347
The
British
Psychological
British Journal of Developmental Psychology (2010), 28, 347-368
©2OiO The British Psychohsicai Society • ! * — f ^ Society
www.bpsjournals.co.uk
A comparison of dyadic interactions and coping
with still-face in healthy pre-term and full-term
infants
Rosario Montirosso'*, Renato Borgatti', Sabina Trojan^,
Rinaldo Zanini^ Ed Tronick^"*'^
'Department of Child and Adolescent Neurology and Psychiatry and Italian NNNS
Centre for Infant Neurobehavioural Study, Scientific Institute 'E. Medea', Bosisio
Parini (Lecco), Italy
^Neonatal Intensive Care Unit, Manzoni Hospital, Lecco, Italy
^Department of Psychology, University of Massachusetts, Boston, USA
"•child Development Unit, Children's Hospital Boston, Harvard Medical School,
Boston, Massachusetts, USA
^Fielding Graduate University, Santa Barbara, California, USA
Pre-term birth has a significant impact on infants' social and emotional competence,
however, little is known about regulatory processes in pre-term mother-infant dyads
during normal or stressful interactions. The primary goals of this study were to
investigate the differences in infant and caregiver interactive behaviour and dyadic
coordination of clinically healthy pre-term compared to full-term infant-mother dyads
and to examine pre-term infants' capacity for coping with stress using the face-to-face
still-face paradigm (FFSF). Fifty mother-infant dyads, including 25 pre-term infants and
25 full-term infants were videotaped during the FFSR All infants were 6-9 months ofage
(corrected for gestational age in the pre-term group). Infant and maternal socioemotional expressivity and self-regulatory behaviours were coded and measures of
dyadic coordination {Matching, Reparation Rate, and Synchrony) were calculated. There
were no significant differences in infant and caregiver socio-emotional behaviours
between the two groups and both groups demonstrated the still-face (SF) effect and the
reunion effea. There was a difference in self-regulatory behaviour. Pre-term infants were
more likely than full-term infants to use distancing (e.g., by turning away, twisting, or
arching) from their mothers during the FFSF. Additionally, during the Reunion episode
of the FFSF pre-term infants showed more social monitoring compared to full-term
infants. Regardless of the birth status, the dyads showed less coordination and a slower
rate of reparation during the Reunion episode than during the Play episode. The higher
proportion of distancing in the pre-term group and the increase in social monitoring
* Correspondence should be addressed to Dr Rosario Montirosso, Scientific Institute ' £ Medea', Via don Luigi Monza,
20 - 23842, ßosisio Parini. Lecco, Italy (e-mail: rosario.montirosso@bp.lnf.it).
DOI: 10.1348/026151009X416429
348
R. Montírosso et al.
suggest that even in normal interactions pre-term infants may experience a higher level
of stress and have less capacity for self-regulation compared to the full-terms and that
pre-term infants appear to use a compensatory strategy of increased social monitoring
to cope with the stress of renegotiating the interaction during Reunion. The findings
suggest that pre-term infants have different regulatory and interactive capacities than
full-term infants.
Pre-term birth is considered to have a subtle but potentially significant impact on
infants' social and emotional development (Field, 1987; Lowe, Woodward, & Papile,
2005; Macey, Harmon, & Easterbrooks, 1987; Minde, Whitelaw, Brown, & Fitzhardinge,
1983), In addition, previous studies have found that pre-term infants' have difficulty
regulating their behavioural states (Wolf et al, 2002), less capacity for self-quieting
(Thoman & Graham, 1986), and limited capacities for coping with stress (Als, 1983),
Taken together, these factors, along with others (e,g,, early separation), increase the
risk for abnormal development of the mother-infant relationship in pre-term infant
mother dyads (Feldman, Weiler, Sirota, & Eidelman, 2003; Muller-Nix et al, 2004),
because they are likely to affect the quality and the dyadic coordination of the
interaction (Feldman, 2006; Korja et al., 2008), Although, previous research has found
that prematurity affects mother-itifant synchrony during face-to-face interactions
(Feldman, 2006; Feldman & Eidelman, 2007; Lester, Hoffman, & Brazelton, 1985) little
is known about the quality of dyadic processes such as matching, mismatching, and
reparation in pre-term dyads. Thus, the primary goals of this study were to investigate
differences in interactive behaviour and dyadic coordination of clinically healthy preterm compared to full-term infant-mother dyads as well as pre-term infants' capacity
for coping with stress.
Our thinking was framed by the mutual regulation model (MRM; Gianino & Tronick,
1988; also see Fogel, 1993; Sander, 2000). The MRM argues that the interaction is
organized by a bidirectional exchange of communicative signals that are used by the
infant and the caregiver to coordinate the interaction and to cope with the stress of
inevitable interactive miscoordinations. From this perspective, the quality of the
interaction is determined by the ability of each participant to cope with external
Stressors, regulate his/her emotional states, express communicative messages, and
respond to his/her partner's affective communications and regulatory needs,
Caregivers' behaviour is guided by itifants' expressive displays (e,g,, gaze, facial
expressions, gestures, and vocalizations). In turn, itifant behavioural and affective states
are affected by the expressive displays of the caregiver, Tronick and Gianino (1986)
hypothesized that infants, and especially pre-term infants (Als, 1983; Mouradian, Als, &
Coster, 2000) have limited regulatory capacities and, therefore, need their caregivers'
regulatory scaffolding to maintain affective regulation and cope with interactive stress.
Thus, we expected differences in pre-term infant-caregiver expressivity and interactive
coordination and differences in the pre-term infant's self-regulatory coping capacity
compared to full term infants.
Studies have found that during thefirstyear of life itifants born prior to term compared
to full-term infants are less responsive and attentive, make fewer vocal and affective
signals, are fussier, and have lower scores on the clarity of their social cues
(Crawford, 1982; Crnic, Ragozin, Greenberg, Robinson, & Basham, 1983; McGehee &
Eckerman, 1983), Pre-term infants evidence more negative affect and gaze aversion
Pre-term infants in still-face paradigm 349
during dyadic interactions (Van Beek, Hopkins, Hoeksma, & Samsom, 1994) and they are
more difficult to arouse to an attentive state and tend to avoid social stimulation (Field,
1981). In contrast, pre term infants have been described as relatively competent in their
interactive behaviour (Schermann-Eizirik, HagekuU, Bohlin, Persson, & Sedin, 1997) and
as more responsive to vocal and affective signals (Barratt, Roach, & Leavitt, 1992)
compared to full-terms.
Maternal social sensitivity is another factor influencing the infants' social experience,
socio-emotional development and the infant-mother relationship. When the infantmother interaction is viewed as a process of mutual regulation (Tronick, 1989) and if
pre-term infants are less clear in their affective communicative signals, one would
expect pre-term infants to require more sensitive tuning of maternal emotional
responsivity and regulatory scaffolding to maintain attention and positive affect (Als,
1983). However, research on the expressive behaviour and responsiveness of mothers
of pre-term infants is conflicting. Researchers have found that mothers of pre-term
infants compared to mothers of full-term itifants are more stimulating (Crawford, 1982;
Crnic et al., 1983; McGehee & Eckerman, 1983) and display less sensitivity to their
infants' affective cues (Feldman & Eidelman, 2007; Malatesta, Grigoryev, Lamb, Albin, &
Culver, 1986). On the other hand, compared to mothers of full-term infants, mothers of
pre-terms have been found to be more responsive (Barratt etal., 1992; Greene, Fox, &
Lewis, 1983) and to show better performance on interactive measures (SchermannEizirik etal., 1997). Part of the discrepancy in ñndings may be related to differences in
measurement and definitions.
Mother-infant dyadic regulatory processes have been defined in a number of
different ways in the literature but have not been examined in pre-term dyads. Studies of
full-term mother-infant dyads have focused on mothers' and infants' ability to change
affective or behavioural states in temporal coordination with one another (synchrony),
to share the lead in interaction (bidirectionality) and to share joint attentional, affective,
or behavioural states at the same moment in time (matching; Beebe & Lachmann, 2002;
Cohn & Tronick, 1987; Feldman, Greenbaum, & Yirmiya, 1999; Jaffe, Beebe, Feldstein,
Crown, & Jasnow, 2001; Tronick & Cohn, 1989). However, interactions are not always
smoothly coordinated but are characterized by interactive mismatching (Gianino &
Tronick, 1988). Mismatching occurs when the infant and the mother are in different
behavioural states (e.g., infant looking and smiling at the mother and the mother looking
away with a neutral facial expression). Tronick (1989) has shown that mismatches are
associated with interactive stress and Tronick and Cohn (1989) found that mothers and
infants spend most of their playtime in mismatching states. However, most mismatches
were corrected in the next interactive step. The process of changing from mismatching
to matching states is referred to as reparation (measured as the rate of change between
matching and mismatching). From the perspective of the MRM (Tronick, 1989, 2003)
reparation resolves the interactive stress of a mismatch and is a key interactive process
that affects the development of the infant's sense of trust in the mother, self-regulation
and coping with stress (Feldman, Greenbaum etal., 1999; Tronick, 2004). Based on the
research on pre-term infants and their mothers, we expected that pre-term dyads would
have less matching of their interactive states, fewer reparations and would likely
develop different ways of coping with the stress of mismatching compared to full-terms.
Many other factors also come into play that may disrupt the organization of the
dyadic co-regulatory system. For example, maternal-itifant separation caused by
standard incubator care along with the stress of medical procedures (Anand & Scalzo,
2000; Feldman, Weiler, Leckman, Kuint, & Eidelman, 1999) are among the negative
350
R. Montirosso et al.
sequelae of pre-term birth. These conditions are Ukely to decrease the opportunities
for mothers to act as effective external organizers or regulators of the infant's
socio-emotional and behavioural states (Als et al, 2004; Eckerman, Hsu, Molitor, Leung,
& Goldstein, 1999; Hofer, 1994; Spangler, Schieche, Ilg, Maier, & Ackermann, 1994).
Thus, aversive conditions affecting early caregiving interactions can lower level of
coordination observed between mothers and premature infants during the first 6 months
of life (Feldman & Eidehnan, 2007). For example, in a group of low- to high-risk infants
(3-5 months of age) Lester et al. (1985) found that pre-term infant-mother dyads were
less able to coordinate their behavioural cycles of affect and attention during face-to-face
social exchanges compared to full-term pairs. Feldman (2006) examined Unks between
neonatal biological rhythms (sleep-wake cyclicity and cardiac vagal tone activity) and
the emergence of interaction rhythms (mother-infant synchrony computed from
microanalysis of face-to-face interactions at 3 months of age). She found that high-risk
premature infants displayed disorganized biological rhythms, lower levels of dyadic
synchrony, a more limited capacity for arousal modulation, and lower thresholds for
negative emotionality. Although, the low risk group of pre-term infants did not differ
from the full-term group on the continuous measures of synchrony and neonatal
orientation, they scored significantly more poorly than the full-term group on negative
emotionality and arousal modulation. In contrast, in a recent micro longitudinal study
Korja et al (2008) found that mother-infant interaction was comparable between preterm and full-term infants at 6 and 12 months of age. Perhaps, the differences seen in
younger infants disappear by the second half of the first year of life.
Differences between full-term and pre-term infants in socio-emotional behaviours
(SEB) have been examined during several types of adult-infant interactions: feeding
(Minde et al, 1983; Singer et al, 2003), undressing the infant (Schermann-Eizirik et al,
1997), and face-to-face play interactions, including peek-a-boo (Eckerman, Oehler, &
Medvin, 1994; Forcada-Guex, Pierrehumbert, Borghini, Moessinger, & Muller-Nix,
2006). However, few studies have studied a context that involves interactional stress or
challenge, yet a stress places different demands on the communicative and social
abilities of the infants, mothers, and dyads and may bring out differences not seen in
non-stressful contexts. For example, Malatesta, Culver, Tesman, and Shepard (1989)
recorded face-to-face interaction involving play and separation/reunion sessions in preterm and full-term infants at 2.5, 5, 7.5, and 22 months. They reported that stressful
situations compared to non-stressful situations and that pre-term birth altered infant
affective expressions and maternal contingency levels.
However, almost no studies have specifically addressed pre-term infants' abilities to
coordinate and repair interactions or their emotional regulation during a stressful
situation. This lack of research is in part due to researchers having few paradigms for
examining infants coping with stress in early infancy (Lewis, Hitchcock, & Sullivan,
2004). One paradigm that has been established as a standard method is the face-to-face
still-face paradigm (FFSF; Adamson & Frick, 2003; Troniek, Als, Adamson, Wise, &
Brazelton, 1978). It is well established that the FFSF is a pow^erful paradigm for
examining infants' socio-emotional competence and abuity to cope with stress (for an
overview see, Adamson & Frick, 2003) and several studies have demonstrated that the
effect of the still-face (SF) is robust among different groups of infants, including both
lo-w- and high-risk samples (Adamson & Frick, 2003; Troniek et al, 2005). During the
FFSF paradigm, infants engage in normal face-to-face interaction -with their caregiver and
also confront the perturbation of the caregiver remaining poker-faced and unresponsive
(SF). Thus, the FFSF paradigm allows for the evaluation of both infants and mothers'
Pre-term infants in still-face paradigm
351
affective and regulatory behaviour and dyadic characteristics during normal interaction
(Play episode), infants' coping capacities during the stress of the SF (SF episode), and
their coping and regulation during the resumption of the normal interaction (Reunion
episode), when mothers and infants must re-establish and repair the interaction
following the stress of the SF. During the SF episode, infants show a typical signature
response known as the SF effect (Adamson & Frick, 2003). They show a dramatic
decrease in smiling, more gaze aversion, and an increase in negative affect. In addition,
infants repeatedly attempt to re-engage the adult by smiling and gesturing while looking
at the interaction partner. When these attempts fail, infants show an increase in negative
affect, gazing away, and self-comforting behaviours. Following the SF in the Reunion
episode, infants show an increase in smiling and eye-contact. However, some studies
show that there is a carry-over of negative effect from the SF episode to the Reunion
episode, indicating that the itifants have to cope with the stress from the SF during the
Reunion episode. The carry-over of negative affect has been labelled the reunion effect
(Adamson & Frick, 2003).
To our knowledge, only one study has looked at the pre-term mother-infant pairs using
the FFSF Segal etal. (1995) used it with groups of black pre-term and full-term motherinfant pairs from middle and lower income levels. No differences in negative affect were
found between groups, but pre-term infants spent less time displaying smiles than fullterms. The premature infants showed the SF effect w'tíh a significant reduction in smiling
from Play to the SF episode, confirming that healthy pre-term infants, like full-terms, have
developed expectations about social interactions. Unfortunately, there was no evaluation
of the mothers' interactive behaviour or the dyadic characteristics of the interactions.
This study evaluated the effects of premature birth and interactional context on
mother-infant affective expressiveness and the dyadic features of their interactions.
Since, differences in levels of social engagement and the quality of maternal
responsiveness have been found between premature infants born at low^ and high
medical risk (Greene et al, 1983; Landry, Chapieski, Richardson, Palmer, & Hall, 1990;
Landry, Smith, Miller-Loncar, & Swank, 1998), we chose to assess healthy pre-term
infants with birth weight appropriate for gestational age, normal psychomotor
development, and a documented absence of brain damages. At the time of testing infants
ranged in age from 6 to 9 months (corrected for gestational age in the pre-term group).
Though this is, a wider age range than used in other studies, we did not expect the age
range to affect our results for several reasons. A number of studies have found that after
the age of 6 months, the SF effect and reunion effect become stable (see Adamson &
Frick, 2003). For example, Striano and Rochat (1999) found no significant age effects on
infant behaviour in the FFSF between 7- and 10-month-olds suggesting that ways of
coping become characteristic of the infant by 6 months of age. Mother-infant dyadic
coordination also is very similar at 6 and 9 months of age (Tronick & Cohn, 1989).
Furthermore, by the second half of theirfirstyear of life, pre-term infants have had more
of a chance than younger pre-term infants to get catch-up developmentally with fullterm infants (Brachfeld, Goldberg, & Sloman, 1980).
From the perspective of the MRM and the literature we expected that pre-terms, as
compared to full-term infants, would evidence less social attentiveness, more negative
and fewer positive affects, and fewer self-regulatory behaviours during the FFSF
paradigm. Second, despite the contradictory empiricalfindingsabout the impact of preterm birth on the mothers' SEB, we expected that mothers of pre-term infants would use
different strategies to help their infants regulate affective states compared with mothers
of full-terms because of the expected differences in their itifants' communicative and
352
R. Montirosso et al.
regulatory behaviours. The research, however, does not allow for a more specific
hypothesis about the form of such differences (e.g., more or less maternal interest or
positive affect). Third, we expected that the dyadic organization of the interaction
would be different among pre-term dyads compared to full-term dyads. In line with
previous SF research (Tronick & Cohn, 1989; Weinberg, Tronick, Cohn, & Olson, 1999)
three measures of coordination (i.e., Matching, Reparation Rate, and Synchrony) were
used to assess the mother-infant dyadic processes. We expected that pre-term dyads, as
compared to full-term dyads, w^ould evidence less synchrony (Lester et al., 1985;
Feidman, 2006). Based on the MRM, we also expected that pre-term dyads compared to
full-term dyads would show less matching and fewer reparations of behavioural and
affective states. Fourth, w^e sought to identify some of the factors (gender, birth status,
developmental quotient, level of maternal depressive symptomatology, socio-economic
status (SES), and maternal SEB) associated with infant SEB during SE Regardless of the
extent to which the data support these hypotheses, thefindingsfrom this study will add
to our understanding of the regulatory capacities of pre-term infants and mothers, the
dyadic features of their interaction and the effects of stress on the infant and the mother.
Method
Participants
Fifty mother-infant dyads, 25 healthy pre-term infants (11 females) and 25 full-term
infants (12 females) participated in the study. All the infants were between 6.8 and
99 months of age (corrected for gestational age in the pre-term group). The pre-term
infants were recruited consecutively from all the infants, born between August 2002
and February 2003 in the NICU at 'A. Manzoni' Hospital, Lecco Gtaly), w^ho met the
following criteria: gestational age (GA) less than i6^^^ weeks (range: 26-36 weeks),
birth weight less than 2,500 g (range: 845-2,450 g), and an absence of serious
medical complications (e.g., grade I intraventricular hemorrhage, any degree of
periventricular leukomalacia, any degree of hearing or visual impairments, congenital
abnormalities). Their mothers were excluded if they were at psychosocial risk due to
a history of drug abuse, mental illness, or had high levels of depressive symptoms
(i.e., greater than the cut-off level on the Beck Depression Inventory [BDI]; Beck,
Ward, Mendelson, Mock, & Erlbaugh, 1961). Twenty-eight (93%) of the 30 eligible
mothers of pre-term infants, we contacted agreed to participate. Three pre-terms
were excluded because they became too distressed to complete the experimental
procedures. Two w^ere members of twin pairs.
Healthy full-term participants were recruited during the same time period from a
list of possible full-term infants obtained from community paediatricians. Selection
criteria for control subjects were: full-term gestation (> 37 weeks, GA range: 37-41),
appropriate weight for GA (birth weight > 2,500, range: 2,540-3,840 g), Apgar scores
of at least 7 at 1 min and 8 at 5 min, no congenital abnormalities, and uncomplicated
prenatal, perinatal, and neonatal courses. Their mothers met the same criteria used
for the mothers of the pre-term participants. Twenty-five (71%) of the 35 mothers of
eligible full-term infants contacted agreed to participate. No fuU-term infants were
members of twin pairs. No full-term infants had to be excluded because of distress
during the procedures. The infant and maternal characteristics of both groups are
reported in Table 1. As can be seen, the selection criteria for both groups resulted in
clinically healthy samples.
Pre-term infants in stili-face paradigm
353
Table I . Infants' and maternal characteristics
Full-term dyads
(N = 25; F = 11)
Characteristics
Infant
G A at birth (v^eeks)
Birth v^^eight (grams)
Age (months)*
Brunet-Lezine score
Maternal
Age (years)
Education (years)
SES
BDI score
Pre-term (dyads
(N = 25; F = 12)
Mean
SD
Mean
SD
39.9
3,293
9,0
101.1
1.2
382
I.I
5.3
32,1
1,516
9.3
100,1
2.8
483
1,2
8,6
33
14.0
68
5.5
4.7
2.9
17.4
3.4
32
12,3
61
4,6
3,6
2,8
23,8
2,4
Note, *GA, gestational age corrected for GA in the pre-term infants; F, female; SES, socio-economic
status; BDI, Beck depression inventory.
Procedure
Mothers of potential participants (pre-terms and full-terms) were recruited by phone.
Participation was voluntary. They were told that the study concerned infant-mother
interactive and communicative behaviour. Mothers who expressed an interest in
participating in the study were scheduled to visit the laboratory of the 'E. Medea'
Scientific Institute at a time when they thought their infants would be rested and alert,
usually between 9 a.m. and noon. The protocol included the video-recording the
mother-infant interaction in the FFSF, completion by the mother of a socio-demographic
questionnaire, a clinical report form, and the BDI, The study was approved by the Ethics
Committee of the 'E, Medea' Scientific Institute and written informed consent was
obtained from all the mothers.
Measures
SES
SES was coded according to the information provided by caregivers on the basis of
Hollingshead's (1975) classification for parental occupation.
Developmental quotient
Developmental quotient (DQ) was determined by the Brunet-Lézine's scale (Brunet &
Lézine, 1955), a widely used, standardized measure that provides general indexes of
mental and psychomotor development relative to group norms in itifants aged 4 months
to 5 years. The Brunet-Lezine is based on early descriptive research by Gesell (Gesell &
Amatruda, 1947), It has well-established reliability and validity. The scale evaluates the
child's development in four areas: posture and gross motor function, eye-hand and finemotor coordination, language, and social reactions. Scores above 90 are considered
normal, 80-90 are below average (i,e,, lo'w normal), 70-79 are considered borderline,
and scores below 70 represent some degree of mental retardation.
354
R. Montirosso et al.
Maternai depression
Maternal depression was evaluated with the BDI (Beck etal., 1961). The BDI is a 21-item
measure of depressive symptoms. Items are rated on a four-point rating scale, indicating
the absence/presence and the range of severity of depressed feelings/behaviours/symptoms. The BDI demonstrates good internal consistency and has concurrent and
discriminant validity in clinical and non-clinical samples (Beck, Steer, & Garbin, 1988).
A score of greater than 12 was used as the cut-off for the clinical range (O'Hara, Rehm, &
Campbell, 1983).
Laboratory setting
FFSF interactions
Caregivers and infants were videotaped during the FFSF procedure, based on the
original paradigm developed by Tronick et al. (1978). The video room was equipped
with a high chair, an adjustable sw^ivel stool for the caregiver approximately 40 cm from
the infant, two cameras (one focused on the infant, the other on the caregiver), and a
microphone. The paradigm is made up of three 2 min episodes: (a) a 2 min face-to-face
play interaction (Play); (b) a 2 min SF interaction (SF), and (c) a 2 min reunion play
interaction (Reunion). Prior to the video-recording, the mothers were instructed to play
with their infants during the Play and Reunion episodes just as they would normally do
at home. For the SF, the mothers were instructed to pose a neutral expressionless face to
their infants while looking at them, but not to smile, talk, or touch their infants. The
signals from the two cameras were edited off-line into a video-recorder to produce a
single image with a simultaneous frontal vie'w of the face, hands and torso of the infant
and mother. For analysis purposes, a computerized digital format was created for each
infant-mother dyad's video clip.
Behavioural coding
Infants' and caregivers' behaviours w^ere coded using the infant and caregiver
engagement phases (ICEP; Weinberg & Tronick, 1998; see also Tronick et al., 2005).
The ICEP system is made up of a set of mutually exclusive infant and caregiver phases of
interactive engagement and several additional codes for regulatory behaviours.
Definitions for ICEP and infant self-regulation codes are provided in Table 2. ICEP were
coded in two separate viewings of the videotape. A third viewing of the tape was devoted
to coding infant regulatory behaviours (i.e., self-comforting/mouthing, hand clasping, and
distancing/turning away from the caregiver). The coding was done from the digital video
by coders masked to the pre-term status of the infants. A digital time display was used to
track time intervals and the time code was automatically entered into a datafile.Software
developed by the E. Medea Scientific Institute's Bioengineering Laboratory allowed
coders to indicate the time measured to within 1-s w^hen a particular behaviour occurred.
This coding procedure produced an absolute frequency count of the ICEP codes and
regulatory behaviours and maintained their temporal sequence within a 1-s interval.
Reliability
Inter observer reliability values for both the ICEP and the additional codes were
determined through percentage agreement and Cohen's kappa (Cohen, I960).
Fifty percent of the Play, SF, and Reunion episodes w^ere selected randomly and were
assessed for agreement between two independent coders. The mean percentage of
Pre-tern) infants in still-face paradigm
355
Table 2. Outline of the encoding system of the ICEP (Weinberg & Troniek, 1998).
Infant engagement
Negative engagement: The infant is negative or protesting. The infant displays negative facial
expressions (e.g., sadness, distress, crying, or grinnacing), complaining, being fussy, crying
vocalizations. When the infant is protesting, he/she often displays facial expressions of anger,
grimaces, and fussing/crying.
Withdrawn: The infant is withdrawn and minimally engaged with the caregiver. This phase often
includes sad facial expressions, whimpering vocalizations, slumped posture, and gaze aversion
Object/environment engagement: The infant is looking at objects that are either proximal (e.g., infant
seat) or distal (e.g., camera). The infant may manipulate proximal objects (e.g., infant chair strap;
caregiver's hands)
Social monitoring: Gazing at caregiver's face/eyes with a neutral or interested facial expression.
Infant may vocalize in a neutral manner
Sociai positive engagement Gazing at caregiver's face/eyes while smiling
Caregiver engagement
Negative engagement: The adult is negative, intrusive or hostile
Withdrawn: The adult is minimally engaged and withdrawn with the infant (disengagement from
infant for gaze direction, facial expressions and/or vocalizing)
Non-infant focused engagement: The adult is not attending to the infant and is involved in a
non-infant focused activity
Social monitor: Gazing at infant with neutral/interested expression or with positive vocalizing.
Social positive engagement: Positive affect (smiles, laughter, exaggerated expressions)
Infant self-regulation
Mouthing: Infant sucks on his/her body (e.g., thumb or wrist)
Seif<lasping: The infant's two hands are touching
Distancing: The infant's shoulders and trunk are rotated sideways from the caregiver and the
infant's head is averted
agreement and Cohen's kappa were .85 and .73 for infants' behaviour, .89 and .75 for
caregivers' behaviour, and .88 and .74 for the regulatory codes.
Data reduction and dependent measures
Dependent measures for the infant, caregiver, and dyad were:
(1) The proportion of time the infant or caregiver were in each ICEP phase was
obtained by dividing the total time of each code by the total length of the episode.
(2) The proportion of time for self-regulatory behaviours was obtained by dividing the
total time of each code by the total length of the episode.
(3) Three measures of coordination were analyzed: Matching, Reparation rate,
and Synchrony. Following procedures from previous studies (Troniek & Cohn,
1989; Weinberg et al, 1999), measures of coordination were defined as follows:
(a) Matching: the extent to which caregivers and infants shared joint ICEP codes;
infant and mother simultaneously in Negative, Withdraw^n, Looking a-way, Social
Monitor, or Social Positive states, (b) Reparation Rate: the rate of change between
mismatching to matching states, (c) Synchrony: the extent to w^hich mothers and
infants simultaneously increased or decreased their level of engagement in the
same direction (more or less engagement) w^ith each other. Synchrony is quantified
by first scaling the infant and mother ICEP codes from less to more engaged and
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R. Montirosso et al.
then calculating the proportion of shared variance at LagO, as indexed by the
square of the cross-correlation between each mother and infant's time series of
mean engagement scale scores. Matching and Synchrony measures differ in that
Matching focuses on the shared or non-shared content of the behaviours of
mothers and infants (they are doing the same thing at the same time), whereas
Synchrony evaluates how mothers and infants change their levels of engagement
with each other over time, regardless of the content of their behaviour (getting
more or less engaged even if they are doing different things). Thus, some dyads
might seldom be in matching states but nonetheless have high-synchrony scores
because they tended to change their level of engagement in the same direction.
Statistical analysis
Pearson correlations were calculated in order to evaluate possible relations between
the infant's age and infant ICEP phases and infant self-regulatory behaviours and
measures of coordination. To assess the effects of group (pre-term vs. full-term) and
interactional context (Play, SF, and Reunion) on infant and maternal ICEP phases
and self-regulatory behaviours, we conducted separate 2 (group) X 3 (episode)
ANOVAs with episodes as repeated measures. For the caregiver, negative engagement,
withdrawn, and non-infant focused engagement were not included in the ANOVA
because of the low proportion of occurrence. Following the techniques used in
previous studies (Tronick & Cohn, 1989; Weinberg etal., 1999), coordination measures
w^ere analyzed as follows: Matching, the adjusted proportions were transformed using
and arcsine transformation' and then examined in a 2 (group) X 2 (episode) ANOVA
w^ith episodes as repeated measures; the Reparation Rate per second was arcsine
transformed and analyzed in a 2 (group) X 2 (episode) ANOVA with the Play and
Reunion play episodes as repeated measures; and Synchrony was evaluated using the
cross-correlations of the Mother and Infant Scale scores in a 2 (group) X 2 (episode)
ANOVA with Play and Reunion play as repeated measures. Because all mothers were
instructed to behave in the same manner during the SF episode, the caregiver and
dyadic variables were analyzed only for the Play and Reunion episodes using a repeated
measures ANOVA. Significant episode effects were evaluated in pair wise comparisons
using post hoc tests w^ith the critical p value for significance adjusted w^ith Bonferroni
correction to control for multiple tests. Effect size was evaluated using the partial Eta
square (Tip), which evaluates the proportion of variance accounted for by each
variable. The conventional cut-offs for T|p = .01, .06, and. 14 for small, medium, and
large effect sizes were used (Green & Salldnd, 2003).
Separate forward stepwise linear regressions were done to identify the significant
predictors of each itifant's SEB (infant ICEP phases and self-regulatory behaviours). The
effect of the following variables were exatnined for each episode of the FFSF procedure:
gender, birth status (full-term or pre-term birth), DQ, BDI scores, and SES. The maximum
number of variables entered into the regression analysis was five, insuring that there
were at least 10 participants for each independent variable (Munro, 1997). All analyses
were performed at a significance level/J < .05.
Recause the dependent variables were expressed as proportions, the data were arcsine transformed. The arcsine
transformation was performed to make the distribution of the variable approximately normal for statistical analysis. Cohen and
Cohen (1983) suggested this transformation for uncorrelating the means and variance of proportional data.
Pre-terw infants in stiii-face paradigm
357
Results
As expected, comparisons (t test) between the full-term and the pre-term groups'
medical and demographic variables revealed that only the infants' GA and birth weight
were significantly different, i(48) = 11.50, p < .001, and i(48) = 12.91, p < 001,
respectively. No associations were found for the correlation of corrected age and DQ.
A chi-square test revealed that gender was not significantly associated with group. There
were no significant differences in age, education, SES, and BDI scores between the
parents of fuU-term and pre-term infants. No significant correlations were found
between the infants' age and infants' behaviour, self-regulation. Matching, Reparation
Rate, or Synchrony. Consistent with findings from previous SF research, these results
suggest that the age range used in the present study w^as not associated w^ith the infant
variables or coordination measures.
Infant and maternal ICEP phases and infant self-regulation
Table 3 presents the adjusted proportion means and SD of infant and maternal ICEP
phases and self-regulatory behaviours for pre-term and full-term infants. Contrary to
expectations, the analysis revealed no significant differences in ICEP codes between
groups across the three episodes for infant and maternal ICEP phases. As expected, a
significant effect was found for self-regulatory behaviours, i='(l,48) = 8.88, p < .01,
T|p = .19. The partial Eta squared level indicates a large effect size (Green & Salkind,
2003): pre-term infants compared to full-term infants showed higher levels of
distancing/turning away (0.10 vs. 0.03, respectively). No differences were found for oral
self-comforting/mouthing and self-clasping.
There were significant differences in infant ICEP phases and self-regulatory
behaviours for the different phases of the EESF: Negative engagement, F(2,86) = 11.63,
p < .00, f]l = .23; Withdrawn, F(_2,86) = 4.80,p < .05, iq^ = .11; Object/environment
engagement, F = (2,86)17.60, p < .001, TI^ = .32; Social monitor, F(2,86) = 4.70,
p < .05, Tip = .11; Social positive engagement, 7^(2,86) = 13.72, p < .001, Tip = .26,
and Distancing/turning away from caregiver, F(2,86) = 6.^0, p < .01, Tip = .14. These
size effects were moderate to large.
As expected, regardless of group membership, a Bonierroni post hoc analysis found
that infants exhibited a greater proportion of negative affect and withdrawn behaviour
during the SE Moreover, there •was an increase in the infant's negative affect in the
Reunion, which did not return to the levels found in the Play episode. In the SE episode
infants also engaged in more self-regulatory behaviours and showed a reduction of Social
Monitoring and Social Positive engagement, both of which returned in the Reunion
episodes to the levels observed in the Play episode. These findings show that both
groups reacted with negative affect to the SF and both had a carry-over effect of negative
affect from the SE into the Reunion episode as well as an increase in positive affect
reflecting the ambivalent nature of the infant's behaviour during the Reunion play. There
was one significant group X episode interaction for Social Monitoring, F(2,86) = 397,
p < .05, Tip = .10. Separate t tests for each episode revealed that during the Reunion
episode, the pre-term dyads showed greater social monitoring than full-term dyads
(respectively, 0.28 vs. 0.17), i(48) = -2.21,p < .05. There were no significant episode
effects (Play vs. Reunion) for the Caregiver Engagement Phases.
The regression analysis evaluating the predictors of infant SEB during the SF
paradigm is presented in Table 4. None of the predictor variables were correlated w^ith
each other at greater than r = .38 indicating little multi-coUinearity. The significant
R. Montirosso et al.
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Pre-terw infants in still-face paradigm
359
predictor was birth status, accounting for 22% of the variance in Distancing during the
Play and accounting for 9% of the variance in Social Monitoring during the Reunion.
Thus, pre-term status was predictive of greater distancing during Play and Social
Monitoring during the Reunion.
Table 4. Linear regression for variables predicting infant SE B during SF paradigm
Episode
Infant behaviour
Predictor
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Measures of coordination
The measures of coordination were assessed in the Play and Reunion episodes. Table 5
presents the adjusted proportion means and SD of measures of coordination for preterm and term infants. There w^as no main effect of group for Social Monitor Match and
Social Positive Match. There were significant episode effects. There was a reduction of
Look Away from Partner Match, P(l,46) = 11.43,/» < .01, T|p = .24, during Reunion
(0.23) as compared to Play (0.34) suggesting that dyads of both groups were more
attentive to their partner or looked less at objects after the stressful condition. There
were fewer Total matches states during Reunion (0.30) than during Play (0.40),
F(l,47} = 7.60, p < .01, Tip = .17, suggesting more difficulty in coordination when
dyads resume interaction after the SF episode. There w^as a significant effect for
Reparation Rate between mismatching and matching states suggesting reparation
rate was slower during Reunion (.11 per second) than during Play (.09 per second),
P(l, 47) = 4.10, p < .05, Tip = .09. There was also a significant episode effect for
Synchrony, F(l, 45) = 4.50, p < .04, r\^ = .11. Across the groups, mothers and infants
showed a higher synchrony score during Reunion (0.32) than during Play (0.25),
indicating that after the perturbation of the SF the direction of their changes in
engagement level was more coordinated. The effect sizes were moderate to large (Green
& Salkind, 2003), suggesting that the Reunion episode is a stressful interaction that
requires a complex mutual dyadic adjustment for the mothers and infants.
Discussion
The findings demonstrate similarities as well as differences in the social behaviour,
coping and qualities of dyadic interactions of pre-term and full-term infants and their
mothers. The lack of findings of group differences fails to support the prediction that
pre-terms would be less socially capable and display less social attentiveness, less
positive expressive behaviour and greater negative emotion than full-terms. These
findings are consistent with previous studies that found no differences in interactive SFB
between pre-term and full-term infants in the second half of the first year (Brachfeld
et al., 1980; Schermann-Eizirik et al, 1997). Nonetheless, as we expected based on the
MRM and the literature there appear to be differences in regulatory behaviours between
the groups. Pre-term infants displayed more distancing from their mothers (e.g., by
turning away, twisting, or arching) than full-term infants across all the episodes.
360
R. Montirosso et al.
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Pre-term infants in still-face paradigm
361
In particular, there was greater distancing during Play. The infant's attempts to increase
physical distance from the caregiver are a sign of stress and a failure of self-regulation
(Gianino & Tronick, 1988). Consequently, a greater use of distancing in the pre-term
group may indicate a greater level of stress and a lower capacity for self-regulation
compared to their full-term counterpart even in the normal interactions. This result and
along withfindingsby others (Mouradian et al., 2000; Wolf eí al., 2002) suggests deficits
of self-regulation in pre-term infants during the first year of life.
Interestingly, pre-term infants also evidenced more social monitoring than full-term
dyads in the Reunion episode subsequent to the stress of SF and prematurity was a
significant predictor of social monitoring during the Reunion. These findings suggest
that pre-term infants may try to deal with the stress of the Reunion with the
compensatory strategy of increasing their social monitoring, a less aroused state than
either positive or negative affective states (Greene et al., 1983; Weinberg & Trotiick,
1997). In other words, they use an other-directed strategy (Gianino & Tronick, 1988) in
an attempt to obtain regulatory support from the adult to modulate their stress because
their own self-directed regulatory mechanisms are inadequate. It should be noted that
the differences found here were not associated to gender, developmental quotient, level
of maternal depressive symptomatology, SES, or maternal SEB. These findings suggest
that these low-risk pre-term infants do not have comparable emotional regulatory
functions to their full-term peers and it may be important to monitor their negative
affect, regulation, arousal, and stress reactivity especially in stressful environments in
order to facilitate their optimal development (Feldman, 2006).
Pre-term infants, like full-term infants, displayed the SF effect: more negative affect and
withdra'wn behaviour, less social and positive engagement, and an increase in distancing
from the caregiver in the SF episode than in the Play episode. These results are in partial
disagreement with the study by Segal et al. (1995). They found no differences in negative
affect between pre-term and full-term infants, but also reported that pre-term infants
spent proportionally less time displaying smiles than full-terms. This difference may be
due to methodological differences. Their coding scheme for positive affect may have been
more sensitive than the coding scheme used in this study, whereas the coding scheme for
negative affect was similar (Segal et al., 1995). There was also a reunion effect (Weinberg
& Tronick, 1996) for both groups: the pre-term as well as the full-term infants displayed an
increase in negative affect, less interest in objects and the environment, a decreased
distancing from the caregiver and the prototypical rebound of social positive
engagement. These results confirm Weinberg and Tronick's (1996) hypothesis that the
process of reparation in the Reunion episode is a stressful and complex task for the infants
because of the ongoing effects of the SF experience and the resumption of positive
interaction. Thefindingof SF and reunion effects for the pre-term infants attest to their
capacity to form social expectations, their sensitivity to stress and their capacities for
coping with stress; that is it speaks to social emotional and regulatory Wellness.
Several studies suggest that in thefirstyear of life mothers of pre-term infants are less
responsive to infants' signals than mothers of full-term infants (Harrison, 1990; Harrison
& Magill-Evans, 1996). By contrast, other studies have found that mothers of pre-term
infants are particularly responsive to their infants' affective signals (Barratt etal, 1992)
and several reported that they may actually exhibit more over stimulating behaviour
(Brown & Bakeman, 1980; DiVitto & Goldberg, 1979; Field, 1979). The results of the
present study do not support the findings of either greater or lesser responsiveness of
mothers of pre-terms compared to mothers of full-terms. Mothers of both pre-terms and
full-terms had similar levels of social monitoring and positive affect. Specifically, in both
362
R. Montírosso et al.
groups the mothers' gaze was focused on their infants' or their infants' activities and the
mothers expressed positive affect (e.g., by vocalizations, motherese, making kissing, or
clicking sounds, and singing) at similar levels. These findings are consistent with
previous research in which mothers of pre-term infants were described as relatively
competent in their interactive behaviour with their infants (Schermann-Eizirik et al.,
1997; Stjernqvist & Svenningsen, 1990). Our results on maternal behaviour are
consistent with the evidence that the differences in maternal social behaviour, observed
in the first 6 months of life between the pre-term and full-term groups, tend to fade
during the second half of thefirstyear of age (Brachfeld et al., 1980). It seems likely that
in the second 6 months of life, full-term as well as pre-term infants' behaviours (e.g.,
social skills) tend to consolidate and mothers' adjustment to their infants, as well as their
increased experience with them may overcome stressful factors such as anxiety about
the infants' health and concerns about depression. Consequently, similar tofindingsby
Landry, Chapieski, & Schmidt (1986), our results suggest that maternal adaptation to
pre-term infants tends to be more appropriate towards the end of the first year of life.
This interpretation is further supported by the lack of differences between the groups
on the three measures of coordination (Matching, Synchrony, and Reparation Rate).
These results were not expected. Previous findings suggested that pre-term dyads show
lower levels of synchrony. However, previous research (Eeldman, 2006; Feidman &
Eidelman, 2007; Lester etal., 1985) quantified social interaction during thefirst6 months of
life (3-5 months). In home observational research. Watt (1986) reported that at 3 months of
age, pre-term dyads had lower levels of interaction and synchrony in comparison with their
full-term counterparts but by 6 months ofage the pre-term dyads showed higher levels of
simultaneous interaction, mutual gaze and were more synchronized than full-term dyads.
Thus, it is possible that, in spite of the differences between full-term and pre-term dyads in
their first months of life, the mutual regulatory capacities of the pre-term become more
effective during the second half of the first year of life, and the quality of interaction
becomes comparable between the two groups (Korja et al., 2008). Ourfindingindicated
that overall for both groups, mother-infant synchrony showed a mean value of 0.09, which
is consistent with earlierfindings.Tronick and Cohn (1989) found that at 6 and at 9 months
ofage, synchrony varied from 0.09 to 0.23 for different mother-infant pairs and Weinberg
etal. (1999) reported a mean value of 0.08. Thus, our results suggest that from 6 months of
age, pre-term dyads may be able to synchronize their engagements in a similar way of fullterm dyads. With regard to Matching and Reparation Rate thefindingsof current study
suggest that pre-term infants and their mothers maintained levels of mutual engagement
and reparation similar to those of full-term dyads. In line with previous studies of this age
range (Cohn & Tronick, 1989), the dyads of both groups spent most of their interaction time
in mismatching states (more than 60%). Withdrawn behaviour and negative match were
extremely rare (less than 1%) while social monitor and positive match occurred on average
about 17% and 15% of the time. Furthermore, for both groups the data indicated that the
dyads spent most of the time in a Look Away from Partner Match (25% and 33%,
respectively). Both mother and infant looked at objects that were either proximal (e.g.,
infant seat) or distal (e.g., light switch). This result suggests that the partners are not only
interested in the dyadic context, but also clearly show other behaviours, oriented 'outside
the relationship'. A possible explanation for this result is that the behaviours refiect the
infant's growing interest in objects and that the dyadic focus on other objects is a positive
developmental change (Feidman, 2007). For example, between 3 and 9 months of age,
episodes of shared gaze decrease to about a third of the time while shared attention to
objects increases dramatically (Landry, 1995).
Pre-term infants in still-face paradigm 363
In this study, the mean reparation rate across the groups was 0,09 per second. This
finding is consistent with Weinberg etal.'s (1999) study, which reported a 0,10 reparation
rate during normal face-to-face interactions at 6 months of age. Thus, in both studies, the
repair rate was about once every 10 s, suggesting that reparations are typical features of
the interaction. Consistent with the theoretical perspective of the MRM, these findings
confirm that in pre-term and full-term dyads, interactions are organized into a matching
and mismatching pattern with reparations resolving the mismatches (Tronick, 1989),
As this mismatch-repair-match organization is similar in both groups, it appears that from
6 months of age neither healthy pre-term infants nor their mothers are compromised in
their capacity to coordinate face-to-face interactions, even when they had to deal with a
stressful condition (i,e,, the SF), Thus, our results on coordination suggest that a favourable
infant-mother relationship may function to attenuate the effects of prematurity on early
socio-emotional delays and/or that healthy pre-term infant dyads are able to achieve a
normal quality of interactive regulation in the second half year of life.
Another sign of the normalcy of these pre-term infants was that, as in the fullterm group, the amount of shared engagement (Total matches) decreased in the
reunion play compared to the first play As has been argued by Weinberg and
Tronick (1996), it is likely that after the stress of the SF, both infants and mothers
find it more difficult to coordinate their social behaviour and maintain mutual
engagement. This is corroborated by the finding that the rate of reparations was
slower during Reunion than during the first play interaction. The finding suggests
that mothers and infants made fewer attempts at reparation during Reunion than
during Play and/or found it more difficult to make repairs of mismatching states.
These data appear to be compatible with interpretations suggesting that the
processes of reparation and mutual regulation are more stressful and complex in the
Reunion episode than in the Play episode preceding the SF (Kogan & Carter, 1996;
Weinberg & Tronick, 1996), Dyads showed a higher synchrony score during the
Reunion episode than in the first play, suggesting that after the SF perturbation these
mothers and infants were more sensitive or vigilant to changes in each other's
engagement. Thus, while synchrony and matching are often seen as measuring
similar phenomena they may not be, A higher synchrony score may indicate that the
dyads tracked each other's behaviour more carefully whereas a lower matching
scores may indicate that they are less able to coordinate their behaviours
successfully. In this perspective, a higher level of synchrony may be indicative of
reduced flexibility in interaction (Tronick & Cohn, 1989) and suggestive of greater
dyadic effort to create more predictability in the interaction (Jaffe et al, 2001),
Thus, while synchrony is typically thought of as an indication of a 'good' interaction
(Stern, 1985), it may actually be a measure of hypervigilance, possibly being used as
a strategy for renegotiating the interaction after a stress. In summary, the lack of
group differences indicates that the pre-term infant-mother dyads reacted typically
to the additional stress of the Reunion episode.
There are several limitations in the present study. The sample size though typical for
many micro analytic studies of interactions is relatively small. The pre-term infants w^ere
relatively healthy so the results cannot be generalized to more at-risk populations of
infants. Replications with a larger sample and greater variations of SES and health status
are needed. The study did not follow-up these infants so that we cannot assess the
relations between the differences in regulatory behaviours and later outcome. It would
also be interesting to have other measures of stress (e,g,, skin conductance. Ham &
Tronick, 2008) on the infants and mothers.
364
R. Montirosso et al.
Nevertheless, the results from this study suggest that it is important to evaluate preterm infants and their mothers in different interactive contexts (normal vs. stressful
conditions) and to obtain measures of their coordination in addition to measures of each
partner's interactive behaviours in order to obtain a better understanding of the
mother-infant interaction. The pre-term infant-mother dyads were able to coordinate
their interactions in a similar manner to full-term dyads. Pre-term dyads also
demonstrated similar capacities for the reparation of interactive matches, which
suggests that pre-term infants experience normal levels of reparation. Thesefindingson
coordination and reparation, along with the findings on the typicality of the pre-terms'
reaction to the SF, demonstrate the coping and social competence of the pre-term
infants and their mothers. In the MRM it is argued that reparation is one of the primary
mechanisms underlying normal development, including the development of trust and
attachment, mastery, the experience that negative affect or stress can be transformed
into positive affect and the elaboration of coping capacities (Tronick, 1989, 2007). The
social competence observed in these healthy pre-term itifant-mother dyads suggests
that their interactive experience is typical and likely to lead to positive developmental
outcomes. These findings can be used clinically to reassure parents, which can further
reduce their anxiety and consequently improve their interaction with their pre-term
infant. A technique may be to explain to parents that miscoordination and mismatching
in their interactions with their itifants is normative along with the value of reparation for
their infants' development. Understanding the importance of the inherent messiness of
interactions may help parents overcome their search for the perfect, wished-for
interaction (Brazelton, 1999) which only serves to make them anxious when the fail to
achieve it. Clinicians also need to see reparation and miscoordinations as normal
interactive processes. Indeed, the findings suggest that the clinician can expect pre-term
infant-mother pairs to be interacting w^ell by 6 months of age, but 'well' must be seen as
involving interactive mismatches and reparations as indicators of normalcy and not as
indicators of something going awry and requiring intervention (Trotiick, 2007).
Acknowledgement
This research was supported by funds from the Italian Health Minister (Ricerca Corrente 2003),
partially supported by an unrestricted educational grant from Chiesi Farmaceutici, and from grants
from the National Institute Child Health & Human Development (R01HD37138 & RO1HDO5O459;
E. T, PI) and the National Science Foundation (NSF 06-511; E. T., PI). The authors wish to thank
the nursing and neonatology staff from the nurseries of the Manzoni Hospital NICU (Lecco) and
community pediatricians in Lecco for their support. We thank Patrizia Cozzi for their support in
the data collection. We also wish to thank Sara Averna, Gloria Mauri, Sonia Monticelli, Viviana
Sabadini, Elisa Zoboli for their help in data coding; when the research was conducted they were
graduate psychology students at the Catholic University of Milan. Furthermore, we are grateful to
Carlo Magni from Scientific Institute Medea's Bioengineering Laboratory for the software and the
computer program used for the video analyses. Thanks are due to Dr Uberto Pozzoli for his
support in the matching analyses. Finally, special thanks go to all infants and their mothers
participating in this study.
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Received 14 February 2008; revised version received 15 January 2009
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