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Infant Behavior & Development 37 (2014) 722–728
Contents lists available at ScienceDirect
Infant Behavior and Development
Brief report
Maternal cradling bias and early communicative interactions:
Implications for early identification of children at risk
Sharon Jones∗
Northeastern State University, Speech Language Pathology, 800 N. Vinita, Tahlequah, OK 74464, United States
a r t i c l e i n f o
Article history:
Received 5 February 2014
Received in revised form 17 June 2014
Accepted 26 August 2014
Available online 24 September 2014
Keywords:
Maternal cradling bias
Early communication development
Infant maternal interactions
1. Introduction
Nurturing mothers cradle their babies during the first months of life while feeding, talking to them, calming and/or
rocking them to sleep. In the late 1970’s, several researchers began to observe a behavior during this interaction. This
behavior appeared to be an unconscious positioning of newborns by their mother to the mother’s left arm during “cradling”
(Bundy, 1979; Ginsburg, Fling, Hope, Musgrove, & Andrews, 1979). Other researchers confirmed in later studies that cradling
bias to the left side was observed when mothers cradled their newborns (Bourne & Todd, 2004; Donnot, 2007; Hopkins,
2004; Matheson & Turnbull, 1998; Reissland, 2000; Reissland, Hopkins, Helms, & Williams, 2009; Sieratzki, Roy, & Woll, 2002;
Sieratzki & Woll, 2002, 2004; Tomaszycki, Cline, Griffin, Maestripieri, & Hopkins, 1997; Turnbull & Bryson, 2001; Turnbull &
Lucas, 1990, 1996; Turnbull, Rhys-Jones, & Jackson, 2001; Vauclair & Donnot, 2005; Woll & Sieratzki, 2002). The incidence of
left side cradling bias has been shown to be around 70% to 80% regardless of culture (Bourne & Todd, 2004) or handedness of
the mother (van der Meer & Husby, 2006; Previc, 1991; Sieratzki & Woll, 1996, 2002; Vauclair & Donnot, 2005). Investigations
into the reason(s) why this particular positioning occurs have included studies on correlations between several known human
traits and innate biases. For example, it was thought that maternal left ear/right hemisphere advantage for the perception
and processing of prosodic speech (Sieratzki et al., 2002) or more specifically the maternal hemispheric specialization of
emotion processing and social/communicative behaviors (Sieratzki & Woll, 2002; Turnbull & Bryson, 2001) would answer the
question regarding why cradling bias to the left occurs; however, has not been empirically proven. Hemispheric asymmetry
of maternal attentional systems (Turnbull & Lucas, 1996), handedness (van der Meer & Husby, 2006; Previc, 1991; Sieratzki
& Woll, 1996, 2002; Vauclair & Donnot, 2005), (Sieratzki & Woll, 2002), maternal hemispheric arousal and attention (Harris,
Almerigi, Carbary, & Fogel, 2001), maternal stress (Bourne & Todd, 2004; Reissland et al., 2009; Sieratzki & Woll, 2002), pitch
of maternal voice in child directed language (Reissland, 2000), maternal affect (Legerstee, Markova, & Fisher, 2007), infant
∗ Tel.: +1 9184443778.
E-mail address: jones179@nsuok.edu
http://dx.doi.org/10.1016/j.infbeh.2014.08.008
0163-6383/© 2014 Elsevier Inc. All rights reserved.
S. Jones / Infant Behavior & Development 37 (2014) 722–728 723
positional bias (Hopkins, 2004), and infant nipple preferences during breastfeeding (Tomaszycki et al., 1997), have been the
subject of investigation regarding their possible connection or contribution to the cradling bias dynamic. Studies, for the
most, part have paid particular attention to the maternal (rather than the neonate) actions during cradling. Researchers have
noted that holding the infant to the left gives the mother optimum access to the newborn’s face in order to read non-verbal
cues regarding the newborn’s state of being (Legerstee et al., 2007; Sieratzki & Woll, 2002, 1996; Vauclair & Donnot, 2005).
Strathearn, Li, Fonagy, and Montague (2008) conducted an fMRI study to determine activation in the mother’s brain during
viewing of their infant’s face. Extensive activation of reward centers in the brain occurred when the mother viewed her
own baby’s face, suggesting that a mother’s brain responds in a reward-related fashion. Their data provided insight into the
neural basis of mother–infant attachment; however, the scans of mothers were not conducted “in context” of cradling an
infant, but merely by looking at photographs.
Until recently, limitations of functional magnetic resonance imaging (fMRI) have precluded investigation of active cradling
using brain imaging. As several authors have demonstrated (Kuhl & Rivera-Gaxiola, 2008; Kuhl, 2010) in their most recent
research, advances in the implementation of new neuroimaging technology exploring neonatal neural activation is possible.
An investigation into the specific neural activation during cradling would provide further insight into what we know about
its role in social communicative development of the newborn.
2. Infant social development
Currently, the literature investigating social development of infants has focused on gaze behaviors and vocalizations
(Brooks & Meltzoff, 2005; Field, 1977; Perry & Stern, 1976; Symons & Moran, 1987; Yale, Messinger, Cobo-Lewis, & Delgado,
2003), as well as newborn behavioral responses to auditory and visual stimuli (Cassia, Valenza, Simion, & Leo, 2008; DeCasper
& Prescott, 2009; Gervain, Macagno, Cogoi, Pena, & Mehler, 2008; de Heering et al., 2008; Kujala et al., 2004; McGurk, Turnure,
& Creighton, 1977; Ruusuvirta, Huotilainen, Fellman, & Naatanen, 2004; Stefanics et al., 2009; Valenza, Leo, Gava, & Simion,
2006; Winkler, Haden, Ladinig, Sziller, & Honing, 2009; Wunderlich, Cone-Wesson, & Shepherd, 2006). Correlations have
been established between early infant organization of attention and later-developing attentional abilities (Schlansker, 1982).
In addition, another positioning “bias” was noted. Gunturkun (2003) observed a rightward head turning bias on the part of
the neonate. The functional goal of this “hardwired” behavior is unknown. This apparently inherent head positioning by the
newborn coupled with the leftward cradling bias by the mother theoretically sets the stage for a notable social as well as
communicative dynamic to occur between mother and newborn in the first hours, days, and weeks of life.
3. Infant communicative behaviors
Descriptions of exactly what constitutes the non-verbal cues that newborns give to their mothers during the act of cradling
have yet to be delineated in the literature; however, the communicative actions of newborns have been the subject of study
for quite some time (Aitken & Trevarthen, 1997; Hofer, 2006; Kaitz, Meschulach-Sarfaty, Auerbach, & Eidelman, 1988;
Meltzoff & Moore, 1983; Trevarthen, 2005; Trevarthen & Aitken, 2001; Wolff, 1959). Lavelli and Fogel (2005) documented
developmental changes in mother–infant face-to-face communication from birth to 3 months and identified developmental
trajectories for the first 12 weeks of life. Their data show much communicative interaction occurring from birth between
the mother and her newborn as well as identifiable shifts in the quality of newborn attentional behaviors around the 8th
week of life.
4. Neonatal neural development: Visual and auditory perception
For many years, the newborn brain was considered as undifferentiated, with areas of specialization arising following the
appropriate stimuli/experiences. Current research has changed this view. Researchers have shown that many of the neonatal
neural structures are functional at birth (Bushnell, 2001; de Haan, Pascalis, & Johnson, 2002; Johnson, 2007; Leppanen,
Moulson,Vogel-Farley,& Nelson, 2007; Simion, Cassia, Turati, & Valenza, 2001; Umilta, Simion, & Valenza, 1996). For example,
studies of cerebral development of fetuses have indicated that the right hemisphere is dominant by 30 weeks gestation
(Chiron et al., 1997; Mento, Suppiej, & Bisiacchi, 2009). Gilmore et al. (2007) have documented a robust growth of cortical
gray matter compared with white matter, as well as posterior to anterior regional specificity of cortical gray matter growth
during the early postnatal period.
Cortical structures utilized for visual processing by the newborn are still unclear as opinion is divided on just how much a
newborn can actually see. Simion et al. (2001) have suggested that neonatal visual systems are innately biased toward a “top
heavy” configuration such as two eyes above a nose and mouth, or similarly a t-shape as opposed to inverted presentations
of both types. Newborn visual systems have been demonstrated to have a preference for faces at birth (Bower, 2001; Cassia
et al., 2008; Goren, Sarty, & Wu, 1975; Leppanen et al., 2007; Simion et al., 2001; Umilta et al., 1996; Valenza et al., 2006).
Umilta et al. (1996) suggested in their study that the infant’s preference for faces was based in sub cortical systems that
were sensitive to specific properties of faces, in other words the basal ganglia, the internal capsule, and/or the limbic system.
Studies of infant processing of emotions on faces suggested that neural systems underlying the differential processing of
this type of stimuli were functional early in life (Leppanen et al., 2007). Acerra, Burnod, and de Schonen (2002) attempted
to create a neural model of visual face processing development that accounts for the both the limited ability of newborn
724 S. Jones / Infant Behavior & Development 37 (2014) 722–728
visual systems to detect contrasts along with their apparent preference for face-like forms. Although more complicated than
stated here, these authors suggested that the neural substrates for newborn face processing may consist of the retina-V1/V2-
colliculus system and that through subsequent experience and maturation, the activation of the right hemisphere fusiform
face area occurs. Findings from other studies support a gradual maturation of visual face processing in infants (de Haan
et al., 2002) with regard to areas of cortical activation; however, Bushnell (2001) conducted a study of newborns viewing
their mothers’ faces and determined that even at an early age face processing and memory establishment may be very rapid.
Johnson (2007) has suggested that one purpose of the early bias for newborns to fixate on face-like stimuli may be to support
bonding between newborn and caregiver.
In the mature brain, viewing faces activates the fusiform face area (Kanwisher, McDermott, & Chun, 1997; Kanwisher
& Yovel, 2006; Pierce, Muller, Ambrose, Allen, & Courshesne, 2001) in the right temporal lobe. Research had also indicated
that the occipital face area and the fusiform face area in the right hemisphere played a lead role in face processing (Rossion
et al., 2003). Rossion et al. (2000) utilized positron emission tomography (PET), to gather data that supported the idea of a
right hemisphere advantage for processing faces as a whole, noting stronger activation in the right middle fusiform gyrus
compared to activation in the left middle fusiform gyrus in adults in a whole face matching task. A neural model of face
processing proposed by Itier, Alain, Sedore, and McIntosh, (2007) stipulated that face- and eye-selective neurons situated
in the superior temporal sulcus region of the human brain responded differently to the face configuration and to the eyes
depending on the face context.
Auditory systems in the newborn have been studied extensively (Anderson et al., 2001; Cheour-Luhtanen et al., 1995;
Clifton, Morrongiello, Kulig, & Dowd, 1981; DeCasper & Prescott, 2009; Gervain et al., 2008; Kujala et al., 2004; McGurk
et al., 1977; Molfese & Molfese, 1979; Ruusuvirta et al., 2004; Slater, Quinn, Brown, & Hayes, 1999; Stefanics et al., 2009;
Tallal & Gaab, 2006; Winkler et al., 2009; Wunderlich et al., 2006). In a study of newborns, Molfese and Molfese (1979) found
evidence of left hemisphere activation in response to specific formant transitions in speech sounds. These authors also noted
that some specialized receptor systems for specific acoustic cues common to speech also appear to be present in the right
hemisphere, although they did not elaborate further.
Concurrently, the auditory system has been shown to be somewhat “hardwired” in newborns for specific auditory stimuli.
Recently Gervain et al. (2008) investigated the mechanisms underlying the acquisition of auditory patterns in newborns.
They posited that a perceptual bias similar to those found in the visual system was present in the auditory system as well;
specifically that repeated patterns of syllables are automatically detected. Gervain et al. (2008) demonstrated that on its first
encounters with language, the newborn brain detects structural regularities. This finding was further supported by Teinonen,
Fellman, Naatanen, Alku, and Huotilainen (2009) whose study demonstrated that the neonatal brain segments word-like
units from a stream of syllables using only the statistical properties such as transitional probabilities and/or frequencies of
co-occurrence between syllables. Neural activation in newborns has been demonstrated in the right hemisphere (to prosodic
aspects) as well in response to auditory stimuli. Support for this was found in a study by Sambeth, Ruohio, Alku, Fellman,
and Huotilainen (2008) whose data demonstrated that when neonates were sleeping, their neural responses to auditory
stimuli decreased dramatically when prosodic aspects were removed. Stefanics et al. (2009) studied the newborn auditory
system and how it processes pitch utilizing event-related brain potentials. They concluded that the neonate auditory system
processes pitch intervals similarly to the adult system. This led them to the supposition that newborn infants can learn music
and speech prosody. The authors of both studies noted the importance of the finding of prosodic processing being present
at birth as an indicator of normal cortical function in newborns. The studies discussed have provided additional support for
the view that the neonate brain is not undifferentiated at birth; in contrast it has at least some sensory processing systems
comparable to the mature structure.
The pairing or integrating of auditory and visual information in the neonate brain during the initial interactions between
mother and newborn is assumed to occur within the context of cradling. The specifics of this integration, and its connec-
tion with social interaction and language development are unknown. Further study focusing on identifying normal versus
abnormal neural activation patterns in the neonate during cradling warrants investigation.
5. The newborn’s experiences during cradling
The question of what purpose is served by a leftward cradling bias in the first 12 weeks of life has not been answered to
date. Many aspects of the act of cradling must be considered in order to form a complete picture of this. Visual pursuit, for
example, is a behavior that newborns develop fairly quickly. Visual fixation and the act of tracking an object (visual pursuit)
is considered a sign of normal neural function. An interesting result of a study of the effects of vestibular and proprioceptive
stimuli on the visual pursuit behaviors of newborns demonstrated that this particular behavior (visual pursuit) was enhanced
by the newborn’s body being positioned either horizontally or semi vertically (Gregg, Haffner, & Korner, 1976), a position
similar to that of being cradled. During the act of being cradled to the left side, the newborn is simultaneously viewing the
maternal face, specifically the left side which is supposedly the most expressive side of the face (Vauclair & Donnot, 2005) and
hearing the maternal voice with his left ear (and possibly hearing the maternal heartbeat with his right ear which is occluded
by his mother’s body). The left ear sends auditory signals composed of prosodic features of the maternal voice to the right
hemisphere where they are supposedly paired with the experience of emotion to add salience to the communicative intent of
the speaker for the infant. Simultaneously the visual information generated from viewing the maternal face, limited though
S. Jones / Infant Behavior & Development 37 (2014) 722–728 725
it may be, is gathered, processed, and paired with an emotion in a similar fashion. The cradling bias appears to facilitate this
process.
In an early study of newborn behaviors, Wolff (1959) observed newborns while sleeping and awake and in response
to specific stimuli (jarring the crib, stroking the face or body, sounds such as bell or cricket, and visual stimuli consisting
of various objects) but did not specifically observe interactions between the mother and newborn during cradling. Wolff
(1959) described some specific behaviors observed in his subjects and attributed the motivation for those behaviors to the
discharge of need-based tension (for example, hunger results in rhythmic braying and kicking; gas pain results in sporadic
screeching). He briefly commented on the possibility of the activities observed having a communicative function as a possible
precursor to language but did not elaborate or pursue this line of thinking further. Other behavioral studies have examined
the neonate’s ability to imitate facial expressions (Kaitz et al., 1988; Meltzoff & Moore, 1983), form attachments (Hofer,
2006) and regulate emotions (Aitken & Trevarthen, 1997) and have speculated on the role these occurrences as a precursor
to the development of language.
6. Implications for language acquisition
Given that leftward cradling has the potential to be a communicative interaction between mother and newborn, several
questions remain. What if anything, does the infant do to facilitate or inhibit leftward cradling? What happens in the infant’s
brain during this interaction? What role this interaction plays in language development? Is there a correlation between
the incidence of leftward cradling bias and developmental disabilities? As more is discovered about the development and
function of human neonatal neural systems, it is not surprising that previously accepted notions regarding the communicative
intent and abilities of the newborn have been questioned with increasing frequency. If it is agreed that language acquisition
occurs on a continuum rather than as a specific event, it seems plausible that the beginnings of language acquisition may occur
within the first moments, hours, days, and weeks of life. In addition to sleeping and eating, the experience of newborns is
largely constituted of specific cradling interaction with their adult caregiver (predominantly the mother). As such, cradling
provides the context for the bulk of the neonate’s initial social and communicative experiences. It is logical to examine
these experiences, gather data, and from such further elucidate the role cradling may have in providing the foundation for
later developing social and communicative abilities. Many fields of study would gain significantly from studies focusing
on mother–infant interactions during these first communicative experiences, as well as studies of neural activation in the
newborn during cradling using newer, comfortable and non-invasive techniques such as electroencephalography (EEG). A
potential study could utilize this fairly recent advance in technology to conduct scans of newborn and mother during the
cradling interaction and identify areas of activation in both subjects. With EEG, the brain dynamics and connectivity in
different states (awake or asleep) can be defined. Such information often reveals pre symptomatic or sub clinical conditions
(Silvestri-Hobson, 2008). EEG scans have been performed on neonates to identify normal patterns of neural function (Eiselt
et al., 1997; Ferri et al., 2003; Field, Diego, Hernandez-Reif, Schanber, & Kuhn, 2002; Grieve, Myers, Stark, Housman, & Fifer,
2005; Hayakawa, Watanabe, Hakamada, Kuno, & Aso, 1987; Korotchikova et al., 2009; Koszer, Moshe, & Holmes, 2007;
Mandelbaum et al., 2000; O’Brien, Lems, & Prechtl, 1987; Paul, Krajca, Roth, Melichar, & Petranek, 2003) although none
has specifically examined neural activity during cradling. Coupling EEG data with visual observations/recordings of the
interaction in terms of maternal as well as newborn behaviors may serve to explain normal neural and behavioral sequences
at this point in development. The use of a behavioral measurement tool such as the neonatal behavior assessment scale (Als,
Tronick, Lester, & Brazelton, 1977) in addition to EEG and behavioral observations would also provide a wealth of data.
7. Implications for early identification of children at risk
Information gleaned from an investigation such as has been suggested here has the potential to identify possible corre-
lations between observations of typical neural activation during the act of cradling and later incidence of developmental
disorders, particularly autism spectrum disorders. In the last three decades, society has seen a marked rise in incidence
of autism spectrum disorders (ASDs) (Fombonne, 2005; Newschaffer, Falb, & Gurney, 2005; Ouellette-Kuntz et al., 2007;
Wing & Potter, 2002). Subsequently, ASDs have been of great interest to researchers from various fields of study (Belmonte
& Yurgelun-Todd, 2003; Booth, Charlton, Hughes, & Happe, 2003; Courchesne, Redcay, & Kennedy, 2004; Hotopf & Bolton,
1995; Mandell, Novak, & Zubritsky, 2005; Mundy, Sigman, & Kasari, 1990; Plaisted, Swettenham, & Rees, 1999; Prizant,
1983; Ramachandran & Oberman, 2007; Schultz et al., 2000; Tager-Flusberg et al., 2009; Taverna, 1998). This fascinating
disorder presents itself in highly heterogeneous ways which makes early identification somewhat difficult prior to 2 years of
age (Lord & Risi, 2000). Early intervention for ASDs has demonstrated significant amelioration in behavioral characteristics
that typically impede communication and social interactions with this population (Goldstein, 2002; Smith, Groen, & Wynn,
2000). Currently the earliest a child can be screened and possibly identified as being at risk for ASDs is about 18 months and
this is primarily through observation of specific behavioral markers (Beauchesne & Kelley, 2004; Gupta et al., 2007; Mandell
et al., 2005).
A sizeable body of research points to a neurobiological etiology of ASDs (Alexander et al., 2007; Boger-Megiddo et al.,
2006; Bruneau, Bonnet-Brilhault, Adrien, & Barthelemy, 2003; Courchesne et al., 2004; Eigsti & Shapiro, 2003; Herbert et al.,
2003; Keary et al., 2009; Piven, Bailey, Ranson, & Arndt, 1997; Powell, 2004; Rutter, 2005). As such, patterns of neural activity
along with specific behaviors characteristic of children at risk for ASDs may be identifiable at a much earlier time, e.g. during
726 S. Jones / Infant Behavior & Development 37 (2014) 722–728
initial and early mother–infant dyads prior to the development and use of verbal language. Approaching cradling bias from a
developmental transactional perspective of child development (Wetherby & Prizant, 2000), this inherently social interaction
could be regarded as integral in the development of communicative and social interactions necessary for the acquisition
of verbal language. The neural patterns characteristic of typical early communicative interactions (during cradling), or lack
thereof, is of particular importance for the possible earlier identification of children at risk for developmental delays such
as ASDs.
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Developmental Science. 2018;21e12610. wileyonlinelibrary.com.docx
 

Maternal cradling bias paper

  • 1. Infant Behavior & Development 37 (2014) 722–728 Contents lists available at ScienceDirect Infant Behavior and Development Brief report Maternal cradling bias and early communicative interactions: Implications for early identification of children at risk Sharon Jones∗ Northeastern State University, Speech Language Pathology, 800 N. Vinita, Tahlequah, OK 74464, United States a r t i c l e i n f o Article history: Received 5 February 2014 Received in revised form 17 June 2014 Accepted 26 August 2014 Available online 24 September 2014 Keywords: Maternal cradling bias Early communication development Infant maternal interactions 1. Introduction Nurturing mothers cradle their babies during the first months of life while feeding, talking to them, calming and/or rocking them to sleep. In the late 1970’s, several researchers began to observe a behavior during this interaction. This behavior appeared to be an unconscious positioning of newborns by their mother to the mother’s left arm during “cradling” (Bundy, 1979; Ginsburg, Fling, Hope, Musgrove, & Andrews, 1979). Other researchers confirmed in later studies that cradling bias to the left side was observed when mothers cradled their newborns (Bourne & Todd, 2004; Donnot, 2007; Hopkins, 2004; Matheson & Turnbull, 1998; Reissland, 2000; Reissland, Hopkins, Helms, & Williams, 2009; Sieratzki, Roy, & Woll, 2002; Sieratzki & Woll, 2002, 2004; Tomaszycki, Cline, Griffin, Maestripieri, & Hopkins, 1997; Turnbull & Bryson, 2001; Turnbull & Lucas, 1990, 1996; Turnbull, Rhys-Jones, & Jackson, 2001; Vauclair & Donnot, 2005; Woll & Sieratzki, 2002). The incidence of left side cradling bias has been shown to be around 70% to 80% regardless of culture (Bourne & Todd, 2004) or handedness of the mother (van der Meer & Husby, 2006; Previc, 1991; Sieratzki & Woll, 1996, 2002; Vauclair & Donnot, 2005). Investigations into the reason(s) why this particular positioning occurs have included studies on correlations between several known human traits and innate biases. For example, it was thought that maternal left ear/right hemisphere advantage for the perception and processing of prosodic speech (Sieratzki et al., 2002) or more specifically the maternal hemispheric specialization of emotion processing and social/communicative behaviors (Sieratzki & Woll, 2002; Turnbull & Bryson, 2001) would answer the question regarding why cradling bias to the left occurs; however, has not been empirically proven. Hemispheric asymmetry of maternal attentional systems (Turnbull & Lucas, 1996), handedness (van der Meer & Husby, 2006; Previc, 1991; Sieratzki & Woll, 1996, 2002; Vauclair & Donnot, 2005), (Sieratzki & Woll, 2002), maternal hemispheric arousal and attention (Harris, Almerigi, Carbary, & Fogel, 2001), maternal stress (Bourne & Todd, 2004; Reissland et al., 2009; Sieratzki & Woll, 2002), pitch of maternal voice in child directed language (Reissland, 2000), maternal affect (Legerstee, Markova, & Fisher, 2007), infant ∗ Tel.: +1 9184443778. E-mail address: jones179@nsuok.edu http://dx.doi.org/10.1016/j.infbeh.2014.08.008 0163-6383/© 2014 Elsevier Inc. All rights reserved.
  • 2. S. Jones / Infant Behavior & Development 37 (2014) 722–728 723 positional bias (Hopkins, 2004), and infant nipple preferences during breastfeeding (Tomaszycki et al., 1997), have been the subject of investigation regarding their possible connection or contribution to the cradling bias dynamic. Studies, for the most, part have paid particular attention to the maternal (rather than the neonate) actions during cradling. Researchers have noted that holding the infant to the left gives the mother optimum access to the newborn’s face in order to read non-verbal cues regarding the newborn’s state of being (Legerstee et al., 2007; Sieratzki & Woll, 2002, 1996; Vauclair & Donnot, 2005). Strathearn, Li, Fonagy, and Montague (2008) conducted an fMRI study to determine activation in the mother’s brain during viewing of their infant’s face. Extensive activation of reward centers in the brain occurred when the mother viewed her own baby’s face, suggesting that a mother’s brain responds in a reward-related fashion. Their data provided insight into the neural basis of mother–infant attachment; however, the scans of mothers were not conducted “in context” of cradling an infant, but merely by looking at photographs. Until recently, limitations of functional magnetic resonance imaging (fMRI) have precluded investigation of active cradling using brain imaging. As several authors have demonstrated (Kuhl & Rivera-Gaxiola, 2008; Kuhl, 2010) in their most recent research, advances in the implementation of new neuroimaging technology exploring neonatal neural activation is possible. An investigation into the specific neural activation during cradling would provide further insight into what we know about its role in social communicative development of the newborn. 2. Infant social development Currently, the literature investigating social development of infants has focused on gaze behaviors and vocalizations (Brooks & Meltzoff, 2005; Field, 1977; Perry & Stern, 1976; Symons & Moran, 1987; Yale, Messinger, Cobo-Lewis, & Delgado, 2003), as well as newborn behavioral responses to auditory and visual stimuli (Cassia, Valenza, Simion, & Leo, 2008; DeCasper & Prescott, 2009; Gervain, Macagno, Cogoi, Pena, & Mehler, 2008; de Heering et al., 2008; Kujala et al., 2004; McGurk, Turnure, & Creighton, 1977; Ruusuvirta, Huotilainen, Fellman, & Naatanen, 2004; Stefanics et al., 2009; Valenza, Leo, Gava, & Simion, 2006; Winkler, Haden, Ladinig, Sziller, & Honing, 2009; Wunderlich, Cone-Wesson, & Shepherd, 2006). Correlations have been established between early infant organization of attention and later-developing attentional abilities (Schlansker, 1982). In addition, another positioning “bias” was noted. Gunturkun (2003) observed a rightward head turning bias on the part of the neonate. The functional goal of this “hardwired” behavior is unknown. This apparently inherent head positioning by the newborn coupled with the leftward cradling bias by the mother theoretically sets the stage for a notable social as well as communicative dynamic to occur between mother and newborn in the first hours, days, and weeks of life. 3. Infant communicative behaviors Descriptions of exactly what constitutes the non-verbal cues that newborns give to their mothers during the act of cradling have yet to be delineated in the literature; however, the communicative actions of newborns have been the subject of study for quite some time (Aitken & Trevarthen, 1997; Hofer, 2006; Kaitz, Meschulach-Sarfaty, Auerbach, & Eidelman, 1988; Meltzoff & Moore, 1983; Trevarthen, 2005; Trevarthen & Aitken, 2001; Wolff, 1959). Lavelli and Fogel (2005) documented developmental changes in mother–infant face-to-face communication from birth to 3 months and identified developmental trajectories for the first 12 weeks of life. Their data show much communicative interaction occurring from birth between the mother and her newborn as well as identifiable shifts in the quality of newborn attentional behaviors around the 8th week of life. 4. Neonatal neural development: Visual and auditory perception For many years, the newborn brain was considered as undifferentiated, with areas of specialization arising following the appropriate stimuli/experiences. Current research has changed this view. Researchers have shown that many of the neonatal neural structures are functional at birth (Bushnell, 2001; de Haan, Pascalis, & Johnson, 2002; Johnson, 2007; Leppanen, Moulson,Vogel-Farley,& Nelson, 2007; Simion, Cassia, Turati, & Valenza, 2001; Umilta, Simion, & Valenza, 1996). For example, studies of cerebral development of fetuses have indicated that the right hemisphere is dominant by 30 weeks gestation (Chiron et al., 1997; Mento, Suppiej, & Bisiacchi, 2009). Gilmore et al. (2007) have documented a robust growth of cortical gray matter compared with white matter, as well as posterior to anterior regional specificity of cortical gray matter growth during the early postnatal period. Cortical structures utilized for visual processing by the newborn are still unclear as opinion is divided on just how much a newborn can actually see. Simion et al. (2001) have suggested that neonatal visual systems are innately biased toward a “top heavy” configuration such as two eyes above a nose and mouth, or similarly a t-shape as opposed to inverted presentations of both types. Newborn visual systems have been demonstrated to have a preference for faces at birth (Bower, 2001; Cassia et al., 2008; Goren, Sarty, & Wu, 1975; Leppanen et al., 2007; Simion et al., 2001; Umilta et al., 1996; Valenza et al., 2006). Umilta et al. (1996) suggested in their study that the infant’s preference for faces was based in sub cortical systems that were sensitive to specific properties of faces, in other words the basal ganglia, the internal capsule, and/or the limbic system. Studies of infant processing of emotions on faces suggested that neural systems underlying the differential processing of this type of stimuli were functional early in life (Leppanen et al., 2007). Acerra, Burnod, and de Schonen (2002) attempted to create a neural model of visual face processing development that accounts for the both the limited ability of newborn
  • 3. 724 S. Jones / Infant Behavior & Development 37 (2014) 722–728 visual systems to detect contrasts along with their apparent preference for face-like forms. Although more complicated than stated here, these authors suggested that the neural substrates for newborn face processing may consist of the retina-V1/V2- colliculus system and that through subsequent experience and maturation, the activation of the right hemisphere fusiform face area occurs. Findings from other studies support a gradual maturation of visual face processing in infants (de Haan et al., 2002) with regard to areas of cortical activation; however, Bushnell (2001) conducted a study of newborns viewing their mothers’ faces and determined that even at an early age face processing and memory establishment may be very rapid. Johnson (2007) has suggested that one purpose of the early bias for newborns to fixate on face-like stimuli may be to support bonding between newborn and caregiver. In the mature brain, viewing faces activates the fusiform face area (Kanwisher, McDermott, & Chun, 1997; Kanwisher & Yovel, 2006; Pierce, Muller, Ambrose, Allen, & Courshesne, 2001) in the right temporal lobe. Research had also indicated that the occipital face area and the fusiform face area in the right hemisphere played a lead role in face processing (Rossion et al., 2003). Rossion et al. (2000) utilized positron emission tomography (PET), to gather data that supported the idea of a right hemisphere advantage for processing faces as a whole, noting stronger activation in the right middle fusiform gyrus compared to activation in the left middle fusiform gyrus in adults in a whole face matching task. A neural model of face processing proposed by Itier, Alain, Sedore, and McIntosh, (2007) stipulated that face- and eye-selective neurons situated in the superior temporal sulcus region of the human brain responded differently to the face configuration and to the eyes depending on the face context. Auditory systems in the newborn have been studied extensively (Anderson et al., 2001; Cheour-Luhtanen et al., 1995; Clifton, Morrongiello, Kulig, & Dowd, 1981; DeCasper & Prescott, 2009; Gervain et al., 2008; Kujala et al., 2004; McGurk et al., 1977; Molfese & Molfese, 1979; Ruusuvirta et al., 2004; Slater, Quinn, Brown, & Hayes, 1999; Stefanics et al., 2009; Tallal & Gaab, 2006; Winkler et al., 2009; Wunderlich et al., 2006). In a study of newborns, Molfese and Molfese (1979) found evidence of left hemisphere activation in response to specific formant transitions in speech sounds. These authors also noted that some specialized receptor systems for specific acoustic cues common to speech also appear to be present in the right hemisphere, although they did not elaborate further. Concurrently, the auditory system has been shown to be somewhat “hardwired” in newborns for specific auditory stimuli. Recently Gervain et al. (2008) investigated the mechanisms underlying the acquisition of auditory patterns in newborns. They posited that a perceptual bias similar to those found in the visual system was present in the auditory system as well; specifically that repeated patterns of syllables are automatically detected. Gervain et al. (2008) demonstrated that on its first encounters with language, the newborn brain detects structural regularities. This finding was further supported by Teinonen, Fellman, Naatanen, Alku, and Huotilainen (2009) whose study demonstrated that the neonatal brain segments word-like units from a stream of syllables using only the statistical properties such as transitional probabilities and/or frequencies of co-occurrence between syllables. Neural activation in newborns has been demonstrated in the right hemisphere (to prosodic aspects) as well in response to auditory stimuli. Support for this was found in a study by Sambeth, Ruohio, Alku, Fellman, and Huotilainen (2008) whose data demonstrated that when neonates were sleeping, their neural responses to auditory stimuli decreased dramatically when prosodic aspects were removed. Stefanics et al. (2009) studied the newborn auditory system and how it processes pitch utilizing event-related brain potentials. They concluded that the neonate auditory system processes pitch intervals similarly to the adult system. This led them to the supposition that newborn infants can learn music and speech prosody. The authors of both studies noted the importance of the finding of prosodic processing being present at birth as an indicator of normal cortical function in newborns. The studies discussed have provided additional support for the view that the neonate brain is not undifferentiated at birth; in contrast it has at least some sensory processing systems comparable to the mature structure. The pairing or integrating of auditory and visual information in the neonate brain during the initial interactions between mother and newborn is assumed to occur within the context of cradling. The specifics of this integration, and its connec- tion with social interaction and language development are unknown. Further study focusing on identifying normal versus abnormal neural activation patterns in the neonate during cradling warrants investigation. 5. The newborn’s experiences during cradling The question of what purpose is served by a leftward cradling bias in the first 12 weeks of life has not been answered to date. Many aspects of the act of cradling must be considered in order to form a complete picture of this. Visual pursuit, for example, is a behavior that newborns develop fairly quickly. Visual fixation and the act of tracking an object (visual pursuit) is considered a sign of normal neural function. An interesting result of a study of the effects of vestibular and proprioceptive stimuli on the visual pursuit behaviors of newborns demonstrated that this particular behavior (visual pursuit) was enhanced by the newborn’s body being positioned either horizontally or semi vertically (Gregg, Haffner, & Korner, 1976), a position similar to that of being cradled. During the act of being cradled to the left side, the newborn is simultaneously viewing the maternal face, specifically the left side which is supposedly the most expressive side of the face (Vauclair & Donnot, 2005) and hearing the maternal voice with his left ear (and possibly hearing the maternal heartbeat with his right ear which is occluded by his mother’s body). The left ear sends auditory signals composed of prosodic features of the maternal voice to the right hemisphere where they are supposedly paired with the experience of emotion to add salience to the communicative intent of the speaker for the infant. Simultaneously the visual information generated from viewing the maternal face, limited though
  • 4. S. Jones / Infant Behavior & Development 37 (2014) 722–728 725 it may be, is gathered, processed, and paired with an emotion in a similar fashion. The cradling bias appears to facilitate this process. In an early study of newborn behaviors, Wolff (1959) observed newborns while sleeping and awake and in response to specific stimuli (jarring the crib, stroking the face or body, sounds such as bell or cricket, and visual stimuli consisting of various objects) but did not specifically observe interactions between the mother and newborn during cradling. Wolff (1959) described some specific behaviors observed in his subjects and attributed the motivation for those behaviors to the discharge of need-based tension (for example, hunger results in rhythmic braying and kicking; gas pain results in sporadic screeching). He briefly commented on the possibility of the activities observed having a communicative function as a possible precursor to language but did not elaborate or pursue this line of thinking further. Other behavioral studies have examined the neonate’s ability to imitate facial expressions (Kaitz et al., 1988; Meltzoff & Moore, 1983), form attachments (Hofer, 2006) and regulate emotions (Aitken & Trevarthen, 1997) and have speculated on the role these occurrences as a precursor to the development of language. 6. Implications for language acquisition Given that leftward cradling has the potential to be a communicative interaction between mother and newborn, several questions remain. What if anything, does the infant do to facilitate or inhibit leftward cradling? What happens in the infant’s brain during this interaction? What role this interaction plays in language development? Is there a correlation between the incidence of leftward cradling bias and developmental disabilities? As more is discovered about the development and function of human neonatal neural systems, it is not surprising that previously accepted notions regarding the communicative intent and abilities of the newborn have been questioned with increasing frequency. If it is agreed that language acquisition occurs on a continuum rather than as a specific event, it seems plausible that the beginnings of language acquisition may occur within the first moments, hours, days, and weeks of life. In addition to sleeping and eating, the experience of newborns is largely constituted of specific cradling interaction with their adult caregiver (predominantly the mother). As such, cradling provides the context for the bulk of the neonate’s initial social and communicative experiences. It is logical to examine these experiences, gather data, and from such further elucidate the role cradling may have in providing the foundation for later developing social and communicative abilities. Many fields of study would gain significantly from studies focusing on mother–infant interactions during these first communicative experiences, as well as studies of neural activation in the newborn during cradling using newer, comfortable and non-invasive techniques such as electroencephalography (EEG). A potential study could utilize this fairly recent advance in technology to conduct scans of newborn and mother during the cradling interaction and identify areas of activation in both subjects. With EEG, the brain dynamics and connectivity in different states (awake or asleep) can be defined. Such information often reveals pre symptomatic or sub clinical conditions (Silvestri-Hobson, 2008). EEG scans have been performed on neonates to identify normal patterns of neural function (Eiselt et al., 1997; Ferri et al., 2003; Field, Diego, Hernandez-Reif, Schanber, & Kuhn, 2002; Grieve, Myers, Stark, Housman, & Fifer, 2005; Hayakawa, Watanabe, Hakamada, Kuno, & Aso, 1987; Korotchikova et al., 2009; Koszer, Moshe, & Holmes, 2007; Mandelbaum et al., 2000; O’Brien, Lems, & Prechtl, 1987; Paul, Krajca, Roth, Melichar, & Petranek, 2003) although none has specifically examined neural activity during cradling. Coupling EEG data with visual observations/recordings of the interaction in terms of maternal as well as newborn behaviors may serve to explain normal neural and behavioral sequences at this point in development. The use of a behavioral measurement tool such as the neonatal behavior assessment scale (Als, Tronick, Lester, & Brazelton, 1977) in addition to EEG and behavioral observations would also provide a wealth of data. 7. Implications for early identification of children at risk Information gleaned from an investigation such as has been suggested here has the potential to identify possible corre- lations between observations of typical neural activation during the act of cradling and later incidence of developmental disorders, particularly autism spectrum disorders. In the last three decades, society has seen a marked rise in incidence of autism spectrum disorders (ASDs) (Fombonne, 2005; Newschaffer, Falb, & Gurney, 2005; Ouellette-Kuntz et al., 2007; Wing & Potter, 2002). Subsequently, ASDs have been of great interest to researchers from various fields of study (Belmonte & Yurgelun-Todd, 2003; Booth, Charlton, Hughes, & Happe, 2003; Courchesne, Redcay, & Kennedy, 2004; Hotopf & Bolton, 1995; Mandell, Novak, & Zubritsky, 2005; Mundy, Sigman, & Kasari, 1990; Plaisted, Swettenham, & Rees, 1999; Prizant, 1983; Ramachandran & Oberman, 2007; Schultz et al., 2000; Tager-Flusberg et al., 2009; Taverna, 1998). This fascinating disorder presents itself in highly heterogeneous ways which makes early identification somewhat difficult prior to 2 years of age (Lord & Risi, 2000). Early intervention for ASDs has demonstrated significant amelioration in behavioral characteristics that typically impede communication and social interactions with this population (Goldstein, 2002; Smith, Groen, & Wynn, 2000). Currently the earliest a child can be screened and possibly identified as being at risk for ASDs is about 18 months and this is primarily through observation of specific behavioral markers (Beauchesne & Kelley, 2004; Gupta et al., 2007; Mandell et al., 2005). A sizeable body of research points to a neurobiological etiology of ASDs (Alexander et al., 2007; Boger-Megiddo et al., 2006; Bruneau, Bonnet-Brilhault, Adrien, & Barthelemy, 2003; Courchesne et al., 2004; Eigsti & Shapiro, 2003; Herbert et al., 2003; Keary et al., 2009; Piven, Bailey, Ranson, & Arndt, 1997; Powell, 2004; Rutter, 2005). As such, patterns of neural activity along with specific behaviors characteristic of children at risk for ASDs may be identifiable at a much earlier time, e.g. during
  • 5. 726 S. Jones / Infant Behavior & Development 37 (2014) 722–728 initial and early mother–infant dyads prior to the development and use of verbal language. Approaching cradling bias from a developmental transactional perspective of child development (Wetherby & Prizant, 2000), this inherently social interaction could be regarded as integral in the development of communicative and social interactions necessary for the acquisition of verbal language. The neural patterns characteristic of typical early communicative interactions (during cradling), or lack thereof, is of particular importance for the possible earlier identification of children at risk for developmental delays such as ASDs. References Acerra, F., Burnod, Y., & de Schonen, S. (2002). Modeling aspects of face processing in early infancy. Developmental Science: 5., (1), 98–117. Aitken, K., & Trevarthen, C. (1997). Self/other organization in human psychological development. Development and Psychopathology: 9., 653–677. 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