Preterm and Term Infants' Perception of Temporally Coordinated Syllable–Object Pairings:...

JSLHR

Article

Preterm and Term Infants’ Perception ofTemporally Coordinated Syllable–Object

Pairings: Implications forLexical Development

Lakshmi Gogate,a Madhavilatha Maganti,b and Agnes Perenyic

Purpose: This experimental study examined term infants(n = 34) and low-risk near-term preterm infants (gestationalage 32–36 weeks) at 2 months chronological age (n = 34) andcorrected age (n =16). The study investigated whether thepreterm infants presented with a delay in their sensitivity tosynchronous syllable–object pairings when compared withterm infants.Method: First, infants were habituated to a single syllable,[tah] or [gah], spoken in synchrony with the motions of 1 of4 toy objects, a crab, a porcupine, a star, or a lamb chop.Next, the infants received 2 syllable- and 2 object-change testtrials, counterbalanced for order.Results: After factoring out differential looking time duringhabituation, the study found that preterm infants showed

attenuated looks to the change in the object and the changein the syllable relative to term infants.Conclusions: These findings suggest that even near-termpreterm infants present with a delay in their sensitivity tosynchrony in syllable–object pairings relative to term infants.Given the important role that synchrony plays in word mappingat 6–9 months, this early delay in sensitivity to synchronymight be an indicator of word mapping delays found in olderpreterm infants.

Key Words: infancy, auditory–visual synchrony perception,preterm infants, developmental delay, intersensory invariance,word-mapping delay

Caregiver communication provides predominantly multi-modal stimulation contained in a dynamic flow ofevents. One type of multimodal stimulation avail-

able to infants during communication is maternal namingwhile simultaneously moving an object, which enablesinfants to map words onto objects (Gogate, Bahrick, &Watson, 2000; Gogate, Bolzani, & Betancourt, 2006;Matatyaho & Gogate, 2008). When an object is named andmoved simultaneously, invariant or amodal information, notspecific to a particular sense modality, is made availableacross auditory and visual senses—a common temporalonset and offset, tempo, and rhythm (also see Bahrick &Lickliter, 2000). Such invariant intersensory informationhighlights the word–object relation by unifying the otherwiseunrelated word and moving object across auditory–visual

modalities and facilitates learning that the word and theobject go together (see review by Gogate & Hollich, 2010).Therefore, mapping of a word onto an object is a perceptuallydrivenmultisensory activity (Smith, 2005) that is facilitated byintersensory perception, in particular, synchrony detection.

Typically developing preverbal infants born to term arehighly sensitive to naming contexts in which spoken syllablesand moving objects are synchronous. Following habituationto a synchronous but not an asynchronous syllable–objectpairing, 2-month-old infants look longer on test trials when achange in the syllable or the object is presented relative tocontrol trials (Gogate, Prince, & Matatyaho, 2009). Seven-and 8-month-olds map two spoken syllables onto two movingobjects, if intersensory invariance is provided, in the formof temporal synchrony, between the syllables and the objects’motions. Whereas the 8-month-olds map two similar syl-lables, [tah] and [gah], onto the two objects, the 7-month-oldsmap two distinct syllables, [tah] and [gih] or [gah] and [tih](Gogate, 2010). Following habituation to the two syllable–object pairings, the infants look longer on test trials when thesyllable–object pairings are interchanged relative to controltrials. Thus, synchrony perception plays an important role ininfants learning to map words onto referents.

Although the evidence from term infants on wordmapping in the presence of synchrony abounds, no studies

aFlorida Gulf Coast University, Fort MyersbUniversity of Hyderabad, Gachibowli, Hyderabad, IndiacSUNY Downstate Medical Center, Brooklyn, NY

Correspondence to Lakshmi Gogate: [email protected]

Editor and Associate Editor: Rhea Paul

Received December 18, 2012Revision received March 27, 2013Accepted May 22, 2013DOI: 10.1044/1092-4388(2013/12-0403)

Journal of Speech, Language, and Hearing Research • 1–12 • A American Speech-Language-Hearing Association 1

JSLHR57-1_Gogate (1st Revision)

have as yet assessed very young preterm infants’ synchronyperception in a word-mapping context especially undertightly controlled experimental conditions. A comparativeobservational study of borderline preterm (32–36 weeksgestational age) and term 6- to 9-month-old infants showedthat mothers of both infant groups used synchrony duringobject naming equally in abundance (approximately 75%)during a 3-min play episode. However, the preterm infantsshowed attenuated learning of the word–object relationsrelative to the term infants, suggesting that they are lesssensitive to synchrony in maternal naming and do not learnthe word mappings (Gogate et al., 2011). Given the impor-tance of synchrony perception to infants’ mapping of wordsonto referents, an investigation of the intersensory perceptualabilities of very young preterm infants in word-mappingcontexts is warranted to see whether their sensitivity differsfrom term infants. In the present study, we experimentallyexamined whether low-risk, borderline1 (gestational age 32–36 weeks) preterm 2-month-olds would show a delay intheir sensitivity to synchrony in arbitrarily paired spokensyllables and moving objects compared with term infants.

In contexts other than word mapping as well, preterminfants are known to be less sensitive to synchronous sightsand sounds than their term counterparts. Three-, 5-, and7-month-old preterm infants (31–36 weeks estimated gesta-tional age) did not match faces and voices on the basis ofsynchrony when compared with term infants of the sameage (Pickens et al., 1994). Low- and high-risk 3-month-oldpreterm infants did not match moving objects to the soundsthey make, again on the basis of synchrony, relative to terminfants (Lawson, Ruff, McCarton-Daum, Kurtzberg, &Vaughan, 1984).

Faces and voices or objects and their impact sounds,however, bear an amodal relation to one another—much ofthe same information is conveyed across auditory and visualsenses (Walker-Andrews, 1994). In contrast, much of lexicaldevelopment entails developing perception to and learning ofarbitrary auditory–visual relations between spoken wordsand referents that must be learned by convention with repeatedexposure to the relation. Although the learning of an arbitraryrelation can be more difficult when compared with learningan amodal relation, term infants are known to learn both typesof relations (see Gogate & Hollich, 2010, for a review).

An important question that begs investigation iswhether preterm infants detect synchrony in spoken syllablesthat are otherwise arbitrarily paired with objects that areembedded in an adult’s showing gesture. Knowing whetherpreterm infants are sensitive to the synchrony that unifiesa spoken syllable and an object in motion can reveal whetherthese at-risk infants, on par with their term counterparts,are ready for lexical development. Alternatively, if a delaywere found in synchrony perception in word-mapping contextsearly on, it might serve as an early indicator of word-mapping

delay in preterm infants. In the future, synchrony detectioncould be used in larger norming studies and, depending onthe results, could be incorporated in the design of diagnostictools to predict word-mapping delays. Furthermore, indi-vidual variations in infants’ synchrony perception mightpredict individual differences in the developmental trajectoryof word mapping, as might individual differences in caregiveruse of synchrony in naming contexts to infants.

In the domain of language development, preterm in-fants present with delays in language comprehension andproduction (Le Normand & Cohen, 1999; Siegel, Cooper,Fitzhardinge, &Ash, 1995; Vohr, 1988; cf. Menyuk, Liebergott,& Schultz, 1995). In a longitudinal study, preterm infantscontinued to show delays in speech and language developmenteven at 2 years (Veen, Ens-Dokkum, Schreuder, Verloove-Vanhorick, & Brand, 2003). The language delays include adelay in the onset of word combinations at 3 years (Bonifacio,1998), a shorter mean length of utterance relative to same-ageterm infants (Field, Dempsey, & Shuman, 1981; Le Normand,Delfosse, Crunelle, & Vittrant, 1995; Oller, Eilers, Steggens,Lynch, & Urbano, 1994), and a delay in grammatical sen-tence composition (Stolt et al., 2006). Although some of thisevidence comes from high-risk preterm infants of very lowbirth weight, near-term infants might also present with delaysthat could easily go unnoticed in the early years (see Raju,2006).

Little is known about the root causes for the languagedelay in preterm infants. Recent neurophysiological studiessuggest that immature preterm newborns (29–32 weeks ges-tational age) discriminate between spoken syllables (e.g., /ba/and /ga/; Mahmoudzadeh et al., 2013) similar to term infants,requiring minimal experience with ambient speech. In con-trast, immature preterm infants (±28 weeks gestational age)discriminate between languages on the basis of their rhythmonly after 6 months of native language experience, similarto term infants (Peña, Pitaluga, & Mehler, 2010). Researchin visual perception suggests that low-risk preterm infantsbenefit from early visual postnatal experience by disengagingor shifting gaze from visual stimuli faster than their termcounterparts in the first 16 weeks (Hunnius, Geuze, Zweens,& Bos, 2008). Experimental studies comparing visual habit-uation and subsequent test performance of low-risk pretermand term infants report effects of infant age, stimulus type,and attention differences correlated with age and stimulustype (see review by Kavšek & Bornstein, 2010; Rose, Feldman,& Jankowski, 2002). These findings, along with the findingsfrom auditory–visual synchrony perception discussed earlier,suggest that early speech discrimination in low-risk preterminfants develops on par with term infants, and visual attentionis enhanced owing to early visual experience, yet auditory–visual temporal synchrony perception may be compromised.

A study comparing preterm and term infants’ earlyperceptual sensitivity to speech paired with an object iswarranted for three specific reasons. First, the fields of childdevelopment and developmental pediatrics suggest thatperceptual learning in early infancy leads to cognitivedevelopment, including language. Thus, for instance, clinicalneurodevelopmental assessments (e.g., the Bayley Scales of

1The proportion of near-term births referred to as late preterm infants(born between 34 and 36 weeks of gestation) has contributed mainly to agradual increase of 0.2% in the preterm birth rate per year according toUS Healthy People 2010 (see Raju, 2006).

2 Journal of Speech, Language, and Hearing Research • 1–12


Infant Development; Bayley, 2006) include items that test in-fants’ perceptual abilities prior to those that test cognitiveabilities. Similarly, examinations of early perceptual abilities ofyoung preterm infants in word-mapping contexts can provideinsights into how perception leads to language comprehension.

Second, some intervention studies have suggested thatmultisensory stimulation (auditory, visual, tactile, and ves-tibular) given to preterm infants soon after birth is positivelycorrelated with their weight gain, arousal and alertness levels,and their ability to feed naturally over several weeks (White-Traut et al., 2002). Given these beneficial effects for preterminfants, and given that term infants perceive intersensoryinvariance in stimulation across the senses early on (see re-views by Gogate & Hollich, 2010; Gogate, Walker-Andrews,& Bahrick, 2001; Hyde, Jones, Flom, & Porter, 2011;Lewkowicz, Leo, & Simion, 2010), it is surprising that studieshave yet to examine very young preterm infants’ sensitivityto synchrony in word–object pairings.

Finally, a comparative study of very young near-termpreterm and term infants that examines their early perceptualsensitivity to spoken syllable–object relations might shedlight on the developmental origins of intersensory perceptionin humans. The auditory–visual perception literature sug-gests that human sensitivity to temporally and spatiallycoordinated auditory–visual stimuli is present at birth andthat the senses are relatively undifferentiated or amodal andinvariant in nature early on (Gibson, 1969). Thus, humannewborns detect amodal information such as temporal syn-chrony, intensity shifts, and spatial co-location in auditory–visual events. Newborns turn their eyes in the direction ofauditory stimuli (Butterworth & Castillo, 1976). They matchauditory–visual stimuli on the basis of their common in-tensity shift (Lewkowicz & Turkewitz, 1980) and temporalsynchrony (Lewkowicz et al., 2010; see Bahrick, 2001, forevidence from 4-week-olds). Newborns match a single arbi-trarily paired auditory–visual event on the basis of synchronyand spatial co-location (Morrongiello, Fenwick, & Chance,1998). In contrast, cross-species evidence from cats and rhesusmonkeys suggests that sensitivity to temporally and spatiallycoordinated auditory–visual stimuli is not present at birth.It develops within the first 7 weeks of postnatal life, drivenlargely by environmental experience (see review by Wallace,2004).

In light of these contrasting findings across species, aninvestigation comparing very young human term with pre-term infants at ages uncorrected and corrected for prema-turity might provide clues to their developing early sensitivityto synchrony in arbitrarily related auditory–visual events.Assuming that all else is comparable, if term and preterminfants at a chronological age of 2 months are found to besensitive to synchrony between a spoken syllable and a mov-ing object, it will suggest that the development of this typeof intersensory perception is driven largely by environmentalexperience (similar to Peña et al., 2010, for rhythmic prop-erties of language), with little or no detrimental consequencesfor preterms’ immature neurosensory system for synchronydetection in word-mapping contexts. Alternatively, if pre-term infants at corrected age alone are sensitive to synchrony

in a syllable–object pairing, it will suggest that the prematureneurosensory system takes greater time to develop and toeventually become sensitive to intersensory invariance on parwith term infants. The underdeveloped neurosensory system(the internal structure) must develop and interact furtherwith the natural environment to perceive intersensory in-variance by 2 months corrected age. Owing to insufficientongoing organismic–environmental interaction (Gogate &Hollich, 2010), preterm infants at 2 months chronologicalage show attenuated sensitivity to synchrony in word-mappingcontexts. In contrast, if preterm infants at 2 months chro-nological and corrected ages are not sensitive to synchronyin a syllable–object pairing, it will suggest that this sensitivityis severely compromised as a result of prematurity anddevelops much later in preterm than in term infants, withpotential detrimental consequences for word-mapping de-velopment as seen at 6–9 months (Gogate et al., 2011).

In the present experimental study, we hypothesizedthat at 2 months chronological age, preterm infants wouldshow attenuated or null sensitivity to a synchronous syllable–object pairing relative to term infants, in part because ofunderdeveloped cortical structures at birth manifesting as animmature sensory system after birth (see Raju, 2006). Morespecifically, we hypothesized that the delayed sensitivitywould manifest as attenuated or null visual recovery to thesyllable or object changes following habituation to the syn-chronous syllable–object pairing. The preterm infants werealso tested at 2 months corrected age, to examine whether theattenuated or null sensitivity to synchronous syllable–objectpairings still persists after correcting for prematurity. Onthe basis of prior experimental findings where even 7-month-old preterm infants showed delayed synchrony perceptionof amodal face–voice stimuli (e.g., Pickens et al., 1994), wehypothesized that at 2 months corrected age as well, preterminfants would show attenuated or null sensitivity to syn-chrony in an arbitrary syllable–object pairing relative to terminfants.

We used an infant-controlled habituation procedure(Horowitz, 1974) that has been previously adapted to ex-amine term infants’ perception of a syllable–object pairing(Gogate, 2010; Gogate et al., 2009; Stager & Werker, 1997).Infants were exposed to a video display of a spoken syllablepaired and in synchrony with the motions of a toy objectduring habituation. They received a single pairing because2-month-old term infants do not learn two synchronoussyllable–object pairings if habituated sequentially to them(Gogate et al., 2009). Following habituation, on test trials weexamined whether infants would show sensitivity to a changein the syllable or the object on separate trials by lookinglonger to the changed relative to the unchanged stimuli.

MethodParticipants

Thirty-four healthy 2-month-old term (M = 61.59 days,SD=5.90; 15 boys and 19 girls) and 34 preterm (M=62.62 days,SD = 5.10; 13 boys and 21 girls) infants from English-speaking

Gogate et al.: Syllable–Object Pairing Perception by Infants 3


homes participated. Of the 34 preterm infants, 12 infantsparticipated again at 2 months corrected age (M = 109.15 days,SD = 14.54).2 Four additional preterm infants participatedat 2 months corrected age alone, resulting in a final sample of16 infants (7 boys and 9 girls). Data collection was in com-pliance with the Protection of Human Subjects’ guidelinesand approved by the institutional review board of SUNYHealth Science Center in Brooklyn. Written consent was ob-tained from the mother prior to infant participation.

The infants were recruited from the birth records ofSUNY Downstate Medical Center, Brooklyn, New York,and resided in its suburbs. They were screened for normalhearing (oto-acoustic emission) and vision (e.g., using a slitlamp to screen for retinopathy because of prematurity) bya neonatologist prior to participation. An inclusion criterionwas that mothers of term and preterm infants have at least12 years of education because parental education and infantdevelopment are positively correlated (Hart & Risley, 1995).

The preterm infants’ gestational age was 32–36 weeks(M = 34.51 weeks, SD = 2.06). They weighed at least 2 lbs(M = 4.89 lbs [2340 g], SD = 1.15 lbs) at birth and had noknown history of medical complications other than prematu-rity. We excluded infants with a medical history of morbiditiesrelated to prematurity, such as acute and/or chronic respi-ratory distress, infections, or severe hyperbilirubinemia, andinfants with congenital anomalies. Of the 34 preterm infantsat 2 months chronological age, 29 were African American,one was Asian American, and four were biracial. Of the16 preterm infants at 2 months corrected age, 10 were AfricanAmerican, two were Asian American, and four were biracial.At 2 months chronological age, 14 additional preterm in-fants were not included in the final sample owing either toexcessive fussiness, fatigue, or sleepiness (n = 10) or to equip-ment failure (n = 4). At 2 months corrected age, eight addi-tional preterm infants were not included in the final sampleowing to fussiness, fatigue, or sleepiness (n = 2) or to equip-ment failure (n = 3), failure to habituate (n = 2), or externalinterference (n = 1).

The term infants served as controls for the preterminfants at chronological and corrected ages. Their gestationalage was 37–41 weeks (M = 38.91 weeks, SD = 0.92). Theyweighed at least 5 lbs (M = 6.90 lbs, SD = 0.98) at birth andhad no known history of medical complications during orafter birth. Of the 34 term infants, 25 were African American,and nine were biracial. Twenty-five additional infants werenot included in the final sample owing to excessive fussiness,fatigue, or sleepiness (n = 18) or to equipment failure (n = 7).

StimuliVideo stimuli of two syllables, [tah] and [gah], each

spoken in synchrony with the motions of a toy object from

one of two sets, either a wooden star and a plastic lamb chopor a plastic crab and a porcupine, were used (Figure 1). Thevideo stimuli contained the following syllable–object pair-ings, [tah]–crab, [tah]–porcupine, [tah]–star, [tah]–lamb chop,[gah]–crab, [gah]–porcupine, [gah]–star, and [gah]–lamb chop.They were identical to those used in the synchronous con-dition of a prior study (Gogate et al., 2009). Each object ina set was of two contrasting colors. A female native speakerof standard American English spoke the syllables in anirregular temporal pattern. The two syllables differed in theironset consonant but not in their nucleus, /a/, or coda, /h/.The onset consonants differed in two dimensions, place ofarticulation and voicing; /t/ was alveolar and voiceless, and/g/ was velar and voiced. The syllables were spoken in iso-lation, rather than in a phrase, to ease memory load (seePlunkett, 2006, for such evidence from older infants) and toeliminate any potential confounding attention effects frompresenting a phrase (surrounding the target syllable) inasynchrony with a moving object. Vowel nucleus elonga-tion and syllable-final aspiration occurred when the syllableswere spoken in isolation and in infant-directed speech (i.e.,with a higher fundamental frequency relative to adult-directed speech). The syllables were presented at a soundpressure level of 65–70 dB. The ambient amplitude wasmeasured with a sound-level meter (Radio Shack, FortWorth, TX).

The object presentations were filmed against a blackbackground, with the objects in the foreground and theactor’s hand and forearm in the background. On the videodisplays, a syllable was spoken simultaneously with handheldforward and diagonal movements of an object, resemblingan act of showing the object while labeling it to infants. Thetempo, rhythm, and intensity shifts of the motions and syl-lable occurrences varied, creating irregular intervals betweensynchronous syllable–object tokens. In an earlier study(Gogate et al., 2009), the video displays were also compu-tationally analyzed for the temporal relatedness or synchronybetween the visual motion and audio energy and were con-firmed to be synchronous. The syllables were spoken at a rateof 30–35 tokens per minute. In addition to these syllable–object displays, a video display of a green and white plasticturtle, whose front legs spun around producing a whirringnoise, was used to test for alertness-fatigue during habituation(Gogate & Bahrick, 1998).

ApparatusFour video decks (Panasonic AG 1980P) connected to

a 4 × 4 input selector (Radio Shack, Fort Worth, TX) wereused to present the audiovisual stimuli on a 20-in. (50.8-cm)color videomonitor (SonyKV 22M10). The monitor facing alarge table and an infant seat placed centrally on the tablewere situated within a testing booth with black cloth panelson three sides (Figure 2). The middle panel surrounded themonitor on each side and contained a peephole to the left andthe right of the monitor from which the observers, hiddenfrom the infant, could record infants’ eye movements. Thesyllables were presented at 65–70 dB via a speaker situated

2This longitudinal sample enabled assessment of preterm infants’developing sensitivity to synchrony in syllable–object relations over timeand reduced the between-subjects variability of the chronological andcorrected age groups.



centrally and under the large table located in front of themonitor. A computer recorded observers’ button presses,which corresponded with infants’ looks to the audiovisualdisplays (see below), and printed the data online in anadjacent room.

ProcedureThe infants were in an alert state at the time of testing.

They were seated in the infant seat approximately 55 cmaway from and facing the video monitor. Prior to the habit-uation phase, infants received a single pretest trial of the turtledisplay to monitor for fatigue. Next, during habituation,infants received a syllable–object pairing sequentially in aninfant-controlled habituation procedure. They received asingle syllable, [tah] or [gah], spoken in synchrony with themotions of one of four toy objects—a crab, a porcupine,a star, or a lamb chop—with type of object and syllablecounterbalanced within the design.

The trial length was infant controlled. Each trial beganwhen an infant fixated on the monitor and was terminatedwhen the infant looked away for 1 s or after 45 s of cumu-lative looking. These shorter cumulative looking and look-away times relative to prior studies (e.g., in Gogate [2010],60 s of cumulative looking and time to look away 1.5 s for7- and 8-month-olds) accommodated younger infants’ shorterattention span, allowing them to disengage easily at theend of a trial and reorient to the video display on the nexttrial (also see Bahrick, 2001; Gogate et al., 2009). The nextvideo clip was played 5 s after trial termination, and the trialbegan again when the infant fixated on the monitor. Pre-term and term infants met the habituation criterion (trackedby the computer) by exhibiting a decrease in looking on twoconsecutive trials that was less than 50% of their meanlooking to the first two habituation trials (i.e., baseline). Thenumber of trials to habituate to a syllable–object pairingwas also infant controlled (i.e., determined by individualtrends in reaching habituation criterion; minimum number oftrials = 6, maximum number of trials = 20).

Figure 2. The testing booth in which infants were habituated andtested.

Figure 1. The two sets of objects used as stimuli: the crab and the porcupine (top row) and the lamb chop and the star (bottom row).



Following habituation, infants received two no-changeposthabituation trials to obviate chance habituation effectsand to control for regression to the mean (Bertenthal, Haith,& Campos, 1983). Following the posthabituation trials,infants received two types of change test trials whose orderwas counterbalanced within each group. These trials con-sisted of a syllable change on two trials and an object changeon two trials. For example, if infants received [tah] with thecrab during habituation, they received [gah] with the crab onthe syllable-change trials and [tah] with the porcupine on theobject-change trials. After these test trials, the infants, onceagain, received a single trial of the moving turtle display tomonitor for alertness-fatigue. Infants’ duration of looks tothe last turtle display was required to be greater than 20%of their looks to the first turtle display to meet the alertnesscriterion and to be included in the final sample (Gogate,2010; Gogate & Bahrick, 1998, 2001; Matatyaho, Gogate,Mason, Cadavid, & Abdel-Mottaleb, 2012; Matatyaho,Mason, & Gogate, 2007).

Identical to the procedure at chronological age, at2 months corrected age infants received a single synchronoussyllable–object pairing in an infant-controlled habituationprocedure, with one exception. At 2months corrected age, the12 infants who returned for the second visit received a syllable–object pairing from an entirely different set than the pairingthey received during the first visit, to eliminate possible con-founding effects of memory for the pairing. For example, ifinfants received [gah] pairedwith the crabduringhabituation atthe first visit, the infants received [tah] paired with the lambchop at the secondvisit during habituation. Identical to the firstvisit, following habituation and two no-change posthabitua-tion trials, the infants received two types of change test trials, asyllable change on two trials andan object change on two trials.

One or two trained observers, who could not see thevideo displays or hear the syllables during the procedure(they wore shielded SONY DR-7 headphones that playedmusic) and who were therefore uninformed about the orderof test trials, monitored infants’ duration of looking to theobject displays during the trials. The number of seconds ofinfants’ looks to the display recorded by the primary observerwas statistically compared with those recorded by a secondobserver for 13 of the 34 (38%) term infants, 12 of the 34 (35%)preterm infants at 2 months chronological age, and 6 of the16 (37%) preterm infants at 2 months corrected age. Reliabilitycomputations yielded a mean Pearson r of .95 (SD = .07) forterm infants, .95 (SD = .10) for preterm infants at 2 monthschronological age, and .99 (SD = .006) at 2 months correctedage. The Cronbach’s alpha was .90 for term infants, .84 forpreterm infants at 2 months chronological age, and .77 at2 months corrected age. The primary observer’s raw scores(seconds) were used in the analyses of the habituation andtest phases.

ResultsHabituation (Learning) Phase

Separate one-way analyses of variance (ANOVAs; usinggeneral linear models to account for the unequal variances)

assessed whether the preterm infants at 2 months chrono-logical and corrected ages showed differential attention to asyllable–object pairing during habituation compared with theterm infants on the mean of the first two habituation trials(baseline), the last two habituation (criterion) trials, the totaltime taken to habituate, and the mean number of trials re-quired to reach habituation criterion to a syllable–object dis-play. The ANOVA of the mean number of trials to reachhabituation criterion by group yielded a marginally significantmain effect of Group, F(2, 81) = 2.70, p = .07. In contrast,the remaining three ANOVAs showed that the term infants’mean looking time differed significantly from that of thepreterm infants on baseline, F(2, 81) = 40.94, p < .001; thelast two habituation trials, F(2, 81) = 10.13, p < .001; andtotal time taken to habituate, F(2, 81) = 17.5, p < .001. Posthoc multiple comparisons (Bonferroni a = .05) of thesevariables across the three groups revealed that the preterminfants’mean looking time at chronological age 2 months onthese measures was significantly attenuated relative to thatof the term infants and the preterm infants at corrected age2 months. On the baseline measure, the preterm infants at2 months chronological age differed significantly from thepreterm infants at corrected age (adjusted mean difference =–14.06 s, p < .001) and the term infants (adjusted meandifference = –17.46 s, p < .001). On the last two habituationtrials, the preterm infants at 2 months chronological agediffered significantly from the preterm infants at correctedage (adjusted mean difference = –5.14 s, p < .001) and theterm infants (adjusted mean difference = –2.9 s, p < .01).On the total time taken to habituate as well, the preterminfants at 2 months chronological age differed significantlyfrom the preterm infants at corrected age (adjusted meandifference = –167.09 s, p < .001) and the term infants(adjusted mean difference = –157.77 s, p < .001). Thus, forpreterm infants, attention increased with age. See Table 1 forunadjusted means and standard deviations by group. Toaccurately assess sensitivity to synchrony and compare testperformance across infant groups (see next section), it becameimperative to factor out the between-group difference inattention (total time taken to habituate) during the habitu-ation phase.

Test PhaseWithin-group comparisons. To examine infants’ sen-

sitivity to temporal synchrony in a syllable–object pairingfollowing habituation, their mean looking time to thesyllable-change and the object-change trials were comparedwith the no-change posthabituation trials within each group.For the term infants at 2 months, a one-way repeatedmeasures ANOVA of trial type (3: mean posthabituation,syllable-change trials, and object-change trials) revealed ahighly significant main effect, F(2, 66) = 20.35, p < .0001.Figure 3 shows the term infants’ mean looking time by trialtype.

In contrast, for the preterm infants at 2 months chro-nological age, a one-way repeated measures ANOVA of trialtype (3: mean posthabituation, syllable-change trials, and



object-change trials) revealed only a marginally significantmain effect, F(2, 66) = 3.08, p = .06. Similarly, for the pre-term infants at 2 months corrected age, a one-way repeatedmeasures ANOVA of trial type (3: mean posthabituation,syllable-change trials, and object-change trials) revealed nomain effect, F(2, 30) = 1.62, p = .22. Figure 3 shows the meanlooking time by trial type for the preterm infants at 2 monthschronological and corrected ages.

Between-group comparison of preterm and term infants.For the purpose of between-group comparisons, for eachof the three groups, first, we computed the visual recoveryscores for syllable- and object-change trials by subtractinginfants’ mean looking time to the two no-change post-habituation trials from their mean looking time to thetwo syllable-change and two object-change trials. Analysesof the distribution of these individual visual recovery scores(positive and negative) to syllable change revealed that 28of the 34 term infants (82%, binomial distribution versuschance [.5], exact p = .0001) showed a positive visual recovery,whereas only 20 of the 34 preterm infants at chronologicalage 2 months (59%, binomial distribution versus chance,exact p = .39) and 10 of the 16 preterm infants at correctedage 2 months (63%, binomial distribution versus chance,exact p = .48) showed a positive visual recovery score. Anal-yses of the distribution of visual recovery scores to objectchange revealed that 30 of the 34 term infants (88%, binomialdistribution versus chance, exact p = .0001) showed a positivevisual recovery, whereas only 20 of the 34 preterm infantsat chronological age 2 months (59%, binomial distributionversus chance, exact p = .39) and 7 of the 16 preterm infantsat corrected age 2 months (43%, binomial distribution versuschance, exact p = .84)3 showed a positive visual recoveryscore.

Next, we assessed whether at 2 months chronologicaland corrected ages, the preterm infants’ visual recoveryscores to syllable and object changes were attenuated relativeto those of the term infants. These two mean visual recoveryscores were subject to a multivariate analysis of covariance(the general linear model procedure accounted for unequal

variances), where group (3) was the between-subjects factorand the total time taken to habituate was the covariate. Forthe visual recovery to syllable change, the analysis revealeda significant main effect of group, F(2, 80) = 4.42, p = .015,h2 = .10, observed power = .75; but no effect of the covariate,F(1, 80) = 0.26, p = .61, h2 = .003, observed power = .08.Post hoc analyses of the group effect (Bonferroni multiplecomparison, a = .05) revealed that the visual recovery tosyllable change of the term infants was significantly greaterthan that of the preterm infants at 2 months chronologicalage (adjusted mean difference = 6.74 s, p = .03) but not at2 months corrected age (adjusted mean difference = 6.15 s,p = .13; see Figure 4). For the visual recovery to objectchange, the analysis once again revealed a significant maineffect of group, F(2, 80) = 6.58, p = .002, h2 = .14, observedpower = .90; but a marginal effect of the covariate, F(1, 80) =3.49, p = .07, h2 = .04, observed power = .46. Post hocanalyses of the group effect (Bonferroni multiple comparisona = .05) revealed that the visual recovery to object changeof the term infants was significantly greater than that of thepreterm infants at 2 months chronological age (adjusted meandifference = 5.76 s, p = .05) and corrected age (adjustedmean difference = 9.5 s, p = .003; see Figure 4 for actualmean difference).

The lack of statistically significant or marginal covar-iate effects suggests that infants’ duration of attention toa synchronous syllable–object pairing during habituationlearning did not significantly predict their test performance.Consequently, even after factoring out the variance ininfants’ attention to the synchronous syllable–object pairingduring habituation across groups (i.e., accounting forthe extant covariate effect), the analyses yielded signifi-cant differences between term and preterm infant groups.At 2 months chronological and corrected ages, preterminfants showed attenuated visual recovery to the syllable andobject changes on the subsequent test relative to their termcounterparts.

Longitudinal comparison of preterm infants at 2 monthschronological and corrected ages. To assess whether testperformance of the preterm infants improved with age, weperformed a multivariate analysis of variance including onlythe longitudinal sample of 12 preterm infants at 2 monthschronological and corrected age. In this analysis of the visualrecovery to object and syllable change, group (2) was the

Table 1. Habituation phase: 2-month-old term and preterm infants’ looking time and standard deviations to a temporally synchronous syllable–object pair.

MeasureTerm infants

(n = 34)Preterm infants CRA

(n = 34)Preterm infants CA

(n = 16)

Mean of first 2 habituation trials (baseline) 39.45a (8.03) 21.99b (7.90) 36.05a (9.33)Mean of the last 2 habituation trials 9.27a (4.07) 6.37b (3.46) 11.51a (4.72)Mean seconds to reach habituation criterion 244.54a (101.60) 138.77b (68.53) 305.86a (149.54)Mean number of trials to habituate 9.53 (3.51) 8.79 (3.22) 11.37 (4.76)

Note. CRA = chronological age; CA = corrected age.a,bWithin-variable Bonferroni comparisons, p < .05.

3These individual percentages of positive visual recovery do not predict ahigh success rate for preterm infants at corrected age even with a largersample size.



within-subjects factor, and the total time taken to habituatewas the covariate. The analysis revealed no main effect ofgroup for the visual recovery to object change, F(1, 21) =0.032, p = .86; or to syllable change, F(1, 21) = 0.68, p = .41;nor was there a covariate effect, F(1, 21) = 1.38, p = .26(Figure 5), suggesting no greater sensitivity to a synchronoussyllable–object pairing with age.

Pretest–posttest ratio comparison across groups. Toassess for possible group differences in infants’ level ofalertness-fatigue during the procedure, we performeda one-way ANOVA by group (3) of the ratio of infants’ looksto the last (posttest) turtle display over their looks to the

first (pretest) turtle display. Once again, we used the generallinear models procedure to account for the unequal variancesin each group. The analysis yielded no significant main effect,F(2, 81) = 0.69, p = .50.

DiscussionThe present findings demonstrate, first of all, that

relative to term infants, even borderline preterm infants, ofgestational age 32 to 36 weeks, show attenuated perceptionof an organized audiovisual event characterized by inter-sensory invariance, in the form of synchrony, between a

Figure 3. Two-month-old preterm (chronological and corrected ages) and term infants’ mean looking in seconds(and standard deviations) during and after habituation to a synchronous syllable–object display by trial type.CRA = chronological age; CA = corrected age. Paired t test, *p < .01.

Figure 4. Infants’ visual recovery (mean looking time to change trials minus mean looking time to no-changeposthabituation trials) to syllable and object change on test. CRA = chronological age; CA = corrected age.a,bWithin-variable Bonferroni multiple comparisons, p < .05.



spoken syllable and a handheld moving object. During theinfant-controlled habituation procedure, although all infantswere given equal opportunity to experience the videos, thepreterm infants, at chronological age 2 months, showedattenuated initial attention to the synchronous syllable–objectpairing (21.10 s) relative to term infants (39.45 s; see baseline,Table 1). This attenuated attention persisted throughout thehabituation process. Whereas the preterm infants at 2 monthschronological age attended to a synchronous syllable–objectpairing for an average of 138.77 s, the term infants attended tothe pairing for a longer time period (244.54 s; see Table 1).

These attention differences during habituation, how-ever, did not significantly predict visual recovery to thechanges on the test. Thus, after factoring out infant attentionduring habituation, on the test trials, we found that thepreterm infants still showed attenuated visual recovery toa change in the syllable and in the object relative to theirterm counterparts. In contrast, the term infants successfullyattended to the synchronous syllable–object pairing duringhabituation and showed a significant visual recovery to thesevery same changes. These results were reflected in the indi-vidual statistics as well. Whereas 82% of the term infantsshowed a positive visual recovery to the syllable change and88% to the object change, only 59% of the preterm infantsshowed a positive visual recovery to the syllable change andthe object change.

Next, the findings suggested that at 2 months correctedage as well, these preterm infants (12 infants provided lon-gitudinal data) continued to show attenuated visual recoveryto the changes in the syllable and the object on the test fol-lowing habituation to a spoken syllable and a synchronoushandheld moving object, relative to their visual recovery at2 months corrected age (Figure 5). When the larger sampleof 16 infants were considered, although duration of attentionduring habituation increased, from chronological age tocorrected age 2 months, it did not result in a correspondingincrease in visual recovery with development (see Figure 4),once again suggesting detrimental learning effects arisingfrom the attenuated sensitivity to the synchronous syllable–

object pairing. The preterm infants showed an improving,albeit insignificant, trend in their visual recovery to syllablechange from chronological age to corrected age but showedno such trend in their visual recovery to object change. Theseresults were evident in the individual statistics as well, withonly 63% of the infants at corrected age showing a positivevisual recovery to the syllable change and 43% to the objectchange. Given the reports on earlier developing vision inpreterm infants because of early environmental exposure(e.g., Hunnius et al., 2008), one might expect that, at corrected2 months, the preterm infants would detect changes in theobject better than at chronological age 2 months. It wastherefore surprising that the infants in the present sample didnot meet this expectation (see Figures 4, between-groupanalyses, and Figure 5, within-group analyses). It is possiblethat for preterm infants, the early auditory experience resultedin a tendency toward early auditory dominance also seenin term infants early on (Gogate et al., 2009; Lewkowicz,2002).

Furthermore, as discussed earlier, the preterm infants,at 2 months chronological age, attended far less to the syn-chronous syllable–object display relative to the term infantsthroughout the habituation process. This lower attention(shorter habituation duration) in very young preterm infants,although not unexpected (Weijer-Bergsma, Wijnrocks, &Jongman, 2008; also see review by Kavšek & Bornstein,2010), is in stark contrast to prior findings from term infantsfor whom faster habituation (also correlated with develop-ment and age; Pecheux & Lecuyer, 1989) is associated withbetter learning outcomes (Colombo, 2001, 2002).

The present finding on lower attention (shorter habit-uation duration), indicating attenuated sensitivity to a syn-chronous syllable–object display, at 2 months chronologicalage also differs from prior findings of older preterm infants.For these infants, a greater number of trials and longer timeto habituate to visual stimuli relative to term infants is as-sociated with slower processing speed (Rose, 1983; Roseet al., 2002). The shorter habituation duration of preterminfants at chronological age 2 months in the present studycannot therefore be attributed to efficient processing of thesynchronous syllable–object display, given that these infantsdemonstrated compromised discrimination of syllables andobjects on the test. Neither can longer habituation durationat corrected age 2 months be attributed to efficient process-ing, given that these infants as well demonstrated compro-mised discrimination on the test.

Thus, in accord with our alternative prediction, thecontinued attenuated sensitivity to a synchronous syllable–object pairing and subsequent attenuated visual recovery tosyllable and object changes on the test suggest that the highlycompromised neurosensory system is simply not ready todetect synchronous auditory–visual information even at2 months corrected age. Consequently, near-term pretermsmay not perceive a synchronous auditory–visual event as aunified event in the same manner as term infants. Rather,sensitivity to synchrony likely develops much later in pretermrelative to term infants who detect synchrony at birth (e.g.,Lewkowicz et al., 2010). Premature infants’ compromised

Figure 5. Preterm infants’ visual recovery (mean looking time to changetrials minus mean looking time to the no-change posthabituationtrials) to syllable and object change on test trials in the longitudinalsample (n = 12) at 2 months chronological age (CRA) and correctedage (CA).



neurosensory systemneeds farmore real-time interactionwiththe multisensory environment to compensate for the delayin synchrony perception. Fantz and Fagan (1975) made asimilar observation in their comparative study of termand low-risk preterm infants’ visual perception: “Evenwithout a difference in the environment [without lengthyhospitalization], the preterm infant may be unable to profitfrom the experiential opportunities in ways that wouldinfluence perceptual development until after further matu-ration of the eye and brain” (p. 12).

The present findings from near-term 2-month-oldpreterm infants taken together with those of several otherspoint to a domain-general perceptual delay in intersensoryinvariance detection. Here, preterm infants showed attenu-ated sensitivity to a synchronous syllable and a movingobject, a word learning context. Others have demonstratedthat older preterm infants show attenuated sensitivity tosynchrony between faces and voices (e.g., Pickens et al.,1994) and moving objects and their sounds (e.g., Lawsonet al., 1984), relative to term infants.

The present findings from term infants replicate thefindings of a prior study of 2-month-olds that demonstratedthat term infants are sensitive to a synchronous syllable–object pairing. In this previous study as well, term infantsshowed a highly significant visual recovery to a syllable andan object change following habituation to a single syn-chronous syllable–object pairing (Gogate et al., 2009). Thepresent findings from term infants are also consistent withearlier findings that term infants are highly sensitive tointersensory invariance in the form of temporal synchrony inauditory–visual speech events in the first few months of life.For example, 2-month-old infants use voice and lip move-ment synchrony to match faces and voices (e.g., Dodd,1979; Patterson & Werker, 2003). As a further example, by3.5 months, infants become adept at matching the emotionexpressions (e.g., happy or sad) of their mother across faceand voice, again on the basis of their everyday experience withinvariant information, including synchrony between themothers’ face and voice (Montague & Walker-Andrews,2002). It must be noted, however, that although term infantsperceive synchrony in auditory–visual speech events, we arenot suggesting that they perceive the stimuli linguistically.Rather, they use a low-level, general-purpose synchrony-detectionmechanism to perceive the co-occurrence of auditory–visual signals (see Hollich, Newman, & Jusczyk, 2005). Insummary, what is clear from the present study is that whereasyoung term infants use this synchrony detection mechanismin numerous contexts, including communication, to makesense of their multisensory world, preterm infants showattenuated ability to use this mechanism at a very early age.

Extending the present findings from 2-month-oldpreterm infants and those of older infants from Pickens et al.(1994) to a broader language-learning context, we surmisethat the delay in preterm infants’ sensitivity to synchronousword–object pairings relative to term infants might indexfuture delays in word mapping and comprehension. In par-ticular, we predict that older preterm infants will experiencedifficulty mapping words onto objects in natural naming

contexts where caregivers use a great deal of synchronybetween spoken words and object motions (Gogate et al.,2000, 2006; Jesse & Johnson, 2008). Consistent with thisprediction, although mothers of 6- to 9-month-old preterminfants used a great deal of synchrony in naming contexts,the infants demonstrated an inability to learn the names forobjects on test, likely once again owing to a delay in detectingthe synchrony (Gogate et al., 2011).

The present research is limited to near-term births anddoes not follow up on infants over the long term to determinetheir language outcomes. Further longitudinal examinationsof older preterm infants in word-mapping contexts are war-ranted to directly assess the extent of the delay in synchronydetection, in near-term and very preterm infants born priorto 32 weeks’ gestation. The generalizability of the synchronydetection delays in word-mapping contexts observed innear-term low-risk preterm infants to infants born below32 weeks of gestation deserves focused attention in researchusing this highly vulnerable population. Longitudinal assess-ments in the 1st, 2nd, and 3rd years are also necessary toexamine the potential link between preterm infants’ attenuatedsynchrony detection in word-mapping contexts early on andvocabulary development in the 2nd year and beyond. Theremay well be an observable long-term effect of attenuatedsynchrony detection, in word-mapping contexts (Gogateet al., 2011), on delayed lexical morphology (Le Normand &Cohen, 1999).

Alternatively, a missed opportunity for synchronydetection and the learning of word mappings in the 1st yearmight lead to alternative developmental paths for learningthese relations in preterm relative to term infants (Gogate &Hollich, 2013). Future studies must be designed to elucidatethe different developmental paths that preterm and terminfants’ auditory–visual perception might take en route tolanguage development. One way to elucidate this develop-mental path, given the salience of synchrony in word-mappingcontexts for typically developing infants, might be to inves-tigate whether caregivers naturally name objects in synchronywith gestures to 2-month-old term but not to preterm infants.Such investigations would attest to the ecological validityof the present findings.

AcknowledgmentsThis research was supported by the Thrasher Research Fund

(02819-1); a Dean’s Research Initiative award, College of Medicine,SUNY Health Science Center at Brooklyn; and a March ofDimes Birth Defects Foundation grant (12-FY08-155) to LakshmiGogate. We thank Stanley Fisher, Eugene Dinkevich, and JoanHittelman for their support of this research. Our special thanks go tothe mothers who participated with their infants. We are especiallygrateful to Dalit Matatyaho, Divya Awal, Li-Fen Chen, Linda Yoo,Samantha Berkule, and Elsa Lee for their help with data collectionand analyses.

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