Although the study of attention and its development has a long and rich history (e.g., Colombo, Reference Colombo2001, for a review; Lansink & Richards, Reference Lansink and Richards1997; Richards & Casey, Reference Richards and Casey1990), more recent work has focused on the role of early attention skills in the emergence and maintenance of adaptive behavior and functioning in a range of domains. Attention skills are thought to be especially important for the regulation of behavior and emotions in infancy and early childhood (e.g., Posner & Rothbart, Reference Posner, Rothbart and Richards1998; Rothbart, Posner, & Boylan, Reference Rothbart, Posner, Boylan and Enns1990; Ruff & Rothbart, Reference Ruff and Rothbart1996). Because deficits in early regulation abilities are considered to be central to childhood psychological problems, and thought to partially constrain subsequent development in a variety of domains (Calkins, Reference Calkins, Brownell and Kopp2008; Calkins & Fox, Reference Calkins and Fox2002; Keenan, Reference Keenan2000), a child's ability to control his or her own experience and expression of negative emotion is critical for adaptive social and emotional functioning. Moreover, the lack of such skills has been implicated as a precursor to the development of both anxiety and antisocial behavior (Calkins & Keane, Reference Calkins and Keane2004; Kindt & Van Den Hout, Reference Kindt and Van Den Hout2001). Thus, basic attentional processes appear to contribute to the development of more sophisticated regulatory processes, such as those involved in the control of emotion, and are implicated in developmental pathways to adaptive and maladaptive functioning throughout life.
Current conceptualizations of child development acknowledge that there are complex interactions among the child's biology, behaviors, and environment (Gottlieb, Reference Gottlieb and Magnusson1997; Sameroff, Reference Sameroff2010; Shonkoff, Reference Shonkoff2010) that impact developmental pathways. Development in any domain is at least partially dependent on fundamental neurophysiological, behavioral, and social processes, which become elaborated and integrated over time (Calkins, Reference Calkins, Bates and Wachs1994, Reference Calkins, Brownell and Kopp2008; Thompson, Lewis, & Calkins, Reference Thompson, Lewis and Calkins2008). This biopsychosocial perspective underscores the contribution of underlying biological processes that interact with the child's environment to produce patterns of growth and change influential to the development of important skills critical for adjustment. This is echoed in a developmental psychopathology perspective that advocates an organizational view of development and underscores the importance of investigating multiple factors, or levels of a given factor, in the context of one another rather than in isolation (Cicchetti & Dawson, Reference Cicchetti and Dawson2002). From this perspective, there are multiple pathways to maladaptive and adaptive outcomes, and a number of contributors may interact in various ways within different individuals to predict disordered behavior and/or multiple variants of emotional functioning (Cicchetti, Reference Cicchetti1984, Reference Cicchetti1993; Cicchetti & Rogosch, Reference Cicchetti and Rogosh1996; Sroufe & Rutter, Reference Sroufe and Rutter1984). In this paper, we use such a perspective to understand the role that early attention processes may play in developmental pathways to adjustment and maladjustment.
In this paper, we adopt the premise that there are fundamental neural and behavioral attentional processes that grow, interact, and integrate throughout development that provide the basis for the development of attention skills and the emergence of adaptive emotion regulation abilities (Thompson & Goodvin, Reference Thompson, Goodvin, Brownell and Kopp2007). However, like others (e.g., Blair, Reference Blair2002; Calkins, Reference Calkins2011), we view this development as a dynamic process involving transactions between the child and his or her environment. Basic research on human neuroplasticity has identified neurocognitive systems underlying attention as displaying a great deal of plasticity in early development (e.g., Sanders, Stevens, Coch, & Neville, Reference Sanders, Stevens, Coch and Neville2006; Stevens & Neville, Reference Stevens, Neville and Gazzaniga2013). During this period of increased plasticity, interactions with caregiver(s) dominate the infant's social environment, making caregiver behavior a key factor contributing to individual differences in the emergence, maturation, and consolidation of behavioral and neurocognitive systems underlying attentional control and subsequent adjustment or maladjustment (Cicchetti & Dawson, Reference Cicchetti and Dawson2002; Luthar, Cicchetti, & Becker, Reference Luthar, Cicchetti and Becker2000).
Throughout the paper, we utilize a developmental psychopathology and neural plasticity framework to highlight the importance of considering both extrinsic environmental (i.e., caregiver behavior) and intrinsic biological (i.e., infant neural functioning) factors, as well as potential dynamic transactional effects between the two, for the development of attentional control. We believe that using such a perspective and considering development across levels of biology, behavior, and environment provides us with insight into the more proximal developmental mechanisms and processes that influence the early development of attention. A greater understanding of early attentional development may not only help to identify critical points of entry for early intervention and prevention but also increase our understanding of the emergence of later emotion regulation capabilities and lead to advances in the diagnosis, prevention, and possible treatment of increasingly prevalent disorders associated with deficits in the regulation of attention and emotion (Fox & Calkins, Reference Fox and Calkins2003).
We begin by highlighting the importance of attentional control for children's behavioral adjustment rooted in the development of emotion regulation abilities. We then review the development of attention behavior and underscore the importance of developing neural systems and caregiver behavior for shaping attentional control. Finally, we posit that the experience-dependent neural plasticity that is characteristic of attention systems in the brain may be one mechanism through which maternal caregiving behavior influences the development of infants’ attentional control in the first year and later emotion regulation abilities known to be influential to childhood psychopathology.
Attention Behavior and Emotional Responding
Attentional control has been of particular interest to researchers aiming to better understand precursors to adaptive emotional functioning and behavioral maladjustment because it has been associated with mechanisms for resolving conflict among thoughts, feelings, and behavioral responses (Rueda, Posner, & Rothbart, Reference Rueda, Posner and Rothbart2005). For example, the ability to control attention is thought to be one process that allows infants to regulate more biologically based emotional reactivity to produce behavior. 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, Reference Posner and Rothbart2000; Rothbart & Bates, Reference Rothbart, Bates and Eisenberg1998). Attention orienting skills in particular have been identified as a critical component of early emotion regulation processes, because orienting has the direct effect of amplifying at a neural level the stimuli toward which attention is directed, thus changing the affective experience of the individual (Rothbart, Posner, & Rosicky, Reference Rothbart, Posner and Rosicky1994).
Given the role attentional processes play in infants’ control of arousal and regulation of affective expression, qualitative shifts in attention skills across the first 12 months of life can be seen as fundamental to the qualitative shifts in emotion regulation that are also observed during this period. The period from 3 to 6 months, for example, marks a major transition for infants in which the ability to voluntarily control their own attention, and subsequently their own arousal level, begins to emerge (Calkins, Reference Calkins, Baumeister and Vohs2004). Rothbart (Reference Rothbart1981, Reference Rothbart1986) found increases in positive affect and decreases in distress in infants this age during episodes of focused attention, providing empirical evidence that control of attention is tied to affective experience during this time period. By the end of the first year, infants are able to employ organized sequences of behavior during emotionally arousing contexts that enable them to disengage, redirect attention, and self-sooth in a flexible manner that suggests that they are responsive to environmental cues and able to adapt their own behavior accordingly (Calkins, Reference Calkins, Baumeister and Vohs2004). The coincident timing of the emergence of more sophisticated attentional control with more adaptive emotion regulation abilities has been proposed as further evidence of an association between the development of the attention system and emotional functioning in the first year of life (Bell & Calkins, Reference Bell, Calkins and Posner2012).
Deviations or delays in the development of attentional control and associated regulation likely contribute to maladaptive developmental trajectories associated with poor regulatory abilities. Thus, the importance of regulation of attention and the management of emotional (and nonemotional) arousal for adaptive functioning has been underscored in work examining the etiology of a range of developmental psychopathologies that all include problems with attention as a common symptom (e.g., Rothbart & Posner, Reference Rothbart, Posner, Cicchetti and Cohen2006). For example, deficits in alerting, attention shifting, and sustaining attention, have been linked to attention-deficit/hyperactivity disorder, with inattentive children showing a decreased ability to maintain an alert state and sustain attention in the absence of valid cues (Casey, Castellanos, Giedd, & Marsh, Reference Casey, Castellanos, Giedd and Marsh1997; Swanson et al., Reference Swanson, Posner, Potkin, Bonforte, Youpa and Cantwell1991).
Orienting and attention-shifting abilities have been theoretically and empirically linked to anxiety, depression, and mood disorders as well (Derryberry & Rothbart, Reference Derryberry and Rothbart1988; Fox, Russo, & Dutton, Reference Fox, Russo and Dutton2002). Because a tendency to focus and ruminate on negative ideations is a symptom of anxiety and depression (Beck, Reference Beck1976), one proposed explanation for this link is that individual differences in orienting and attention shifting may be related to the time and effort spent dwelling on negative stimuli (Rothbart & Posner, Reference Rothbart, Posner, Cicchetti and Cohen2006). In addition, neuroimaging data has shown that cognitive–behavioral therapy, an effective treatment for depression, resulted in change in neural networks that included areas involved in attention (Cicchetti & Posner, Reference Cicchetti and Posner2005; Goldapple et al., Reference Goldapple, Segal, Garson, Lau, Bieling and Kennedy2004; Mayberg, Reference Mayberg2003). Given these direct associations, and that attentional processes have been suggested as a mechanism through which infants and toddlers gain control of arousal and regulate affective expression, a better understanding of the development of attentional control within the first year is critical for advancing our knowledge of the development of emotion regulation and emotional competence thought to underlie later behavioral adjustment (Bronson, Reference Bronson2000; Calkins, Reference Calkins, Baumeister and Vohs2004).
The Development of Attention Behavior in the First Year
Attention is typically defined as achieving and maintaining an alert state, orienting to sensory events, and controlling thoughts and feelings (Posner & Fan, Reference Posner, Fan and Pomerantz2008). The measurement of infant visual attention has a long history as a tool for assessing various aspects of early development and has been shown to be a significant predictor of childhood cognitive functioning and associated outcomes (Colombo, Reference Colombo2002; Posner & Fan, Reference Posner, Fan and Pomerantz2008). Early developmental work on infant attention used visual habituation paradigms (i.e. repeated stimulus presentations) and looking duration as the primary measures of attentional control. This body of literature led to the notion that development of attention over the first year was primarily characterized by a linear decrease in the duration of looking, with younger infants (e.g., 3-month-olds) looking for more prolonged periods relative to older infants (e.g., 7-month-olds; Colombo & Mitchell, Reference Colombo, Mitchell, Colombo and Fagen1990). However, a comprehensive meta-analysis (Colombo, Harlan, & Mitchell, Reference Colombo, Harlan and Mitchell1999) of the data on the development of look duration over infancy revealed evidence for three fairly distinct phases of attention development. From birth to 8–10 weeks, look duration increases and is thought to reflect an increase in alertness and attention engagement abilities. During the 3- to 6-month period, look duration declines and is thought to be reflective of more sophisticated information processing leading to shorter durations of attention engagement needed to process a stimulus. From 7 months on, looking duration plateaus or may gradually increase in response to more complex or dynamic stimuli. Thus, maintaining an alert state and orienting to sensory events are the primary components of infants’ attentional abilities very early in life, but attentional flexibility and the capacity to control and manipulate attention is evident by the end of the first year (e.g., Rothbart et al., Reference Rothbart, Posner and Rosicky1994; Ruff & Rothbart, Reference Ruff and Rothbart1996).
Despite clear developmental patterns of looking behavior associated with attention processes, early work also demonstrated individual differences in duration of looking that were relatively stable within an individual across testing occasions and associated with later attention performance (Colombo, Mitchell, O'Brien, & Horowitz, Reference Colombo, Mitchell, O'Brien and Horowitz1987). For instance, infants with longer looking times tended to perform more poorly than their shorter looking peers on visual recognition and memory tasks, especially when the amount of exposure to stimuli was limited (e.g., Colombo, Mitchell, Coldren, & Freeseman, Reference Colombo, Mitchell, Coldren and Freeseman1991). Longer looking times have also been associated with delays in the ability to disengage and shift visual attention, suggesting a perseveration of attention beyond what is necessary for stimulus processing. This has led to the hypothesis that individual differences in attention measured by looking duration reflect the speed of information processing, which has been shown in work from a number of different groups to be related to multiple aspects of later functioning (for a review, see Colombo, Kapa, & Curtindale, Reference Colombo, Kapa, Curtindale, Oakes, Cashon, Casasola and Rakison2010), including emotion regulation (Diaz & Bell, Reference Diaz and Bell2011). Essentially, shorter looking times may reflect better attention and information-processing abilities, which allows infants to receive accurate and important information from their surroundings more quickly. The result of this is a greater potential for learning from the visual environment and responding flexibly and efficiently to environmental demands (Ruff & Rothbart, Reference Ruff and Rothbart1996).
Following the initial work on looking duration as an indicator of attention functioning, a major contribution to the study of attention in development came with the application of cognitive neuroscience methods to demonstrate that infant looking is not a unidimensional behavior, but rather represents a variety of attentional states and components that work together to influence looking behavior. These components include the processes of orienting and engaging attention, disengaging attention, shifting attention, and sustaining attention (also called endogenous attention). A number of studies found that infants’ look durations very early in development are directly related to these specific components of visual attention and may be an early indicator of their development. For example, look duration during a familiarization episode was significantly correlated with later attention disengagement in 3- and 4-month-olds (Frick, Colombo, & Saxon, Reference Frick, Colombo and Saxon1999), and attention disengagement, distribution, and shifting in 5- to 9-month-olds (Jankowski & Rose, Reference Jankowski and Rose1997). Developmental work has shown that these components of attention typically emerge sequentially in development with orienting and engaging attention emerging early and disengaging, shifting, and sustaining attention emerging later in the first year. In addition, these behaviors are exhibited and seem to serve a common purpose for the infant across cognition and emotion contexts, providing support for the general involvement of attention in regulatory processes across a variety of environmental situations and demands (e.g., Johnson, Posner, & Rothbart, Reference Johnson, Posner and Rothbart1991).
The elaboration of this basic developmental work in the last 20 years has supported the existence of three brain networks that contribute to attention and underlie the emergence of these behaviors: the alerting, orienting, and executive attention network(s) (Posner & Dehaene, Reference Posner and Dehaene1994; Posner & Petersen, Reference Posner and Petersen1990). Alerting is the most basic aspect of attention and describes the state of wakefulness and arousal of an organism that is present from birth; the emergence of the alerting network prior to 3 months of age is thought to underlie the initial increase in infants’ looking behavior (Colombo et al., Reference Colombo, Harlan and Mitchell1999). The orienting network is involved in the selection of information from sensory input and allows the infant to begin to disengage fixation and voluntarily shift visual attention (Posner & Peterson, Reference Posner and Petersen1990). The orienting network is functionally mature between 3 and 6 months and is thought to underlie the decline in looking that occurs in the middle of the first year (Colombo, Reference Colombo2001; Courage, Reynolds, & Richards, Reference Courage, Reynolds and Richards2006). Executive attention involves mechanisms for resolving conflict among both internal and external information, including conflict among thoughts, feelings, and behavioral responses (Rueda, Posner, et al., Reference Rueda, Posner and Rothbart2005). This conflict resolution is necessary for the volitional and more controlled aspects of the attentional system that are reflected in the plateau in looking at the end of the first year, and theorized to underlie the downstream development of emotion regulation and executive functions (Berger, Tzur, & Posner, Reference Berger, Tzur and Posner2006; Cuevas & Bell, Reference Cuevas and Bell2014). Its central role in multiple aspects of cognitive and emotional functioning has made executive attention the focus of much developmental and adult work that reveals that one function of the executive attention network in the brain is to monitor and resolve conflict at the neural level using dynamic coordination of promotion and suppression of activation in various brain areas that are central to regulatory efforts across cognition and emotion domains (Berger et al., Reference Berger, Tzur and Posner2006; Rothbart et al., Reference Rothbart, Posner and Rosicky1994; Rothbart, Sheese, & Posner, Reference Rothbart, Sheese and Posner2007).
Because the early emergence of more sophisticated regulatory strategies is heavily reliant on the development of the executive attention network during the latter half of the first year of life (Fox & Calkins, Reference Fox and Calkins2003; Grolnick, Bridges, & Connell, Reference Grolnick, Bridges and Connell1996; Kopp, Reference Kopp2002; Silk, Shaw, Skuban, Oland, & Kovacs, Reference Silk, Shaw, Skuban, Oland and Kovacs2006), delays or disruptions in the development of the executive attention network may be one source of individual differences in the development of effective emotion regulation and may result in elevated risk for developing early psychopathology such as internalizing and externalizing behavior problems (e.g., Calkins, Reference Calkins, Bates and Wachs1994, Reference Calkins2010; Calkins & Keane, Reference Calkins and Keane2004). Thus, individual differences or disruptions in the development of the executive attention network are likely to have a cascade effect on development in associated cognitive and emotional domains that rely heavily on attention. These differences may arise as a result of biological factors within the child or because of variations in environmental input during the period of rapid development of this network in the first year. Understanding the influence of each of these factors as well as potential variations in their dynamic effect on one another within an individual can provide useful information for understanding individual patterns of adaptation and maladaptation.
Extrinsic and Intrinsic Influences on Attention Development
A developmental psychopathology framework necessitates examination of both intrinsic and extrinsic factors to better understand the development of regulatory processes, including attentional control (Calkins, Reference Calkins, Bates and Wachs1994; Fox & Calkins, Reference Fox and Calkins2003). For the purposes of this paper, we use the term intrinsic to mean those individual differences that are biologically based (e.g., Calkins, Reference Calkins, Bates and Wachs1994; Fox, Reference Fox1994; Fox & Calkins, Reference Fox and Calkins2003; Fox, Henderson, & Marshall, Reference Fox, Henderson, Marshall, Nelson and Luciana2001), and we focus on underlying neural systems that support and are engaged in processes of attention. Extrinsic factors are environmental (e.g., Calkins, Reference Calkins, Bates and Wachs1994; Fox & Calkins, Reference Fox and Calkins2003), and because the most salient environment to an infant is the caregiving environment, we limit our discussion to the manner in which caregivers shape and socialize infants’ development through patterns of caregiving behavior.
Although we consider these two factors independently in the following sections, we adopt an integrative approach to the study of the development of attention by underscoring the joint contribution of caregiving and neurophysiological processes related to attentional control. Infants and children bring with them strong biological characteristics that underlie their attentional development and are likely present from birth (e.g., Bell et al., Reference Bell, Batterink, Currin, Pakulak, Stevens and Neville2008; Posner, Rothbart, Sheese, & Tang, Reference Posner, Rothbart, Sheese and Tang2007; Rueda, Rothbart, McCandliss, Saccamanno, & Posner, Reference Rueda, Rothbart, McCandliss, Saccomanno and Posner2005). However, these biological underpinnings, including the neural systems underlying attention, are thought to be at least partially modified by environmental input (Bakermans-Kranenburg, van IJzendoorn, Pijlman, Mesman, & Juffer, Reference Bakermans-Kranenburg, van IJzendoorn, Pijlman, Mesman and Juffer2008; Sheese, Voelker, Rothbart, & Posner, Reference Sheese, Voelker, Rothbart and Posner2007; Stevens, Sanders, & Neville, Reference Stevens, Sanders and Neville2006). Thus, considering the integration between intrinsic and extrinsic factors known to influence the development of attention may be more informative than considering each in isolation and may advance our knowledge regarding the plasticity of neurophysiological processes underlying the development of attentional control.
Intrinsic neural systems
The emergence of the alerting, orienting, and executive attention systems in the first year is strongly associated with intrinsic neurophysiological processes. These processes underlie the connectivity of neural circuitry thought to be implicated in the growth and change of attentional abilities. Each of these networks is composed of a different set of brain structures and exhibits a unique developmental trajectory paralleling the emergence of associated attention behavior reviewed earlier (Colombo & Cheatham, Reference Colombo, Cheatham and Kail2006; Posner & Fan, Reference Posner, Fan and Pomerantz2008). Alerting attention behaviors are associated with the locus coruleus of the pons and right frontal and parietal cortex, while orienting behavior is associated with areas of the frontal eye fields, inferior and superior parietal lobe, and the superior colliculus, a midbrain structure involved in control of gaze movements. The volitional attentional control that defines executive attention is associated with activation of a neural network including 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, Reference Posner, Fan and Pomerantz2008).
There is some evidence that from very early in development there is at least rudimentary overlap in the functional connectivity of these networks, although activation between brain regions comprising these networks becomes increasingly coordinated during the latter half of the first year with significant development continuing into early childhood (Berger et al., Reference Berger, Tzur and Posner2006; Posner, Rothbart, Sheese, & Voelker, Reference Posner, Rothbart, Sheese and Voelker2012). Work using functional magnetic resonance imaging functional connectivity (i.e., measurement of synchronization in activity from distinct areas) during a resting state has revealed that in neonates, parietal areas associated with the orienting network exhibit strong connectivity to the lateral and medial frontal areas associated with the executive attention network (Posner et al., Reference Posner, Rothbart, Sheese and Voelker2012). By 2 years of age, the ACC exhibits strong connectivity to both the parietal and frontal areas associated with alerting, orienting, and executive attention (Gao et al., Reference Gao, Zhu, Giovanello, Smith, Shen and Gilmore2009). Thus, although the potential for coordination among brain areas comprising these networks seems to be present early, stronger and more specific connections continue to emerge and strengthen with development and experience.
Neural connections within the executive attention network specifically have been implicated as the most critical for supporting developing regulatory abilities and have therefore been the focus of much theoretical and empirical work (Posner & Rothbart, Reference Posner, Rothbart and Richards1998, Reference Posner and Rothbart2009; Rothbart et al., Reference Rothbart, Sheese and Posner2007). Methodological limitations make examining the development of a network of brain areas difficult, especially in infancy. Thus, researchers have begun to focus on specific areas of the brain involved in the development of more sophisticated attentional control. A consistent finding across work utilizing developmental and adult populations is that activity of the ACC and prefrontal cortex is preferentially active in tasks that involve executive attention (Posner & Fan, Reference Posner, Fan and Pomerantz2008).
A number of researchers have argued that the ACC and associated areas of the midfrontal cortex are central to the development of the executive attention network because they function to monitor, regulate, and resolve conflicting information from other neural networks (e.g., Botwinick, Braver, Barch, Carter, & Cohen, Reference Botwinick, Braver, Barch, Carter and Cohen2001). Much empirical data from adult work has supported this idea and revealed that a core set of functions subsumed by the ACC facilitate coordination of an integrated network of neural areas that work together in executive attention tasks (Botwinick et al., Reference Botwinick, Braver, Barch, Carter and Cohen2001; Bush, Luu, & Posner, Reference Bush, Luu and Posner2000). The ACC seems to be particularly important because it serves as a sort of “relay station” coordinating input and output from multiple areas involved in the control of both cognition and emotion (Posner et al., Reference Posner, Rothbart, Sheese and Tang2007). Neural activity measured at the midline of the frontal lobe is thought to reflect activity of the ACC, and is consistently shown to be present in “higher order” processes of attention regardless of task domain (Posner & DiGirolamo, Reference Posner, DiGirolamo and Parasuraman1998; Posner & Rothbart, Reference Posner, Rothbart and Richards1998). Developmental imaging work has also supported the role of the ACC in attention and revealed that the extent of ACC activation is consistently related to a child's observed performance on laboratory tasks, as well as parental reports of self-regulation and emotional control abilities (Posner & Rothbart, Reference Posner, Rothbart and Richards1998), suggesting that ACC activation is integral to attentional processes from early in development.
The prefrontal cortex also plays a functional role in the deployment of attention, and in particular, attentional involvement in the processing and regulation of cognition, emotion, and behavior. This is because the prefrontal cortex is one of the primary areas with inputs and outputs to the ACC that underlie the effortful regulation of behavior (Posner & Rothbart, Reference Posner, Rothbart, Bertelson, Eelen and Ydewalle1994, Reference Posner, Rothbart and Richards1998). The ACC uses reciprocal connections between the prefrontal cortex and structures of the limbic, autonomic, visceromotor, and endocrine systems to perform the task of governing cognitive, attentional, and emotional processes (Davidson, Putnam & Larson, Reference Davidson, Putnam and Larson2000; Davis, Bruce, & Gunnar, Reference Davis, Bruce and Gunnar2002; Lane & McRae, Reference Lane, McRae and Beauregard2004; Luu & Tucker, Reference Luu, Tucker and Beauregard2004). The involvement of attentional control in emotional regulation strategies is therefore facilitated by the overlap in the neural circuitry via the ACC and the areas of prefrontal cortex involved in both emotion regulation and sustained attention (Beauregard, Levesque, & Paquette, Reference Beauregard, Levesque, Paquette and Beauregard2004; Ernst et al., Reference Ernst, Liebenauer, King, Fitzgerald, Cohen and Zametkin1994; Rubia et al., Reference Rubia, Halari, Smith, Mohammed, Scott and Giampietro2008; Smith, Taylor, Brammer, Toone, & Rubia, Reference Smith, Taylor, Brammer, Toone and Rubia2006). Thus, activation within the prefrontal cortex may also play a particularly important role in the development of attention behavior in infancy that is associated with later emotion regulation development.
Despite promising theoretical conceptualizations of the development of the executive attention network and the interconnectedness of attention and emotion processes in the brain in infancy, empirical work providing data to support these ideas is limited by available methods practical for use with infants. Attentional control 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, while processing in irrelevant channels is inhibited (Rueda, Posner, et al., Reference Rueda, Rothbart, McCandliss, Saccomanno and Posner2005; Orekhova, Stroganova, & Posikera, Reference Orekhova, Stroganova and Posikera2001). Therefore, neural activity measured at the scalp level is one method that can provide a direct measure of attention processes in the brain. Electroencephalogram (EEG) methodology provides a measure of neural activation that is ideal for developmental work because it is noninvasive and able to be tolerated even by very young infants. The EEG signal is a measure of brain electrical activity that is recorded via electrodes on the scalp and results from summated postsynaptic neuronal potentials firing in synchrony (Davidson, Jackson, & Larson, Reference Davidson, Jackson, Larson, Cacioppo, Tassinary and Berntson2000). 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, Reference Kagan, Snidman, Kahn and Towsley2007). From this, measures of EEG power and event-related potentials (ERPs) can be derived that provide information about the extent and timing of cortical activity at rest and in response to specific situations or stimuli. It is also possible to derive a measure of EEG coherence, thought to reflect the presence and strength of anatomical connections in the brain (e.g., Coan & Allen, Reference Coan and Allen2004; Nunez, Reference Nunez1981).
EEG power is the root mean square average amplitude of the EEG signal within a frequency band of interest (Pizzagalli, Reference Pizzagalli, Cacioppo, Tassinary and Bernston2007). EEG coherence is the frequency-dependent cross-correlation of electrical signals between two scalp electrode sites (Nunez, Reference Nunez1981; Thatcher, Krause, & Hrybyk, Reference Thatcher, Krause and Hrybyk1986) and a measure of phase synchrony between spatially distinct neural generators (Mundy, Fox, & Card, Reference Mundy, Fox and Card2003). Some theorists have argued that coherence provides a measurement of neural network integrations and differentiations by providing an index of the strength and number of synaptic connections between brain regions (Nunez, Reference Nunez1981; Thatcher, Reference Thatcher, Dawson and Fischer1994). Unlike power, coherence is not affected by arousal, eyes open versus eyes closed conditions, or by changes in state (e.g., alert vs. sleepy); in this way, measures of coherence and power are independent. Thus, whereas EEG power can provide a measure of brain function, coherence can provide a measure of neural organization and development, and both may be useful in the study of the development of attention networks in infancy.
Unlike spontaneous EEG, which is recorded continuously across time and provides measures of power and coherence, ERPs are voltage oscillations in the ongoing EEG signal that are time locked to the occurrence of a specific physical or mental event (Picton et al., Reference Picton, Bentin, Berg, Donchin, Hillyard and Johnson2000). These potentials can be recorded at the scalp level and extracted from the continuous EEG data through a process of filtering and then averaging across like trials, which results in a waveform containing components of interest. These components occur at a particular time (latency) and amplitude and can therefore provide information about the timing and amount or extent, as well as approximate topographical location, of neural activation in response to an external stimulus or demand (Reynolds, Guy, & Zhang, Reference Reynolds, Guy and Zhang2011). In this way, ERP measures may provide valuable insight into the development of both early, automatic attentional processes, and the more effortful control of attention characteristic of executive attention that emerges later in the first year.
Despite its potential utility to provide early evidence for neural networks associated with attention in infancy, relatively little work has examined the development of executive attention in infancy using EEG methodology. Further, existing work linking EEG and attentional functioning in development has focused primarily on EEG power and ERPs; no work that we are aware of has utilized EEG coherence in relation to attention development in an infant sample. Research examining the development of EEG power across infancy and early childhood has primarily assessed the 6- to 9-Hz frequency band, which is the dominant frequency in infancy and has been shown to be involved in both cognitive and emotional processing (Bell, Reference Bell2001, Reference Bell2002, Reference Bell2012; Fox, Henderson, Rubin, Calkins, & Schmidt, Reference Fox, Henderson, Rubin, Calkins and Schmidt2001; Stroganova, Orekhova, & Posilera, Reference Stroganova, Orekhova and Posikera1999). The 6- to 9-Hz infant alpha band is thought to approximate the adult alpha band, which has consistently been associated with attentional modulation of cortical networks in adult work (e.g., Orekhova et al., Reference Orekhova, Stroganova and Posikera2001; Ray & Cole, Reference Ray and Cole1985).
Developmental studies have found that relative power in the 6- to 9-Hz frequency band shows a peak at central electrode sites around 7 to 10 months of age and is most evident during periods of quietly attending to a stimulus; this peak reaches maximum amplitude at 24 months of age during similar conditions (Bell & Fox, Reference Bell and Fox1992; Galkina & Boravova, Reference Galkina and Boravova1996; Marshall, Bar-Haim, & Fox, Reference Marshall, Bar-Haim and Fox2002; Orekhova et al., Reference Orekhova, Stroganova and Posikera2001; Stroganova, Orekhova, & Posikera, Reference Stroganova, Orekhova and Posikera1998; Stroganova et al., Reference Stroganova, Orekhova and Posikera1999). Further, recent work using looking time methodology during a familiarization paradigm found that 5-month-olds who had shorter looking durations (fast habituators) had higher power in 6- to 9-Hz EEG activity at all electrodes at baseline than did infants who showed longer looking (slow habituators; Diaz & Bell, Reference Diaz and Bell2011). This finding may be indicative of different levels of brain maturation resulting in individual differences in attention behavior in the first year (e.g., Cuevas & Bell, Reference Cuevas and Bell2014; Marshall et al., Reference Marshall, Bar-Haim and Fox2002).
Evidence for the role of neural activity in attention behaviors in infancy has been found in an additional frequency band as well. Stroganova and colleagues (Orekahova, Stroganova, & Posikera, Reference Orekhova, Stroganova and Posikera1999; Stroganova et al., Reference Stroganova, Orekhova and Posikera1998) found activity of the 4- to 6-Hz theta band to be related to attention processes in infants during tasks requiring anticipation of an expected event. Specifically, activity in this frequency band increased during anticipatory attention in 7-month-olds, and at prefrontal and frontal scalp locations this increase was positively related to the amount of time infants spent engaged in attention (Stroganova et al., Reference Stroganova, Orekhova and Posikera1998). Theta activity is abundant in infant EEG and is therefore sometimes considered a precursor to the adult alpha rhythm (Markand, Reference Markand1990; Orekhova et al., Reference Orekhova, Stroganova and Posikera2001). Although an increase in theta activity is known to accompany positive emotional reactions in infants (Maulsby, Reference Maulsby1971; Nikitina, Stroganova, & Posikera, Reference Nikitina, Stroganova, Posikera, Trojan and Stastny1987; Stroganova & Posikera, Reference Stroganova, Posikera and Adrianov1993), these authors interpreted the enhancement of the theta rhythm over the frontal lobes during anticipatory attention as reflective of activity of the executive attention system (Stroganova et al., Reference Stroganova, Orekhova and Posikera1998). This was because of the effortful nature of the attention behavior involved and because a similar positive correlation between theta power at the frontal and prefrontal locations and performance on tasks that require effortful control of attention has been found in adult work (e.g., Lang, Lang, Diekmann, & Kornhuber, Reference Lang, Lang, Diekmann and Kornhuber1987). In follow-up work, this group also found that better attention performance was associated with higher amplitude EEG power values in both the theta and the alpha frequency band ranges in 7- to 12-month-old infants during internally (anticipatory) and externally (visual display) controlled attention tasks, although this result was strongest for EEG measured during the externally controlled attention condition (Orekhova et al., Reference Orekhova, Stroganova and Posikera2001). Thus, these studies provide evidence that neural activity in multiple frequency bands in infancy is related to attention development in the first year. This neural activity may be particularly related to the development of executive attention because it occurs at scalp locations associated with executive attention in adults (Orekhova et al., Reference Orekhova, Stroganova and Posikera2001; Ray & Cole, Reference Ray and Cole1985), and is most evident during more effortful (as opposed to automatic) attention processes in infants.
A separate line of work providing information about the neural underpinnings of attention in infancy has found negative going components of the ERP that are associated with the development of attention processes (the negative component [Nc]; e.g., Courchesne, Ganz, & Norcia, Reference Courchesne, Ganz and Norcia1981; Nelson, Reference Nelson, Dawson and Fischer1994) and deliberate attentional and cognitive control (the N200 component; Gehring & Willoughby, Reference Gehring, Willoughby, Ullsperger and Falkenstein2002; Luu, Flaisch, & Tucker, Reference Luu, Flaisch and Tucker2000; Parasuraman, Reference Parasuraman1998; Potts, Martin, Burton, & Montague, Reference Potts, Martin, Burton and Montague2006; Yeung, Holroyd, & Cohen, Reference Yeung, Holroyd and Cohen2005). For example, behavioral work measuring error detection in infancy has shown that by 7 months of age infants look longer (i.e., devote more attention) to an erroneous scenario than an expected one (Wynn, Reference Wynn1992). Berger et al. (Reference Berger, Tzur and Posner2006) extended this work by measuring ERP during this behavioral paradigm and showed that 7-month-old infants also displayed an ERP component that discriminated correct from incorrect trials in frontal midline locations. In addition, this ERP component was identical in morphology and observed scalp location to an ERP component (the error-related negativity) found in error detection work with adults that has been determined to come from the ACC (Dehaene, Posner, & Tucker Reference Dehaene, Posner and Tucker1994). Thus, this finding was interpreted as evidence that even in the first year of life the anatomy of the executive attention system is at least partly in place and measurable at the scalp level using EEG methodology (Posner et al., Reference Posner, Rothbart, Sheese and Tang2007).
Other work using ERP methodology to examine the neural underpinnings of attention in the first year found that the amplitude of the Nc component is related to individual differences in attention behaviors and attentional engagement. The amplitude of the Nc reflects the extent of neuronal firing and is thought to be a measure of allocation of “neural attention” in response to salient stimuli or events in developmental populations (e.g., Courchesne et al., Reference Courchesne, Ganz and Norcia1981; Nelson, Reference Nelson, Dawson and Fischer1994). Moreover, source localization work using high-density electrodes suggests that the cortical sources of the Nc are likely the same frontal areas associated with attention in adults (e.g., ACC and prefrontal cortex; Reynolds, Courage, & Richards, Reference Reynolds, Courage and Richards2010; Reynolds & Richards, Reference Reynolds and Richards2005; Richards, Reynolds, & Courage, Reference Richards, Reynolds and Courage2010). One study, for example, found that the amplitude of the Nc component in response to novel and familiar stimuli was distinct for infants who were short lookers (fast to habituate) versus longer lookers (slow to habituate) in a familiarization epoch. Only 6-month-olds who were short lookers showed a greater amplitude of the Nc component in response to novel stimuli compared to familiar stimuli at midline frontal electrodes likely reflecting activity of the ACC (Guy, Reynolds, & Zhang, Reference Guy, Reynolds and Zhang2013). Additional studies have shown that the amplitude of the Nc is impacted by a stimuli's salience and the infants’ level of attentional engagement with a stimulus (e.g., de Haan & Nelson, Reference de Haan and Nelson1997, Reference de Haan and Nelson1999; Reynolds et al., Reference Reynolds, Courage and Richards2010; Reynolds & Richards, Reference Reynolds and Richards2005). By combining ERP measures with heart rate measures of attention, Richards (Reference Richards2003a, Reference Richards2003b) showed that the Nc is greater in amplitude during sustained attention than during attention termination. Thus, these studies provide further evidence that activity of the neural system for executive attention is present early in development and is associated with individual differences in attention behavior.
In sum, the presence of established, predictable neural networks underlying the early development of alerting, orienting, and executive attention provides a strong biological basis for increased attention control across the first year of life. The executive attention network, and in particular the ACC and the prefrontal cortex that are part of this network, are associated with the emergence of more volitional attentional control and provide a neural mechanism for the overlap among emotion, cognition, and attention processes in development. The neural network for executive attention appears to serve as a neural regulator between different areas of the brain thought to be associated with emotion and cognition processes, making it the target of much research examining the role of attention in regulatory functioning in a variety of domains. Research assessing the activation of the executive attention network is limited in developmental and infant populations. However, there is some evidence that the executive attention network is present and overlaps and coordinates with other neural systems underlying attention from early in development. Measuring neural activity at the scalp level may help to address this gap in the literature because it appears to be one way in which researchers can assess activation of the executive attention system in infants as young as 6 and 7 months of age. Although the early development of attentional control is strongly impacted by these intrinsic biological factors, the development of attentional systems is thought to be one of the most malleable (Stevens & Neville, Reference Stevens, Neville and Gazzaniga2013), and is therefore susceptible to extrinsic environmental influences. Thus, it is necessary to also consider the impact of salient factors in the child's environment, such as caregiver behavior, in the early development of attentional abilities.
Extrinsic caregiver influences
Despite evidence for a strong neural basis for the emergence of attention processes, conceptual and empirical work has shown that caregiver behavior also plays a role in the development of biological and behavioral regulatory processes involved in attentional control (Calkins & Hill, Reference Calkins, Hill and Gross2007; Crockenberg & Leerkes, Reference Crockenberg and Leerkes2004; Fox & Calkins, Reference Fox and Calkins2003; Swingler, Perry, Calkins, & Bell, in press). Others (e.g., Calkins, Reference Calkins, Baumeister and Vohs2004, Reference Calkins, Brownell and Kopp2008; Grossmann & Grossmann, Reference Grossmann, Grossmann, Parkes, Stevenson-Hinde and Marris1991; Kopp, Reference Kopp1982; Kopp & Neufeld, Reference Kopp, Neufeld, Davidson, Scherer and Goldsmith2003; Posner & Rothbart, Reference Posner, Rothbart and Richards1998) have further suggested that the reason that early caregiving is critical to infants’ developing capacities for self-regulated attention and emotion is that these processes develop in the context of an infant–caregiver dyad in which caregivers initially act as external regulators of their infant's regulatory rhythms, affect, and attention, thereby exerting direct influence over both biological and behavioral processes.
A biopsychosocial perspective motivates multilevel research to assess relations between social influences and biological and behavioral indicators of the factors that may be implicated in developmental pathways to attentional control, emotion regulation, and child adjustment. Therefore, in the following section, we consider the way in which social interactions between caregivers and infants play a role in the development of attention at both a biological and a behavioral level. Understanding social influences on each level of child functioning allows us to better capture the complex associations between extrinsic and intrinsic factors for developmental outcomes and may be more informative than considering levels in isolation. Given that the focus of the majority of work linking caregiving to attention has been conducted within the emotion realm, we begin with a focus on theoretical and empirical work addressing caregiver influences on the development and use of infants’ attention-based behaviors to regulate emotion, and then transition to a review of current literature regarding the role of caregiver behaviors for developing neurophysiological processes underlying attention.
Caregiver influences on attention behaviors
The early life of the infant is primarily concerned with the regulation of state and distress, and attention-based behaviors are one mechanism through which independent control of arousal and regulation of affect is attained. To the extent that the caregiver can appropriately read infant signals early in development and respond in ways that minimize an infant's distress or elicit positive interaction, the infant will learn from and integrate these experiences into an emerging behavioral repertoire of regulatory skills (Calkins, Graziano, Berdan, Keane, & Degnan, Reference Calkins, Graziano, Berdan, Keane and Degnan2008). Posner and Rothbart (Reference Posner, Rothbart and Richards1998) have noted that prior to 3 months of age, caregivers are heavily involved in helping the infant to regulate his or her own state and report holding and rocking as the main means of quieting the infant. However, beginning around 3 months of age, many caregivers (especially in Western cultures) report attempting to redirect infant attention by distracting their infants from distress and bringing their attention to positive or neutral stimuli (Posner & Rothbart, Reference Posner, Rothbart and Richards1998). As infants attend to neutral stimuli, they are often quieted and distress diminishes (Harman, Rothbart, & Posner, Reference Harman, Rothbart and Posner1997). Thus, early control of orienting and attention processes, which serves to diminish distress and negative affect for the infant, is largely in the hands of caregivers and dependent on their ability to utilize attention processes in this way (Posner & Rothbart, Reference Posner, Rothbart and Richards1998).
During the second half of the first year, more direct control of attention passes from the caregiver to the infant, such that the infant becomes increasingly able to employ independent attentional strategies to self-regulate, or engage caregiver attention when needed. A history of shared experiences that are effective in reducing infants’ arousal may lead infants to independently employ attention strategies in challenging situations that have been effective in reducing distress in the past. By establishing synchronous and well-regulated communicative patterns, caregivers can create a coregulatory context in which infants associate their own behaviors and the caregiver's behaviors with accompanying changes in their emotional state and arousal (Gianino & Tronick, Reference Gianino, Tronick, Field, McCabe and Schneiderman1988; Kopp, Reference Kopp1989). For instance, caregivers may engage in facial and vocal cues that distract infants when they are distressed, thereby introducing the redirection of infant attention as an emotion regulation strategy. By utilizing distraction techniques, caregivers give infants opportunities to learn that shifts in attention can coincide with decreases in negative affect (Spinrad & Stifter, Reference Spinrad and Stifter2002). Infants who repeatedly experience reduced negative affect through these interactions may then develop and repeat similar behaviors when confronting challenging situations independently. In this way, the same attentional mechanisms that initially get practiced through repeated dyadic interactions may provide the basis for the emergence of independent comforting and distraction behavior used to regulate emotion in early infancy, and lay the groundwork for more effortful control of emotion and cognition in late infancy and early childhood (Posner & Rothbart, Reference Posner, Rothbart and Richards1998).
Cross-sectional and longitudinal studies have supported the association between caregiving behavior during dyadic interaction and the child's use of attention-based regulatory strategies. Calkins and Johnson (Reference Calkins and Johnson1998), for example, found that when mothers used more positive guidance, their 18-month-old infants engaged in more distraction and gaze aversion strategies during frustrating events. Conversely, negative maternal behaviors, including overcontrol and intrusiveness across a variety of contexts, have been found to be negatively related to the use of distraction and sustained attention in a sample of toddlers (Calkins, Smith, Gill, & Johnson, Reference Calkins, Smith, Gill and Johnson1998). This relation has been demonstrated earlier in life as well; mothers and fathers who were more sensitive had 4-month-old infants who displayed increased attention orienting toward a caregiver during a challenge (Braungart-Rieker, Garwood, Powers, & Notaro, Reference Braungart-Rieker, Garwood, Powers and Notaro1998). Similarly, mothers who were more sensitive in interactions that took place prior to a still-face episode had infants who showed more attention-seeking behaviors (e.g., looking to her, smiling, and reaching) and greater positive affect during the still-face episode (Kogan & Carter, Reference Kogan and Carter1996; Mesman, van IJzendoorn, & Bakermans-Kranenburg, Reference Mesman, van IJzendoorn and Bakermans-Kranenburg2009).
Finally, joint attention work has shown that infants who spend more time engaged in collaborative joint attention during a parent-involved frustration task avert their attention away from the object of frustration more frequently, providing support for the suggestion that parents who establish shared attention during interaction may facilitate the development of the infant's ability to use his or her own attention to reduce distress (Morales, Mundy, Crowson, Neal, & Delgado, Reference Morales, Mundy, Crowson, Neal and Delgado2005). Thus, there is clear empirical evidence that attentional processes that serve to help the infant regulate arousal and affect independently are learned in the context of repeated dyadic interactions with a caregiver early in development. However, variability in caregivers’ sensitivity to cues from the infant and effectiveness at using attentional strategies to help the infant regulate early in life appear to be related to individual differences in infants’ use of attention strategies to help regulate themselves during challenging situations.
Although these findings suggest a link between caregiver behavior during dyadic interaction and infants’ use of attention control in the service of emotion regulation, almost no empirical work has examined the influence of early caregiving behavior on the child's developing attention abilities outside of an emotional or challenging context. This is despite theoretical work postulating (a) the importance of early caregiving behavior for the child's regulatory development in the first year, and (b) the importance of the child's early emerging attention abilities for subsequent emotion regulation. Thus, understanding the influence of caregiving behavior on attention processes on multiple levels of functioning may be a critical component to understanding how environmental factors influence pathways to adaptive development in infancy.
Caregiving influences on neurophysiological underpinnings of attention
Although the majority of the focus in the empirical literature has been on the ways that caregiver behavior effects behavioral manifestations of attention behaviors supporting emotion regulation, a growing body of theoretical and empirical work has suggested that caregivers may also influence children's functioning at a biological level (Calkins & Hill, Reference Calkins, Hill and Gross2007; Propper & Moore, Reference Propper and Moore2006). Because emergent attentional development and regulation strategies are thought to be partially dependent on the basic control of physiological processes (Porges, Reference Porges2003) and neurological organization (Rothbart et al., Reference Rothbart, Sheese and Posner2007), caregiver behavior that supports each of these early in development should lead to children who are more successful at controlling attention, emotion, and behavior (Calkins et al., Reference Calkins, Graziano, Berdan, Keane and Degnan2008).
Most work examining the effects of caregiving behavior on children's physiological functioning has focused on autonomic measures of cardiac vagal regulation in the context of emotional challenge. In general, this work has found that mothers who are sensitive and engage in more responsive parenting and mutual affect regulation have children with better autonomic functioning at rest and in response to a challenge, while more maternal intrusiveness and restrictive parenting is associated with less optimal patterns of autonomic functioning (Calkins et al., Reference Calkins, Smith, Gill and Johnson1998, Reference Calkins, Graziano, Berdan, Keane and Degnan2008; Haley & Stansbury, Reference Haley and Stansbury2003; Moore & Calkins, Reference Moore and Calkins2004). This is evidence that caregiving behaviors influence physiological functioning of the autonomic nervous system associated with regulation, but neural systems of attention in the central nervous system are also likely to be influenced by environmental input because they demonstrate such pronounced plasticity and malleability in early development (e.g., Stevens & Neville, Reference Stevens, Neville and Gazzaniga2013).
Emerging empirical work has begun to provide evidence that early relational experiences are closely related to neural development. This work is predicated on the notion that basic neural circuitry established during the first years of life lays the groundwork for later changes (e.g., Propper & Moore, Reference Propper and Moore2006) and is capable of being molded by the social environment (De Bellis, Reference De Bellis2001; Gunnar, Fisher, & the Early Experience, Stress, and Prevention Network, Reference Gunnar and Fisher2006; Nelson, Reference Nelson, Shonkoff and Meisels2000; Propper & Moore, Reference Propper and Moore2006). Work on neuroplasticity has demonstrated that longer developmental trajectories are associated with more malleability in a neural system as a result of the prolonged period of time in which they are susceptible to environmental input (Stevens & Neville, Reference Stevens, Neville and Gazzaniga2013). Social experience is thought to be especially salient in the first 2 years of life when a spurt in brain growth characterized by an overproduction of synapses occurs (Nelson, Thomas, & de Haan, Reference Nelson, Thomas, de Haan, Kuhn, Siegler, Damon and Lerner2006). 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, Reference Greenough, Black, Gunnar and Nelson1992; Nelson & Bloom, Reference Nelson and Bloom1997; Singer, Reference Singer1995). Thus, a caregivers’ ability to facilitate regulated experiences using attention early in development may have long-term effects on the structure and function of neural systems for attention. Caregivers create environments for the infant in which adaptive, or maladaptive, neurological organization is facilitated through the activation of specific brain areas that can have the direct effect of creating and/or strengthening synaptic connections between these areas (Black & Greenough, Reference Black and Greenough1986; Cicchetti & Lynch, Reference Cicchetti, Lynch, Cicchetti and Cohen1995). In effect, this may be how the caregiving environment directly influences the hardwiring of the neural networks for attention in development.
Some support for this hypothesis has been found in animal research and studies of impoverished and abnormal social environments characterized by neglect or abuse (Chugani et al., Reference Chugani, Behan, Muzik, Juhász, Nagy and Chugani2001; Curtis & Cicchetti, Reference Curtis and Cicchetti2007; Gunnar et al., Reference Gunnar and Fisher2006; Marshall & Fox, Reference Marshall and Fox2004; McEwen, Reference McEwen1999; Rutter & O'Connor, Reference Rutter and O'Connor2004). These studies have shown repeatedly that poor environmental experiences are related to abnormal structural (e.g., De Bellis, Reference De Bellis2001) and functional (e.g., Rutter & O'Connor, Reference Rutter and O'Connor2004) brain development. Evidence from animal models shows that caregiving affects infant's biological and behavioral systems of regulation through the environment the caregiver provides, rather than through inherited traits. For example, Meaney and colleagues found that high levels of certain maternal caregiving behaviors in rodents affected the neurological systems associated with stress responses that have long-term influence on stress-related illness, physiological, and cognitive functioning in their offspring (Champagne & Meaney, Reference Champagne and Meaney2001; Francis, Caldji, Champagne, Plotsky, & Meaney, Reference Francis, Caldji, Champagne, Plotsky and Meaney1999). These maternal behaviors were important in the nursing “foster” mother, rather than a biological mother, indicating early caregiving experience, rather than biology, as the critical factor affecting neural development and later functioning (Champagne & Meaney, Reference Champagne and Meaney2001). Similarly, in a sample of human infants, Hane and Fox (Reference Hane and Fox2006) found that variation in quality of parenting among mother–infant dyads was related to different patterns of frontal brain activity as measured by infants’ EEG asymmetry. Thus, the early social environment can have a direct effect on the experience-dependent maturation and organization of neural systems that may function to promote adaptive or maladaptive outcomes.
Caregiver influences on the neural underpinnings of attentional control have not been well examined. Nevertheless, in the same way that a history of dyadic interactions with a caregiver who effectively uses attention-based distraction techniques to regulate the infant may lead to the infant learning how to modulate his or her own behavior, repeated experience in these dyadic interactions may also be strengthening connections and patterns of responding at the neural level. Posner and Rothbart (Reference Posner and Rothbart2000) contend that attention has the effect of boosting activity in brain areas involved in processing information in the environment (e.g., language areas in the case of word stimuli). Thus, one way that caregiver–infant interactions may train the infant in the control of distress is by creating situations in which the infant's attention is focused (or redirected) away from a negative or distress-inducing stimulus, as a result activating neural connections in the brain that are associated with attention, engagement, and positivity, for example, rather than with negativity or stress. Activation of these brain areas then has the effect of strengthening and shaping the connections between the prefrontal and midfrontal areas that have been shown to underlie attentional control and the ability to manage emotional arousal to produce regulated behavior later in development. Contrast this with a caregiver who is not able to effectively redirect an infant from a distressing or negativity inducing situation; in this case, a different set of neural connections remains activated for an extended period while the infant continues to experience distress and likely an elevated stress response related to this experience. This process would have long-reaching consequences for the child, because challenges requiring similar effortful control of attention and behavior arise later in toddlerhood and early childhood, and the neurological system for regulating brain areas involved in these processes has been “primed” by these early experiences. Thus, depending on the child's experiences with a caregiver early in infancy, he or she may be activating a network of well-established neural connections for regulating input between brain areas necessary for dealing with these challenges, or the child may be activating a network associated with the experience of negativity and stress, which is less likely to deal effectively with these challenges and likely to instead elicit maladaptive behavior.
Although no work that we are aware of has tested these ideas specifically, there is evidence that experience with an adult can have a direct influence on brain activity associated with attention processes in development. Striano, Reid, and Hoehl (Reference Striano, Reid and Hoehl2006) examined the effect of engagement in joint attention with an adult on the attentional Nc component of the ERP in 9-month-old infants. Their results indicated that the Nc displayed a larger peak amplitude (indicating greater allocation of “neural attention”) in response to viewing an object when infants viewed the object following interactive joint attention with an adult relative to a non-joint-attention interaction. Although not directly testing the ideas we are suggesting here, this result provides some early support for the idea that interaction with an adult can have an effect on activation of attention systems at the neural level. In addition, the direction of this effect suggests that joint attentional engagement between an infant and an adult, like that which occurs in sensitive and responsive caregiving, results in an increase in activity of areas of the brain that have been shown to underlie executive attention in development. This is promising evidence 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 attentional control.
Translational Implications
Longitudinal work examining developmental processes across multiple developmental domains and at multiple levels of child functioning can provide much-needed information about the etiology of developmental psychopathology, thereby providing targets and early points of entry for translational and intervention work designed to alter trajectories of maladjustment. The development of attentional control is an important focus of work like this, because it has been shown to be foundational to functioning in a variety of domains and linked with multiple pathological disorders, including attention-deficit/hyperactivity disorder, anxiety, and depression (Casey et al., Reference Casey, Castellanos, Giedd and Marsh1997; Swanson et al., Reference Swanson, Posner, Potkin, Bonforte, Youpa and Cantwell1991). Throughout this paper, we underscore that the development of attention and underlying neural networks show a high degree of plasticity, making attentional control a good candidate for successful intervention. Recent intervention work designed to target other aspects of functioning has been shown to be effective in changing the neural mechanisms of selective attention in typically developing preschool and early school-aged children, as well as in children with learning problems and children who are at risk for reading impairments (Stevens, Coch, Sanders, & Neville, Reference Stevens, Coch, Sanders and Neville2008; Stevens et al., Reference Stevens, Harn, Chard, Currin, Parisi and Neville2013; Yamada, Stevens, Harn, Chard, & Neville, Reference Yamada, Stevens, Harn, Chard and Neville2011). In all cases, increases in effects of attention on neural processing were associated with behavioral changes in other domains, highlighting the importance of attention in overall development and suggesting that interventions targeting attention and underlying neural networks could have far-reaching implications for behavior and adaptive functioning.
Perhaps as a result of the broad influence of attention on adjustment in a variety of developmental domains, attention training has recently been implicated in curricula for preschool and school-age children. Thus, researchers have been able to demonstrate that attentional training is associated with improvements in behavioral and neurophysiological indices of attention, as well as with measures of academic outcomes and nonverbal intelligence (Bodrova & Leong, Reference Bodrova and Leong2007; Chenault, Thomson, Abbott, & Berninger, Reference Chenault, Thomson, Abbott and Berninger2006; Diamond, Barnett, Thomas, & Munro, Reference Diamond, Barnett, Thomas and Munro2007; Rueda, Rothbart, et al., Reference Rueda, Rothbart, McCandliss, Saccomanno and Posner2005). Most central to our focus here is evidence from a family-based training program designed to improve brain systems for selective attention in preschool children (Neville et al., Reference Neville, Stevens, Pakulak, Bell, Fanning and Klein2013). In an evaluation study of this program low socioeconomic status preschoolers were randomly assigned to the training group, which combined training sessions for caregivers as well as attention training for children, or one of two control groups (Neville et al., Reference Neville, Stevens, Pakulak, Bell, Fanning and Klein2013). Results indicated that electrophysiological measures of children's brain functions (ERPs) supporting selective attention, standardized measures of cognition, and parent-reported child behaviors all favored children in the treatment group relative to both control groups. In addition, the most favorable outcomes were observed in more parent-focused (as opposed to child-focused) training models. This study further highlights the plasticity of neural networks underlying attention and provides evidence that interventions targeting child attention, as well as caregiver behaviors that support children's attentional capabilities, can influence neural mechanisms of attentional control. Results of this work also support the idea that caregiving behavior has a direct effect on the development of neural systems underlying attention. Thus, caregiver behavior that supports the early development of attentional control in infancy may be an important target of applied work and future interventions designed to support and promote adaptive child functioning across a variety of emotional, social, cognitive, and academic domains.
Conclusions
Understanding the early development of attention is critical for understanding pathways to adaptive child functioning in a variety of domains, including emotion regulation and early developing problem behaviors (Bell & Calkins, Reference Bell, Calkins and Posner2012; Calkins, Reference Calkins, Brownell and Kopp2008; Calkins et al., Reference Calkins, Graziano, Berdan, Keane and Degnan2008). We have focused on the development of attention during early infancy and illustrated that shifts in attention skills across the first 12 months of life are fundamental to shifts in emotion regulation that are also observed during this period. Given these early links, we along with others (e.g., Bell & Calkins, Reference Bell, Calkins and Posner2012; Fox & Calkins, Reference Fox and Calkins2003; Posner & Rothbart, Reference Posner, Rothbart and Richards1998; Rothbart et al., Reference Rothbart, Posner and Rosicky1994, Reference Rothbart, Sheese and Posner2007) suggest that early attentional processes may be one mechanism through which infants gain control of emotional arousal, regulate affective expression, and begin to develop more sophisticated attention-based behavioral strategies during early childhood.
As we show in the current paper, both intrinsic biological factors and extrinsic environmental factors, measured at multiple levels of child functioning and in the context of one another, are influential to the emergence of attentional control (Cicchetti, Reference Cicchetti1984, Reference Cicchetti1993; Cicchetti & Rogosch, Reference Cicchetti and Rogosh1996; Sroufe & Rutter, Reference Sroufe and Rutter1984). The executive attention network, specifically, seems to be a primary intrinsic neural mechanism through which attention and emotion become integrated in the first year. However, a caregiver's effectiveness at using control of attention to help infants regulate also has a direct influence on attention behaviors and may have long-term effects on the biological structure and function of the developing executive attention network (Black & Greenough, Reference Black and Greenough1986; Cichetti & Lynch, Reference Cicchetti, Lynch, Cicchetti and Cohen1995).
We have suggested that if caregiving behaviors in the first year of life influence the neuroanatomical development of the executive attention network, we should see an effect of caregiving behavior in the first year on attention-based behavior and associated neural activity. In addition, because the early development of attention abilities have been theorized to provide the foundation for later emotion regulation development, from a timing perspective, it may be that early caregiving behaviors have the most influence on the development of attention behavior and associated neural underpinnings, which then influence later emotion regulation behaviors as a result of dependence on many of the same neural areas. Thus, caregiver influence on neural activation associated with the organization of the executive attention network in development may be a mechanism through which maternal caregiving behavior influences the development of infants’ attentional control and subsequent abilities such as emotion regulation and effortful control. No work that we are aware of has empirically tested these ideas with infants, but examining these questions in longitudinal, process-oriented models of regulatory development that incorporate multiple levels of analysis, including the neural, behavioral, and environmental, will be integral to understanding both normative and nonnormative development of attention control, which may have downstream effects for functioning in areas that rely on the attention control such as emotion regulation.
