Developing Attention in Typical Children PDF

Handbook of Clinical Neurology, Vol. 173 (3rd series) Neurocognitive Development: Normative Development A. Gallagher, C. Bulteau, D. Cohen and J.L. Michaud, Editors https://doi.org/10.1016/B978-0-444-64150-2.00019-8 Copyright © 2020 Elsevier B.V. All rights reserved...

Handbook of Clinical Neurology, Vol. 173 (3rd series) Neurocognitive Development: Normative Development A. Gallagher, C. Bulteau, D. Cohen and J.L. Michaud, Editors https://doi.org/10.1016/B978-0-444-64150-2.00019-8 Copyright © 2020 Elsevier B.V. All rights reserved Chapter 18 Developing attention in typical children related to disabilities MICHAEL I. POSNER1*, MARY K. ROTHBART1, AND HABIBOLLAH GHASSEMZADEH2 1 Department of Psychology, University of Oregon, Eugene, OR, United States 2 Department of Psychiatry, Tehran University of Medical Sciences, Tehran, Iran Abstract We define attention by three basic functions. The first is obtaining and maintaining the alert state. The second is orienting overtly or covertly to sensory stimuli. The third is selection among competing responses. These three functions correspond to three separable brain networks. Control of the alert state develops in infancy but continues to change till adulthood. During childhood, the orienting network pro- vides a means of controlling affective responses, e.g., by looking away from negative events and toward positive or novel events. The executive network mediates between competing voluntary responses by resolving conflicts. Executive control improves rapidly over the first 7 years of life. Autistic spectrum disorders and attention deficit hyperactivity disorder are two disorders that have been shown to involve deficits in attention networks. We examine connections between developing attention networks and these disorders. INTRODUCTION chapter we relate the framework based on individual differences in brain networks of attention to neuro- In this chapter we examine networks of the human brain developmental disorders. in relation to child development. Advances in this field, mainly imaging the resting state (Fair et al., 2009), have allowed examination of the living human brain as it METHODS OF EXAMINING BRAIN develops prior to birth to adulthood. Among the many CHANGES networks that have been studied is the development of We begin this chapter with a review of the methods for attention networks, which are particularly important examining brain changes during development. These for an understanding of developmental disabilities. We include studies of the brains of infants and children that concentrate on the development of brain areas that carry were examined after death and newer methods for out three functions of attention: (1) obtaining and main- studying developmental change using brain imaging. taining the alert state (alerting); (2) orienting to sensory events (orienting); and (3) resolving conflict among Anatomy competing responses (executive). We examine efforts to measure individual differences in attention and The human brain roughly quadruples in weight between relate them to other aspects of the child’s temperament birth and age 6, by 6 reaching 90% of its adult volume and behavior. Although there is much we do not know (Brown and Jernigan, 2012). From 1939 until the late about typical brain development, what we do know 1960s, Conel (1939–1967) examined infant and child provides a useful framework for thinking about neuro- brains from autopsies. Over the decades, he was able developmental disorders. In the final section of our to examine under a microscope changes in number of *Correspondence to: Michael I. Posner, Department of Psychology, 1227 University of Oregon, Eugene, OR 97403, United States. Tel: +1-541-346-4939, E-mail: [email protected] 216 M.I. POSNER ET AL. synapses, their density, and the increased complexity of While task-related fMRI can trace changes during dendritic trees. In all areas of the cortex, he found that development, the ages that could be studied have been synaptic density increased after birth and then declined, limited by the inability of very young children to carry reaching adult levels first in the primary sensory cortex out task instructions. By examining brain activity at rest, and much later in frontal areas (Huttenlocher and it is now possible to trace changes in brain connectivity in Dabholkar, 1997). attention networks that are present during early develop- ment and even in utero. Structural images Structural findings using magnetic resonance imaging Resting-state imaging (MRI) provide further support for the increase and then decrease in neurons (gray matter) in some brain areas The discovery that many brain networks first shown to with age, as measured by both cortical thickness and sur- be active during tasks also show correlated brain activ- face area (Wierenga et al., 2014). The largest changes in ity even when the person is at rest (Raichle, 2009) brain size are due to increases in myelinated fibers (white allowed the use of graph theory (Fair et al., 2009) to matter), which increase linearly from infancy to adult- map the early development of network activity (Gao hood (Zilles, 2005). The axons of these long projections et al., 2009). Resting-state methods can be applied to are myelinated earlier than those connecting the two the fetus (Thomason et al., 2015) or at any age after birth hemispheres, while myelin in the association areas takes because they do not require the use of a task. Both the the longest time to develop and shows the largest individ- orienting and executive attention networks are known ual differences during development (see Brown and to be active during rest (Dosenbach et al., 2007; Fair Jernigan (2012) for additional information on structural et al., 2009). changes in development). The frontal and parietal nodes of the orienting net- These structural findings point to the importance of work (described later in this chapter) are active and con- connectivity between neural areas during development. nected during infancy. The presence of frontal midline Functional imaging of adults using positron emission nodes of the executive attention network has been tomography and functional magnetic resonance imaging imaged at rest during the first months of life (Gao (fMRI) have consistently shown that most common et al., 2013), although connectivity with other brain human tasks involve a number of widely separated brain structures is sparse. A significant increase in connectivity regions, often including both the cortex and subcortical is evident by 2 years of age (Gao et al., 2009) and con- areas (Posner and Rothbart, 2007a,b). Because these sep- tinues to develop slowly across the childhood years arated brain areas must be connected when carrying out (Fair et al., 2009). During infancy and early childhood, even very simple cognitive tasks, such as shifting atten- most brain networks involve short connections between tion between areas of the visual field, the role of white adjacent brain areas, but long connections important for matter connections is critical in the efficiency and timing self-regulation develop slowly over childhood (Fair of task performance. et al., 2009; Gao et al., 2009). Although some of the resting state results may be due to movement of young Task-related functional imaging children during the scan, behavioral data also show the slow development of self-regulation through increased Early functional MRI for cognitive research involved long connections in later childhood. subtracting images of the brain obtained during an ex- The ability to resolve conflict, which is critical for perimental task from those obtained in a closely related self-regulation and for maintaining coherent goal- control task. While MRI provides evidence on the brain directed behavior, involves the executive attention net- areas involved in a task, methods such as electrical work. This network develops over the first 7 years of life encephalography (EEG) and magnetic encephalography (Rueda et al., 2004; Fjell et al., 2012). In the next section (MEG) can indicate when and in what order these brain we describe in more detail the role of the attention areas are activated (Posner et al., 2006). Functional imag- networks. ing based on correlations of MRI activation across brain areas helps examination of communication between these areas (Posner et al., 2006). Most tasks involve a net- BRAIN NETWORKS OF ATTENTION work of brain areas that must be orchestrated during per- Alerting formance. In many tasks, young children activate more brain areas during a task and often show more extensive The alert state involves the activity in the locus coeru- activation within each area than young adults (Brown leus of the brain stem, the source of the brain’s nor- and Jernigan, 2012). epinephrine (NE). This system activates frontal and  DEVELOPING ATTENTION IN TYPICAL CHILDREN 217 parietal lobes but has little direct input into the more gained considerable control in the ability to disengage ventral areas of the visual system. The early life of their gaze from one visual location and move it to the infant is very much concerned with states of alert- another, and greater orienting skill in the laboratory is ness. The newborn infant spends nearly three quarters associated with lower temperamental negative emotion- of the time sleeping (Colombo and Horowitz, 1987), ality and greater soothability as reported by parents and many of the changes in the alert state depend upon (Johnson et al., 1991). external input (e.g., rocking or walking with the infant). One of the features of attention in the first year of life There is a dramatic change in the percentage of the is the ability to sustain attention on a target. Ruff and infant’s time awake by the twelfth postnatal week. Rothbart (2001) indicate this as a general expression of Infants then can maintain the alert state during much temperament, and this type of attention is related to other of the daytime hours although this ability still depends cognitive abilities such as object exploration, language heavily upon external stimulation. development, and problem solving. An important factor In adult studies, the preparation for responding in the growth of sustained attention is the contribution obtained from warning cues (phasic alertness) can be caregivers make to the initiation and sustaining attention. measured by comparing the speed and accuracy of It has been shown that the duration of an infant’s atten- response to targets with and without warning signals tion to an object is related to the caregivers’ shared visual (Posner, 2008). Presentation of warning cues prior to attention and interest in that object (Mundy and targets allows the person to get ready to respond by Newell, 2007). increasing their state of alertness. The warning signal The main growth of sustained attention occurs from 5 interrupts the resting state and increases the alert state. to 9 years and after that a plateau is seen from 9 to 12 years One way to examine brain changes following a warning with only minor improvements (Betts et al., 2006, p. is by registering patterns of brain-generated electrical 217). Any deficit in sustained attention may cause learn- activation (i.e., EEG) while warning cues are processed. ing problems in the school years, because the child is Typically, after the appearance of a cue predicting the expected to concentrate on the relevant part of the envi- upcoming occurrence of a target, there is a negative var- ronment and select the most important part of it (Betts iation of brain activity that is sustained up until the target et al., 2006). appears (Walter, 1964). This electrophysiologic index is Resting-state brain imaging data have indicated that called the contingent negative variation (CNV). The the orienting network described in this section shows CNV and other slow waves have been related to changes greater connectivity with output systems during infancy from the resting state to the attentive state, identified than do brain areas associated with the executive atten- using fMRI (Raichle, 2009). Deficits in the alerting net- tion network described in the next section (Gao et al., work have been identified as one origin of attention 2009). Connections also change over the life span. deficit hyperactivity disorder (ADHD) (Halperin and Between infancy and childhood, a transition occurs in Schultz, 2006), and these deficits have been associated the attention networks involved in control. At 7 months, with the abnormal activities in frontal and parietal control, including the regulation of distress (Rothbart, regions related to attention control processes (Cao 2011), mainly involves the orienting network, but by et al., 2008). 4 years, the executive network becomes dominant in self-regulation. We do not believe that control through orienting ends with the preschool transition. Adults con- Orienting tinue to show control from orienting, looking away from Orienting to sensory information involves a brain net- disturbing or highly arousing events (Rothbart and work that includes the dorsal and ventral parietal lobe, Sheese, 2007). However, the growing influence of exec- frontal eye fields, and subcortical areas, including the utive control allows the person’s internally controlled pulvinar and superior colliculus (Corbetta and goals to become increasingly dominant. Shulman, 2002; Petersen and Posner, 2012). While Infants show mostly local connections, and children orienting is most often studied using visual events, aged nine also show many shorter connections than do the source of orienting seems to involve the same brain adults. Adults show more segregation of the orienting network irrespective of sensory modality. However, the and executive attention networks and longer connections specific sensory system at which attention influences (Dosenbach et al., 2007; Fair et al., 2007, 2008). While input depends upon the input modality (e.g., the visual there is evidence that younger participants move more system for a visual cue). during scans and this could reduce the ability to image For newborns, control of orienting is initially influ- long connections (Power et al., 2012), in our view, it enced by both the sensory input and the caregiver seems unlikely that this problem will change the (Haith, 1980). By 4 months, however, infants have conclusions discussed earlier. 218 M.I. POSNER ET AL. Executive attention incongruent flanking stimuli (pointing in the opposite direction as the target). The participants needed to In adults, the executive attention network involves the resolve conflict between the target and flankers in the anterior cingulate gyrus, the anterior insula, and underly- incongruent condition, and the ability to resolve such a ing striatum (similar to the cingulo-opercular network in conflict is a measure of the efficiency of executive fMRI studies; Petersen and Posner, 2012). The anterior attention. cingulate and insula have a unique projection cell. This Up until 7 years of age, the size of the right anterior cell, called the Von Economo neuron (Allman et al., cingulate was the best predictor of children’s ability to 2005), is thought to be important in communication resolve conflict, as measured by reaction time (RT) dif- between the cingulate and other brain areas. This neuron ferences between congruent and incongruent flankers. is not present in macaque monkeys and expands greatly After the age of 7, overall RT was most related to the in frequency between great apes and humans. efficiency of white matter connections. This study sup- It is difficult to assess executive attention in infants ports the anatomical results described previously in because they do not follow task instructions, and care- illustrating the importance of white matter connectivity givers provide much of the regulation of infant behavior. between the anterior cingulate and other brain areas as Effortful control (EC) is a high temperament factor a key component of self-regulation. derived from parent reports on children’s behavior The development of executive attention has also been (Rothbart and Rueda, 2005). EC is defined as the ability traced into the primary school period (Rueda et al., 2004) to withhold a dominant response to carry out a nondomi- using RT to incongruent flankers–congruent flankers to nant one. In temperament questionnaires, parents are measure children’s ability to resolve conflict. Overall, asked about their children’s specific behavior within children’s RTs were much longer than adults’, but con- the last 2 weeks (e.g., in putting away toys after play). siderable development in the speed of resolving conflict Parents readily respond to such questions, and their was observed from 4 to about 7 years of age. The ability answers to many questions can be aggregated to form to resolve conflict on the flanker task, as measured by a factor called EC. EC can be measured in children increases in RT, and errors with incongruent, compared 2 years of age and older, although aspects of orienting to congruent flankers, remained about the same from and emotion can be measured from early infancy age 7 to adulthood. When the difficulty of the conflict (Rothbart, 2011). During infancy, temperament scales task is increased by other demands, however, such as include orienting, fear, anger, soothability, and positive switching between rules, mapping the input information affect (Rothbart, 2011). Children above age 3–4 years to the response, or holding more information in working can perform tasks that involve voluntary responding such memory, continued development of conflict resolution is as pressing keys to visual input. In multiple studies, found beyond age 7 (Davidson et al., 2006). higher EC in questionnaire measures is positively corre- lated with more efficient performance in resolving con- flict in laboratory tasks (executive attention) (Rothbart INDIVIDUAL DIFFERENCES and Rueda, 2005). Network scores Infants orient longer when a display is an error (Wynn, 1992), and this behavior at 7 months was asso- Although the brain networks of attention are common to ciated with activity in a set of EEG electrodes at the everyone, they do not operate with equal efficiency. Two frontal midline that localize to the anterior cingulate, quite different methods are used to examine individual an important node of the executive network (Berger differences in these networks. The first involves measur- et al., 2006). However, the typical regulation of behav- ing the efficiency of each network within a single cogni- ior found in adults, that is, to slow down following an tive task most often requiring a speeded response. The error, seemed not to emerge until about age 3 years Attention Network Task (ANT) (Fan et al., 2002) uses (Jones et al., 2003). This fits with the findings in resting the flanker task (Eriksen and Eriksen, 1974) and provides state studies that the executive network is poorly cues to the time or location of the target. Subtractions of connected to other brain areas during infancy but that RTs allow a measure for each network. This task can be this connectivity increases during childhood (Gao used in various versions with children of 4 years and et al., 2013). older as well as with adults of any age. The scores, repre- An important developmental fMRI study (Fjell et al., senting the efficiency of each network, are mainly inde- 2012) involved 750 participants from 4 to 21 years of pendent (Fan et al., 2002), although there are significant age. A conflict task was used in which a visual arrow correlations under some conditions, e.g., when the tasks target is surrounded by either congruent flanking stimuli are made more difficult (Fan et al., 2009). Moreover, as (pointing in the same direction as the target) or discussed earlier the flanker task used in the ANT has  DEVELOPING ATTENTION IN TYPICAL CHILDREN 219 been shown to depend upon the size of the anterior Genes and development cingulate cortex (ACC) during early childhood (Fjell If particular attention networks are associated with a et al., 2012). neuromodulator, it becomes possible to test the idea that While RT difference scores are convenient and the genes related to specific modulators influence atten- represent a reasonable effort to obtain relatively pure tion in predictable ways. These studies use genes with measures of mental operations on a group basis, a recent frequent polymorphisms, and have found that genes review criticized the reliability of RT difference scores related to NE affect alerting but not orienting as mea- for studying individual differences (Draheim et al., sured by the ANT, while those genes related to the 2019). Nonetheless, there are significant correlations cholinergic system influence orienting but not alerting between network scores and a second method of mea- (Fan et al., 2003; Green et al., 2008; Posner et al., suring individual differences in attention through the 2014). It has also been shown that dopamine and sero- use of parent-report questionnaires of infant and child tonin have effects on time to resolve conflict (Posner temperament (Rothbart, 2011). It has been found, as et al., 2014). This work provides a useful framework discussed previously, that EC from questionnaire data for determining genes related to specific attention correlates with the difference between congruent and networks. incongruent flankers in the ANT (Rothbart and Rueda, Studies of infants and children provide strong links 2005). The ability to relate a cognitive task to parent between early temperament and later attention networks. reports of their child’s EC has allowed a wide range of A longitudinal study from 7 months to 7 years (Rothbart important observations. EC has been shown to be related et al., 2011; Posner et al., 2014) found that genes related to the ability of parents to train their children in prosocial to attention were associated with positive and negative behavior (Kochanksa et al., 2000). Thus, network effi- affect (Sheese et al., 2009) early in life. Early parent ciency as measured by the ANT can be related to signif- reports of temperament were also related to later network icant behavioral differences, further supporting efforts to performance. For example, the speed at resolving con- understand the mechanisms underlying self-regulation. flict at 7 years was related to parent report of their Using a different measure of EC in early childhood, infants’ positive affect, while infant perceptual sensitiv- Moffitt et al. (2011) found that self-control predicted ity was related to later alerting, and infant approach to critical adult outcomes such as in income, health, and objects related to later orienting (Posner et al., 2014). social relations more than 30 years later. Thus, each of the networks is related to a different temperament dimension during infancy. This finding Molecular mechanisms supports the close relation between early temperamental One aspect of the ANT is measurement of orienting by characteristics of affect, sensitivity, and approach and use of cues that move attention to the location of the tar- later attention networks. Whether early temperament is get. This measure of the ANT has been widely used in only a predictor of later attentional networks or is some- animal research with rodents and primates (Marrocco how instrumental in the development of these networks and Davidson, 1998; Corbetta and Shulman, 2002; is not known. However, the gene X environment inter- Beane and Marrocco, 2004). One study using these cues actions described in the following sections suggest an found that injections of NE antagonists, such as clonidine important role for parenting in shaping network or guanfacine, to rats blocked the improvement in RT development. from alerting cues but did not alter the improvement in Part of the relation between early temperament and RT from cues that directed the rat’s attention to a partic- later attention rests on genetic variability, but substan- ular location (orienting). On the other hand, cholinergic tial evidence exists also for experience as found in gene antagonists blocked improvement from orienting cues X environment interactions. For example, impulsivity, a but had no effect on RT improvement to warning signals key factor in ADHD has been related to aspects of the (Beane and Marrocco, 2004). Other studies, mainly with quality of parenting, but only for those children with primates, have shown that orienting is carried out by a version of the dopamine 4 receptor gene, which had ventral and dorsal parts of the parietal lobe, together with 7 repeats of a particular 48 base pairs (Sheese et al., the frontal eye fields and subcortical areas (Corbetta and 2007). This finding suggests that the 7-repeat allele Shulman, 2002). Although it is well known that neuro- was needed for a correlation between parental quality modulators can influence each other and that their and the temperament trait of impulsivity. A different effects are not independent (Trofimova and Robbins, study (Bakermans-Kranenburg et al., 2008) randomly 2016), the Marrocco findings show that specific effects assigned children with the 7-repeat allele and those of individual modulators can be shown for simple task without it to a program of parental training. The components. parent training intervention was effective in reducing 220 M.I. POSNER ET AL. impulsivity but only for those children with the 7-repeat DEFICITS OF ATTENTION allele, thus indicating that the 7-repeat is critical for Our chapter is not meant to provide a review of disor- the difference in child behavior found following the ders related to attention (see disorders section of this intervention. volume and Posner et al., 2019). However, in some The importance of experience in the development of cases the normal development of brain networks related brain networks of attention in early life is enlarged by to attention provides illumination of disorders. This is the finding that the orienting network is present very true partly because each of the networks has been asso- early in development. During infancy, parents work ciated with a dominant neuromodulator as shown in to obtain control of attention through such devices as Table 18.1. In this part of the chapter we examine the presenting novel objects. These not only attract the role of different attention networks in understanding infant’s attention and serve to aid soothing (Harmon Autism and ADHD. et al., 1997) but are also likely to activate frontal areas related to the executive network, possibly aiding in executive attention development (Shulman et al., Autistic spectrum disorder (ASD) 2009). The executive networks in adults involve sepa- Autistic spectrum disorders (ASDs) have been rate areas of the anterior cingulate that provide control characterized and defined in the DSM-5 (American of emotion and cognition (Bush et al., 2000; Beckman Psychiatric Association, 2013) as neurodevelopmental et al., 2009). conditions consisting of two categories of impairments: (1) deficits in communication and social interactions and (2) restricted or repetitive patterns of behavior. Deficits of attention and attentional problems have Theory of mind (ToM) been recognized as an important factor in ASD. For Among many different cognitive abilities associated with example, deficits found in cognitive studies of autistic attention, recognition memory (Reynolds and Romano, children include a failure to orient to targets even when 2016), working memory (Fougnie, 2008), and theory nonsocial cues indicate where in space a likely target will of mind (ToM) (Shaw et al., 2017) have been studied occur (Townsend and Courchesne, 1994; Landry and extensively by different investigators. In a review paper, Bryson, 2004). A review of attention networks involved Reynolds and Romano (2016) reported a significant overlap in neural systems involved in executive attention Table 18.1 and working memory. Supporting this idea, the cortical Brain attention networks, anatomy, and dominant source of the negative central event-related potential neuromodulators component found in visual studies was localized to areas of prefrontal cortex. Significant gains on working mem- Network Modulator ory tasks overlap with key periods for development of sustained attention and the orienting and the executive Alerting Norepinephrine Beane and networks. Marrocco (2004) In a study by McGlamery et al. (2007) on the relation Locus coeruleus of attention, executive function, and ToM, kindergarten Right frontal cortex children identified by teachers as showing attention Right parietal cortex difficulties had lower scores on false belief measures Orienting Acetycholine Beane and related to the ToM as well as behavioral difficulties asso- Marrocco ciated with executive dysfunction than those identified as (2004) having fewer attentional difficulties. Superior parietal lobe In summary, the development of attention networks Temporal parietal has been traced by behavioral task performance and by junction resting state MRI. Portions of each network are present Superior colliculus in infancy and are related to individual differences in Pulvinar Executive emotion. The connection between the nodes of attention ACC Dopamine Petersen and networks develops slowly over childhood and is in- Posner fluenced by the interaction of genes and the parental (2012) environment. The development of attention networks Insula supports both self-regulation and the child’s understand- Striatum ing of other minds.  DEVELOPING ATTENTION IN TYPICAL CHILDREN 221 in autism concluded that those with ASD showed a sig- ACKNOWLEDGMENTS nificant deficit in the orienting network (Keehn et al., The research for this chapter was supported in part by 2013). Imaging studies of cued orienting showed inferior grants N00014-15-2148 and N00014-19-1-2015 from parietal hypoactivity as well as poorer performance the Office of Naval Research to the University of (Haist et al., 2005). Deficits in cerebellar and parietal Oregon. The authors appreciate the help of Pascale gray matter are also frequently reported for children with Voelker in this research. autism (Townsend and Courchesne, 1994). An early def- icit in orienting could by itself be important in commu- REFERENCES nication problems, which critically depend on social referencing. As is pointed out by Townsend et al. Allman JM, Watson KK, Tetreault NA et al. (2005). Intuition (2012), as early as 6 months of age, infants who later and autism: a possible role for von economo neurons. meet diagnostic criteria for autism exhibit abnormal Trends Cogn Sci 9: 367–373. https://doi.org/10.1016/ j.tics.2005.06.008. motor development and unusual visual attention. While American Psychiatric Association (2013). Diagnostic and sta- they have also documented deficits in the executive net- tistical manual of mental disorders, fifth edn American work in autism (Townsend et al., 2012), the early pres- Psychiatric Association, Washington, DC. ence of an orienting deficit may play an important part Beckmann M, Johansen-Berg H, Rushworth MFS (2009). in the progress and possible remediation of the deficit. Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. J Neurosci 29: 1175–1190. Attention deficit hyperactivity disorder Bakermans-Kranenburg MJ, Van IJzendoorn MH, (ADHD) Pijlman FTA et al. (2008). Experimental evidence for There is evidence that ADHD may involve a deficit in differential susceptibility: dopamine D4 receptor poly- alerting, either alone (Halperin and Schultz, 2006) or morphism (DRD4 VNTR) moderates intervention effects on toddlers’ externalizing behavior in a randomized con- in conjunction with an executive deficit (Johnson trolled trial. Dev Psychol 44: 293–300. https://doi.org/ et al., 2008). Halperin and Schultz (2006) argue that 10.1037/0012-1649.44.1.293. the ADHD disorder may arise in a deficit in subcortical Beane M, Marrocco R (2004). Cholinergic and noradrenergic modulating systems. Several studies of children with inputs to the posterior parietal cortex modulate the com- ADHD have shown deficits that appear to involve alert- ponents of exogenous attention. In: MI Posner (Ed.), ing (Halperin and Schultz, 2006), and the disorder often Cognitive neuroscience of attention. Guilford, New York, is thought to show lateralized features of right hemi- pp. 313–325. sphere damage that would fit with right hemisphere Berger A, Tzur G, Posner MI (2006). Infant babies detect arith- lateralization of tonic alerting. metic error. Proc Natl Acad Sci U S A 103: 12649–12653. Later in the disorder, executive deficits are demon- https://doi.org/10.1073/pnas/0605350103. strated. In one study using the ANT, ADHD children Betts J, Mckay J, Maruff P et al. (2006). The development of sustained attention in children: the effect of age and task showed combined alerting and executive attention defi- load. Child Neuropsychol 12: 205–221. cits (Johnson et al., 2008). The executive attention net- Brown TT, Jernigan TL (2012). Brain development during the work deficit was also found in adults who had been preschool years. Neuropsychol Rev 22: 313–333. https:// diagnosed with ADHD as children. When performing a doi.org/10.1007/s11065-012-9214-1. task requiring the resolution of conflict ADHD adults, Bush G et al. (1999). Anterior cingulate cortex dysfunction in unlike the controls, did not activate the ACC but, instead, attention deficit/hyperactivity disorder revealed by fMRI showed activation in the anterior insula (Bush et al., and the counting Stroop. Biol Psychiatry 45: 1542–1552. 1999). These two structures are strongly connected in Bush G, Luu P, Posner MI (2000). Cognitive and emotional resting state MRI studies, and both structures are unique influences in the anterior cingulate cortex. Trends Cogn in having neurons specialized for strong remote connec- Sci 4 (6): 215–222. tivity. These features may be the reason why both may Cao Q, Zang Y, Zhu C et al. (2008). Alerting deficits in children with attention deficit/hyperactivity disorder: play a role in the resolution of conflict and self-regulation. event-related fMRI evidence. Brain Res 1219: 159–168. In this chapter we have summarized some of the Colombo J, Horowitz FD (1987). Behavioral state as a lead var- advances in understanding the development of attention iable in neonatal research. Merrill-Palmer Q 33: 423–438. in the normal brain. While attention networks are Conel JL (1939–1967). The postnatal development of the common to all humans, individual differences in their human cerebral cortex vol I-VIII, Harvard University efficiency can be influenced jointly by interactions bet- Press, Cambridge, MA. ween genes and experience. Understanding of individual Corbetta M, Shulman GL (2002). Control of goal directed and differences in the development of attention networks may stimulus driven attention in the brain. Nat Rev Neurosci 3: help to further illuminate developmental disorders. 201–215. https://doi.org/10.1038/nrn755. 222 M.I. POSNER ET AL. Davidson MC, Amso D, Anderson LC et al. (2006). Haith MM (1980). Rules that babies look by: the organizaton Development cognitive control and executive functions of new born visual activity, Psychology Press, New York. from 4 to 13 years: evidence from manipulations of mem- Halperin JM, Schultz KP (2006). Revisiting the role of the ory, inhibition, and task switching. Neuropsychologia prefrontal cortex in the pathophysiology of attention defi- 44: 2037–2078. https://doi.org/10.1016/j.neuropsychologia. cit/hyperactivity disorder. Psychol Bull 132: 560–581. 2006.02.006. https://doi.org/10.1037/0033-2909.132.4.560. Dosenbach NUF, Fair DA, Miezin FM et al. (2007). Distinct Harman C, Rothbart MK, Posner MI (1997). Distress and brain networks for adaptive and stable task control in attention interactions in early infancy. Motiv Emot 21: humans. Proc Natl Acad Sci U S A 04: 1073–1978. 27–43. Draheim C, Mashburn CA, Martin JD et al. (2019). Reaction Huttenlocher PR, Dabholkar JC (1997). Regional differences time in differential and developmental research: a review in synaptogenesis in human cerebral cortex. J Comp and commentary on the problems and alternatives. Neurol 387: 167–178. Psychol Bull 145: 508–535. Johnson MH, Posner MI, Rothbart MK (1991). Components of Eriksen BA, Eriksen CW (1974). Effects of noise letters upon visual orienting in early infancy: contingency learning, the identification of a target letter in a nonsearch task. anticipatory looking and disengaging. J Cogn Neurosci 3: Percept Psychophys 16: 143–144. 335–344. https://doi.org/10.1162/jocn.1991.3.4.335. Fair DA, Dosenbach NUF, Church JA et al. (2007). Johnson KA, Robertson IH, Barry E et al. (2008). Impaired Development of distinct control networks through segrega- conflict resolution and alerting in children with ADHD: tion and integration. Proc Natl Acad Sci U S A 104: evidence from the ANT. J Child Psychol Psychiatry 49: 13507–13512. https://doi.org/10.1073/pnas.0705843104. 1339–1347. Fair D, Cohen AL, Dosenbach AUF et al. (2008). The maturing Jones LB, Rothbart MK, Posner MI (2003). Development of achitecture of the brain’s default network. Proc Natl Acad executive attention in preschool children. Dev Sci 6: Sci U S A 105: 4028–4032. https://doi.org/10.1073/ 498–504. pnas.0800376105. Keehn B, Muller RA, Townsend J (2013). Atypical attentional Fair DA, Cohen AL, Power JD et al. (2009). Functional brain networks and the emergence of autism. Neurosci Biobehav network develop from a “local to distributed” organization. Rev 37/2: 164–183. PLoS Comput Biol 5: 1–13. https://doi.org/10.1371/jour- Kochanska G, Murray KT, Harlan ET (2000). Effortful control nal.pcbi.1000381. in early childhood: continuity and change, antecedents and Fan J, McCandliss BD, Sommer T et al. (2002). Testing the implications for social development. Dev Psychol 36: efficiency and independence of attentional networks. 220–232. J Cogn Neurosci 3 (14): 340–347. Landry R, Bryson SE (2004). Impaired disengagement of Fan J, Fossella JA, Summer T et al. (2003). Mapping the attention in young children with autism. J Child Adolesc genetic variation of executive attention onto brain activity. Psychiatry 45: 1115–1122. Proc Natl Acad Sci USA 100: 7406–7411. Marrocco RT, Davidson MC (1998). Neurochemistry of atten- Fan J, Gu X, Guise KG et al. (2009). Testing the behavior inter- tion. In: R Parasuraman (Ed.), The attentive brain. MIT action and integration of attentional networks. Brain Cogn Press, Cambridge, MA, pp. 35–50. 70: 209–220. McGlamery ME, Ball SE, Henley TB et al. (2007). Theory of Fjell AM, Walhovd K, Brown T et al. (2012). Multimodal mind, attention and executive function in kindergarten imaging of the self-regulating brain. Proc Natl Acad Sci boys. Emot Behav Diffic 12: 29–47. U S A 109: 19620–19625. https://doi.org/10.1073/ Moffitt TE et al. (2011). A gradient of childhood selfcontrol pnas.1208243109. predicts health, wealth and public safety. Proc Natl Fougnie D (2008). The relationship between attention and Acad Sci USA 108: 2693–2698. https://doi.org/10.1073/ working memory. In: NB Johansen (Ed.), New research pnas.1010076108. on short-term memory. Nova Science Publishers, Inc.1–45. Mundy P, Newell L (2007). Joint attention, social cognition Gao W, Zhu H, Giovanello KS et al. (2009). Evidence on the and the anterior/posterior attention systems. Curr Dir emergence of the brain’s default network from 2-week old Psychol Sci 16 (5): 269–274. year healthy pediatric subjects. Proc Natl Acad Sci U S A Petersen SE, Posner MI (2012). The attention system of the 106: 6790–6795. human brain: 20 years after. Annu Rev Neurosci 35: Gao W, Gilmore JH, Shen D et al. (2013). The synchronization 71–89. https://doi.org/10.1146/annurev-neuro-062111- within and interaction between the default and dorsal atten- 150525. tion networks in early infancy. Cereb Cortex 23: 594–603. Posner MI (2008). Measuring alertness. Ann N Y Acad Sci https://doi.org/10.1093/cercor/bhs043. 1129: 193–199. https://doi.org/10.1196/anals.1417.011. Green AE, Munafo MR, DeYoung CG et al. (2008). Using Posner MI, Rothbart MK (2007a). Educating the human brain, genetic data in cognitive neuroscience: from growing pains American Psychological Association, Washington, DC. to genuine insights. Nat Rev Neurosci 9: 710–720. Posner MI, Rothbart MK (2007b). Research on attention net- Haist F, Adamo M, Westerfield M et al. (2005). The functional works as a model for the integration of psychological sci- neuroanatomy of spatial attention in autism spectrum dis- ence. Annu Rev Psychol 58: 1–23. https://doi.org/10.1146/ order. Dev Neuropsychol 27 (3): 425–458. annurev.psych.58.110405.085516.  DEVELOPING ATTENTION IN TYPICAL CHILDREN 223 Posner MI, Sheese B, Odludas Y et al. (2006). Analyzing and Townsend J, Keehn B, Westerfield M (2012). Abstaction of shaping neural networks of attention. Neural Netw 19: mind, attention in autism. In: MI Posner (Ed.), Cognitive 1422–1429. https://doi.org/10.1016/j.neunet.2006.08.00. neuroscience of attention, second edn Guilford, Posner MI, Rothbart MK, Sheese BE et al. (2014). Developing New York, pp. 357–373, Ch. 25. attention: behavioral and brain mechanisms. Adv Neurosci Trofimova I, Robbins TW (2016). Temperament and Article ID 405094. arousal systems: a new synthesis of differential psycho- Posner MI, Rothbart MK, Ghassemzadeh H (2019). Restoring logy and functional nueorchemistry. Neurosci Biobehav attention networks. Yale J Biol Med 92/1: 139–143. Rev 64: 382–402. https://doi.org/10.1016/j.neubiorev.2016 Power JD, Barnes KA, Snyder AZ et al. (2012). Spurious but sys-.03.008. tematic correlations in functional connectivity MRI networks Walter G (1964). The convergence and interaction of visual, arise from subject motion. Neuroimage 59: 2142–2154. auditory and tactile stimuli in human non-specfic cortex. https://doi.org/10.1016/j.neuroimage.2011.10.018. Ann N Y Acad Sci 112: 320–361. Raichle ME (2009). A paradigm shift in functional brain imag- Wierenga L, Langen M, Ambrosino S et al. (2014). Typical ing. J Neurosci 29: 127–134. https://doi.org/10.1016/ development of basal ganglia, hippocampus, amygdala j.neuroimage.2011.10.018. and cerebellum from age 7 to 24. Neuroimage 96: 67–72. Reynolds GD, Romano AC (2016). The development of Wynn K (1992). Addition and subtraction by human infants. attention systems and working memory in infancy. Nature 358: 749–750. https://doi.org/10.1038/358749a0. Front Syst Neurosci 10: 15. https://doi.org/10.3389/fnsys. Zilles K (2005). Evolution of the human brain and compara- 2016.00015. tive cyto- and receptor architecture. In: S Dehaene, Rothbart MK (2011). Becoming who we are: temperament and J-R Duhamel, MD Hauser, G Rizzolatti (Eds.), From mon- personality in development, Guilford Press, New York. key brain to human brain. MIT Press, Bradford Books, Rothbart MK, Rueda MR (2005). The development of Cambridge, MA, pp. 41–56. effortful control. In: U Mayr, E Awh, SW Keele (Eds.), Developing individuality in the human brain: a tribute to FURTHER READING Michael I. Posner. American Psychological Association, Washington, DC, pp. 167–188. Craig F, Margari F, Legrottaglie AR et al. (2016). A review of Rothbart MK, Sheese BE (2007). Temperament and emotion executive function deficits in autism spectrum disorder and regulation. In: JJ Gross (Ed.), Handbook of emotion regu- attention-deficit/hyperactivity disorder. Neuropsychiatr lation. Guilford Press, New York, pp. 331–350. Dis Treat 12: 1191–1202. Rothbart MK, Sheese BE, Rueda MR et al. (2011). Goriounova NA, Heyer DB, Wilbers R et al. (2018). Large and Developing mechanisms of self-regulation in early life. fast human pyramidal neurons associate with intelligence. Emot Rev 3 (2): 207–213. eLife 7: e41714. Rueda MR, Fan J, Halparin J et al. (2004). Development of atten- Hernandez-Andrade E, Yeo LM, Mody S et al. (2015). tion during childhood. Neuropsychologia 42: 1029–1040. Age-related increases in long-range connectivity in fetal Ruff H, Rothbart M (2001). Attention in early development: functional neural connectivity networks in utero. Dev themes and variations, Oxford University Press, New York. Cogn Neurosci 11: 96–104. Shaw JA, Bryant LK, Malle BF et al. (2017). The relationship Hogeveen J, Krug MK, Elliott MV et al. (2018). Proactive con- between the joint attention and theory of mind in neuro- trol as a double-edged sword in autism spectrum disorder. typical adults. Conscious Cogn 51: 268–278. J Abnorm Psychol 127: 429–435. Sheese BE, Voelker PM, Rothbart MK et al. (2007) Parenting Lynch G, Gall CM (2013). Mechanism based approach quality interacts with genetic variation in Dopamine for rescuing and enhancing cognition. Front Neurosci Receptor DRD4 to influence temperament in early child- 7: 143. hood. Dev Psychopathol 19: 1039–1046 Piscopo D, Weible A, Rothbart MK et al. (2018). Changes Sheese BE, Voelker P, Posner MI et al. (2009). Genetic in white matter in mice resulting from low frequency variation influences on the early development of reac- brain stimulation. Proc Natl Acad Sci U S A 115: tive emotions and their regulation by attention. Cogn 6639–6646. Neuropsychiatry 14 (4): 332–355. Poole D, Gowen E, Warren PA et al. (2018). Visual-tactile selec- Shulman GL, Astafiev SV, Franke D et al. (2009). Interaction tive attention in autism spectrum condition: an increased of stimulus-driven reorienting and expectation in ventral influence of visual distractors. J Exp Psychol Gen 147: and dorsal frontoparietal and basal ganglia-cortical net- 1309–1324. https://doi.org/10.1037/xge0000425. works. J Neurosci 29: 4392–4407. Posner MI (2020). General intelligence in the age of neuroim- Thomason ME, Grove LE, Lozon TA et al. (2015). Age-related aging. Trends Neurosci Educ 18: 10026. increases in long-range connectivity in fetal functional Posner MI, Rothbart MK (2018). Temperament and brain net- neural connectivity networks in utero. Dev Cogn works of attention. Philos T R Soc B 373: 20170254. Neurosci 11: 96–104. https://doi.org/10.1098/rstb.2017.0254. Townsend J, Courchesne E (1994). Parietal damage and the Voelker P, Rothbart MK, Posner MI (2016). A polymorphism narrow spotlight of spatial attention. J Cogn Neurosci 6: related to methylationinfluences attention during perfor- 220–232. mance of speeded skills. AIMS Neurosci 3: 40–55.