PSYC 210 LU Development of Attention Behavior in Infants Discussion

PSYC 210
RESEARCH ARTICLE EXPLORATION ASSIGNMENT INSTRUCTIONS
OVERVIEW
The purpose of this Research Article Exploration Assignment is to increase your knowledge
of development during infancy and to help you learn to use scholarly research effectively. You
will: 1) locate and download one scholarly article from the list provided at the end of this
document; 2) explore the content, identifying pertinent information; and 3) write a clear and
concise description of and reflection of your experience. In addition, you will also gain
experience in using a new software program (Adobe Reader).
INSTRUCTIONS
1. Select 1 article from the list provided below (page 2 of this document).
2. Download a PDF copy of the article from the Jerry Falwell Library (also available
through the Resources section).
If you do not have the free Adobe PDF Reader installed on your computer, please
download it. If you need assistance with the download or installation, contact the IT
HelpDesk at 866-447-2869.
3. Read the article, identifying the following information by highlighting the text and
labeling it with a comment bubble (see the sample article provided in the Resources
section). Please identify only one item for each of the following:
a. Journal information (name, date, volume/issue, page range).
b. Title
c. Author name and credentials.
d. Purpose statement.
e. Hypothesis.
f. Significant term.
g. Conclusion: what significant information was gained from this research?
h. Limitation(s).
i. Strength(s).
j. References
4. Write a brief reaction essay.
In 250–400 words:
a) Briefly summarize the main points of your article (what did you learn about
development during infancy?). Be sure to cite any information you include, and
provide a reference entry at the end of your essay.
b) Describe what you learned about how the scientific study of human
development is conducted.
c) Identify the skills or abilities involved in this assignment that will help you in
further uses of scholarly resources.
d) Include an APA-formatted title page and reference page.
5. Submit two separate documents for this assignment:
Page 1 of 2
PSYC 210
a. Upload the PDF of your chosen article with comments and highlighting as noted
above. If you have never done this before, please see the tutorial video in the
Resources section.
b. Upload your reaction essay by attaching a separate MS Word document.
How to access an article:
1. Copy the article title from one of the articles below.
2. Go to the Jerry Falwell Online Library (liberty.edu/library) and paste the title in the “Search
Anything” box located on the landing page.
3. Select your article (look on the right side of your screen).
4. When you have opened your article, look for a button or link that allows you to download a
PDF.
5. If you have any difficulty with this please contact your instructor or call one of our librarians
at 434-582-2221 or see other options for help at https://www.liberty.edu/library/onlinestudents/.
Note: articles also available in Resources section.
Please choose one of the following articles:
Cheung, C. H. M., Bedford, R., Saez De Urabain, Irati R, Karmiloff-Smith, A., & Smith, T. J.
(2017). Daily touchscreen use in infants and toddlers is associated with reduced sleep and
delayed sleep onset. Scientific Reports, 7(1), 46104-46104.
https://doi.org/10.1038/srep46104
Lucca, K., Pospisil, J., & Sommerville, J. A. (2018). Fairness informs social decision making in
infancy. PloS One, 13(2), e0192848-e0192848.
https://doi.org/10.1371/journal.pone.0192848
Swingler, M. M., Perry, N. B., Calkins, S. D., & Bell, M. A. (2017). Maternal behavior predicts
infant neurophysiological and behavioral attention processes in the first year.
Developmental Psychology, 53(1), 13-27. https://doi.org/10.1037/dev0000187
Page 2 of 2
Developmental Psychology
2017, Vol. 53, No. 1, 13–27
© 2016 American Psychological Association
0012-1649/17/$12.00 http://dx.doi.org/10.1037/dev0000187
Maternal Behavior Predicts Infant Neurophysiological and Behavioral
Attention Processes in the First Year
Margaret M. Swingler, Nicole B. Perry,
and Susan D. Calkins
Martha Ann Bell
Virginia Tech
This document is copyrighted by the American Psychological Association or one of its allied publishers.
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
University of North Carolina at Greensboro
We apply a biopsychosocial conceptualization to attention development in the 1st year and examine the
role of neurophysiological and social processes on the development of early attention processes. We
tested whether maternal behavior measured during 2 mother⫺child interaction tasks when infants (N ⫽
388) were 5 months predicted infant medial frontal (F3/F4) EEG power and observed attention behavior
during an attention task at 10 months. After controlling for infant attention behavior and EEG power in
the same task measured at an earlier 5-month time point, results indicated a significant direct and positive
association from 5-month maternal positive affect to infant attention behavior at 10 months. However,
maternal positive affect was not related to medial frontal EEG power. In contrast, 5-month maternal
intrusive behavior was associated with infants’ task-related EEG power change at the left frontal location,
F3, at 10 months of age. The test of indirect effects from 5-month maternal intrusiveness to 10-month
infant attention behavior via infants’ EEG power change at F3 was significant. These findings suggest
that the development of neural networks serving attention processes may be 1 mechanism through which
early maternal behavior is related to infant attention development in the 1st year and that intrusive
maternal behavior may have a particularly disruptive effect on this process.
Keywords: attention, infancy, EEG power, maternal behavior, neural networks
2016; Posner & Fan, 2008; Sarver et al., 2012). Attention development in early infancy is dominated by an emerging ability to
maintain an alert state and orient to sensory events in the environment (Posner & Fan, 2008). By the second half of the first year,
however, attentional flexibility and the capacity to effortfully
control, manipulate, and sustain attention become increasingly
prevalent (e.g., Rothbart, Posner, & Rosicky, 1994; Ruff & Rothbart, 1996). Despite extensive documentation of the rapid emergence of more sophisticated volitional attention beginning toward
the end of the first year, relatively little empirical work has
examined early factors that may influence this process.
Biopsychosocial theories of development posit that neurophysiological, behavioral, and social processes become elaborated and
integrated over time to shape subsequent functioning (e.g.,
Calkins, 1994, 2008; Thompson & Goodvin, 2007; Thompson,
Lewis, & Calkins, 2008). The development of attention, specifically, has strong biological underpinnings but is also influenced by
transactions between the child and his or her social environment
(e.g., Blair, 2002; Calkins, 2011; Colombo & Salley, 2015; Colombo & Saxon, 2002; Swingler, Perry, & Calkins, 2015). Indeed,
human neuroplasticity research has revealed that neurocognitive
systems like those involved in attention are characterized by a
great deal of plasticity in early development (e.g., Sanders, Stevens, Coch, & Neville, 2006; Stevens & Neville, 2013), when
interaction with caregivers dominates the infants’ social environment. Thus, caregiver behavior may contribute to individual differences in the emergence, maturation, and consolidation of rapidly changing neural systems underlying attention behavior
(Cicchetti & Dawson, 2002; Luthar, Cicchetti, & Becker, 2000;
Posner, Rothbart, Sheese, & Voelker, 2014). To better understand
Infant visual attention has a long history as an early measurement tool for studying development across a number of domains
and has been shown to be a predictor of childhood socioemotional
skills, cognitive competencies, intellectual and language outcomes,
and academic achievement (Colombo, 2002; Colombo & Salley,
2015; Cuevas & Bell, 2014; Perry, Swingler, Calkins, & Bell,
This article was published Online First August 8, 2016.
Margaret M. Swingler and Nicole B. Perry, Department of Human
Development and Family Studies, University of North Carolina at Greensboro; Susan D. Calkins, Department of Psychology, University of North
Carolina at Greensboro; Martha Ann Bell, Department of Psychology,
Virginia Tech.
Susan D. Calkins is now at the Department of Human Development and
Family Studies, University of North Carolina at Greensboro.
This research was supported by Grants HD049878 and HD043057 from
the Eunice Kennedy Shriver National Institute of Child Health and Human
Development (NICHD) awarded to the last author. The content of this
article is solely the responsibility of the authors and does not necessarily
represent the official views of the NICHD or the National Institutes of
Health. We are grateful to the families for their participation in our research
and to our research teams at the University of North Carolina at Greensboro and Virginia Tech for their assistance with data collection and coding.
In particular, we acknowledge Cynthia L. Smith for advising on maternal
interaction coding; Christy Wolfe, Annie Cardell, and Anjoli Diaz for
training and supervising coding; and Katherine Morasch, Kimberly Cuevas, Vinaya Raj, and Tara Patterson for their help with the EEG data.
Correspondence concerning this article should be addressed to Margaret
M. Swingler, UNCG- 248 Stone Building. PO Box 26170, Greensboro, NC
27402. E-mail: mmswingl@uncg.edu
13
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SWINGLER, PERRY, CALKINS, AND BELL
the impact of caregiving behavior on the early development of
attention processes, we examined whether two specific maternal
behaviors, positive affect and intrusiveness, predicted neurophysiological and behavioral attention processes in infants from 5 to 10
months of age.
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This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
Importance of Attention Behavior in
Early Development
The development of attention in the first year has been of
particular interest to researchers aiming to better understand precursors to adaptive functioning because it has been associated with
mechanisms for resolving conflict among thoughts, feelings, and
behavioral responses (Rueda, Posner, & Rothbart, 2005). In particular, control of attention is thought to contribute to the regulation of emotional reactivity, resulting in more socially appropriate
and adaptive behavior in infancy and early childhood. Indeed,
emotion regulation in the first year has been largely described and
defined in terms of attentional and motoric control mechanisms
that emerge early in development and operate primarily to regulate
distress (Posner & Rothbart, 2000; Rothbart & Bates, 1998).
By the end of the first year, infants are able to employ organized
sequences of behavior in emotionally arousing contexts that enable
them to disengage, redirect attention, and self-sooth in a flexible
manner (Calkins, 2004). The coincident timing of the emergence
of more sophisticated sustained and controlled attention behavior
with more adaptive emotion regulation abilities in the second half
of the first year has been proposed as evidence of an association
between the development of attention and emotional functioning in
infancy and beyond (Bell & Calkins, 2012). Accordingly, deviations or delays in the development of attention processes and
associated regulation likely contribute to maladaptive developmental trajectories associated with poor regulatory abilities. A
recent empirical study from our lab provided some preliminary
evidence for this; greater observed behavioral attention measured
during an attention task at 10 months was associated with less
observed behavioral frustration during a challenging task at 3 years
of age (Perry et al., 2016). Importantly, in this work neural activity
measured during the attention task at 10 months was also associated with later emotion regulation behavior through an association
with 10-month attention behavior. Therefore, understanding the
development of neural, behavioral, and contextual processes associated with early attentional control is particularly important when
aiming to better understand early antecedents of later behavior
problems and psychopathology.
Neurophysiological Underpinnings of
Attention Behavior
Data from work using electrophysiological and neuroimaging
techniques has shown that one function of attention at the neural
level is to increase the “gain” or salience of an attended stimuli or
event relative to an unattended one (e.g., Hillyard, Vogel, & Luck,
1998). This can occur either as an increase in neural activity
associated with the processing of that stimuli or event or a suppression of activity to other irrelevant stimuli or ambient noise
(Colombo & Salley, 2015; Neill & Westberry, 1987), with either
case making it more likely that neural connections surrounding
that stimulus or event are learned or acted upon and that connec-
tions between neural areas involved are strengthened (Colombo &
Salley, 2015). Thus, one consequence of attention processes at the
neural level is a reinforcement of coordinated or synchronous
neural activity within and across areas of the brain, which likely
facilitates other cognitive and regulatory processes for the infant
(Albright, Jessell, Kandel, & Posner, 2000; Colombo & Salley,
2015; Steinmetz et al., 2000). This neural synchrony has been
theorized to provide the basis for higher-order cognitive abilities,
including the formation of neurocognitive networks which lead to
the emergence of new behavior (Bressler & Tognoli, 2006; Fries,
2005). A large body of theoretical and empirical work supports the
existence of three neural networks that contribute to attention and
whose development mirrors the emergence of increasingly sophisticated attention behavior: the alerting, orienting, and executive
attention network or networks (Petersen & Posner, 2012; Posner &
Dehaene, 1994; Ruff & Rothbart, 1996). Recent work with resting
state functional connectivity using fMRI has shown that extensive
development of these networks proceeds rapidly so that adult-like
connectivity is present by the end of the first year (Gao, Gilmore,
et al., 2013; Gao, Zhu, et al., 2009).
We focus our examination on the executive attention network,
whose development is thought to underlie the more purposeful and
controlled aspects of attention that allow infants to voluntarily
engage and sustain their own attention toward the end of the first
year. The more volitional control of attention behavior that defines
executive attention is associated with activation of a neural network that includes the anterior cingulate cortex (ACC) in the
medial frontal lobe, lateral frontal and prefrontal cortex, and basal
ganglia, which help to start and control movement (Posner & Fan,
2008). By 2 years of age, the ACC exhibits strong connectivity to
both parietal and frontal areas associated with alerting, orienting,
and executive control of attention, making it a central component
of neural networks for attention (Gao et al., 2009). Empirical work
with noninfant samples has found that one function of the executive attention network is to monitor and resolve conflict at the
neural level, including conflict among thoughts, feelings, and
behavioral responses (Berger, Tzur, & Posner, 2006; Rothbart et
al., 1994; Rothbart, Sheese, & Posner, 2007). This has led to the
argument that the ACC and associated areas of midfrontal cortex
are central to the emergence of more sophisticated attention and
regulatory behavior because they function to monitor, regulate,
and resolve conflicting information from other neural networks
that might be activated in cognitive and emotional challenges (e.g.,
Botvinick, Braver, Barch, Carter, & Cohen, 2001).
Despite promising theoretical conceptualizations of the development of attention processes in the brain that underlie attention
behavior in infancy, empirical work providing data to support
these ideas is limited by methodology practical for use with
infants. Attention exerts its influence in the brain by modulating
the activity of neural systems involved in information processing
such that information processing in the attended channel is facilitated, whereas processing in irrelevant channels in inhibited
(Hillyard et al., 1998; Orekhova, Stroganova, & Posikera, 2001;
Rueda et al., 2005). Electroencephalogram (EEG) methodology
provides a noninvasive measure of neural activity measured at the
scalp level during spontaneous behavior and is therefore ideal for
developmental work while still providing a direct measure of
attention processes in the brain. The EEG signal is a measure of
brain electrical activity that is recorded via electrodes on the scalp
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MATERNAL BEHAVIOR AND INFANT ATTENTION PROCESSES
and results from summated postsynaptic neuronal potentials firing
in synchrony (Davidson, Jackson, & Larson, 2000). This synchronization of activity leads to a dominant frequency of oscillation
that is measureable at electrode sites placed at specific scalp
locations (e.g., Kagan, Snidman, Kahn, & Towsley, 2007). From
this, measures of EEG power, or the root-mean-square voltage of
the EEG signal within a frequency band of interest (Pizzagalli,
2007), can be derived that provide information about extent and
location of cortical activity. This activity can be measured at rest
and in response to specific situations or stimuli requiring attention
and is useful in the study of the development of attention networks
in infancy.
Although work with adults and infants has revealed potential
associations between attention performance and multiple frequency bands at multiple scalp locations (see Orekhova, Stroganova, & Posikera, 1999, 2001; see also a review by Saby &
Marshall, 2012), the vast majority of developmental EEG work has
identified the developmental alpha (6 to 9 Hz) frequency band as
the dominant frequency in infancy and early childhood and has
demonstrated its prevalence during both cognitive and emotional
processing in early development (e.g., Bell, 2001, 2002, 2012; Bell
& Fox, 1992; Diaz & Bell, 2011; Fox et al., 2001; Marshall,
Bar-Haim, & Fox, 2002; Orekhova et al., 2001). In addition, the 6to 9-Hz developmental alpha band has been suggested to approximate the adult alpha band, which has been associated with attentional modulation of cortical activity in adult work (e.g., Orekhova
et al., 2001; Ray & Cole, 1985).
Task-related changes in EEG power (in comparison to baseline)
are hypothesized to represent activation of brain areas underlying
specific scalp electrodes (Cuevas & Bell, 2011) recruited for task
performance and have been used as indicators of cognitive processing during laboratory tasks with infants and young children
(e.g., Bell, 2001, 2002; Wolfe & Bell, 2004, 2007) and adults (see
Klimesch, 1999 for a review). The 6- to 9-Hz developmental alpha
band has been shown to discriminate overall performance (Bell,
2001) and individual correct and incorrect responses (Bell, 2002)
on a working memory and inhibitory control task and on overall
performance on a sustained attention task (Orekhova et al., 2001)
in previous work with infants in the second half of the first year.
In general, this work has found that tasks which require cognitive
processing and attentional engagement result in increases in EEG
power from baseline to task in the 6- to 9-Hz frequency band (e.g.,
Bell, 2001; Bell & Wolfe, 2007; Orekhova et al., 2001) and that
individual differences in baseline to task changes in power are
associated with individual differences in task performance (Bell,
2001). In addition, task-related change in 6- to 9-Hz power, and
associations with task performance, becomes increasingly localized to frontal lobe locations with age, suggesting a preferential
role for activity of the frontal lobe for cognition and attention
processes in development (e.g., Bell, 2001, 2002; Orekhova et al.,
2001; Wolfe & Bell, 2004, 2007).
Neural activity from medial frontal scalp areas may at least
partially reflect activity of the ACC, and is consistently shown to
be present in higher order processes of attention regardless of task
domain in work with older children and adults (Posner & Rothbart,
1998; Posner & DiGirolamo, 1998). In a recent empirical paper
utilizing the same dataset as the current study, we found that
medial frontal 6- to 9-Hz EEG activity during an attention task was
associated with concurrent observed attention behavior at 10
15
months of age (Perry et al., 2016). Interestingly, this relationship
varied by hemisphere; an increase in right frontal (F4) power was
associated with more time spent looking at task stimuli while an
increase in power at the analogous left frontal location (F3) was
associated with less time spent attending. These findings are consistent with research in adults and older children showing a right
hemisphere specialization for attention based performance and that
right hemisphere volumes of the ACC and other frontal structures
correlate with performance on tasks requiring attention and response inhibition (Casey et al., 1997a, 1997b; Durston et al.,
2001). Thus, right frontal activity during attention processes may
be an optimal pattern of neurophysiological response from very
early in development, which we expect to replicate here, with
downstream consequences for attention behavior and associated
functioning in development.
Other infant work has demonstrated that larger baseline and task
specific 6- 9-Hz EEG power values at frontal locations are associated with better performance on an attention task (Diaz & Bell,
2011) and on working memory tasks that rely on attention shifting
(e.g., Bell, 2002; Bell & Wolfe, 2007; Cuevas & Bell, 2011).
Taken together, these results suggest that neural activity within the
frontal cortex may play a particularly important role in the development of infants’ observed attention behavior. EEG methodology
utilizing attention task related change in EEG power at medial
frontal scalp locations (F3/F4) may be one way to examine an
association between neural activity potentially linked with the
executive attention network and change in observed attention
behavior.
The Role of Caregiving on Behavioral
Attention Processes
Behavioral changes in attention in the first year have been well
documented and there is clear theoretical, and emerging empirical,
support for a neural basis for this change. However, relatively little
work has examined factors in the infant’s environment that may
influence this relationship in the first year. Applying a biopsychosocial perspective to the development of attention emphasizes the
importance of including both intrinsic biological factors (e.g.,
functioning of neural systems for attention outlined above) as well
as extrinsic environmental factors (e.g., caregiver behavior). Because of the increased plasticity during early development (e.g.,
Sanders, Stevens, Coch, & Neville, 2006; Stevens & Neville,
2013), interactions with caregivers may be a key factor contributing to individual differences in the emergence, maturation, and
consolidation of behavioral and neurocognitive systems underlying attentional abilities (Colombo, 2004).
Kopp (1982) and others (e.g., Calkins, 2004; Calkins, 2008;
Grossman & Grossman, 1991; Kopp & Neufeld, 2003; Posner &
Rothbart, 1998) have theorized that early caregiving has a strong
influence on the infant’s developing regulatory capabilities, which
include attention processes. This is because much of infant behavior develops in the context of an infant-caregiver dyad in which
caregivers initially act as external regulators of their infant’s
behavior (Calkins, 2008; Calkins & Fox, 2002; Kopp, 1982;
Sroufe, 2000). Although there is a relatively little work specifically
examining the influence of caregiver behavior on attention development in the first year, empirical studies have revealed that
caregivers initially regulate their infant’s arousal and attention by
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16
SWINGLER, PERRY, CALKINS, AND BELL
being aware of their infant’s capacity to receive and use stimulation (e.g., Brazelton, Koslowski, & Main, 1974; Sander, 1975;
Stern, 1977). For example, in their extensive work on the regulation of distress, Posner and Rothbart (1998) have noted that by 3
months many caregivers attempt to redirect infant attention by
using distraction techniques to bring their infant’s attention to a
positive or neutral stimuli, a caregiver’s effective use of these
strategies is thought to shape the infant’s developing capacity for
using these same strategies independently (Posner & Rothbart,
1998).
Caregiving behavior has rarely been examined in relation to
attentional development specifically; however, parental sensitivity,
warmth, and positive reinforcement have been associated with a
host of later positive socioemotional, cognitive, and academic
outcomes in child development (NICHD ECCRN, 1999, 2003;
Rimm-Kaufman, Pianta, Cox, & Bradley, 2003). Empirical work
on parenting has demonstrated that caregiver behavior is sensitive
when it occurs in response to an infant’s cues and is modified by
the infant’s behavior or state; thus, in the context of attentional
engagement, a sensitive caregiver responds with stimulation when
the infant is under aroused and reduces it when the infant is
engaged or overly stimulated. Thus, a sensitive caregiver who
shows more positive affect during interactions with their infant
may reinforce infant attentional engagement and exploration with
positive vocalizations, affect, or behavioral cues while infants are
attending, and only intervene and redirect attention when necessary and in response to the infant’s signals for a need for such
intervention. Because a sensitive and nonintrusive caregiver is able
to follow the infant’s lead to facilitate and support the infant’s own
attentional engagement, this may promote the development of
fundamental intrinsic processes which support independent attentional engagement for the infant. In contrast, intrusive caregiving
behavior is characterized by interventions that are not in response
to infants’ mood, state, or interest (Jacobvitz & Sroufe, 1987) and
are often in direct competition to the infants’ own source of
attentional engagement and interaction. Thus, intrusive caregiving
behavior has the potential to create rapidly shifting and disorienting sources of arousal and stimulation that place external demands
on the infant’s attention and may disrupt intrinsically controlled
attention processes. Indeed, previous work has demonstrated that
negative and intrusive caregiving behavior is associated with behavioral, academic, and social adjustment problems in later childhood (Cookston, Harrist, & Ainslie, 2003; Culp, Hubbs-Tait, Culp,
& Starost, 2000; Pike & Plomin, 1996; Rubin, Burgess, Dwyer, &
Hastings, 2003). Thus, caregiver levels of positive affect and
intrusive behavior in the context of routine interactions with the
infant may have the ability to facilitate or impede the development
of attentional processes at both a behavioral and neurophysiological level.
Influence of Caregiving on Neurophysiological
Attention Processes
Emerging empirical work has begun to provide evidence that
early relational experiences are closely related to neural development. The theoretical bases for this work comes from the idea that
basic neural circuitry established during the first years of life lays
the groundwork for later changes (e.g., Propper & Moore, 2006)
and is capable of being molded by the social environment (De
Bellis, 2001; Gunnar, Fisher, & the Early Experience, Stress, &
Prevention Network, 2006; Nelson, 2000; Propper & Moore,
2006). Social experience is thought to be especially salient in the
first two years of life when a spurt in brain growth characterized by
an overproduction of synapses occurs (Nelson, Thomas, & de
Haan, 2006). During this process, environmental experiences are
thought to directly influence the synaptic connections that persist
and are strengthened, or which are selectively eliminated due to
lack of use (Greenough & Black, 1992; Nelson & Bloom, 1997;
Singer, 1995). Recent work by our research group (Bernier,
Calkins, & Bell, 2016) has provided previously lacking empirical
support for the notion that normative variation in caregiving behavior early in development is predictive of individual differences
in brain development. Specifically, we found that more maternal
positivity during interactions when infants were 5 months of age
was associated with greater infant EEG alpha and theta baseline
power at 10 and 24 months, and greater increases in baseline
power between each age. Importantly, this effect was specific to
EEG power measured at frontal locations only; suggesting that
development of the frontal lobe, which is associated with emerging
attention and executive function abilities, may be especially sensitive to normative variation in caregiver behavior. Thus, caregiver
behavior and, in particular, a caregiver’s ability to support and
facilitate the infant’s early use of attention may have long term
effects on the structure and function of neural systems associated
with attention.
A second area of research has provided evidence that experience
with an adult can have a direct effect on brain activity associated
with attention processes in development. For example, engagement in joint attention with an adult when viewing an object results
in a larger peak amplitude of the Nc component of the eventrelated potential (indicating greater allocation of “neural attention”) in 9-month-old infants compared with a nonjoint attention
interaction condition (Striano, Reid, & Hoehl, 2006). The direction
of this effect suggests that joint attentional engagement, like that
which occurs in sensitive and responsive caregiving, results in
increased activity of areas of the brain associated with executive
attention in development. This suggests that one role of sensitive
caregiving behavior early in development may be to increase
activity in brain areas associated with neural networks of attention,
thereby strengthening connections between these areas and helping
to create a neural network for attention processes.
The Current Study
A large amount of theoretical and emerging empirical work
suggests that there are biological characteristics that are likely
present from birth that underlie the rapid attentional development
that occurs in the first year of life (e.g., Posner, Rothbart, &
Sheese, 2007; Rueda, Rothbart, McCandliss, Saccamanno, & Posner, 2005). However, these biological underpinnings, including
the neural systems underlying attention, are thought to be at
least partially modified by environmental input (BakermansKranenburg, van IJzendoorn, Pijlman, Mesman, & Juffer, 2008;
Sheese, Voelker, Rothbart, & Posner, 2007; Stevens, Sanders, &
Neville, 2006). The caregiving environment is arguably the most
important and influential context for infant development and caregiver manipulation of infant attention in the context of regulation
of infant distress has been well documented. Caregiver behavior in
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MATERNAL BEHAVIOR AND INFANT ATTENTION PROCESSES
17
their calculated due dates and were typically developing (see Table
1 for final sample size for each variable at each time point). For
mothers who reported educational information (N ⫽ 378), 97%
graduated from high school, 6% had a technical degree, 42% had
a bachelor’s degree, and 22% had a graduate degree. Mothers
were, on average, 29 years old (SD ⫽ 6) when the infants were
born. Families who did not return for a 10-month laboratory
assessment (n ⫽ 43) included those who could not be located,
moved out of the area, declined participation, or did not respond to
phone and letter requests to participate at the 10-month visit. There
were no significant differences between families who did or did
not participant at both time points in terms of child sex, race,
maternal education, or any of the primary study variables.
the context of typical daily interactions has been less well studied
in its potential relation to the infant’s developing attention behavior and underlying neural systems. Although caregiver behavior
that is positive and sensitive is likely to have a reinforcing impact
on the infant’s attention development, intrusive caregiver behavior
may actively disrupt attention processes for the infant. We examine whether maternal positive affect and intrusive behavior measured at 5 months in the context of two play based interactions
predicts infants’ attention behavior and associated neural activity
at 5 and 10 months. In a recent paper using data from the same
sample of infants as the current work, we found that normative
variation in caregiver behavior related to developmental change in
baseline EEG power from 5 to 24 months (Bernier et al., 2016).
Thus, we hypothesize that early maternal caregiving behavior
exhibited during regular interaction with the infant may have an
effect on the development of infants’ attention behavior through its
influence on the infant’s developing neurophysiological systems
supporting attention development. This work provides an important empirical test of the widespread theoretical belief that the
expansive influence of quality of caregiving behavior on a wide
range of child functioning occurs through children’s neural circuity (Belsky & de Haan, 2011; Bernier et al., 2016; Gunnar, 2003).
Procedures
Data were collected at both research locations using identical
protocols. Research assistants from each location were trained
together by the project’s Principal Investigator on protocol administration, as well as on behavioral and psychophysiological data
collection and coding. To ensure that identical protocol administration was maintained between the labs, the Blacksburg site
periodically viewed DVD recordings and psychophysiology files
collected by the Greensboro lab. To ensure that identical coding
criteria were maintained between labs, the Blacksburg lab provided reliability coding for behavioral data and verification of
artifact screening and data editing for psychophysiology data collected and coded by the Greensboro lab.
Upon arrival at the research laboratory, participants were
greeted by a research assistant who explained the study procedures
and obtained signed consent from the mother. After a brief
warm-up period, infants were fitted with the EEG cap and participated in a variety of behavioral tasks assessing cognitive and
emotional development. The start and end times of tasks were
marked in the EEG record by a research assistant in an adjacent
room who viewed the session via video feed from two wall
mounted cameras. The session video feed was digitally recorded
for later behavioral coding. Parents were paid $50 for each laboratory visit.
Method
Participants
As part of a longitudinal study examining individual differences
in the development of cognition and emotion across early development, 410 infants were recruited by two research locations
(Greensboro, NC and Blacksburg, VA), with each location recruiting half of the total sample. Infants were recruited via commercial
mailing lists, newspaper birth announcements, and word of mouth.
Of the 410 infants, 22 were reported to have been born with low
birth weight (i.e., less than 2,700 g) or were diagnosed with
developmental delay and were excluded from the final sample.
Therefore, the current study used data from 388 infants (199 girls,
189 boys; 303 Caucasian, 48 African American, 17 multiracial, 2
Asian, 14 other, 4 not reported) who were born within 15 days of
Table 1
Correlations and Descriptive Statistics for Study Variables
Variable
1
2
3
4
5
6
7
8
1. Maternal positive affect (5 m)
2. Maternal intrusiveness (5 m)
3. EEG power ⌬F3 (5 m)
4. EEG power ⌬F4 (5 m)
5. EEG power ⌬F3 (10 m)
6. EEG power ⌬F4 (10 m)
7. Attention behavior (5 m)
8. Attention behavior (10 m)
M
SD
Minimum
Maximum
Skew
(SE)
N
—
⫺.14ⴱⴱ
.02
⫺.01
⫺.04
⫺.01
.20ⴱⴱ
.20ⴱⴱ
2.63
.52
1.38
4.00
.52
(.13)
357
—
⫺.10
⫺.05
.12ⴱ
.09
⫺.16ⴱⴱ
⫺.06
1.34
.38
1.00
3.25
1.66
(.13)
357
—
.43ⴱⴱ
⫺.01
.08
.02
.04
.03
.31
⫺.95
1.47
.12
(.13)
355
—
.05
.10
.10
.12ⴱ
.06
.32
⫺1.10
1.41
.09
(.13)
355
—
.55ⴱⴱ
⫺.03
⫺.12ⴱ
.08
.31
⫺.91
.94
⫺.05
(.13)
331
—
⫺.05
.02
.09
.35
⫺.94
1.02
.59
(.13)
331
—
.35ⴱⴱ
58.94
17.07
20.80
94.84
.01
(.13)
370
—
60.65
13.22
27.66
94.73
.07
(.13)
343
ⴱ
p ⬍ .05.
ⴱⴱ
p ⬍ .01.
18
SWINGLER, PERRY, CALKINS, AND BELL
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Measures
Neural activity. EEG was recorded during a 1-min baseline
and during a visual attention task at 5 and 10 months. The procedure for obtaining baseline EEG was identical at both visits;
infants sat on their mothers’ laps and watched a research assistant
manipulate a toy containing brightly colored balls on a testing
table, 1.1 m in front of them. This baseline procedure quiets the
infant, yields minimal eye and gross motor movements, and allows
the infant to tolerate the EEG cap (e.g., Bell, 2001, 2012; Diaz &
Bell, 2011; Fox, Henderson, Rubin, Calkins, & Schmidt, 2001).
Recordings were made from 16 left and right scalp sites: frontal
pole (Fp1, Fp2), medial frontal (F3, F4), lateral frontal (F7, F8),
central (C3, C4), temporal (T7, T8), medial parietal (P3, P4),
lateral parietal (P7, P8), and occipital (O1, O2). All electrode sites
were referenced to Cz during recording. EEG was recorded using
a stretch cap (Electro-Cap International, Inc.; Eaton, OH; E1-series
cap) with tin electrodes in the 10/20 system pattern. After the cap
was placed on the head, a small amount of abrasive gel was placed
into each recording site and the scalp gently rubbed. Conductive
gel was then added to the recoding sites. Electrode impedances
were measured and accepted if they were below 20 k⍀.
The electrical activity from each lead was amplified using
separate Bioamps (James Long Company; Caroga Lake, NY).
During data collection, the high-pass filter was a single pole RC
filter with a 0.1-Hz cut-off (3 dB or half-power point) and 6 dB per
octave roll-off. The low-pass filter was a two-pole Butterworth
type with a 100 Hz cut-off (3 dB or half-power point) and 12-dB
octave roll-off. Activity for each lead was displayed on the monitor
of the acquisition computer. The EEG was digitized online at 512
samples per second for each channel to eliminate the effects of
aliasing. The acquisition software was Snapshot-Snapstream
(HEM Data Corp.; Southfield, MI) and the raw data were stored
for later analyses. Prior to the recording of each subject a 10-Hz,
50-uV peak-to-peak sine wave was input through each amplifier.
This calibration signal was digitized for 30 s and stored for
subsequent analysis. To ensure that the EEG data being collected
was as clean as possible, a visual inspection of the incoming data
from each electrode was performed by a trained experimenter
viewing the data on a computer in a control room adjacent to the
testing room. This experimenter also viewed the testing session via
camera and inserted event marks in the EEG data at the start and
finish of the baseline and attention tasks while the data was being
collected. These event marks were later used to segment the
baseline and attention task portions from the ongoing EEG record
for data analyses.
EEG data were examined and analyzed using EEG Analysis
software developed by James Long Company. Data were first
re-referenced via software to an average reference configuration
(Lehmann, 1987). The average reference EEG data were artifact
scored for eye movements using a peak-to-peak criterion of 100
uV or greater, and for gross motor movements using a peak-topeak criterion of 200 uV or greater. Segments of EEG data that
were scored as containing artifact were eliminated from all subsequent analyses. No artifact correction procedures were used. The
data were then analyzed with a discrete Fourier transform (DFT)
using a Hanning window of 1-s width and 50% overlap. Across
infants, the mean number (and proportion) of artifact-free DFT
windows during the baseline and attention tasks was 76.2 (.60) and
57.9 (.51), respectively, for the 5-month assessment; 57.07 (.46)
and 61.28 (.50), respectively, for the 10-month assessment. Differences in artifact-free DFT windows available for analyses between ages were primarily due to increases in gross motor artifact
as infants became increasingly physically active and mobile (baseline) and longer task times as infants’ sustained attention increased
(attention task) between 5 and 10 months.
Power was computed for the 6- to 9-Hz developmental alpha
frequency band, which is the dominant frequency for infants and
young children (Bell & Fox, 1992; Marshall, Bar-Haim, & Fox,
2002) and is used by infant EEG researchers to investigate both
cognitive and emotional processing (Bell, 2001, 2002, 2012; Diaz
& Bell, 2011; Fox et al., 2001; Orekhova et al., 2001), and
attentional modulation of cortical activity (e.g., Orekhova et al.,
2001; Ray & Cole, 1985). Therefore, the 6- 9-Hz frequency band
was both developmentally appropriate, and the most likely to
reveal associations with differences in attention behavior in our
infant sample. Power was expressed as mean square microvolts
and data were transformed using the natural log (ln) to normalize
the distribution. We derived a measure of task-related neural
activity at medial frontal scalp locations by subtracting baseline
EEG power from EEG power during the attention task at the
medial frontal electrode sites (F3 and F4). We chose to only
examine these medial frontal sites because of the well-established
role of the frontal cortex for attention processes (Posner & Fan,
2008) and previous work from our research group using data from
the same sample of infants and mothers demonstrating that an
effect of maternal behavior on infant and toddler EEG alpha power
was specific to frontal electrode locations only (Bernier et al.,
2016).
Attention behavior. At the 5- and 10-month laboratory visit
infants sat on their mothers’ laps 1.1m from the edge of the testing
table (90 cm [L] ⫻ 60 cm [W] ⫻ 75 cm [H]) and were presented
with a glove puppet adorned with facial features on the palm of the
glove and small bells attached to each fingertip (Cuevas & Bell,
2014; Diaz & Bell, 2011; Perry et al., 2016). The glove puppet was
presented until the infant looked at the glove four separate times,
with each look separated by at least 3 s during which the infant
looked away (procedure and criteria adapted from Diamond, Prevor, Callender, & Druin, 1997). Although this procedure ensured
that each infant was given multiple opportunities to direct their
attention to the stimuli, it resulted in different task times for each
participant (Cuevas & Bell, 2014). Thus, a proportion score of time
looking at the glove puppet in relation to the total task time was
used as the measure of infant attention. In the current study, a
greater proportion of time spent attending to the puppet was
indicative of greater behavioral attention.
Looking data were coded offline to determine proportion of time
looking. A video camera was placed behind and above the experimenter’s head and focused to maintain a close-up split-screen
view of the glove and the infant’s face. A research assistant coded
each infant’s look duration from a video recording of the laboratory session using the Video Coding System software developed
by James Long Company (Caroga Lake, NY). An additional
independent observer coded at least 20% of the recordings to
confirm reliability of coding. Intraclass correlations exceeded .91
for proportion of looking at each age at each study site.
Observed maternal behavior. Maternal behavior was observed at the 5-month laboratory visit during two sequential play
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MATERNAL BEHAVIOR AND INFANT ATTENTION PROCESSES
based interaction tasks with the mother and infant. For each task,
the mother was asked to turn so that she was facing her infant and
to interact with him or her as she normally would. During the toy
free-play task mothers were given two age appropriate infant toys
and asked to play with the infant for two minutes. This was
followed immediately by a peek-a-boo task in which mothers were
instructed to play peek-a-boo with their infant for an additional
two minutes using their hands or a provided washcloth.
Maternal behavior was coded in 30-s epochs during the mother⫺child interaction tasks using a coding scheme adapted from
previous work (Fish, Stifter, & Belsky, 1991; Shapiro & Mangelsdorf, 1994; Calkins, Hungerford, & Dedmon, 2004). Maternal
behavior across the epoch was rated on a scale ranging from 1 (no
evidence of the behavior) to 4 (consistent, high levels of the
behavior). The current analyses examined two dimensions of maternal behavior during mother-infant interaction: maternal positive
affect and maternal intrusiveness.
Maternal positive affect during the toy free play and peek-a-boo
tasks was defined as positive affect the mother expressed either
through tone of voice such as infant directed speech with positive
intonation and tone, facial expressions such as smiling or laughing,
or a combination of the two. Maternal intrusiveness was defined as
insensitive, overcontrolling behavior during which the mother
ignored or overrode the infant’s behavioral cues and initiations of
play or interaction in favor of her own behavioral agenda during
the toy free-play or the peek-a-boo game. Examples of intrusive
behaviors were failing to modulate her own behavior in response
to the infant turning away, pulling away, or expressing negative
affect toward the mother, a toy, or activity; overwhelming or
overstimulating the infant with a continuous barrage of toys or
play instead of letting the infant pace the play or interaction;
ignoring or interrupting the infant’s interest in a toy or activity by
introducing a different toy or activity, taking a toy or object away
from the infant when the infant was playing with it, or not allowing
the infant to touch a toy the mother was holding. Maternal behavior was also scored as intrusive if mothers physically manipulated
the infant’s hands or face to make them perform an action or
manipulation, especially if the infant was objecting to maternal
interference or was already independently playing.
Final scores for maternal behavior on each task were created by
summing scores across epochs and dividing by the number of
epochs to create an average maternal positive affect and maternal
intrusiveness score for the task. Since maternal behavior on the
two interaction tasks was significantly positively correlated (r ⫽
.45, p ⬍ .001 for positive affect; r ⫽ .30, p ⬍ .001 for intrusiveness) average maternal positive affect and intrusiveness scores
were created by averaging the scores for the two interaction tasks.
Reliability coding for maternal behavior was accomplished on at
least 20% of the sample for each task (range of 22% to 30%). The
interclass correlations (ICCs) between each pair of coders were
examined and determined to be acceptable for each task (range ⫽
.82⫺.96).
Results
A path analysis was conducted to examine the associations
between maternal behavior, infant attention behavior, and medial
frontal EEG activity utilizing Mplus (Version 7; Muthén &
Muthén, 2015). Full information maximum likelihood (FIML) was
19
used to handle missing data; all data were missing at random.
Maternal education was included as a covariate; as expected based
on previous work (e.g., Bernier et al., 2016; Mills-Koonce et al.,
2007; NICHD Early Child Care Research Network, 2004) it was
associated with our observed measures of maternal positive affect
(␤ ⫽ .19) and intrusiveness (␤ ⫽ ⫺.13) here as well (see Figure
1). Moreover, because baseline EEG power is used in the calculation of EEG power change and may also be individually associated with attention behavior, baseline EEG power values at 5 and
10 months were entered into the model as control variables.
Finally, given our interest in examining whether maternal behavior
predicted changes in medial frontal EEG activity from 5 to 10
months, and whether these changes were subsequently related to
changes in infant’s attention behavior from 5 to 10 months,
5-month EEG power change and 5-month observed behavioral
attention during the attention task were also controlled for in the
model. Descriptive statistics and bivariate correlations for the
primary study variables are provided in Table 1.
The hypothesized model fit well, ␹2 (40, N ⫽ 388) ⫽ 65.437,
p ⫽ ⬍.01, CFI ⫽ .96, RMSEA ⫽ .04 [CI ⫽ .02, .05] (unstandardized coefficients are presented in Table 2 and standardized
coefficients are presented in Figure 1). Below, we walk through
specific model pathways that directly reflect our primary research
questions. First, we sought to address whether changes in medial
frontal EEG activity (as indexed by EEG power change from
baseline to task at medial frontal scalp locations F3 and F4) were
associated with changes in infant attention behavior during the
glove puppet attention task at 10 months. After controlling for
5-month EEG power change and 5-month attention behavior,
baseline to task increases in EEG power at medial frontal locations
F3 and F4 at 10 months were associated with the amount of time
infants spent attending to the glove puppet at 10 months, although
the specific pattern of association varied by hemisphere (see Figure 1). An increase in EEG power change from baseline to task at
10 months at the right frontal medial location, F4, was associated
with more time spent looking at the puppet during the attention
task. In contrast, an increase in EEG power change from baseline
to task between 5 and 10 months at the left frontal medial location,
F3, was associated with less time spent looking at the puppet.
An additional aim of this work was to examine whether maternal positive affect and intrusiveness at 5 months predicted changes
in infants’ attention processes from 5 to 10 months. With regard to
changes in attention behavior, the direct path from maternal intrusiveness at 5 months to the percentage of total time spent looking
at the glove puppet during the attention task at 10 months was not
significant. However, higher levels of maternal positive affect at 5
months was directly associated with greater time spent attending at
10 months after controlling for time spent attending at 5 months,
suggesting that more maternal positive affect at 5 months is
associated with greater increases in infants observed attention
behavior in this task from 5 months to 10 months (see Figure 1).
We also sought to examine associations between maternal positive affect and intrusiveness and changes in infant’s medial frontal
EEG activity from 5 to 10 months during the attention task.
Maternal positive affect was not directly related to infants’ baseline to attention task change in EEG power values at either medial
frontal location. Maternal intrusiveness at 5 months was associated
positively with infant’s 10-month baseline to attention task change
in EEG power values at the left frontal midline location, F3, after
SWINGLER, PERRY, CALKINS, AND BELL
20
Baseline EEG F3
(5 months)
Maternal Edu
EEG Power ∆ F
(5 months)
Baseline EEG F3
(10 months)
A en on Behavior
(5 months)
.19**
EEG Power ∆ F3
(10 months)
.33**
A
-.14**
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This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
Maternal Posi ve
Affect
(5 months)
.52**
Maternal
Intrusiveness
(5 months)
n on Behavior
(10 months)
EEG Power ∆ F4
(10 months)
-.13**
Maternal Edu
EEG Power ∆ F4
(5 months)
Baseline EEG F4
(10 months)
Baseline EEG F4
(5 months)
Figure 1. Standardized estimates for the indirect effects model predicting 10-month attention behavior.
Italicized wording delineates variables included for the purposes of controlling for previous levels. Bold pathway
delineates significant associations among primary variables of interest. ⴱ p ⬍ .05. ⴱⴱ p ⱕ .01.
controlling for 5-month baseline to task change in EEG power at
this location (see Figure 1). This suggests that greater maternal
intrusiveness during interactions at 5 months is associated with
greater increases in attention-related power change at the left
medial frontal location F3 from 5 months to 10 months. In contrast, intrusiveness was not associated with infants’ baseline to
attention task change in power values at the right medial frontal
location, F4.
Finally, we aimed to assess whether maternal positive affect and
intrusiveness were indirect predictors of infant attention behavior
via 5- to 10-month change in infants’ medial frontal EEG activity
during the attention task. Although it was hypothesized that early
maternal positive affect may be indirectly related to 10-month
observed attention through an effect on changes in neural activation from 5 to 10 months, maternal positive affect at 5 months was
not significantly associated with medial frontal neural activity at
either electrode location at 10 months (see Figure 1). Thus, the
indirect effects could not be considered. Maternal intrusiveness at
5 months was not associated with infant’s baseline to task EEG
power change at the right medial frontal location, F4, but was
positively associated with EEG power change at the left medial
frontal location, F3 (see Figure 1). Therefore, only the indirect
effect from maternal intrusiveness at 5 months to infant observed
attention at 10 months via 10-month change in neural activity at
the left medial frontal electrode site F3 (controlling for 5 month
levels of both) was tested. To test this indirect effect, a biascorrected bootstrapping procedure (10,000 draws) was performed.
This approach has been shown to generate the most accurate
confidence intervals for indirect effects, reducing Type I error rates
and increasing power over other similar tests (MacKinnon, Lockwood, & Williams, 2004). The indirect path was significant (unstandardized estimate ⫽ ⫺.61, 95% BC bootstrap [CI ⫺1.9,
⫺.02]), indicating that greater maternal intrusiveness when infants
were 5 months was associated with less time spent attending to the
glove puppet task stimulus at 10 months, through its association
with an increase in neural activation at 10 months at the left medial
frontal location during the attention task.
Discussion
We examined the role of maternal behavior during interaction
with their infants at 5 months of age on the infants’ developing
neural and behavioral attention processes in the second half of the
first year of life. We proposed that maternal behavior may have a
direct effect on infant’s developing attention behavior, but that it
may also have an indirect effect on attention behavior through an
effect on infants’ neural attention systems which rapidly develop
to adult-like connectivity and functioning by the end of the first
year (Gao et al., 2009, 2013). Thus, we hypothesized that we might
find an effect of maternal behavior measured in interactions at 5
months on infants’ neural systems for attention, measured as
neurophysiological responses to an attention task at 10 months of
age.
MATERNAL BEHAVIOR AND INFANT ATTENTION PROCESSES
21
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This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
Table 2
Unstandardized Model Estimates
Covariance
Maternal Positive Affect (5m) ↔ Maternal Intrusiveness (5m)
Baseline EEG F3 (5m) ↔ Baseline EEG F4 (5m)
EEG Power ⌬F3 (5m) ↔ EEG Power ⌬F4 (5m)
Baseline EEG F3 (10m) ↔ Baseline EEG F4 (10m)
EEG Power ⌬F3 (10m) ↔ EEG Power ⌬F4 (10m)
Covariate
Maternal Edu (5m) ¡ Maternal Positive Affect (5m)
Maternal Edu (5m) ¡ Maternal Intrusiveness (5m)
Baseline EEG F3 (10m) ¡ EEG Power ⌬F3 (10m)
EEG Power ⌬F3 (5m) ¡ EEG Power ⌬F3 (10m)
Baseline EEG F3 (5m) ¡ EEG Power ⌬F3 (5m)
Baseline EEG F4 (10m) ¡ EEG Power ⌬F4 (10m)
EEG Power ⌬F4 (5m) ¡ EEG Power ⌬F4 (10m)
Baseline EEG F4 (5m) ¡ EEG Power ⌬F4 (5m)
Attention Behavior (5m) ¡ Attention Behavior (10m)
Focal path
Maternal Positive Affect (5m) ¡ EEG Power ⌬F3 (10m)
Maternal Positive Affect (5m) ¡ EEG Power ⌬F4 (10m)
Maternal Positive Affect (5m) ¡ Attention Behavior (10m)
Maternal Intrusiveness (5m) ¡ Attention Behavior (10m)
Maternal Intrusiveness (5m) ¡ EEG Power ⌬F3 (10m)
Maternal Intrusiveness (5m) ¡ EEG Power ⌬F4 (10m)
EEG Power ⌬F3 (10m) ¡ Attention Behavior (10m)
EEG Power ⌬F4 (10m) ¡ Attention Behavior (10m)
We found that change in task-related medial frontal EEG activity was related to time spent attending during the attention task at
10 months of age even after controlling for prior levels of attention
behavior and EEG in the same task at 5 months. Our findings
indicated that the direction of this relationship varied by hemisphere. A baseline to task increase in EEG power at the right
frontal location (F4) was associated with more time spent attending during the task at 10 months. In contrast, an increase in power
from baseline to task at the analogous left frontal location (F3) was
associated with less time spent attending. Because this sample was
used in our previous work addressing the role of behavioral and
neural attention processes for the development of emotion regulation, it is not surprising that we found the same pattern of results
at 10 months with regard to hemispheric differences (Perry et al.,
2016).
These findings are consistent with both clinical and developmental research that has shown a right hemisphere specialization
for attention based performance and demonstrated that volumes of
the right anterior cingulate of the ACC and other structures of the
right frontal cortex correlate with performance on tasks requiring
attention and response inhibition in middle childhood and early
adolescence (Casey et al., 1997a, 1997b; Durston et al., 2001).
These results also demonstrate that although greater right frontal
activity is associated with greater proportion of time spent attending, greater left frontal activation during an attention task is related
to less time spent attending and may suggest a potential disadvantage for left frontal activation during attention processes in infancy. We interpret these findings to suggest that right frontal
activity during attention processes is an optimal pattern of neurophysiological response from very early in development and that
deviations in this pattern of neural response may have downstream
Estimate
SE
p
⫺.03
.23
.04
.22
.05
.010
.019
.005
.020
.006
.007
.000
.000
.000
.000
.09
⫺.04
⫺.27
⫺.07
⫺.21
.38
.01
⫺.27
.25
.024
.017
.028
.049
.029
.153
.051
.028
.041
.000
.012
.000
.167
.000
.608
.861
.000
.000
⫺.02
.01
3.14
⫺1.21
.09
.09
⫺6.67
5.36
.032
.036
1.367
1.993
.050
.053
2.495
2.197
.477
.893
.022
.545
.049
.098
.008
.015
consequences for attention behavior and for other areas of functioning that rely on attention development.
In our prior work, we have demonstrated that attention behavior
in infancy predicts later emotion regulation abilities and that there
is an indirect effect linking early neurophysiological functioning
during attention processes to later emotion regulation abilities
through early attention behavior (Perry et al., 2016). Given the link
between the early development of attention processes and the later
development of more sophisticated emotional and cognitive abilities (e.g., Posner et al., 2014), a better understanding of environmental factors that may facilitate or impede attention development
at both the biological and behavioral levels is important. Thus, our
primary goal in the current article was to extend our previous work
and examine specific caregiving behaviors in the first year that
may influence the development of attention behavior as well as
associated neurophysiological functioning.
Our results indicate that maternal positive affect at 5 months had
a direct positive effect on infant attention behavior at 10 months,
even after controlling for infants’ 5-month attention behavior.
Thus, maternal positivity during interactions early in development
seems to have a facilitative effect on infants’ developing attention
capabilities; infants who have experienced more positivity during
interactions with their mother earlier in development show more
evidence of independent attentional engagement and visual exploration toward a new stimulus at 10 months of age. One interpretation for this finding is that infants who have experienced high
levels of positivity during early interactions with their mother may
be inclined to look at and engage more with a new stimulus as a
result of a history of interactions in which new stimuli are often
paired with positive vocal and facial cues from the mother. With
this positivity, mothers may be signaling to their infants that these
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22
SWINGLER, PERRY, CALKINS, AND BELL
new objects are safe and interesting and should be attended to and
explored. In addition, infant attentional engagement has likely
been consistently met with positivity and reinforcement from the
mother, thereby promoting the likelihood of infant attentional
engagement in the future.
Although maternal positive affect at 5 months was significantly
associated with infants’ attention behavior at 10 months, positive
affect did not show a significant association with infant medial
frontal EEG activity during the attention task at 10 months. This
result was contrary to our original hypothesis that maternal positivity would be related to differences in neural activity associated
with attention processes in early development. However, this finding has led us to consider an alternative hypothesis that a history
of maternal positivity during interactions may have a reinforcing
effect on the developmental progression of attention processes that
occur in a common fashion across individuals in typical development. That is, the ability to sustain attention and independently
engage and disengage attention is naturally increasing during this
developmental period in general, and this is theorized to be at least
partially a result of normative development of neural networks
associated with attention processes. Thus, mothers who show more
positivity during interactions with infants early in development
may be creating more opportunities for the infant’s attention to be
engaged and pairing this engagement with reinforcing positive
stimulation and feedback. These increased opportunities for attentional engagement, as well as an established association between
attentional engagement and positive or rewarding social stimulation, may lead to increased attentional engagement behavior, but
may not change the natural development of neural networks for
attention that is occurring during this time. Thus, mothers who are
more positive may reinforce a natural proclivity to engage with
and attend to new stimuli, resulting in differences in infant attention behavior but not in the neural activity specifically associated
with this behavior. In fact, recent work from our lab has shown that
maternal positive affect may be associated with increases in baseline frontal EEG power between 5 and 10 months (Bernier et al.,
2016). Thus, maternal positive affect may influence the activity of
the frontal lobe in this period of development, but this may not
extend to activity specifically associated with attention processes.
In contrast to positive affect, we did not find a direct effect of
maternal intrusiveness at 5 months on infant attention behavior at
10 months. However, higher levels of maternal intrusiveness during the 5-month interaction were significantly associated with
greater activity at the left medial frontal electrode location (F3)
during performance of the attention task. Intrusive caregiving
behavior is characterized by unsolicited assistance or intervention
and attempts to change the child’s behavior, which can often lead
to distress or avoidance and shutting down to avoid overstimulation and protect from an overload in information processing and
overarousal (e.g., Ainsworth, Blehar, Waters, & Wall, 1978; Belsky, Rovine, & Taylor, 1984; Tronick, 1989). Because intrusive
caregivers do not appear to be sensitive to infant attentional
engagement and arousal needs, they may often interrupt or interfere with the infant’s own attention processes to impose their own.
During the first year of life, when rapid change in the neural
processes supporting attention development is occurring, these
interventions may have long-reaching consequences for the development of neural connections that support the emergence of more
sophisticated and complex attention behavior in development.
Given that maternal positive affect was not significantly associated with EEG power change at either medial frontal location, we
could not examine a potential indirect association with attention
behavior. However, the indirect effect from maternal intrusiveness
to observed attention behavior via neurophysiological attention
processes was significant. Specifically, higher levels of maternal
intrusiveness during interactions when the infant was 5 months
was associated with less attention behavior during the attention
task at 10 months through its relationship with greater left medial
frontal (F3) activity during the task. Although this is a preliminary
finding that will require systematic follow-up in future work, this
is an intriguing result that suggests that intrusive maternal behavior
early in development may have a disruptive effect at the neural
level on developing attention processes that leads to measurable
differences at the behavioral level.
Neural networks that subserve attention processes and give rise
to change in attention behavior are rapidly developing during this
period and may follow a typical pattern of development such that
increased neural connections lead to the emergence of more complex, sophisticated, and nuanced attention abilities. Experience
using these more sophisticated attention abilities in turn leads to
increased specialization and connection of neural areas for attention. However, factors in the environment that disrupt the infant’s
attention experience may have the ability to alter or impact the
neural development processes. By consistently interrupting and
disrupting their infant’s attentional engagement and experience,
intrusive mothers may be preventing the environmental input
necessary for the development of neural specialization and connections associated with attention processes in the brain. A second,
but not mutually exclusive, alternative is that intrusive mothers
may actually be altering the pattern of neural activity that occurs in
the context of attentional engagement by interfering with the
infant’s attention and creating additional demands in which the
infant has to abandon their own attentional engagement or goals in
favor of the mother’s external demands on the infant’s attention. In
either case, accumulated experience with intrusive caregiving appears to be related to the infant’s own attentional abilities by the
second half of the first year, and an effect on infant’s neural
activity during attention appears to be one mechanism through
which this occurs.
Although these findings are intriguing and provide important
preliminary evidence for theories regarding factors in the caregiving environment that may shape the development of behavioral and neural attention processes, these data were collected as
part of a longitudinal study examining multiple aspects of early
cognitive and emotional development and associated psychophysiology. Future work designed to systematically and carefully examine the role of early maternal interactive behavior on
infants’ developing attention abilities and associated neural
development is necessary to more formally test these hypotheses. For example, we examined maternal behavior in the context
of two free-play interaction episodes; future work should examine maternal behavior across multiple contexts, including
those designed specifically to engage infant attention and elicit
maternal control of infant attentional processes across the first
year. Similarly, we examined infant attention behavior during
the presentation of a novel stimulus designed to elicit interest
and looking in infants. However, future studies should examine
infant attention abilities more rigorously in tasks designed to
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MATERNAL BEHAVIOR AND INFANT ATTENTION PROCESSES
examine multiple dimensions of attention, which may be
mapped specifically to underlying neural activity associated
with the development of neural networks.
It will also be important for future work examining these
questions to utilize different samples of infants and motherinfant dyads. Although the current sample was relatively diverse, the majority of mothers in our sample had a college
education or higher (65%). As education level and income have
both been associated with maternal sensitivity in a variety of
other work (e.g., Bernier et al., 2016; Mills-Koonce et al., 2007;
NICHD Early Child Care Research Network, 2004) and were
related to our measures of maternal positive affect and intrusiveness here, an important goal for future work will be to
recruit mother⫺infant dyads with more variability in these
measures.
In addition, these data were not designed to examine factors
that may predict maternal sensitivity and parenting behavior.
Some of these factors may lie within the mother; for example,
maternal depression has been shown to predict both maternal
behavior during interactions with infants (e.g., Cohn, Campbell,
Matias, & Hopkins, 1990; Cohn & Tronick, 1989; Field, Sandberg, et al., 1985) as well as measures of infant electrical brain
activity (e.g., Dawson, Frey, Panagiotides, Yamada, Hessl, &
Osterling, 1999; Field, Fox, Pickens, & Nawrocki, 1995).
Therefore, maternal depression is an important variable that
should be included in future work to further pull apart associations between maternal behavior, infant neural activity, and
attention development. Moreover, much theoretical and emerging empirical work suggests that parent– child interactions are a
result of complex bidirectional and reciprocal influences such
that certain child temperaments or biological predispositions
may elicit more optimal parenting (e.g., Perry, Mackler,
Calkins, & Keane, 2013), which in turn could contribute to
biological and neural development influencing child functioning. Future work using longitudinal cross-lagged designs measuring multiple assessments of parent and child functioning,
and neural development, will be necessary for testing such
hypotheses.
In sum, our work suggests that greater maternal intrusiveness
during interactions at 5 months of age is one factor that is
associated with a potentially suboptimal pattern of neural activity during attention processes at 10 months, which has negative effects on infant attention behavior at 10 months of age,
but may also have cascading negative effects for later development. For example, in our previous work we found that neural
activity during our attention task at 10 months was associated
with emotion regulation in the preschool years through an effect
on attention behavior in infancy. Taken together with our previous work, a pattern of findings emerges in which more right
frontal (F4) activity during an attention task at 10 months is
associated with greater attentional engagement behavior at 10
months and greater emotion regulation capabilities (less frustration) at 3 years, through its association with greater attentional abilities at 10 months. In contrast, more left frontal (F3)
activity is associated less attentional engagement behavior at 10
months and less regulation (greater frustration) at 3 years,
through its association with less attentional engagement at 10
months (Perry et al., 2016). Our work here demonstrates that
maternal intrusiveness in the first year is one environmental
23
factor that can predict the pattern of neural activity present
during the attention task, and that this has implications for
attention behavior. Given that right hemisphere dominance for
attention related tasks has been found in previous work with
older kids and adults we have hypothesized that right frontal
activity during attentional engagement at 10 months of age may
be an optimal “default” pattern of development, which fosters
the emergence of more sophisticated attention behavior by the
end of the first year. In contrast, greater left frontal activity may
be evidence of a suboptimal, potentially disordered pattern that
occurs because of disruption in the environment, like intrusive
caregiving, which precludes the strong right hemisphere connections that best serve attention processes and results in less
optimal neural responses and concurrent and prospective behavioral attention and regulatory deficits. This is an intriguing
and important finding that should be carefully investigated in
future longitudinal work.
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