the period of sucrose administration (i.e., they were not visually engaged). These infants therefore were excluded during the test; their participation terminated after the first minute of sucrose delivery. The next infant, therefore, was assigned to the engaged-sucrose condition. Group characteristics did not differ. Five of the eight engaged-water andfiveof the eight engaged-sucrose infants were boys as were four of the non-engaged-sucrose infants. The three unsuccessful infants were girls. Body weights at the time of testing averaged 4,496, 4,284, 4,320, and 4,431 g, respectively for the four groups. Twenty-six of the 27 infants were breast-fed; the exception was an infant in the non-engaged-sucrose group who was both breast- and bottle-fed. A mean of 1.6 hr had elapsed since the time of last feeding. Procedures. The procedures described above for the 4-week-old infants were followed in exact detail in the present study except that every effort was made to either hold or avoid the infant's gaze during the delivery period or thereafter. Visual contact was avoided by focusing on the infant's forehead during the test period. The dependent measures were the same as in Experiment 1 with the exception of visual engagement, which was an assigned variable in Experiment 2. An additional measure scored from the videotapes, directed looking, was coded when the infant's eyes were directed toward the eye region of the experimenter's face.

SWEET TASTE
60 i sucrose engaged water engaged
nonengaged sucrose

1095

TREATMENT

Time (in minutes)

Figure 3. Mean time (SE) spent crying by 4-week-old infants who were either visually engaged (open columns) by the experimenter or who were prevented from establishing eye contact (filled columns) with her. The data from the 3 infants who did not have their eyes open during sucrose treatment (unsuccessful) are included. B = baseline; P = posttreatment.

Results and Discussion

Figure 3 illustrates how sucrose or water affected crying in water-engaged, sucrose-engaged, and non-engaged-sucrose infants. The overall MANOVA test of the main effect of the three treatment conditions on any of 15 dependent variables (crying, HR, and directed looking at each of the 5 min of the experiment for which there was complete data) yielded a statistically significant result, F(2, 18) = 9.981,p < .001. The mean percentage of crying during treatment was 6.10% (SD = 7.01) for the sucrose-engaged condition, 39.3% (SD = 13.7) for the non-sucrose-engaged condition, and 51.5% (SD = 25.1) for the waterengaged condition. Two sample t tests demonstrated that crying during the pretreatment phase did not differ among groups but that differences during treatment between sucrose-engaged and nonengaged-sucrose groups and between water-engaged and sucrose-engaged groups were statistically significant, t(S) = -14.64, p < .0001 and f(8) = -4.94, p < .001 for sucroseengaged versus nonengaged-sucrose infants and water-engaged versus sucrose-engaged infants, respectively). No comparisons were undertaken for the posttreatment phase because the crying of water-engaged and non-engaged-sucrose infants was so vigorous that, out of consideration for both infant and mother, the experiment was terminated during the first posttreatment minute for six of the eight water-engaged and seven of the eight nonengaged infants. All of these infants had returned to baseline levels of crying. All 8 of the engaged-sucrose infants successfully completed the experiment with virtually no crying at all.

Thus, tasting 1 ml of sucrose per minute for each of 4 min eliminated crying in 4-week-old infants provided that they were visually engaged at the time of sucrose delivery. Calming through visual engagement during sucrose delivery is particularly impressive because this was the first meeting between infants and experimenter and her physical appearance often differed considerably from that of the mothers. Sucrose alone reduced crying by about 40%, far less than in newboms or 2week-olds. Moreover, visually engaging infants during water treatment was no more effective than delivering water alone. Water engagement only modestly reduced crying during the initial minute, the time of marked diminution in crying of sucroseengaged infants. Sucrose delivered during visual engagement also affected HR (see Figure 4). The mean HR for sucrose-engaged infants was 166.41 BPM (SD = 8.46) compared with 181.06 BPM (SD = 7.72) for the non-engaged-sucrose group and 184.04 (SD = 7.68) for the water-engaged group. Because of unanticipated differences in baseline HR between treatment groups, baseline HR was entered as a covariate in the MANOVA test of the effect of treatment group on HR (with HR for Minutes 2-5 of the experiment as dependent variables). Even controlling for baseline HR, differences among treatment groups were statistically significant, F(4, 14) = 6.279, p < .01. It is also clear that the suppressed HR cannot be attributed to visual engagement per se because HR in the water-engaged group remained elevated at 181-189 BPMs. The amount of time that infants spent in both directed (at

1096
200 -i
3

ZEIFMAN, DELANEY, AND BLASS

sucrose engaged water engaged nonengaged sucrose

190-

u
QJ XJ

180-

0)

17

160-

150

TREATMENT

Time (in minutes)

Figure 4. Mean heart rate (SE) of infants presented in Figure 3. Heart rate remained at reduced levels in the engaged infants after sucrose termination. B = baseline; P = posttreatment.

the eye region of the experimenter's face) and nondirected looking did not differ significantly according to treatment condition, although scores for the nonengaged condition were consistently lower than for both engaged conditions (see Figure 5). In all three groups, directed looking never dipped below 26 s/min or 43% of the time. Such high levels of directed looking in each of the three treatment groups suggest that infants remain highly motivated to seek out eye contact in spite of the experimenter's failure to reciprocate (in the nonengaged condition), and their own continued distress (in both the water-engaged and nonengaged-sucrose conditions). Thesefindingshave three noteworthy aspects. First, sucrose did gain control over the nonengaged infants' behavior as it reoriented their gaze to the experimenter's face despite the infants' continued crying. Second, the search was directed toward establishing visual contact and it was sustained without diminution for the entire stimulation period. The purposiveness of this search was compelling. It seemed as if the infants were deliberately seeking contact with the experimenter's eyes. We find it unlikely that the nonengaged infants were crying because they could not establish contact. Recall that they started treatment in a crying state and that the crying levels decreased during treatment by about 40%. Moreover, their search behavior did not diminish substantially during the treatment period, suggesting that this behavior pattern was not subject to extinction, at least in the time frame of this study. Third, eye opening, relative to newborns, was independent of state. Four-week-old infants generally had their eyes open during crying and, unlike newborns, they did not have to become calm in order for their eyes to open.

In short, we have demonstrated a qualitative transition in motivational complexity of human infants between Postnatal Weeks 2 and 4 as it relates to the ability of sucrose to calm. Infants can be quieted by sucrose and their HR normalized, but only if the sucrose is delivered when the infant and the person delivering the solution are looking at each other. Neither sweet taste alone, nor visual engagement alone, suffice to cause the changes in either crying or HR reported here. General Discussion The present studies have identified changes in how sucrose calms agitated human infants during thefirstpostnatal month. Our behavioral and physiological referent was the newborn, for whom even 0.1 or 0.2 ml tastes of sucrose mobilized central mechanisms of calming, pain relief, and energy conservation (Blass & Ciaramitaro, 1994; Blass & Hoffmeyer, 1991; Smith et al., 1990). The earliest change in sucrose control was quantitative: 2-week-olds quieted when ingesting 12% sucrose in a volume of 0.5 ml per taste. The qualitative change of not bringing the hand to the mouth during or following sucrose stimulation suggests that feeding systems, which incorporate hand-mouth integration, have started to differentiate from other motivational systems. The similarities between newborns and 2-week-old infants, however, are more impressive than the differences. For both, sucrose (in 0.5 ml aliquots) essentially eliminated crying, which did not return to baseline levels during the 3-min posttreatment period. HR was normalized and remained so after sucrose termination. Activity was modestly reduced. Thus, 2-week-olds'

SWEET TASTE

1097

sucrose engaged water engaged nonengaged sucrose

10

Time (in minutes)

Figure 5. Mean (SE) amount of directed looking per minute of infants that were visually engaged or nonengaged during sucrose delivery. Infants in the nonengaged group attempted to establish visual contact with the experimenter almost 50% of the time during sucrose delivery. B = baseline; P = posttreatment.

behavioral and physiological adjustments were influenced exclusively by proximate sweet stimulation. Distal-visual stimulation did not influence crying, either during or following sucrose administration. Other forms of oral stimulation (e.g., pacifiers), quiet infants of this age. By one month, on the other hand, profound changes have occurred in the organization of affect and in cardiac control. In the absence of visual contact, sucrose reduced crying by only 40% and crying achieved baseline levels during the poststimulation period. In fact, it reached a level of intensity that warranted terminating the study in 7 of the 8 infants who had each received a total of 4 ml of 12% sucrose. Sucrose fully arrested crying at 4 weeks of age, however, but only in infants visually engaged by the experimenter. This was the rule in Experiment 1, in which visual engagement was not attempted experimentally, and in Experiment 2, in which it was explicitly manipulated. The changes cannot be attributed to eye contact alone because water-engaged infants reduced crying marginally during treatment and then reinitiated vigorous crying during the posttreatment period. To be fully effective, sucrose must be delivered when infant and deliverer are visually engaged. We believe that this reflects an emergent property of specific conjoint stimulation of gustatory and visual afferents. Visual engagement in the absence of sucrose delivery, as in the case of infants who received water, only modestly influenced infant behavior. Likewise, sucrose in the absence of visual engagement was also only moderately suc-

cessful. The control experiment (Experiment 2), in which sucrose-treated infants looked at the experimenter's face but without eye contact, demonstrated that the success of the engaged-sucrose treatment could not be attributed to the infant searching for or being distracted by the experimenter's face because nonengaged infants had a full view of the adult face and studied it. Yet, crying was not arrested. Thus, within the context of crying or distress, particular classes of visual and gustatory afferents must occur conjointly in order for calm and bradycardia to be induced and maintained. One might argue for a simple additivity of visual and gustatory effects. Wefindthis unlikely on four grounds. First, water was ineffective during the first treatment minute, whereas sucrose-engaged infants reduced their crying dramatically. Second, almost all quieting in water and nonengaged infants occurred duringfluiddelivery and not during intervals separating delivery, suggesting a focus of attention to the ingestive act and not a state change caused by the act. Third, there was virtually no effect of water ingestion in engaged infants on HR. Fourth, whatever changes were induced in sucrose-alone or water-engaged infants did not carry into the poststimulation period, whereas changes obtained in sucrose-engaged infants endured. Four-week-old infants who received sucrose while visually engaged kept their eyes open and directed at the experimenter's face almost all of the time. During the disorganization of crying, newborns do not seem to be able to focus on external sources of stimulation. In contrast, 4-week-olds can focus their gaze even

1098

ZEIFMAN, DELANEY, AND BLASS

when crying and hyperactive. In fact, they actively sought to establish eye contact when the experimenter purposefully averted her gaze. This represents a major qualitative change in the relationship between affective state and motor control. It is important to place constraints on the current phenomena. Sucrose serves as a calming agent, presumably through the opioid pathways identified in studies in human newborns and infant rats. Sucrose is not the only agent that calms distressed infants. Sucking a pacifier and being held which use nonopioid pathways, also calm (Barr et al., 1991). Sucking a pacifier, for newborns anyway, elicits eye opening as well (Blass & Ciaramitaro, 1994). Whether visual engagement that was necessary to make sucrose a more effective stimulus in the present study also has the same deterministic role for pacifier effects can be determined empirically. Although eye engagement is clearly sufficient to potentiate calming, its necessity has not been established. Conceivably any complex visual stimulus would be effective, although the present data argue against this interpretation because looking at a face with eye contact precluded did not calm infants who received sucrose. Moreover, tracking the experimenter's head movements was not the critical feature because the experimenter's head moved to thwart the infants' attempts at eye contact. Presumably, the infants were able to detect these movements. Still, the current experiments have not eliminated the possibility that other engaging visual stimuli would be effective when coupled with sucrose delivery. One possible outcome of eye contact enhancing and sustaining calm and bradycardia when combined with sucrose is that it provides positive affective valance to the representations of mother and other significant caretakers who induce this state. Newborns learn about and prefer the mother's visual (Bushnell et al., 1983; Pascalis et al., 1995) and olfactory (Cernoch & Porter, 1985) features, but these features do not contribute to the change in the infant's state, even in 2-week-olds. By 4 weeks of age, the features do contribute as demonstrated here, but they do not have to be the caretaker's specific features. Thus, visual engagement in the current situation has the properties of an unconditioned stimulus when presented with sucrose. We suggest that through multiple contact episodes under normal circumstances, the mother's (caretaker's) specific visual features take on affective value that ultimately allows these features to independently calm the infant at a distance. The visual dimension of the bond between the infant and the mother may become established, in part, because it is the particular features of the mother that are calming and not necessarily because these features have been associated with calm induced by contact or suckling. There are other obvious sources of individual discovery such as the voice of the person providing contact comfort, nursing, or stimulation (normally, the mother). Early achievement of individual representations may also be obtained through imitative interactions in which infants develop strategies for interacting with different individuals or representing particular interactions that they've had with a given person (Meltzoff & Moore, 1994). The textures of the infant's representation and motivation systems are so rich, as we are discovering, that multiple pathways for their enhancement should be sought. HR and gross motor activity were also reduced in engaged 4week-olds. Because these changes, in newborns at least, reflect

the engagement of opioid mechanisms that manage energy conservation, we suggest that this coordinated system is also available to the 1-month-old but that access to it is more complex. Within this context, hand-mouth behavior has moved outside the domain of sucrose-induced changes in both 2- and 4-weekold infants. That sucrose-calmed infants did not bring their hands to their mouths has a number of possible explanations, the simplest being a marked increase in arm mass without a commensurate increase in strength. However, infants who were calmed by sucrose in Experiment 2 did not appear to even attempt to bring their hands to their mouths. The loss of hand-in-mouth selfquieting from the newborn period over the first 9 weeks of life has been attributed by some to changes in tonic posture (Hopkins, Janssen, Kardaun, & van der Schoot, 1988). Alternatively, whereas taste alone caused the hand to be brought to the mouth in newborns, deprivation plus oral stimulation may be necessary for the feeding system to gain control over handmouth activity in older infants. AH of the infants in Experiment 2 were nursed by their mothers. The nursing-suckling situation differs sufficiently from the current test arrangement that we see minimal room for overlap in either conditioned or unconditioned stimuli between the two settings. In particular, nursing always occurs within the context of the infant being held by its mother. Infants here were either tested in their beds or on a sofa. They were not held during testing. Milk is extracted from the breast through a particular motor pattern. Sucrose was delivered noncontingently through syringe and did not elicit sucking movements; licking or mouthing were the rule. Finally, sucrose taste differs markedly from milk flavor. On these grounds we favor a maturational, emergent-property interpretation of the presentfindingsas opposed to the effectiveness of visual engagement reflecting conditioning experiences. Thesefindingsare of obvious relevance to the development of face recognition in humans. Morton and Johnson (1991), who have written thoughtfully on this issue have identified two processes, CONSPEC and CONLERN, that determine facial recognition. The CONSPEC process is available to the infant at birth and appears to be a low-level feature recognition system for attracting the infant to human faces. According to theory, this aspect of the system does not discriminate a particular feature among different individuals. The present findings suggest that a qualitative change occurs by 4 weeks that impacts the mechanism(s) that form representations of particular faces and provides them with affective value. Motivational changes, therefore, may parallel cognitive ones. Thus, over time, the emotional state elicited by the events surrounding nursing may become an integral portion of the infant's representation of her mother. The present studies encourage expanding on and validating this hypothesis. References
Apgar, V. (1953). A proposal for a new method of evaluation in the newborn infant. Current Research in Anesthesia and Analgesia. 32. 260-267. Ashmead, D. H., Reilly, B. M., & Lipsitt, L. P. (1980). Neonates' heart rate, sucking rhythm, and sucking amplitude as a function of sweet taste. Journal ofExperimental Child Psychology, 29,264-281.

SWEET TASTE

1099

Barr, R. G., McMullan, S. J., Spiess, H., Leduc, D. G., Yaremko, J., Qualitative and quantitative considerations. Developmental Psychology, 28, 804-810. Barfield, R., Francoeur, T. E., & Hunziker, U. A. (1991). Carrying as colic "therapy": A randomized controlled trial. Pediatrics, 87, 623- Bushnell, I. W. R., Sai, E, & Mullin, J. T. (1983). Neonatal recognition of mother's face. British Journal of Developmental Psychology, 7, 3630. 15. Barr, R. G., Pantel, M. S., Wright, J. H., Gravel, R. G., & Young, S. N. Cernoch, J. M., & Porter, R. H. (1985). Recognition of maternal axil(1995, March-April). The "sucrose effect" is a "sweetness effect" in lary odors by infants. Child Development, 56, 1593-1598. crying newborns. Paper presented at the conference of the Society for Crook, C. K.., & Lipsitt, L. P. (1976). Neonatal nutritive sucking: Research in Child Development, Indianapolis, IN. Effects of taste stimulation upon sucking rhythm and heart rate. Barr, R. G., Quek, V., Cousineau, D., Oberlander, T. E, Brian, J. A., & Child Development, 47, 518-522. Young, S. N. (1994). Effects of intraoral sucrose on crying, mouthing Desor, J., Mailer, Q, & Turner, R. (1973). Taste in acceptance of sugars and hand-mouth contact in newborn and six-week-old infants. Deby human infants. Journal ofComparative Psychological Psychology, velopmental Medicine Child Neurology, 36, 608-618. 84. 496-501. Blass, E. M., & Ciaramitaro, V. (1994). Oral determinants of state, Engen, T, Lipsitt, L. P., & Peck, M. B. (1974). Ability of newborn inaffect, and action in newborn humans. Monographs ofthe Societyfor fants to discriminate sapid substances. Developmental Psychology, 10, Research in Child Development, 59, 1-102. 741-744. Blass, E. M., Fillion, T. J., Rochat, P., Hoffmeyer, L. B., & Metzger, Hopkins, B., Janssen, B., Kardaun, O, & van der Schoot, T. (1988). M. A. (1989). Sensorimotor and motivational determinants of handQuieting during early infancy. Early Human Development, 18, 111mouth coordination in 1-3-day-old human infants. Developmental 124. Psychology, 25, 963-975. Meltzoff, A. N., & Moore, M. K. (1994). Imitation, memory, and the Blass, E. M., Fillion, T. J., Weller, A., & Brunson, L. (1990). Separation representation of persons. Infant Behavior and Development, 17, 83of opioid from nonopioid mediation of affect in neonatal rats: Nono100. pioid mechanisms mediate maternal contact influences. Behavioral Morton, J., & Johnson, M. H. (1991). CONSPEC and CONLERN: A Neuroscience, 104(4), 625-636. two-process theory of infant recognition. Psychological Review, 98, Blass, E. M., & Fitzgerald, E. (1988). Milk-induced analgesia and com164-181. forting in 10-day-old rats: Opioid mediation. Pharmacology, Bio- Pascalis, Q, de Schonen, S., Morton, J., Deruelle, C, & Fabre-Grenet, chemistry & Behavior, 29, 9-13. M. (1995). Mothers, face recognition by neonates: A replication and Blass, E. M., Fitzgerald, E., & Kehoe, P. (1987). Interactions between an extention. Infant Behaviour and Development, 18, 79-85. sucrose, pain and isolation distress. Pharmacology, Biochemistry and Rao, M., Blass, E. M., Brignol, M. J., Marino, L., & Glass, L. (1993). Behavior, 26. 483-489. Effect of crying on energy metabolism in human neonates. ProceedBlasS, E. M., Ganchrow, J. R., & Steiner, J. E. (1984). Classical condiings of the American Pediatric Society, 33, 309. tioning in newborn humans 2-48 hours of age. Infant Behavior and Rochat, P., Blass, E. M., & Hoffmeyer, L. B. (1988). Oropharyngeal Development, 7, 125-134. control of hand-mouth coordination in newborn infants. Developmental Psychology, 24, 459-463. Blass, E. M., & Hoffmeyer, L. B. (1991). Sucrose as an analgesic in Shide, D. J., & Blass, E. M. (1989). Opioid-like effects of intraoral innewborn humans. Pediatrics, 87, 215-218. fusions of corn oil and polycose on stress reactions in 10-day-old rats. Blass, E. M., & Shah, A. (1995). Pain reducing properties of sucrose in Behavioral Neuroscience, 103, 1168-1175. human newborns. Chemical Senses, 20, 29-35. Shide, D. J., & Blass, E. M. (1991). Opioid mediation of odor preferBlass, E. M., & Shide, D. J. (1993). Endogenous cholecystokinin reences induced by sugar and fat in 6-day-old rats. Physiology & Behavduces vocalization in isolated 10-day-old rats. Behavioral Neurosciior, 50,961-966. ence, 107, 488-492. Smith, B. A., Fillion, T. J., & Blass, E. M. (1990). Orally mediated Blass, E. M., Shide, D. J., Zaw-Mon, C, & Sorrentino, J. (1995). sources of calming in 1- to 3-day-old human infants. Developmental Mother as shield: Differential effects of contact and nursing on pain Psychology, 26,731-737. responsivity in infant rats: Evidence for nonopioid mediation. Behavioral Neuroscience, 109,342-352. Received March 2,1994 Blass, E. M., & Smith, B. A. (1992). Differential effects of sucrose, frucRevision received February 5, 1996 tose, glucose, and lactose on crying in 1- to 3-day-old human infants: Accepted February 11, 1996