|

Received: 14 July 2020    Accepted: 13 December 2021

DOI: 10.1111/infa.12451

RESEARCH ARTICLE

Spontaneous movements, motor milestones,

and temperament of preterm-­born infants:
Associations with mother–­infant attunement

Orna Lev-­Enacab1,2  | Efrat Sher-­Censor2   | Christa Einspieler3  |

Orit Achamyelesh Jacobi2  | Galia Daube-­Fishman2  |
Sara Beni-­Shrem1

1
Maccabi Health Care Service, Haifa,
Israel
2
University of Haifa, Haifa, Israel
3
Medical University of Graz, Graz,
Austria
Correspondence
Orna Lev-­Enacab, Maccabi Health Care
Service and University of Haifa, Haifa,
Israel.
Email: levorna26@gmail.com
Funding information
Faculty of Social Sciences, University
of Haifa; Maccabi Health Care Service;
Israeli Physiotherapy Society
Abstract
Preterm-­born infants and their mothers are at higher
risk of showing less attuned interactions. We sought
to identify characteristics of preterm-­born infants as-
sociated with the attunement of mother–­infant inter-
actions at the corrected ages of 3–­4  months, looking
specifically at motor behaviors. We focused on infants’
spontaneous movements, achievement of motor mile-
stones, and temperament, which at this young age is
often manifested via movement. Sixty preterm-­born in-
fants (Mdngestation age in weeks = 33, 57.38% male, corrected
age Mdn = 14 weeks, interquartile range = 13–­16) and
their mothers participated. Independent observers rated
mother–­infant attunement, infants’ spontaneous move-
ments, and infants’ achievement of motor milestones.
Mothers reported infant temperament. We found in-
fants’ smooth and fluent movement character and con-
tinual fidgety movements were associated with better
attunement in terms of higher maternal sensitivity and
non-­intrusiveness and higher infant responsiveness and
involvement. Unexpectedly, infants’ achievement of
motor milestones was not significantly associated with
mother–­infant attunement, and maternal reports of in-
fants’ higher soothability were associated with lower

© 2022 International Congress of Infant Studies.

| wileyonlinelibrary.com/journal/infa
412     Infancy. 2022;27:412–432.
LEV-­ENACAB et al.      |  413

maternal sensitivity. The study illustrates the value of

including the assessment of infants’ spontaneous move-
ments, designed for early detection of neurological
deficiencies, in research and in clinical practice with
parents and preterm-­born infants.

1  |  I N T RO DU CT ION

During the first six months of life, preterm-­born infants are at risk of experiencing poorer quality
of interactions with their mothers, which puts the infants at risk of poorer socio-­emotional and
cognitive development (e.g., Gueron-­Sela et al., 2015; Korja et al., 2012). Certain behavioral char-
acteristics of preterm-­born infants may contribute to difficulties in mother–­infant interactions.
The present study examined three potentially relevant characteristics of infants at the corrected
ages (CA) of 3–­4  months that involve motor behaviors: (1) atypical or abnormal spontaneous
movements, such as vigorous arching of the body; (2) slower achievement of gross motor mile-
stones; and (3) more difficult temperament. We assessed the latter because movement is a key
modality through which temperament is expressed at this young age (Planalp et al., 2017). Studies
have shown that all three are more prevalent among preterm-­ than term-­born infants (Di Rosa
et al., 2016; Fjørtoft et al., 2016; although the evidence regarding temperament is less consistent;
Cassiano et al., 2020). To the best of our knowledge, research on the associations between the
characteristics of spontaneous movements and the quality of the interactions between infants
born preterm and their mothers is scarce (Lev-­Enacab et al., 2015). In addition, the few studies
examining the contributions of the achievement of gross motor milestones or of temperament
to the quality of mother–­infant interactions have reported mixed results (e.g., White-­Traut et al.,
2018, versus Treyvaud et al., 2009; Feldman, 2006, versus Harel-­Gadassi et al., 2020).

2   |   AT T UN EME N T OF T HE IN TERACTION BETWEEN

M OT H E RS A N D PR ET E R M -­B OR N INFANTS

Researchers have offered several closely related constructs to characterize the quality of mother–­
infant interactions. Here, we use the term attunement, a dyadic construct reflecting reciprocal
multilevel behaviors of the mother and the infant (Bornstein, 2013). Maternal attunement in-
volves sensitive behaviors (Bartling et al., 2010; Bornstein, 2013), namely being attentive to the
infant's cues, interpreting them accurately, and responding to them appropriately and in a timely
manner (Ainsworth, 1969). Sensitive mothers show positive affect, warm concern, and social
responsiveness to their infants’ needs (Bartling et al., 2010; Bornstein, 2013) without intrusive-
ness, i.e., without interfering, overstimulating, or overprotecting the infant (Biringen et al., 2014;
Bornstein, 2013). Infants contribute to attunement by being engaged with their mothers, signal-
ing their needs, responding positively to their mothers’ bids, and initiating interactions (Biringen
et al., 2014; Bornstein, 2013).
Mother–­infant attunement fosters infants’ exploration and quick recovery from distress
(Ainsworth, 1969; Bornstein, 2013). It predicts better developmental outcomes of full-­term
and preterm infants alike, including forming secure attachment, showing better cognitive
 |
414       LEV-­ENACAB et al.

development and language skills in toddlerhood, and displaying higher social competence and
fewer behavior problems in early and late childhood (Biringen et al., 2014; Gueron-­Sela et al.,
2015). Moreover, preterm-­born infants whose mothers participated in a sensitivity training
program at the Neonatal Intensive Care Unit (NICU) showed improved cerebral white-­matter
micro-­structural development when they reached full-­term age (Milgrom et al., 2010).
Unfortunately, dyads of mothers and their preterm-­born infants may have less attuned in-
teractions than mothers and full-­term infants, especially during the first 6 months of life (e.g.,
Harel-­Gadassi et al., 2020; Vaccaro et al., 2021; but see Bilgin & Wolke, 2015). In particular, moth-
ers of preterm-­born infants tend to be less sensitive, show less affectionate touch and be more
intrusive than mothers of full-­term infants (e.g., Feldman & Eidelman, 2007; Korja et al., 2012;
Vaccaro et al., 2021). At the same time, preterm-­born infants tend to show less positive mood and
are less engaged in interactions with their mothers than term-­born infants (Harel et al., 2011).
Several explanations of these group differences have been offered. The early, unexpected, and
sometimes traumatic delivery of a preterm infant may lead to increased maternal self-­blame and
concerns about an inability to protect the infant (Harel-­Gadassi et al., 2020; Korja et al., 2012).
When this is coupled with a prolonged hospitalization in the NICU, which involves separation
from the newborn, maternal sensitivity may be compromised (Neri et al., 2017). Other explana-
tions focus on the infants. Preterm-­born infants are abruptly and prematurely separated from
their optimal uterine environment to less optimal conditions; this might hamper the healthy
maturation process of the central nervous system, specifically the brain stem, the amygdala-­
limbic system, and the prefrontal cortex (Feldman, 2006; Tamm et al., 2020). Consequently,
preterm-­born infants may show more gaze aversion and less clear communicative intentions
(e.g., Feldman, 2006; Harel et al., 2011).
Our goal was to extend this literature. Specifically, we examined whether certain motor behav-
iors of infants born preterm may contribute to difficulties in the attunement of their interactions
with their mothers.

3   |   S P O NTAN EOU S M OVE M E NTS AND ATTUNEMENT OF

M OT H E R– I­ N FAN T IN T E R ACT IONS

The first motor behavior we examined was infants’ spontaneous movements. Infants move spon-
taneously, i.e., without intention or a specific trigger, until the CA of 5  months. Spontaneous
movements appear over the entire body in variable sequences and complexity. Their richness
and complexity indicate the intactness of the neural system (e.g., Peyton et al., 2017). Thus, spon-
taneous movements are usually used to detect neurodevelopmental deficiencies, such as cerebral
palsy and minor neurological deficiencies (e.g., Einspieler et al., 2019). The highest predictive
value of infants’ spontaneous movements is between the CA of 3–­5  months and is based on
the assessment of fidgety movements (FMs) and movement character (e.g., Bruggink et al., 2008;
Einspieler et al., 2019). Normal FMs are tiny and elegant movements, characterized by small
amplitudes, moderate speed, and variable accelerations of neck, trunk, and limbs in all directions
(Einspieler et al., 2004). Their appearance indicates a healthy nervous system. Typically, they
occur continuously or intermittently between 3 and 5 months CA (Ferrari et al., 2016). Abnormal
appearance of FMs manifests in larger amplitude, faster speed, and jerkiness; this type of FMs is
rare and indicates an increased risk for minor neurological deficiencies, such as developmental
coordination disorder (Bruggink et al., 2008, 2009). Finally, the absence of FMs indicates a high
risk for severe neurologic dysfunction, such as cerebral palsy (e.g., Einspieler et al., 2019).
LEV-­ENACAB et al.      |  415

Another salient aspect of spontaneous movement is movement character, representing the

characteristics of all gross movements of the infant. Typical movement character includes smooth,
fluent, and complex movements of arms, legs, and trunk in variant directions (Einspieler et al.,
2004). Such movement character predicts typical development (e.g., Fjørtoft et al., 2013). Infants’
movement character is considered atypical when spontaneous movements are monotonous,
jerky, stiff, or tremulous. Atypical movement character indicates a higher risk for minor motor
deficiencies, such as coordination disorder or other developmental disorders, such as autism and
learning disorders (Bruggink et al., 2008; Fjørtoft et al., 2013; Zappella et al., 2015). Movement
character that is cramped synchronized (i.e., at least two limbs and the trunk contract simultane-
ously and thereafter relax simultaneously) is considered abnormal and predicts severe cerebral
palsy (e.g., Einspieler et al., 2019).
Infants’ FMs and movement character might be associated with the attunement of mother–­
infant interactions for two reasons. First, normal and continual FMs and a smooth and fluent
movement character create a sense of cuteness and elegancy in the infants’ movements (De
Raeymaecker, 2006; Einspieler et al., 2019). Infants’ cuteness is an evolutionary protective mech-
anism that elicits motivation for caregiving in adults and increases adults’ attention and posi-
tive affect toward infants (Glocker et al., 2009; Kringelbach et al., 2016; Sherman et al., 2013).
Perceived cuteness has mostly been studied in the context of infants’ facial features (e.g., Glocker
et al., 2009). Nevertheless, recent research suggests other physical characteristics of infants, in-
cluding smells, sounds, and perceived health, contribute to perceived cuteness and are associated
with increased parental instinctual caregiving behaviors (Golle et al., 2015; Kringelbach et al.,
2016). Thus, it is reasonable to expect that normal and continual FMs and smooth and fluent
movement character would contribute to the perception of the infant as cute and would be asso-
ciated with more attuned maternal behavior. Second, in their early months, infants express their
emotions and communication initiatives mainly via movements (De Raeymaecker, 2006; Egmose
et al., 2019). A monotonous movement character, such as repetitive kicking and arm movements
or jerky and stiff movements might hamper infants’ ability to initiate and maintain eye contact
with their mothers and express their emotional intentions. These poorer communicative behav-
iors may challenge mothers’ ability to respond in a sensitive and non-­intrusive way.
We investigated the association between infants’ spontaneous movement and the attunement
of the mother–­infant interaction in a pilot study of a small sample of infants born preterm at
the CA of 3–­4 months (Lev-­Enacab et al., 2015). We found the continual expression of FMs was
associated with more sensitive maternal touch and holding. In addition, infants’ atypical move-
ment character was related to lower maternal sensitivity when putting infants down as well as to
infants’ lower responsiveness and involvement. To the best of our knowledge, these associations
have not been examined in other studies. Therefore, our first goal was to reexamine the links
between infants’ spontaneous movements and the attunement of their interactions with their
mothers in a larger sample of infants born preterm.

4   |   AC H I E V E ME N T OF M OTOR MILESTONES AND

AT T U NE M E NT OF M OT H E R –­I N FANT INTERACTIONS

The second motor behavior that may be associated with mother–­infant attunement is infants’
achievement of motor milestones, which is typically assessed in routine pediatric checkups to
detect developmental delays and motor disorders (Di Rosa et al., 2016). It could be expected that
particularly during the first 6 months of life, slower achievement of motor milestones would be
 |
416       LEV-­ENACAB et al.

associated with infants’ lower ability to respond to and initiate interactions with their moth-
ers. White-­Traut et al. (2018) suggested faster achievement of head control, one of the main
achievements of motor development during the first months of life, is crucial for initiating and
preserving interactions with the mother. In addition, better stability of the trunk and the head in
supported sitting position enables infants to move their hands more easily toward midline and
toward their caregivers’ face and body. This, in turn, may facilitate infants’ responsiveness to and
involvement with their mothers (Iverson, 2010) and consequently facilitate maternal sensitivity.
Preterm-­born infants generally present slower achievement of motor milestones than term-­
born infants, especially during the first year of life (Di Rosa et al., 2016). Yet research on the
links between the achievement of motor milestones and the attunement of mother–­infant in-
teractions is scant and inconsistent. Three studies found maternal sensitivity, non-­intrusiveness,
and a related construct of mutual mother–­infant responsiveness were associated with a faster
achievement of motor milestones of infants born preterm at the CA of 6  weeks (White-­Traut
et al., 2018), 6 months (Feldman et al., 2002), and 12 months (Pridham et al., 2002). A fourth
study showed that infants with low birthweight, whose mothers touched them more frequently
at the CA of 3 months, achieved their motor milestones faster at 12 months CA (Weiss et al.,
2004). However, in a fifth study focusing on preterm infants at the CA of 9 months, the associa-
tion of maternal sensitivity and non-­intrusiveness with faster motor milestone achievement was
documented only among preterm-­born infants with extremely low birthweight and not among
preterm-­born infants with low birthweight or full-­term infants (Neri et al., 2017). Finally, in a
sixth study of preterm-­born infants at the CA of 24 months, maternal sensitivity was associated
with slower achievement of motor milestones (Treyvaud et al., 2009). Hence, our second aim was
to reexamine the links between preterm-­born infants’ achievement of motor milestones and the
attunement of their interactions with their mothers.

5   |   T E M P E RAM E N T AN D AT TUNEMENT OF MOTHER–­

I N FA NT I NT E R ACT ION S

The third infants’ characteristic examined in this study was temperament. Temperament is con-
sidered a psychobiological characteristic that is evident in infants’ reactivity to stimuli in the
environment (Rothbart et al., 2000). It can be characterized along the following four dimensions:
Surgency refers to infants’ positive affectivity expressed via motor activity level, and smiling and
laughter (Gartstein & Rothbart, 2003). Negative affectivity reflects infants’ distress in response
to physical limitations (i.e., frustration) and sudden changes (i.e., fear; Gartstein & Rothbart,
2003). Soothability refers to the ability of infants to recover from distress in response to caregiv-
ers’ soothing efforts (Rothbart, 1986). The fourth dimension reflects self-­regulation capacities
or the ability to self-­modulate negative and positive affectivity. It involves skills that begin to
emerge at the age of 12 months. Yet one of its components, Duration of orientation, which taps
attention span to object or activity, is evident from birth (Rothbart, 1986).
It is important to consider temperament when studying infants’ motor behaviors because
during the young ages of 3–­5  months, bodily movement is a central modality through which
temperament is expressed (Planalp et al., 2017). Surgency is reflected in the frequency and in-
tensity of gross movements and movements of the face when smiling and laughing (Gartstein
& Rothbart, 2003; Rothbart, 1986). Negative affectivity is manifested by extensive upper and
lower limb movements, squirming, and back arching (Egmose et al., 2019). Soothability is evi-
dent through changes in infants’ gross movements and movements of the face from movements
LEV-­ENACAB et al.      |  417

that express distress or fussiness to movements reflecting calmness. Duration of orientation is

reflected in eye, head, and neck movement toward and away from stimuli or objects in the envi-
ronment (Rothbart, 1986).
It could be expected that lower surgency, higher negative affectivity, and lower soothability
and duration of orientation would hamper infants’ ability to maintain attuned interactions with
their mothers (Cassiano et al., 2020; Feldman, 2006; Harel et al., 2011). They might also frus-
trate the mothers and challenge their ability to attune their behavior to their infants, elicit their
infants’ responsiveness, and structure positive interactions with them (Feldman et al., 2002).
However, research on the associations between infant temperament and mother–­infant inter-
action has reported inconsistent results. A study of term-­born infants at the ages of 2–­3 months
found high negative affectivity was associated with higher maternal intrusiveness and lower
infant responsiveness (Mäntymaa et al., 2006). A second study of 3-­month-­old preterm-­born
and full-­term-­born infants and their mothers found infants’ orientation of attention and self-­
modulation of emotional arousal, but not negative affectivity, were associated with more attuned
mother–­infant interactions (Feldman, 2006). A third recent study of preterm and full-­term-­born
infants at the CA of 9 months found negative affectivity was associated with maternal respon-
siveness to non-­distress cues of the infant, but not with maternal intrusiveness or mothers’
positive regard (Vaccaro et al., 2021). Yet other studies of term-­born infants at the ages of 10–­
12 months (Haselbeck et al., 2018; Martins et al., 2012) and of preterm-­born infants at the CA
of 9 months (Poehlmann et al., 2012) and 18 and 36 months (Harel-­Gadassi et al., 2020) did not
find significant associations between the temperament of infants and the attunement of mother–­
infant interactions. It is possible that the associations between infant temperament and the qual-
ity of mother–­infant interactions are stronger during the first months of life (Feldman, 2006;
Mäntymaa et al., 2006). To the best of our knowledge, however, only Feldman (2006) has focused
on preterm-­born infants during the first 6 months of life. Hence, we reexamined this link.

6  |  T H E P RE SE N T ST U DY

We examined the associations of spontaneous movements, motor milestones, and temperament

of infants born preterm with the attunement of their interactions with their mothers at the CA of
3–­4 months. When studying mother–­infant interactions during the first 6 months of life, it may
be important to consider the modalities of maternal behaviors (Feldman & Eidelman, 2007).
In particular, maternal sensitivity displayed in touch and holding constitutes a central mode of
early interactions (Mantis et al., 2014). Parental vocalization is also considered key for preterm-­
born infants, as it facilitates infants’ vocalization during hospitalization in the NICU and is pre-
dictive of infants’ language and cognitive skills at 7 and 18 months (Caskey et al., 2014). Finally,
a study of preterm-­born infants indicated that forming and maintaining eye contact with infants
promoted mutual touch between infants and their mothers (Mantis et al., 2014) and a study of
full-­term-­born infants found maternal eye contact enhanced infants’ self-­regulation at 4 months
(Harel et al., 2011). Building on these earlier findings, we assessed maternal sensitivity across the
modalities of touch and holding, vocalization, and eye contact.
We focused on infants at the CA of 3–­4 months for three reasons. First, at these ages, most in-
fants born preterm have poorer head and body control than full-­term infants (Di Rosa et al., 2016).
Thus, their dependency on maternal attunement through holding is higher. Second, 3–­4 months
CA is considered the beginning of infants’ intentional social behaviors with their parents. Hence,
this age is optimal for assessing infants’ emerging responsiveness to and involvement with their
 |
418       LEV-­ENACAB et al.

mothers (Trevarthen & Aitken, 2001). Third, this age is optimal for evaluating spontaneous
movements because FMs are presumably at their best performance and continuity level during
this period (Ferrari et al., 2016).
We hypothesized that typical and continual spontaneous movements, more advanced motor
milestones, and less difficult temperament, in terms of higher surgency, lower negative affectiv-
ity, and higher soothability and duration of orientation would be associated with better attune-
ment of the mother–­infant dyad. Put differently, we expected each of these infant characteristics
would be associated with higher maternal sensitivity, lower maternal intrusiveness, and higher
infants’ responsiveness to and involvement with the mother.

7  |  M ET H OD

7.1  |  Participants

The present study was conducted according to guidelines laid down in the Declaration of Helsinki,
with written informed consent obtained all parents before data collection. All procedures in this
study were approved by the Helsinki Ethics Committee at the Maccabi Health Care Services and
the Human Research Review Board of the University of Haifa, Israel (#201/2015). Sixty Israeli
mothers and their preterm-­born infants participated in this study. Thirty-­nine of these dyads
participated in our pilot study (Lev-­Enacab et al., 2015). Dyads were recruited via flyers in NICUs
and pediatric clinics, and electronic flyers were published on social networks sites for mothers of
infants. Of the 80 mothers who responded to the flyers, eight refused to be video-­recorded, and
11 postponed their approval; by the time they agreed, their infants were older than 22 weeks CA.
The remaining 61 mother–­infant dyads participated in the study. Considering this was the first
study to examine the interplay between the aforementioned motor behaviors of infants born pre-
term and the attunement of their interactions with their mothers, we chose to focus on healthy
infants. Therefore, exclusion criteria were intra-­uterine growth retardation, perinatal asphyxia,
genetic or metabolic diseases, hearing impairment, retinopathy of prematurity, major congenital
defects, oxygen treatment after release from the NICU, or any operation during or after hospi-
talization. One infant met one of the criteria. Data collected for this infant and her mother were
not included in analyses.
Thirty-­seven (61.66%) mothers were Jewish native Israeli; 10 (16.67%) were Jewish Israeli im-
migrants from Eastern Europe, North America, or North Africa; 5 (8.33%) were Muslim–­Arab
native Israeli; 4 (6.67%) were Christian–­Arab native Israeli; 3 (5%) were Christian–­non-­Arab im-
migrants from Eastern Europe; 1 (1.67%) was Druze native Israeli. This distribution suggests
the sample was representative of the diverse Israeli society from which it was drawn (Israel
Central Bureau of Statistics, 2021). Mothers’ age range was 20–­47 years (Mdn = 35, Interquartile
range = 31.25–­38.00), and all except three were married. The educational level of the mothers
ranged from high school diploma (12 mothers, 20.00%) to a doctorate (1 mother, 1.67%). Forty-­
eight (80.00%) had post-­high school education.
Participating infants (35  males, 58.33%) were at the CA of 12 to 22  weeks (Mdn  =  14,
Interquartile range = 13–­16). Infant were born between 26 and 34 weeks of gestation (Mdn = 33,
Interquartile range  =  30–­34). Twenty (33.33%) were firstborns, and 19 (31.67%) were one of
twins. Only one twin from each pair was randomly selected for participation. Infants’ birth-
weight ranged from 715 to 2600  gr (M  =  1763.92  gr, SD  =  454.51). Thirty-­five (58.33%) were
born in a cesarean labor. Seventeen (25.4%) did not need any medical interventions in the NIUC,
LEV-­ENACAB et al.      |  419

35 (52.2%) received mild interventions, such as phototherapy for neonatal jaundice, and nine
(13.4%) needed breathing support for more than 3 days or received caffeine therapy. Forty-­one
(68.33%) mothers kangarooed their infant (i.e., held the infant “skin to skin”) in the NICU for at
least 4 days.

7.2  |  Procedure

Data were collected during 2012–­2014 by trained developmental physiotherapists. Home visits
were conducted for all participants except for three families who preferred to meet at the pediat-
ric clinic. The meeting was set at a time when the infant was likely to be awake and calm. If the
infant showed signs of distress during data collection, the assessment was stopped and resumed
only if the infant calmed down. The study procedures were as follows.
First, to assess infants’ spontaneous movements, we followed the protocol of the General
Movement Assessment according to Prechtl (Einspieler et al., 2004) and videotaped the in-
fants lying supine on a mattress, partially dressed, and without any stimulation for approx-
imately four minutes. During this time, mothers were asked to complete a temperament
questionnaire (The Infant Behavior Questionnaire; Rothbart, 1981) and a demographic ques-
tionnaire. One infant turned repeatedly to a side-­lying position. Thus, the spontaneous move-
ments of this infant could not be assessed. Next, to assess the attunement of mother–­infant
interactions, mothers were invited to join their infants on the mattress and play with them for
10 minutes as they usually did, but without any toys or a pacifier. This type of unstructured
“social play” is common in research of mother–­infant and mother–­child interactions (e.g.,
Miller & Harwood, 2002; Zreik et al., 2017). As we were interested in examining maternal
sensitivity in the modality of touch and holding, we asked the mothers to pick up the infant
from the mattress and put the infant down at least once during the interaction. The timing
of picking up, holding, and putting the infant down was the mothers’ choice. However, if the
mother did not pick up the infant or did not put the infant down on the mattress within nine
minutes, she was reminded to do so by the researcher. The mother–­infant interactions were
videotaped. Finally, to assess motor milestones, infants were videotaped while positioned by
the researcher supine, prone, sitting, and standing in accordance with the administration
procedure of the Alberta Infant Motor Scale (AIMS; Piper et al., 1994). The assessment of
motor milestones of one infant was not completed, because the infant was distressed and did
not calm down.

7.3  |  Assessments

7.3.1  |  Mother and Infant Attunement (MIA)

This coding system was adapted by the first and second authors from the widely used Emotional
Availability Scales (EAS; Biringen et al., 2000; see a review in Biringen et al., 2014) (Lev-­Enacab
& Sher-­Censor, 2012). The second author is an expert coder of the EAS. In line with the EAS,
the MIA coding system examined maternal sensitivity and non-­intrusiveness, as well as infants’
responsiveness and involvement. Because we were interested in examining maternal sensitiv-
ity separately in each modality, we expanded the maternal sensitivity scale from the EAS to
three subscales: sensitivity of touch and holding, sensitivity of vocalization, and sensitivity of eye
 |
420       LEV-­ENACAB et al.

contact. The subscale of sensitivity of touch and holding was based also on the measurement of
maternal touch of preterm-­born infants (Feldman, 1998; Feldman, Eidelman, et al., 2002).

Maternal sensitivity
As noted above, maternal sensitivity comprised three subscales.
Sensitivity in the modality of touch and holding was subscale consisted of sensitivity of touch
(i.e., kissing, patting, hugging, or using a deep touch the infant seemed to enjoy and while show-
ing positive affect toward the infant); sensitivity of picking up the infant from the mattress (i.e.,
gradually picking the infant up while keeping the infant's body, especially the head and hands,
gathered); sensitivity of holding the infant (i.e., in an attuned holding, the infant is held close to
the mother's body and the infant's head and neck are supported); sensitive speed of changing the
infant's position while held in the mother's arms (i.e., the mother changes the infant's position in
her arms gradually and is attentive to the infant's reactions); sensitivity of putting the infant down
on the mattress (i.e., the mother puts her infant down slowly and carefully while being attentive
to the infant and keeping the infant's body, especially head and neck, safe and gathered). Except
for sensitivity of touch, which was coded using a 7-­point scale, the other aspects of maternal
sensitivity in the modality of touch and holding were rated using 6-­point scales. The scores were
highly intercorrelated (.32 < r < .59, p's < .05, respectively). As we did not have specific hypoth-
eses for these modalities, we aggregated them based on their mean, after transforming them to
z-­scores. Higher scores reflected higher sensitivity in the modality of touch and holding.
Sensitivity of vocalization was rated using a 6-­point scale ranging from “1” non-­sensitive vocal-
ization (i.e., using a hostile tone of voice or a very loud voice that seemed to startle the infant or
a verbal communication that was hostile to or mocked the infant) to “6” highly sensitive vocal-
ization (i.e., a pleasant vocalization and verbal communication that seemed to match the infant's
cues).
Sensitivity of eye contact was coded on a 6-­point scale ranging from “1” low sensitivity (i.e.,
mothers who avoided eye contact) to “6” high sensitivity (i.e., mothers who frequently looked at
their infants, in a manner attuned to the infants, thereby creating a synchronized eye contact).
The intercorrelations of the scores of mothers’ sensitivity of touch and holding, vocalization,
and eye contact were high and ranged from.57 to.79, p's < .05. Hence, we formed a maternal sen-
sitivity aggregated score by averaging their z-­scores.

Maternal Non-­Intrusiveness
Mothers were rated on a 6-­point non-­intrusiveness scale, reflecting their respect of the infant's
autonomy. High scores represented lack of interference in and interruptions of the infant's move-
ments and positions. Lower scores indicated that mothers were overstimulating, changing in-
fants’ positions frequently and abruptly, interfering with their activity, or overprotecting them.

Infants’ responsiveness
This 6-­point scale reflected infants’ response to their mothers’ interactive suggestions. A score
of “1” represented avoidance or reluctance to engage with the mother, and a score of “6” repre-
sented responses to maternal suggestions with a positive affect.

Infants’ involvement
This 6-­point scale indicated infants’ initiations of interaction with their mother by, for example,
making eye contact. A score of “1” represented lack of initiations and “6” represented frequent
initiations.
LEV-­ENACAB et al.      |  421

As the correlation between infants’ responsiveness and involvement was high (r  =  .90,
p < .01), and as we did not have specific hypotheses for either scale, we combined their mean
scores to one scale, infants’ attunement.
The fifth author, who was blind to other information regarding the families, was trained by
the first author and coded the dyadic interactions. To establish reliability, 15 (25%) dyads were
also coded by the first author. Both coders were developmental physiotherapists with an MA in
child development. Inter-­rater agreement of the MIA scales was good and ranged from ICC = .83
(sensitivity of holding the infant) to ICC = .99 (sensitivity of vocalization). Average ICC across
scales was .93. Disagreements were resolved through discussion, until consensus was reached.
For information on the reliability and validity of the MIA scales obtained in our pilot study, see
Lev-­Enacab et al. (2015).

7.3.2  |  General Movement Assessment (GMA) according to Prechtl

The GMA is widely used to assess infants’ spontaneous movements and is considered the most ac-
curate for early diagnosis of neurodevelopmental disorders (e.g., Bruggink et al., 2009; Einspieler
et al., 2019, 2004; Snider et al., 2008). We used the GMA to code the following aspects of infants’
spontaneous movements.

Fidgety Movements (FMs)

FM is the predominant movement pattern in the awake, non-­crying, or fussy infant, between
3 and 5  months CA. FMs’ temporal organization of infants with neurotypical development is
either continual or intermittent and is characterized by small amplitude, moderate speed, and
variable acceleration of movements of the neck, trunk, and limbs in all directions (Einspieler
et al., 2019). Infants’ FMs were coded as “2” normal expression, “1” abnormal expression (i.e., the
amplitude, speed, and jerkiness were moderately to greatly exaggerated), or “0” absent (non or
sporadic FMs were observed during the recording). Next, we assessed the temporal organization
of infants’ FMs using the Temporal Organization of FMs Scale. We assigned a score of “2” when
the temporal organization of FMs was continual; i.e., FMs occurred frequently with very short
pauses of 1–­2 seconds and were present all over the body. We assigned a score of “1” when the
temporal organization of the infant's FMs was intermittent; i.e., FMs occurred in all body parts,
but the frequency was low, with pauses of around 10 seconds. Finally, we assigned a score of “0”
when the FMs were sporadic or absent; i.e., they were seldom seen or occurred with pauses of
over 1 minute (Einspieler et al., 2015). All infants who had absent FMs were assigned a score of
"0" on the FMs temporal organization scale. Only one infant in this sample was rated as show-
ing abnormal FMs. The temporal organization of the infant's FMs was continual, and therefore
he received a score of “2” on the FMs temporal organization scale. Because this infant may be
considered an outlier, we preformed the analyses with and without him, and obtained similar
results. Thus, we included this infant in the reported results. All other infants received a score
of normal FMs and were rated with scores of “2” (continual) or “1” (intermittent) on the FMs
temporal organization scale. For parsimony, we used only the FMs’ temporal organization scale
in data analyses.

Movement character
Movement character reflects the variability, complexity, and sequence of movements of the
limbs, neck, and trunk. Smooth and fluent, variable, and complex movements were scored as
 |
422       LEV-­ENACAB et al.

“2” (typical). We assigned a score of "1" (atypical) when the infant showed monotonous, jerky,
or stiff movements, movements with large or small amplitude, or movements with reduced com-
plexity. A cramped synchronized movement (e.g., limbs and trunk muscles contracting almost
simultaneously and relaxing almost simultaneously) was scored as “0” (abnormal; Einspieler
et al., 2019). None of the participating infants showed abnormal movement character. As the
FMs temporal organization and movement character were closely associated (Kendall's T = .51,
p < .01) and to reduce the number of variables, we computed the mean of the two scores. We
labeled the new construct infants’ spontaneous movements. Scores ranged from “0” to “2”, with
higher scores reflecting typical and continual spontaneous movements.
Video recordings of infants’ spontaneous movements were assessed by the first author, a de-
velopmental physiotherapist with an MA in Child Development, who was certified for coding
the GMA. To establish inter-­rater reliability, the third author, a physiologist and an expert and
licensed tutor for the GMA, who was blind to all other information on the participants, also
coded 30 video recordings (50.00%). These included the 15 dyads for whom, as described above,
the first author coded the MIA scores. Inter-­rater agreement was good (KappaFMs continuity = .69;
KappaMovement Character = 1.00). Agreement was comparable to or exceeded the inter-­rater agree-
ment reported in prior research (e.g., Einspieler et al., 2019). Disagreements were resolved
through discussion until consensus was reached.

7.4  |  Alberta Infant Motor Scale (AIMS)

The AIMS is a widely used motor development assessment. It is commonly used in clinics and
research settings to assess motor delays in term-­born and preterm-­born infants (e.g., Knorr et al.,
2017; Piper et al., 1994). The AIMS examines the rate of infants’ achievement of motor milestones
from birth to 18 months, as observed in four positions: supine, prone, sitting, and standing. The
observer minimally intervenes when needed by positioning the infant and/or by playing with
the infant to encourage the infant to exhibit the most advanced motor milestones. To calculate
the AIMS score, the number of fully performed milestones is calculated for each position sepa-
rately and summed to a total raw score. Next, the total raw score is converted to a percentile
age-­dependent norm scale (Darrah et al., 1998). A cutoff point of less than 10th percentile has
70% sensitivity to later motor deficiencies (Darrah et al., 1998). We converted the percentile raw
scales to a 6-­point scale, ranging from “1” (below 5th percentile) to “6” (above 75th percentile).
The assessments were videotaped and rated by the fourth author, a developmental physiother-
apist, who is well trained and qualified to use the AIMS coding system. She was blind to all other
information on the participants. The first author also coded 15 of the cases (25%) for inter-­rater
reliability, which was excellent (ICC = .94), similar to previous reports (ICC = .99; Piper et al.,
1992). These 15 cases were the same as the ones for whom the first author coded the MIA scores.

7.5  |  Infant Behavior Questionnaire (IBQ)

Mothers responded to 94 items of the IBQ describing infants’ temperament-­related behaviors

(Rothbart, 1981). Mothers were invited to rate the frequency of infants’ behaviors observed over
the past two weeks using a 7-­point scale ranging from “1” never to “7” always, with “X” as non-­
relevant. Three items were omitted from data analyses, because participating mothers rated them
as non-­relevant. Two of these items do not apply for infants at the ages of 3–­4 months (namely,
LEV-­ENACAB et al.      |  423

approaching at once when introduced to a dog or a cat and soothing in responses to a security
object). The third was an open-­ended question regarding “other soothing techniques” which
mothers tended to use.
The remaining 91 items were grouped to four dimensions (Rothbart, 1986). Surgency in-
cluded 32 items reflecting level of motor activity, which indicated the frequency and intensity of
infants’ gross movements during daily activities (e.g., “During feeding, how often did the baby
squirm or kick?”), and smiling and laugher under safe conditions (e.g., “When put into bath
water, how often did the baby smile?”). Negative affectivity included 39 items reflecting infants’
distress to limitation, namely, fussing and crying when waiting for food or put in a confining
place or position (e.g., “How often during the last week did the baby protest when being put in
a confining place [infant seat, play pen, car seat, etc.]?”); and fear reactions, namely showing
distress in response to sudden changes and latency of movement toward a new person or object
(e.g., “How often during the last week did the baby cry or show distress at a loud sound [blender,
vacuum cleaner, etc.]?”). Soothability included nine items tapping infants’ reduced fussing and
crying in response to mothers’ soothing efforts (e.g., “Have you tried the technique of rocking in
the past two weeks? If so, how often did this method soothe the baby?”). Duration of orientation
was consisted of 11 items capturing infants’ attention span when looking at or interacting with a
single object or activity (e.g., “How often did the baby repeat the same movement with an object
for 2 min or longer [e.g., kicking or hitting a mobile]?”). After reveres coding of relevant items,
internal reliability was calculated using Cronbach's α; it was .89 for surgency, .95 for negative
affectivity, .78 for soothability, and .87 for duration of orientation.

7.6  |  Family demographics and infants’ neonatal characteristics

Mothers were invited to complete a demographic questionnaire on their age, education level,
family status, number of children, birth order, ethno-­cultural origin, and infant gender. In addi-
tion, they were asked to report the infants’ birth week of gestation, birth date, birthweight, length
of stay in the NICU, medical interventions the infant received and the use of kangaroo care in
the NICU.

8  |  R E S U LTS

Descriptive statistics are provided in Table 1. The distribution of all variables was sufficiently
normal to render parametric statistics valid (Afifi et al., 2007). The following background vari-
ables were associated with the study variables: lower birthweight was correlated with slower
achievement of motor milestones (r  =  .28, p  =  .032) and older maternal age and birth order
were related to mothers’ reports of lower levels of infants’ surgency (r = −.30 p = .022; r = −.33,
p = .012 respectively). Thus, birthweight, mother age, and birth order were considered in further
analyses.
The study hypothesis was first examined using bivariate correlations between infants’ charac-
teristics (i.e., spontaneous movements, achievement of motor milestones, temperament dimen-
sions) and the mother–­infant attunement. As shown in Table 2, infants’ typical and continual
spontaneous movements were associated with higher maternal sensitivity and non-­intrusiveness,
as well as higher infant attunement. Faster achievement of motor milestones was significantly
associated with higher maternal non-­intrusiveness but not with maternal sensitivity or infant
 |
424       LEV-­ENACAB et al.

T A B L E 1   Descriptive statistics of study variables (N = 60)

Variable M (SD) Range

Mother–­infant attunement
Maternal sensitivity (z-­scores)a 0.00 (0.81) −2.06 to 0.98
Maternal non-­intrusiveness 4.58 (1.32) 1.00 to 6.00
Infant attunement 4.58 (1.21) 1.00 to 6.00
Infants’ spontaneous movements (n = 59)b 1.53 (0.50) 0.50 to 2.00
Infants’ achievement of motor milestones (percentile rank; 4.14 (1.06) 1.00 to 6.00
n = 59)c
Infants’ temperament (n = 57)d
Surgency 4.20 (0.68) 2.62 to 5.70
Negative affectivity 2.85 (0.63) 1.17 to 4.53
Soothability 5.02 (1.11) 2.71 to 7.00
Duration of orientation 4.58 (1.17) 2.11 to 6.64
a
Maternal sensitivity was based on maternal sensitivity of touch and holding, vocalization, and eye contact subscales. To
aggregate them, they were transformed to z-­scores and then averaged.
b
One infant turned repeatedly to a side-­lying position. Thus, spontaneous movements could not be assessed.
c
The assessment of one infant was not completed, because the infant was distressed and did not calm down.
d
The reports of three mothers were unavailable due to a technical error.

T A B L E 2   Intercorrelations of study variables (N = 57–­60)

1 2 3 4 5 6 7 8 9
1. Maternal sensitivity –­ .74** .71** .36* .07 −.22 −.07 −.27* −.25
2. Maternal non-­intrusiveness –­ .52** .46** .30* −.23 −.09 −.17 −.20
3. Infant attunement –­ .36** .09 −.10 −.07 −.03 −.08
4. Infants’ spontaneous –­ .36** .03 .16 .12 −.06
movementsa
5. Infants’ achievement of motor –­ −.03 −.07 −.01 −.15
milestones
6. Infants’ surgency –­ .−.05 .32* .52*
7. Infants’ negative affectivity –­ −.06 −.07
8. Infants’ soothability –­ .22
9. Infants’ duration of orientation –­
a
Associations involving spontaneous movements were evaluated using the Spearman tests.
*p < .05; **p < .01.

attunement. Lower soothability was significantly associated with higher maternal sensitivity but
not with maternal non-­intrusiveness or infant attunement. Infants’ surgency, negative affectivity,
and duration of ordination were not related to mother–­infant attunement.
In the next step, we conducted regression analyses. Maternal sensitivity and maternal non-­
intrusiveness were the dependent variables in the regression models. The results of correlation
analyses informed the selection of variables for each model. Among background variables, only
birthweight was associated with a study variable that was significantly correlated with mother–­
infant attunement, namely infants’ achievement of motor milestones, and hence it was the
LEV-­ENACAB et al.      |  425

T A B L E 3   Regression results of attunement of maternal sensitivity and non-­intrusiveness on infants’

negative affectivity, achievement of motor milestones, and spontaneous movements (N = 56–­59)

Maternal sensitivity Maternal non-­intrusiveness

Variable in regression β (entry) β (final) ΔR2 β (entry) β (final) ΔR2

Block 1 –­ .01
Birthweight –­ –­ .08 −.04
Block 2 .08* .08*
Infants’ soothability −.29* −.34** –­ –­
Infants’ achievement –­ –­ .30* .19
of motor milestones
Block 3 .15** .16**
Infants’ spontaneous .40** .43**
movements
Total R 2 .24 .25
Final model F (2, 53) = 8.20*** F (3, 54) = 6.14**
*p < .05; **p < .01; ***p < .001.

only background variable included in the regression analyses. The first block of the regression
model of maternal sensitivity included infants’ soothability; this was followed by infants’ sponta-
neous movements in the second block. The first block of the regression model of maternal non-­
intrusiveness included infants’ birthweight. The second block included infants’ achievement of
motor milestones; this was followed by spontaneous movements in the third block. We included
soothability or the achievement of motor milestones and spontaneous movements in separate
blocks because we wanted to document the unique contribution of each of these variables to the
explained variance of the attunement of mother–­infant interaction. Spontaneous movements
were entered in the final block because we wanted to examine its added value in research of
mother–­infant interaction, which to the best of our knowledge was not examined thus far.
As Table 3 shows, both soothability and infants’ spontaneous movements contributed sig-
nificantly to the explained variance in maternal sensitivity. Lower soothability and typical
and continual spontaneous movements were associated with higher maternal sensitivity. As
also shown in Table 3, faster achievement of motor milestones was significantly associated
with higher levels of maternal non-­intrusiveness after controlling for infant birthweight.
Yet the effect became non-­significant when we included spontaneous movements in the re-
gression model. Only the spontaneous movements contributed significantly to the explained
variance of maternal non-­intrusiveness in the final regression model. More specifically, in-
fants’ typical and continual spontaneous movements were associated with higher maternal
non-­intrusiveness.

9  |  DI S C USSION

Our goal was to identify characteristics of preterm-­born infants that are associated with the
attunement of mother–­infant interactions, looking specifically at motor behaviors. We found
infants’ spontaneous movement was the only characteristic consistently associated with attune-
ment. As hypothesized, typical and continual spontaneous movements were associated with
 |
426       LEV-­ENACAB et al.

mothers’ attunement in terms of higher maternal sensitivity and non-­intrusiveness and with
infants’ attunement in terms of higher responsiveness and involvement.
Previous work has found infants’ cuteness facilitates parental caretaking and fosters increased
attention and positive affect toward the infant (Glocker et al., 2009; Golle et al., 2015; Kringelbach
et al., 2016). Thus, the elegancy and cuteness of infants’ smooth and fluent gross movements that
accompany the continual expression of FMs (de Raeymaecker, 2006; Einspieler et al., 2016, 2019)
may facilitate mothers’ positive affect and responsiveness. Infants with repetitive and/or stiff
movements with low/intermittent continuity of FMs may look less cute in their movements, and
this may lead to less frequent expressions of positive affect by their mothers (Golle et al., 2015).
At the same time, infants’ smooth and fluent spontaneous movements may enable them to
initiate and maintain positive engagement in the interaction. Repetitive, jerky, and stiff move-
ments may hamper infants’ ability to bring their arms and legs to and maintain them at the
midline or at the direction of their mother's face (Fjørtoft et al., 2016), thus limiting their ability
to initiate and maintain interactions (Egmose et al., 2019). Mothers may unintentionally respond
to these difficulties in less sensitive and more intrusive ways. For example, mothers may unin-
tentionally “chase” their infants and intrusively move the infants’ body and face toward them to
maintain longer eye-­to-­eye contact and turn-­taking. Infants’ jerky and stiff movements may also
lead mothers to hold the infants too tightly and change their position abruptly and firmly when
picking up, holding, and putting the infants down.
Another interpretation of the association between infants’ spontaneous movements and
mother–­infant attunement is that infants’ more typical and continual spontaneous movements
could be a proxy for a less medically involved course of recovery from preterm birth and/or a
less complicated medical situations, which led to a preterm birth, with these infants being more
capable of engaging in the interaction. In line with the study of Fjørtoft et al. (2016), our data
did not reveal significant associations between infants’ gestational age, medical condition or
interventions in the NICU and their spontaneous movements or mother-­–­infant attunement.
Nevertheless, future studies may benefit from assessing more thoroughly various prenatal and
postnatal medical risks.
The results of this research replicated those of our pilot study's smaller sample (Lev-­Enacab
et al., 2015). We have extended this earlier work by documenting that spontaneous movements
are associated not only with maternal sensitivity and infant attunement but also with mater-
nal non-­intrusiveness and by showing that the links between the spontaneous movements and
mother–­infant attunement hold when controlling for two additional characteristics of the in-
fants, achievement of motor milestones and temperament. To the best of our knowledge, these
are the only two studies to examine links between spontaneous movement and early mother–­
infant interaction. Additional studies are needed to replicate the results.
The current study indicated that faster achievement of motor milestones was correlated only
with maternal non-­intrusiveness, not with maternal sensitivity or infant attunement. Moreover,
the link between the achievement of motor milestones and maternal non-­intrusiveness became
non-­significant when taking into account infants’ spontaneous movements. Our research joins
the few studies on this issue. Previous work has reported inconsistent results (Feldman, Eidelman,
et al., 2002; Pridham et al., 2002; Weiss et al., 2004; White-­Traut et al., 2018; versus Neri et al.,
2017; Treyvaud et al., 2009). Notably, only one of these studies involved infants younger than
6 months (White-­Traut et al., 2018). This study documented a positive effect of an early interven-
tion program for mothers of preterm infants on the motor development of the infants at the CA
of 6 weeks. All other studies included older infants. Younger infants have fewer motor abilities;
hence, the differences between fast and slow achievement of motor milestones (i.e., infants who
LEV-­ENACAB et al.      |  427

are classified at the 75th percentile or above and those classified at or below the 5th percentile;
Piper et al., 1994) are smaller. This may hinder the ability to detect significant associations with
infant-­mother interactions. Future studies may benefit from a wider age range of infants born
preterm to further understand whether the achievement of motor milestones is associated with
the attunement of mother–­infant interactions.
Our hypothesis of an association between infants’ difficult temperament and lower attune-
ment of interactions was not supported. Unexpectedly, only one aspect of infants’ tempera-
ment was associated with only one aspect of mother–­infant interactions, and the direction of
the association was contrary to our hypothesis: Higher soothability was associated with lower
maternal sensitivity. This finding suggests that mothers who reported their infants were more
adaptive to their soothing techniques tended to respond to their infants’ signals in a less attuned
manner. A possible explanation of this finding is related to the fact that infants’ soothability
was reported by the mothers. Maternal sensitivity involves accurate interpretation of infants’
emotional states and emotional needs (Ainsworth, 1969). It could be that less sensitive mothers
tended unintentionally to perceive their infants’ soothability less accurately, and viewed them
as needing less or briefer soothing to recover from distress (Benoit et al., 1997).
Prior research with older infants born preterm did not find significant links between tem-
perament and the quality of mother–­infant interactions (e.g., Poehlmann et al., 2012; Vaccaro
et al., 2021). We are aware of one study of 3-­month-­old preterm-­born infants that examined this
link. Unlike our study, this study found infants’ duration of orientation and self-­modulation of
emotional arousal (the latter measure is not included in the mothers’ self-­reports we used) were
associated with higher mother–­infant synchronization, rated using a microanalytic coding sys-
tem (Feldman, 2006). As our study and this former research used different measures of infant
temperament and mother–­infant interactions, more research is needed to shed light on whether
infant temperament is related to preterm-­born infants’ and mothers’ behaviors during early in-
teractions. Future studies may also benefit from recruiting larger samples to better examine the
potential moderating role of temperament in the links between infants’ motor behaviors and
mother–­infant attunement (Ghera et al., 2006).
Several limitations of the study suggest fruitful directions for future research. First, data were
collected concurrently, thus precluding the interpretation of causal effects. Spontaneous move-
ment, the achievement of motor milestones, and soothability may shape the behavior of the infant
and consequently the behavior of the mother during shared interactions. Nevertheless, mother–­
infant interactions may also influence infants’ motor behaviors, and color maternal reports of
infants’ soothability. A recent pilot study of an early intervention for preterm-­born infants with
abnormal movement character, in which the medical staff and parents practiced typical and con-
tinual sequences of movement character with the infants, found this intervention improved in-
fants’ spontaneous movements (Soloveichick et al., 2020). Furthermore, the infants in this study
showed normal motor and cognitive development at the ages of 2 and 4 years (Soloveichick et al.,
2020). Such intervention studies, as well as longitudinal studies, are needed to enrich our un-
derstanding of the bi-­directional associations between motor behaviors of infants born preterm
and their early interactions with their parents. The second limitation is the sample selection; we
included only low-­risk families (i.e., the majority of mothers were married and had a high level
of education) and low-­risk preterm-­born infants (none had cramped synchronized movements,
and all were healthy preterm-­born infants). More research is required before we can generalize
our findings to high-­risk dyads.
Despite these limitations, our research suggests the evaluation of spontaneous movements of
preterm-­born infants, typically used to detect early neurological deficiencies (Einspieler et al.,
 |
428       LEV-­ENACAB et al.

2019), should be included in research on early interactions between preterm-­born infants and
their mothers. Our study also suggests that early intervention and prevention programs for par-
ents of preterm-­born infants should attempt to raise the awareness of parents regarding infants’
spontaneous movements and soothability and their possible associations with the attunement of
parent–­infant interactions.

ACKNOWLEDGEMENTS
This research was supported by the Israeli Physiotherapy Society, Maccabi Health Care Service
and the Herta and Paul Amir Faculty of Social Sciences, University of Haifa, Israel. We would
like to thank the families who participated in this research, and Einav Manor from the NICU in
Rambam Hospital, Haifa, Israel, for her help in the recruitment of families.

CONFLICT OF I NTEREST
The third author, Professor Einspieler Christa is a licensed tutor of the General Movement
Assessment (GMA) according to Prechtl.

ORCID
Efrat Sher-­Censor  https://orcid.org/0000-0003-2961-3129

REFERENCES
Afifi, A. A., Kotlerman, J. B., Ettner, S. L., & Cowan, M. (2007). Methods for improving regression analysis for
skewed continuous or counted responses. Annual Review of Public Health, 28, 95–­111. https://doi.org/10.1146/
annur​ev.publh​ealth.28.082206.094100
Ainsworth, M. D. (1969). Maternal sensitivity scales. Power, 6, 1379–­1388.
Bartling, K., Kopp, F., & Lindenberger, U. (2010). Maternal affect attunement: Refinement and internal valida-
tion of a coding scheme. International Journal of Developmental Science, 4(1), 1–­17. https://doi.org/10.3233/
DEV-­2010-­4101
Benoit, D., Zeanah, C. H., Parker, K. C., Nicholson, E., & Coolbear, J. (1997). “Working model of the child interview”:
Infant clinical status related to maternal perceptions. Infant Mental Health Journal: Official Publication of the
World Association for Infant Mental Health, 18(1), 107–­121. https://doi.org/10.1002/(SICI)1097-­0355(19972​
1)18:1<107::AID-­IMHJ8​>3.0.CO;2-­N
Bilgin, A., & Wolke, D. (2015). Maternal sensitivity in parenting preterm children: A meta-­analysis. Pediatrics,
136(1), e177–­e193. https://doi.org/10.1542/peds.2014-­3570
Biringen, Z., Derscheid, D., Vliegen, N., Closson, L., & Easterbrooks, M. (2014). Emotional availability (EA):
Theoretical background, empirical research using the EA Scales, and clinical applications. Developmental
Review, 34(2), 114–­167. https://doi.org/10.1016/j.dr.2014.01.002
Biringen, Z., Robinson, J. L., & Emde, R. N. (2000). Appendix B: The emotional availability scales (an abridged
infancy/early childhood version). Attachment & Human Development, 2(2), 256–­270. https://doi.
org/10.1080/14616​73005​0085626
Bornstein, M. H. (2013). Mother-­infant attunement: A multilevel approach via body, brain, and behavior. In M.
Legerstee, D. W. Haley, & M. H. Bornstein (Eds.), The infant mind: Origins of the social brain (pp. 266–­298).
The Guilford Press.
Bruggink, J. L. M., Einspieler, C., Butcher, P. R., Stremmelaar, E. F., Prechtl, H. F. R., & Bos, A. F. (2009). Quantitative
aspects of the early motor repertoire in preterm infants: Do they predict minor neurological dysfunction at
school age? Early Human Development, 85(1), 25–­36. https://doi.org/10.1016/j.earlh​umdev.2008.05.010
Bruggink, J. L. M., Einspieler, C., Butcher, P. R., Van Braeckel, K. N. J. A., Prechtl, H. F. R., & Bos, A. F. (2008). The
quality of the early motor repertoire in preterm infants predicts minor neurologic dysfunction at school age.
The Journal of Pediatrics, 153(1), 32–­39. https://doi.org/10.1016/j.jpeds.2007.12.047
Caskey, M., Stephens, B., Tucker, R., & Vohr, B. (2014). Adult talk in the NICU with preterm infants and develop-
mental outcomes. Pediatrics, 133(3), e578–­584. https://doi.org/10.1542/peds.2013-­0104
LEV-­ENACAB et al.      |  429

Cassiano, R. G., Provenzi, L., Linhares, M. B. M., Gaspardo, C. M., & Montirosso, R. (2020). Does preterm birth
affect child temperament? A meta-­analytic study. Infant Behavior and Development, 58, 101417. https://doi.
org/10.1016/j.infbeh.2019.101417
Darrah, J., Piper, M., & Watt, M. J. (1998). Assessment of gross motor skills of at-­risk infants: Predictive validity
of the Alberta Infant Motor Scale. Developmental Medicine & Child Neurology, 40(7), 485–­491. https://doi.
org/10.1111/j.1469-­8749.1998.tb153​99.x
De Raeymaecker, D. M. (2006). Psychomotor development and psychopathology in childhood. International
Review of Neurobiology, 72, 83–­101. https://doi.org/10.1016/S0074​-­7742(05)72005​-5­
Di Rosa, G., Cavallaro, T., Alibrandi, A., Marseglia, L., Lamberti, M., Giaimo, E., Nicotera, A., Bonsignore, M., &
Gagliano, A. (2016). Predictive role of early milestones-­related psychomotor profiles and long-­term neuro-
developmental pitfalls in preterm infants. Early Human Development, 101, 49–­55. https://doi.org/10.1016/j.
earlh​umdev.2016.04.012
Egmose, I., Væver, M. S., Smith-­Nielsen, J., Varni, G., & Køppe, S. (2019). Motor activity and spatial proximity:
Relationships to infant emotions and maternal postpartum depression. Infant Behavior and Development, 57,
101335. https://doi.org/10.1016/j.infbeh.2019.101335
Einspieler, C., Bos, A. F., Krieber-­Tomantschger, M., Alvarado, E., Barbosa, V. M., Bertoncelli, N., Burger, M.,
Chorna, O., Del Secco, S., DeRegnier, R.-­A., Hüning, B., Ko, J., Lucaccioni, L., Maeda, T., Marchi, V., Martín,
E., Morgan, C., Mutlu, A., Pansy, J. & Marschik, P. B. (2019). Cerebral Palsy: Early markers of clinical pheno-
type and functional outcome. Journal of Clinical Medicine, 8(10), 1616. https://doi.org/10.3390/jcm81​01616
Einspieler, C., Bos, A. F., Libertus, M. E., & Marschik, P. B. (2016). The general movement assessment helps
us to identify preterm infants at risk for cognitive dysfunction. Frontiers in Psychology, 7, 406. https://doi.
org/10.3389/fpsyg.2016.00406
Einspieler, C., Prechtl, H. F. R., Bos, A. F., Ferrari, F., & Cioni, G. (2004). Prechtl’s method on the qualitative assess-
ment of general movements in preterm, term and young infants. Mac Keith Press.
Einspieler, C., Yang, H., Bartl-­Pokorny, K. D., Chi, X., Zang, F. F., Marschik, P. B., Guzzetta, A., Ferrari, F., Bos, A.
F., & Cioni, G. (2015). Are sporadic fidgety movements as clinically relevant as is their absence? Early Human
Development, 91(4), 247–­252. https://doi.org/10.1016/j.earlh​umdev.2015.02.003
Feldman, R. (1998). Mother-­newborn coding system manual. Tel Aviv, Israel: Bar-­Ilan University Press.
Feldman, R. (2006). From biological rhythms to social rhythms: Physiological precursors of mother-­infant syn-
chrony. Developmental Psychology, 42(1), 175. https://doi.org/10.1037/0012-­1649.42.1.175
Feldman, R., & Eidelman, A. I. (2007). Maternal postpartum behavior and the emergence of infant–­mother and
infant–­father synchrony in preterm and full-­term infants: The role of neonatal vagal tone. Developmental
Psychobiology, 49(3), 290–­302. https://doi.org/10.1002/dev.20220
Feldman, R., Eidelman, A. I., Sirota, L., & Weller, A. (2002). Comparison of skin-­to-­skin (kangaroo) and traditional
care: Parenting outcomes and preterm infant development. Pediatrics, 110(1), 16–­26. https://doi.org/10.1542/
peds.110.1.16
Feldman, R., Weller, A., Sirota, L., & Eidelman, A. I. (2002). Skin-­to-­skin contact (kangaroo care) promotes
self-­regulation in premature infants: Sleep-­wake cyclicity, arousal modulation, and sustained exploration.
Developmental Psychology, 38(2), 194–­207. https://doi.org/10.1037/0012-­1649.38.2.194
Ferrari, F., Frassoldati, R., Berardi, A., Di Palma, F., Ori, L., Lucaccioni, L., Bertoncelli, N., & Einspieler, C. (2016).
The ontogeny of fidgety movements from 4 to 20 weeks post-­term age in healthy full-­term infants. Early
Human Development, 103, 219–­224. https://doi.org/10.1016/j.earlh​umdev.2016.10.004
Fjørtoft, T., Evensen, K. A. I., Øberg, G. K., Songstad, N. T., Labori, C., Silberg, I. E., Loennecken, M., Møinichen,
U. I., Vågen, R., Støe, R., & Adde, L. (2016). High prevalence of abnormal motor repertoire at 3 months cor-
rected age in extremely preterm infants. European Journal of Paediatric Neurology, 20(2), 236–­242. https://
doi.org/10.1016/j.ejpn.2015.12.009
Fjørtoft, T., Grunewaldt, K. H., Løhaugen, G. C. C., Mørkved, S., Skranes, J., & Evensen, K. A. I. (2013). Assessment
of motor behaviour in high-­risk-­infants at 3 months predicts motor and cognitive outcomes in 10 years old
children. Early Human Development, 89(10), 787–­793. https://doi.org/10.1016/j.earlh​umdev.2013.06.007
Gartstein, M. A., & Rothbart, M. K. (2003). Studying infant temperament via the revised infant behavior question-
naire. Infant Behavior and Development, 26(1), 64–­86. https://doi.org/10.1016/S0163​-6­ 383(02)00169​-8­
Ghera, M. M., Hane, A. A., Malesa, E. E., & Fox, N. A. (2006). The role of infant soothability in the relation be-
tween infant negativity and maternal sensitivity. Infant Behavior and Development, 29(2), 289–­293. https://
doi.org/10.1016/j.infbeh.2005.09.003
 |
430       LEV-­ENACAB et al.

Glocker, M. L., Langleben, D. D., Ruparel, K., Loughead, J. W., Gur, R. C., & Sachser, N. (2009). Baby schema in
infant faces induces cuteness perception and motivation for caretaking in adults. Ethology, 115(3), 257–­263.
https://doi.org/10.1111/j.1439-­0310.2008.01603.x
Golle, J., Probst, F., Mast, F. W., & Lobmaier, J. S. (2015). Preference for cute infants does not depend on their eth-
nicity or species: Evidence from hypothetical adoption and donation paradigms. PLoS One, 10(4), e0121554.
https://doi.org/10.1371/journ​al.pone.0121554
Gueron-­Sela, N., Atzaba-­Poria, N., Meiri, G., & Marks, K. (2015). The caregiving environment and developmental
outcomes of preterm infants: Diathesis stress or differential susceptibility effects? Child Development, 86(4),
1014–­1030. https://doi.org/10.1111/cdev.12359
Harel, H., Gordon, I., Geva, R., & Feldman, R. (2011). Gaze behaviors of preterm and full-­term infants in nonsocial
and social contexts of increasing dynamics: Visual recognition, attention regulation, and gaze synchrony.
Infancy, 16(1), 69–­90. https://doi.org/10.1111/j.1532-­7078.2010.00037.x
Harel-­Gadassi, A., Friedlander, E., Yaari, M., Bar-­Oz, B., Eventov-­Friedman, S., Mankuta, D., & Yirmiya, N. (2020).
Do developmental and temperamental characteristics mediate the association between preterm birth and the
quality of mother-­child interaction? Infant Behavior and Development, 58, 101421. https://doi.org/10.1016/j.
infbeh.2020.101421
Haselbeck, C., Niederberger, U., Gubi-­Kelm, S., Jahn, F., Dautwiz, F., & Siniatchkin, M. (2018). Secure attachment
style appears to compensate for the effect of prenatal maternal distress regarding difficult infant tempera-
ment development. Zeitschrift Für Kinder-­und Jugendpsychiatrie Und Psychotherapie, 47, 239–­251. https://
doi.org/10.1024/1422-­4917/a000606
Israel Central Bureau of Statistics. (2021). Retrieved from https://www.cbs.gov.il/en/subje​cts/Pages/​Popul​ation​
aspx
Iverson, J. M. (2010). Developing language in a developing body: The relationship between motor development
and language development. Journal of Child Language, 37(2), 229–­261. https://doi.org/10.1017/S0305​00090​
9990432
Knorr, A., Stewart, J. E., McCormick, M. C., Gauvreau, K., & Belfort, M. (2017). Using the Alberta Infant Motor
Scale (AIMS) to screen for motor delay in former preterm infants: A validation study. Pediatrics, 140, 51.
https://doi.org/10.1542/peds.140.1_Meeti​ngAbs​tract.51
Korja, R., Latva, R., & Lehtonen, L. (2012). The effects of preterm birth on mother–­infant interaction and at-
tachment during the infant’s first two years. Acta Obstetricia Et Gynecologica Scandinavica, 91(2), 164–­173.
https://doi.org/10.1111/j.1600-­0412.2011.01304.x
Kringelbach, M. L., Stark, E. A., Alexander, C., Bornstein, M. H., & Stein, A. (2016). On cuteness: Unlocking
the parental brain and beyond. Trends in Cognitive Sciences, 20(7), 545–­558. https://doi.org/10.1016/j.
tics.2016.05.003
Lev-­Enacab, O., & Sher-­Censor, E. (2012). Mother and infant attunement coding manual. University of Haifa.
Lev-­Enacab, O., Sher-­Censor, E., Einspieler, C., Daube-­Fishman, G., & Beni-­Shrem, S. (2015). The quality of spon-
taneous movements of preterm infants: Associations with the quality of mother–­infant interaction. Infancy,
20(6), 634–­660. https://doi.org/10.1111/infa.12096
Mantis, I., Stack, D. M., Ng, L., Serbin, L. A., & Schwartzman, A. E. (2014). Mutual touch during mother–­infant
face-­to-­face still-­face interactions: Influences of interaction period and infant birth status. Infant Behavior
and Development, 37(3), 258–­267. https://doi.org/10.1016/j.infbeh.2014.04.005
Mäntymaa, M., Puura, K., Luoma, I., Salmelin, R. K., & Tamminen, T. (2006). Mother’s early perception of her
infant’s difficult temperament, parenting stress and early mother–­infant interaction. Nordic Journal of
Psychiatry, 60(5), 379–­386. https://doi.org/10.1080/08039​48060​0937280
Martins, E. C., Soares, I., Martins, C., Tereno, S., & Osório, A. (2012). Can we identify emotion over-­regulation in
infancy? Associations with avoidant attachment, dyadic emotional interaction and temperament. Infant and
Child Development, 21(6), 579–­595. https://doi.org/10.1002/icd.1760
Milgrom, J., Newnham, C., Anderson, P. J., Doyle, L. W., Gemmill, A. W., Lee, K., Hunt, R. W., Bear, M., & Inder,
T. (2010). Early sensitivity training for parents of preterm infants: Impact on the developing brain. Pediatric
Research, 67(3), 330–­335. https://doi.org/10.1203/PDR.0b013​e3181​cb8e2f
Miller, A. M., & Harwood, R. L. (2002). The cultural organization of parenting: Change and stability of behavior
patterns during feeding and social play across the first year of life. Parenting: Science and Practice, 2(3), 241–­
272. https://doi.org/10.1207/S1532​7922P​AR0203_03
LEV-­ENACAB et al.      |  431

Neri, E., Agostini, F., Baldoni, F., Facondini, E., Biasini, A., & Monti, F. (2017). Preterm infant development,
maternal distress and sensitivity: The influence of severity of birth weight. Early Human Development, 106,
19–­24. https://doi.org/10.1016/j.earlh​umdev.2017.01.011
Peyton, C., Yang, E., Msall, M. E., Adde, L., Støen, R., Fjørtoft, T., Bos, A. F., Einspieler, C., Zhou, Y., Schreiber, M.
D., Marks, J. D., & Drobyshevsky, A. (2017). White matter injury and general movements in high-­risk preterm
infants. American Journal of Neuroradiology, 38(1), 162–­169. https://doi.org/10.3174/ajnr.A4955
Piper, M. C., Darrah, J., Maguire, T. O., & Redfern, L. (1994). Motor assessment of the developing infant (Vol. 1, pp.
1–­14). Philadelphia: Saunders Press.
Piper, M. C., Pinnell, L. E., Darrah, J., Maguire, T., & Byrne, P. J. (1992). Construction and validation of the Alberta
Infant Motor Scale (AIMS). Canadian Journal of Public Health = Revue Canadienne de. Sante Publique, 83,
S46–­50.
Planalp, E. M., Van Hulle, C., Gagne, J. R., & Goldsmith, H. H. (2017). The infant version of the Laboratory
Temperament Assessment Battery (Lab-­TAB): Measurement properties and implications for concepts of tem-
perament. Frontiers in Psychology, 8, 846. https://doi.org/10.3389/fpsyg.2017.00846
Poehlmann, J., Hane, A., Burnson, C., Maleck, S., Hamburger, E., & Shah, P. E. (2012). Preterm infants who are
prone to distress: Differential effects of parenting on 36-­month behavioral and cognitive outcomes. Journal of
Child Psychology and Psychiatry, 53(10), 1018–­1025. https://doi.org/10.1111/j.1469-­7610.2012.02564.x
Pridham, K. F., Brown, R., Clark, R., Sondel, S., & Green, C. (2002). Infant and caregiving factors affecting weight-­
for-­age and motor development of full-­term and premature infants at 1 year post-­term. Research in Nursing &
Health, 25(5), 394–­410. https://doi.org/10.1002/nur.10047
Rothbart, M. K. (1981). Measurement of temperament in infancy. Child Development, 52, 569–­578. https://doi.
org/10.2307/1129176
Rothbart, M. K. (1986). Longitudinal observation of infant temperament. Developmental Psychology, 22(3), 356–­
365. https://psycn​et.apa.org/doi/10.1037/0012-­1649.22.3.356
Rothbart, M. K., Ahadi, S. A., & Evans, D. E. (2000). Temperament and personality: origins and outcomes. Journal
of Personality and Social Psychology, 78(1), 122. https://doi.org/10.1037/0022-­3514.78.1.122
Sherman, G. D., Haidt, J., Iyer, R., & Coan, J. A. (2013). Individual differences in the physical embodiment of care:
Prosocially oriented women respond to cuteness by becoming more physically careful. Emotion, 13(1), 151–­
158. https://doi.org/10.1037/a0029259
Snider, L. M., Majnemer, A., Mazer, B., Campbell, S., & Bos, A. F. (2008). A comparison of the general movements
assessment with traditional approaches to newborn and infant assessment: concurrent validity. Early Human
Development, 84(5), 297–­303. https://doi.org/10.1016/j.earlh​umdev.2007.07.004
Soloveichick, M., Marschik, P. B., Gover, A., Molad, M., Kessel, I., & Einspieler, C. (2020). Movement imitation
therapy for preterm babies (MIT-­PB): A novel approach to improve the neurodevelopmental outcome of
infants at high-­risk for cerebral palsy. Journal of Developmental and Physical Disabilities, 32(4), 587–­598.
https://doi.org/10.1007/s1088​2-­019-­09707​-­y
Tamm, L., Patel, M., Peugh, J., Kline-­Fath, B. M., & Parikh, N. A. & Study, C. I. N. E. P. (2020). Early brain abnor-
malities in infants born very preterm predict under-­reactive temperament. Early Human Development, 144,
104985. https://doi.org/10.1016/j.earlh​umdev.2020.104985
Trevarthen, C., & Aitken, K. J. (2001). Infant intersubjectivity: Research, theory, and clinical applications. Journal
of Child Psychology and Psychiatry, 42(1), 3–­48. https://doi.org/10.1017/S0021​96300​1006552
Treyvaud, K., Anderson, V. A., Howard, K., Bear, M., Hunt, R. W., Doyle, L. W., Inder, T. E., Woodward, T. E., &
Anderson, P. J. (2009). Parenting behavior is associated with the early neurobehavioral development of very
preterm children. Pediatrics, 123(2), 555–­561. https://doi.org/10.1542/peds.2008-­0477
Vaccaro, S. M., Tofighi, D., Moss, N., Rieger, R., Lowe, J. R., Phillips, J., & Erickson, S. J. (2021). The association of
infant temperament and maternal sensitivity in preterm and full-­term infants. Infant Mental Health Journal,
42(3), 374–­385. https://doi.org/10.1002/imhj.21915
Weiss, S. J., Wilson, P., & Morrison, D. (2004). Maternal tactile stimulation and the neurodevelopment of low birth
weight infants. Infancy, 5(1), 85–­107. https://doi.org/10.1207/s1532​7078i​n0501_4
White-­Traut, R. C., Rankin, K. M., Yoder, J., Zawacki, L., Campbell, S., Kavanaugh, K., Brandon, D., & Norr, K. F.
(2018). Relationship between mother-­infant mutual dyadic responsiveness and premature infant develop-
ment as measured by the Bayley III at 6 weeks corrected age. Early Human Development, 121, 21–­26. https://
doi.org/10.1016/j.earlh​umdev.2018.04.018
 |
432       LEV-­ENACAB et al.

Zappella, M., Einspieler, C., Bartl-­Pokorny, K. D., Krieber, M., Coleman, M., Bölte, S., & Marschik, P. B. (2015).
What do home videos tell us about early motor and socio-­communicative behaviours in children with autistic
features during the second year of life—­an exploratory study. Early Human Development, 91(10), 569–­575.
https://doi.org/10.1016/j.earlh​umdev.2015.07.006
Zreik, G., Oppenheim, D., & Sagi-­Schwartz, A. (2017). Infant attachment and maternal sensitivity in the Arab
minority in Israel. Child Development, 88(4), 1338–­1349. https://doi.org/10.1111/cdev.12692

How to cite this article: Lev-­Enacab, O., Sher-­Censor, E., Einspieler, C., Jacobi, O. A.,
Daube-­Fishman, G., & Beni-­Shrem, S. (2022). Spontaneous movements, motor
milestones, and temperament of preterm-­born infants: Associations with mother–­infant
attunement. Infancy, 27, 412–­432. https://doi.org/10.1111/infa.12451