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11 Paying Attention to a Field in CrisisPsychiatry, Neuroscience, and FunctionalSystems of the Brain

Amir Raz and Ethan Macdonald

Introduction

A few short weeks before the long-awaited publication of DSM-5,Thomas Insel, director of the National Institute of Mental Health(NIMH), stated that the manual suffers from a “lack of validity” (Insel,2013). To remedy this problem, he envisaged a new direction for psych-iatry whereby clinicians and researchers classify disorders based on under-lying neurobiological causes rather than on highly variable symptoms.

The anticipation of DSM-5 and professional efforts surrounding itgenerated unprecedented questioning from both consumers and practi-tioners. The public, advocacy groups, and even senior members of thepsychiatric community raised questions, not only regarding decisions toinclude or exclude specific types of problems from the revised manualbut also concerning the scientific foundation of the whole enterprise.Many of these criticisms were based on recognizing the limited advancesthat have been made in the biological understanding and treatment ofmental disorders.

Psychiatry aims to link behavioral science to underlying mechanisms,using the techniques of neuroscience. Yet decades of work on cognitive,molecular, and systems neuroscience have taught most scientists a lessonin humility: despite an enormous investment in research with anemphasis on the neural correlates of typical and atypical behavioral“phenotypes,” breakthroughs are sorely lacking. In spite of the globalefforts and the accumulation of a large body of findings, the lack ofclinical advances has undermined many working assumptions concern-ing the neurobiological basis of psychiatric distress.

The genetic and neuroimaging revolutions – which seemed poised toelucidate and ultimately explain conditions categorized as psycho-pathologies and psychiatric disorders – have produced modest resultsthat speak only obliquely to the vast, complex dynamics revealed bybehavioral science. Many scholars are disillusioned with imaging stud-ies of the living human brain, and further recognize that genetic

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polymorphisms putatively appearing to increase risk of schizophreniain one person may actually predispose another to bipolar disorder(Bilder, 2011). Furthermore, some scientists argue that the therapeuticeffects of drugs that comprise the backbone of modern psychiatry –

antidepressants and atypical antipsychotics – are largely indistinguish-able from placebos in common clinical situations (Raz & Harris, inpress). These findings challenge the extent to which the study ofpharmaceutical drugs contributes to our understanding of psycho-logical conditions.

Neuroscience and biology have given us neither the hoped for refine-ment of diagnostic criteria nor the sensitivity and specificity requiredfor effective clinical practice. Psychiatry needs an entirely new approachthat would allow us to understand – in a tangible way – the diversityof experience in illness and in health. Whereas older models of theDSM represented psychiatric illnesses as categories discontinuouswith “normal” functioning, the NIMH strategy with respect to theResearch Domain Criteria (RDoC) project emphasizes the potentialcontinuity of psychopathology with normal functioning. For example,RDoC recognizes “attention” as a construct under the “cognitivesystems” domain in the belief that examining its underlying mechan-isms may account for both everyday behavior and related pathologies,such as ADHD.

Recent neuroimaging studies have clarified some of the neuroanatom-ical pathways involved in attention networks. Appreciating the challengescognitive neuroscience faces, as well as the limitations of current tech-niques, is important in assessing the strength of particular neuroscientificfindings and their implications for psychiatry and psychology. Criticshave censured cognitive neuroscience for interpreting neuroimagingresults in naïve ways that amount to a “new phrenology” (Uttal, 2001).These criticisms are justified in many areas of research, where reverseinferences and unsupported assumptions run rampant, as well as in someunscrupulous clinical applications, but they do not invalidate the field asa whole (Raz, 2012). But imaging the living brain and drawing conclu-sions from the enormous amount of data collected poses both technicaland conceptual challenges.

In that spirit, our chapter sketches a new model for psychiatry thatdraws on recent work in the cognitive neuroscience of attention. Weprovide a detailed example of how operationalizing psychological andmental terms – in this case, “attention” – as a functional “organ system”

(Posner & Fan, 2008) opens avenues to the integration of biobehavioralscience and clinical psychiatry and allows us to transcend the old clinicaldichotomy of functional and organic (Raz & Wolfson, 2010).

274 Amir Raz and Ethan Macdonald


Why Should Psychiatrists Pay Attention to the ScientificStudy of Attention?

Attention is a central theme in cognitive science, linking brain withbehavior and advancing psychology with the techniques of neuroscience.Although experimental psychology has probably examined the topic ofattention more than any other field (Raz & Buhle, 2006), the cognitiveneuroscience of attention involves a larger social context that extends farbeyond laboratory experiments, with innovative applications to mentalhealth, education, human performance, and many other domains(Posner, 2012a). By understanding attention in terms of the orchestra-tion of several separate control networks, we can consolidate behavioral,imaging, and genetic findings into a coherent whole. Moreover, we canelucidate individual differences in attention and outline the roles of earlyexperience, upbringing, and environment in the development of atten-tion networks. The scientific study of attention, therefore, provides crit-ical insights into an alternative model that can help reorient psychiatry.

In the following sections, we show how viewing attention as a func-tional organ system – with its own anatomy, circuitry, and cellularstructure – aids in our conceptualization of many psychopathologies.Moreover, we will argue that the pathologies of attention comprise asizeable domain within the field of psychiatry and provide a way to groupproblems that transcends traditional diagnostic categories. Thisapproach builds on our knowledge of the evolutionary and developmen-tal bases of a principle brain mechanism of voluntary control, and thuspaves the way to a better understanding of how genetics and culturetogether shape control systems. By studying the unique neurobiologicaland functional characteristics of brain networks, researchers can system-atically search for genetic variations (e.g., polymorphisms) associatedwith differences in the regulation of cognition, emotion, thought,and action. Identifying this kind of variation can shed considerable lighton both typical and atypical behaviors and provide critical insights topsychiatry.

The mapping of the human genome offers the potential to increaseunderstanding of how biology and environment interact to produceindividual differences in temperament and other dimensions of humanbehavior and functioning. Many genes exhibit variations that code fordifferent phenotypes, which, in turn, can alter the efficiency of specificattention networks. The dopamine 4 receptor gene (DRD4), forexample, has several versions that differ in having two, four, or sevenrepeats of a portion of the gene, and these variations may correlate withthe temperamental trait of sensation-seeking – the tendency to seek out

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novel, varied, and intense sensory experiences (LaHoste et al., 1996).These genetic variations interact with specific aspects of the social envir-onment. Thus, in the presence of the seven-repeat DRD4 variant,parenting has a significant effect on an array of temperamental dimen-sions that correspond to some of the symptoms found in childrendiagnosed with ADHD (Sheese, Voelker, Rothbart, & Posner, 2007).Children with the seven-repeat allele who had a lower quality ofparenting had unusually high levels of sensation-seeking, includingimpulsivity. By identifying children who are more susceptible to environ-mental factors, we can determine which children will benefit most fromtherapies that aim to improve attention. Hence, genetic variation pro-vides a tool for refining our understanding of environmental influences.

A systematic account of the biological substrates of attention and theirrelation to social processes can clarify the impact that genetic variationhas on each network. For example, experimental studies examiningspatial orienting suggest that anxious people orient toward negative andpositive targets in a similar manner, but highly anxious individuals havetrouble disengaging from the negative target when the cue is invalid(Posner, Walker, Friedrich, & Rafal, 1984). These findings complementdata from recent studies showing an inverse correlation between negativeaffect and effortful control (e.g., Rothbart, 2011). Overall, this researchsuggests that clinicians may use attention training as a strategy to bolsterexecutive attention and help patients disengage from negative ideation.

The three-network model of attention systems described in this chap-ter provides researchers and practitioners with tools to examine clinicalinterventions, rehabilitation programs, educational methods, and evenparenting styles. By construing attention as a functional organ system, wefocus on its functional connectivity, neuroanatomy, network dynamics,cellular structure, and electrochemical mechanisms. This multilevel inte-grative view shows the way toward interdisciplinary work unifying thesocial world, life experiences, biological processes, and computationalsciences.

Although attention networks occupy a central place in psychologicaland cognitive science, they have had relatively limited application inmental health theory and practice. Looking into the past and projectinginto the future, attention research may be expected to have a much widerimpact. Half a century ago, researchers largely focused on demonstratingthat attention changes specific operations in the information-processinghierarchy – from input all the way to behavioral outcome. However, sincethe 1990s, neuroimaging has increasingly elucidated the focal brain areasthat subserve attention networks. Investigators now study the brainregions within these networks that operationalize the computations



performed by attention and monitor their patterns and rhythmicactivations in real time. Present since early childhood, attention networksevolve throughout the life span and into adulthood via changes in con-nectivity (Posner, Rothbart, Sheese, & Voelker, 2014). Although geneticvariations interacting with environment give rise to individual differencesin the efficiency of control networks that compose attention, recentfindings show that practice can improve the operation of specific atten-tion networks by altering overarching brain states (Rabipour & Raz,2012). Future studies may lead to new methods to ameliorate deficien-cies and enhance performance.

Attention as a Functional Organ System:A Metaphor for a New Psychiatry

The notion of attention is part of our everyday “folk psychology.”Titchener (1909) considered attention “the heart of the psychologicalenterprise”; and William James (1890) contended that, “Everyone knowswhat attention is. It is the taking possession of the mind in clear and vividform of one out of what seem several simultaneous objects or trainsof thought.” This subjective definition, which construes attention intui-tively as a unitary process under voluntary control, bears little resem-blance to the working models of attention developed by cognitiveneuroscientists (Posner, 2012a), who view attention in terms of a varietyof networks that coordinate or facilitate much of human experience andconsciousness.

We will outline a view of attention as a set of three distinct networks(alerting, orienting, and executive attention). Overall, we consider“attention” to be a “functional organ system.” According to the OED,an organ “system” refers to “a set of organs or parts in an animal bodyof the same or similar structure, or subserving the same function,” asexemplified by the digestive system. The term “functional” organ systemserves to bridge an outdated dichotomy between “functional” (i.e., psy-chological) and “organic” (biological) mental disorders (Beer, 1996) thatcontinues to influence clinical thinking (Miresco & Kirmayer, 2006).

Over the last half-century, the three-network model of attention hasbeen continually refined (Posner, 2012a). Although most of the researchhas focused on visual attention, this approach generalizes across allsensory modalities (Posner, 2012b). Briefly, alerting can be conceptual-ized as a foundation upon which orienting and executive attention rest.It maintains sensitivity to incoming stimuli. Orienting concerns the selec-tion of information from incoming stimuli. Lastly, executive attentioninvolves complex higher-order processing, including conflict monitoring



and inhibitory control (Posner & Fan, 2008; Posner & Petersen, 1990).Each network is associated with its own set of physiological activations,neuroanatomical structures, and neuromodulators (see Table 11.1;Posner & Fan, 2008; Rueda, Posner, & Rothbart, 2011).

As neuroimaging studies have shown, a wide variety of cognitive taskscorrespond to brain signal changes distributed over a set of neural areas;each of these areas relate to specific mental operations that contribute tothe overall cognitive task (Posner & Raichle, 1994, 1998). In the study ofattention, the specific neural areas identified have been more consistentthan for many other cognitive functions. For example, in order to shiftvisual attention to a new object, one has to disengage attention from itscurrent focus, move it to the location of the new target, and engage thenew object. Many experiments have shown that specific areas of the brainare involved in the operations of disengage (i.e., the parietal lobe), move(i.e., the superior colliculus), and engage (i.e., the pulvinar), and theseareas collectively form a functional control system (Posner, 2012b).Together, these loci perform the task of orienting (cf. Losier & Klein,

Table 11.1. Attention Systems Involved in Visual Attention

FunctionAnatomicalStructures

Neuromodulator/Neurotransmitter Brain Sites Measures

Orienting Superior parietalTemporalparietal junctionFrontal eye fieldsSuperiorcolliculus

Acetylcholine A1, V1, S1(Primary auditory,visual, andsomatosensorycortexes)

Eye-tracking

Alerting Locus coruleusRight frontal andparietal cortex

Norepinephrine Orienting system Autonomicchanges,event-relatedpotentials

ExecutiveAttention

AnteriorcingulateLateral ventralPrefrontalBasal ganglia

Dopamine All over the brain Stroop,McGurk,Simon,Go/NoGo,Stop task

Brain structures that house the three control networks active in studies of a tripartitebroad classification of attention, the corresponding dominant neuromodulators, and thesites of function. Although this illustration focuses on vision, the sources of attention effectsappear similar in other modalities (Macaluso, Frith, & Driver, 2000). Adapted from“Attention as an Organ System” by M. J. Posner & J. Fan (2008).



2001). Because attention involves specialized networks to carry outdifferent functions, damage to any module can produce distinct impair-ments in achieving and maintaining the alert state, orienting to sensoryevents, or controlling thoughts and feelings (Raz & Buhle, 2006).

Localizing mental operations in separate, yet connected, brain areassuggests a solution to the old problem of how brain localization couldoccur when widely diffuse damage is observed to produce the samegeneral behavioral effect (e.g., extinction; Karnath & Rorden, 2012).To perform an integrated task, the brain must orchestrate the activityof a distributed network of functionally related anatomical regions; yet,the computations underlying any single mental operation (for example,engagement during orienting, which is orchestrated by the pulvinar)occurs locally. In this view, brain regions coordinate to perform multiplecognitive functions and are not solely defined by the few mental oper-ations ascribed to them in a particular theoretical model or experimentalsetting (Macdonald & Raz, 2014).

The following sections present evidence for each attentional networkand outline their implications for conceptualizing, diagnosing, andtreating psychiatric conditions.

Alerting Attention

Alerting often appears as a foundational form of attention characterizedby individual sensitivity to incoming stimuli, be they visual or othersensory types (Posner, 2012a). In laboratory studies, any stimuli pre-sented to a subject will produce brain activity and physiological arousalcompared to the resting state. To separate the activity underlying alertingattention from the resting state, alerting responses are generally meas-ured during the interval between a warning signal and a stimulus. Duringthis period, brain physiology reflects activity suppression, and the para-sympathetic nervous system engages as an individual prepares for a swiftresponse to the anticipated stimuli. Alerting increases the efficiency ofsensory processing, including processing nontarget stimuli, such as dis-tractors, and influencing orienting and attention networks as needed.Unfortunately, research on the alerting network has been relativelylimited, compared with the volume of work on executive and orientingattention networks. As a result, despite the alerting network’s fundamen-tal role in attention, we know less about it.

Anatomically, alerting involves operations in the right frontal and rightparietal regions (Posner, 2012a). Evidence in support of this localizationincludes lesion studies, wherein damage to the right parietal cortex, butnot the left, has been associated with diminished alerting capacities



(Posner, Inhoff, Friedrich, & Cohen, 1987). Recent neuroimaging stud-ies corroborate these findings, showing activity in the parietal and frontalregions during the alert state (Raz & Buhle, 2006). Using a combinationof separate modalities, a plausible functional anatomy of the alert statehas been posited (Figure 11.1).

The primary neurotransmitter of the alerting network is norepineph-rine (NE), which is known to cause widespread effects within the regionsthat underlie alerting. The source of the brain’s NE pathways, the locuscoeruleus, appears to be the substrate for the influence of attention onarousal (Posner, 2012a), and warning signals trigger activity in this area(Aston-Jones & Cohen, 2005). Drugs that reduce or inhibit the release ofNE can block the effect of warning signals (Marrocco & Davidson,1998), whereas NE release enhancers may have the opposite effect(Posner, 2012a). The NE pathway originating in the locus coeruleusconnects to regions of the frontal and parietal lobe, where it influencesother networks. Studies designed to distinguish between orienting andalerting responses suggest that NE is a primary neuromodulator for thealerting system (Beane & Marrocco, 2004).

Pathologies of alerting due to individual differences in NE modulationhave not been directly studied, although other influences on the alertingnetwork have been identified. For example, some people with ADHDand learning disorders have a genetic variation in the alpha-2A receptorgene ADRA2A (Posner, 2012a), which may reflect alertness functioning.Children with ADHD also have increased difficulty maintaining an alertstate without a warning signal (Swanson et al., 1991), as well as poorerperformance with stimuli presented to the right hemisphere (Posner,2012a). Of course, some degree of alerting attention is needed for nearlyevery experimental task of attention. Understanding the bases of individ-ual differences in alerting may allow for more nuanced conceptualiza-tions of cognitive functioning.

Orienting Attention

The vast majority of studies on attention have involved orienting tosensory – predominantly visual – events. Orienting, which involves eithereffortful or reflexive directing of awareness to a stimulus, exists in twomajor forms: overt and covert. This distinction depends on whether overtphysical actions (e.g., eye movements) accompany directing awareness toa new stimulus. Of the three types of attention networks, orientingprovides the strongest evidence of mental operations, and researchersusually decompose it into a number of subsidiary processes (e.g.,engaging, disengaging, moving). Results from studies since the 1980s,



Figure 11.1 A sketch of the functional anatomy of the attentionnetworks.The pulvinar, superior colliculus, superior parietal lobe, and frontal eyefields are often activated in studies of the orienting network. Thetemporoparietal junction is active when a target occurs at a novellocation. The anterior cingulate gyrus is an important part of theexecutive network. Right frontal and parietal areas are active whenpeople maintain the alert state.Note: PUL: pulvinar; SC: superior colliculus; SPL: superior parietallobe; FE: frontal eye fields; TPJ: temporoparietal junction; ACG:anterior cingulate gyrus; RFA: right frontal area. Adapted withpermission from “Hypnosis and Neuroscience: A Cross Talk BetweenClinical and cognitive research” by A. Raz & T. Shapiro, 2002, Archivesof General Psychiatry, 59(1), 88. Copyright © (2002) American MedicalAssociation. All rights reserved.



including clinical, experimental, and imaging studies, support thegeneral approach toward localization but suggest somewhat differentdecompositions of the operations involved. As new methods of neuroi-maging have become available, increasingly sophisticated experimentshave been applied to the problem of orienting to sensory input.

Anatomical regions associated with visual orienting include the tem-poroparietal junction, superior parietal lobe, frontal eye fields, and thesuperior colliculus (Posner, 2012a). A paradox of lesion studies in theearly 1980s was that the superior parietal lobe seemed to be the area mostrelated to producing difficulty in disengaging from a current focus ofattention. Yet, most clinical data point to inferior lesions in the tempor-oparietal junction and/or the superior temporal lobe to account forneurological “extinction”; that is, when simultaneously stimulated oneither side of a perceptual field, the patient only perceives stimulus onone side – even if the patient can identify both stimuli when presentedseparately (Vuilleumier & Rafal, 2000). Event-related imaging studieshave served to reconcile this difference. We now know that lesions in twoseparate regions in a hemisphere can produce difficulty in shifting atten-tion to stimuli in the contralateral visual field, but for quite differentreasons. Lesions of the temporoparietal junction or superior temporallobe are important when a novel or unexpected stimulus occurs. Whenfunctioning normally, this area allows disengagement from a currentfocus of attention in order to shift to the new event. It also plays a criticalrole in producing the core elements of the hemispatial neglect syndrome(or extinction), in which a person becomes unaware of or inattentive tosensations and events on one side of the body. In addition, considerableclinical evidence suggests that in humans, lateralization in the right-temporal parietal junction may be more important to the deficit thanlateralization in corresponding areas of the left hemisphere (Mesulam,1981; Perry & Zeki, 2000). A different brain region, the superior parietallobe (SPL), appears critical for voluntary shifts of attention following acue. Event-related functional magnetic resonance (fMRI) studies havefound this region to be active following a cue that informs the personto shift attention covertly (i.e., without eye movement) to the target(Corbetta, Kincade, Ollinger, McAvoy, & Shulman, 2000). The SPL ispart of a larger network that includes frontal eye fields and the superiorcolliculus; this network appears to orchestrate both covert shifts of atten-tion and eye movements toward targets (Corbetta, 1998). During visualsearch – when people voluntarily move their attention from location tolocation while searching for a visual target – the SPL is also active. Bylinking the findings of lesion studies with converging evidence fromevent-related imaging studies, research on orienting has identified a



network of behavioral and anatomical features collectively responsiblefor the movement of attention in either a covert or overt manner(Figure 11.1 and 11.2).

Further distinctions between covert and overt orienting have beenposited at a cellular level (Posner, 2012a). For instance, a specific typeof neuron seems to be involved in covert shifts of attention (Schafer &Moore, 2007; Thompson, Biscoe, & Sato, 2005), which also continuesto attend to, or hold, the locations of cues during delay intervals(Armstrong, Chang, & Moore, 2009). Thus, cellular differentiation con-tributes to the distinction between motor systems involved in saccadesand circuits involved in covert orienting.

Cholinergic systems play a vital role in orienting attention. Even incases where NE release, and therefore warning signals, cannot occur,orienting can still take place (Marrocco & Davidson, 1998). Studies inmonkeys have utilized the acetylcholine (ACh) blocker, scopolamine(which slows covert orienting), to elucidate the role of ACh in orienting(Davidson & Marrocco, 2000). These findings further point to differ-ences in neurotransmitters between alerting and orienting systems.

Abnormalities in the orienting network may contribute to neuropsycho-logical conditions. For example, Alzheimer’s patients with degenerationin the superior parietal lobe have difficulty dealing with cues in thecentral visual field that are meant to inform them to shift their attention(Parasuraman, Greenwood, Haxby, & Grady, 1992). In addition, of thetwo main pathways that process visual information in the brain, theventral information-processing stream represents the “what” stream,which seems to identify objects rather than locate them in space. Patientswith lesions of the thalamus (e.g., the pulvinar) show subtle deficits invisual-orienting tasks that are likely related to the ventral information-processing stream. It seems plausible, therefore, that a critical element oforienting would be a vertical network of brain areas related to voluntaryeye movements and to processing novel input, but a precise model thatincludes a role for all visual areas implicated in orienting is still lacking.

The methods of neuroimaging have proven useful in testing the gen-eral proposition that mental operations involved in a given task aredistributed across multiple brain areas (Posner & Raichle, 1998). Nearlytwo decades of work have shown many tasks to be associated with theactivation of widely spaced networks that are presumed to carry outparticular operations. We are still unsure as to the exact operations thatoccur at each location, even in a relatively simple act such as shiftingattention to a novel event. However, imaging data link clinical observa-tions with experimental results to support the general idea of localizationof specific operations.



Figure 11.2 Cross-sectional views of the three attentionnetworks.The alerting network shows thalamic activation, the orienting networkshows parietal activation, and the conflict network shows anterior cingulatecortex activation. The color bar shows fMRI signal level (Z-scores) abovethe 0.05 significance threshold. fMRI images collected from 16 healthyadults performing the ANT in a 3 Tesla MRI scanner (Fan et al., 2001).Reprinted fromNeuroImage, 26, J. Fan, B.D.McCandliss, J. Fossella, J. I.Flombaum, &M. I. Posner, “The activation of attentional networks,”p. 476, Copyright 2005, with permission from Elsevier.



Executive Attention

The executive attention network is perhaps the most multifaceted of thefunctional systems of attention, involving the neural processing requiredfor resolution of conflicts, monitoring, and self-regulation. Commontests of executive attention generally include perceptual conflicts orhigher-level brain processing (e.g., Stroop or visual search tasks), andperformance on such tasks of executive attention has proven amenable totop-down modulation (Lifshitz, Aubert Bonn, Fischer, Kashem, & Raz,2012) and cognitive training (Rabipour & Raz, 2012). Moreover, cogni-tive training programs aimed at strengthening executive attention net-works have been found to increase intelligence and self-regulation scoresin children (Rueda, Checa, & Santonja, 2008). Although this networkhas long been associated with the handling of sensory conflicts, recentfindings now illuminate the wide-reaching implications of executiveattention in self-regulation.

The executive attention network, while interacting with other forms ofattention, is anatomically distinct. Exploration of brain activity in thecingulate during tasks of conflict resolution (Pardo, Pardo, Janer, &Raichle, 1990; Posner, 2012a) led to the discovery of the network. Inconflict paradigms, including Stroop tasks, the anterior cingulate cortex(ACC) becomes active and contributes to a dynamic process of conflictmonitoring and top-down control with the dorsolateral prefrontal cortex(MacDonald, Cohen, Stenger, & Carter, 2000). Utilization of modifiedStroop paradigms has further illuminated a distinction between emo-tional and cognitive areas of the ACC (Bush et al., 1998) – a discoverythat has implications for executive control of cognitive and emotionalimpulses. The major areas of executive attention interface with function-ally adjacent brain areas, while maintaining their autonomy as a distinctnetwork (Figure 11.1 and Figure 11.2).

Areas of the executive attention network exhibit particular cellmorphologies that provide clues regarding function. Spindle cells arefound in areas of the ACC and anterior insula that are unique to greatapes and humans (Posner, 2012a). Their presence, as well as the timecourse of their development, suggest higher cortical functioning concur-rent with the development of executive attention. Of course, these cellsare not necessarily the same ones that are active during fMRI scans, butfurther investigation into the function of these cells might provide keyinsights.

As behavioral genetics advances, novel research paradigms have begunto unravel relationships between genes and executive attention. Forexample, DRD4 and MAOA polymorphisms, selected for study because



of the importance of dopaminergic pathways in executive attention, havebeen correlated with performance on an attention network test, andalleles have been identified that correlate both with increasedACC activity and enhanced conflict resolution (Fan, Fossella, Sommer,Wu, & Posner, 2003). Studies of such genetic variation, while in theirinfancy, will lead to better understanding of the complex gene-brain-environment interactions during development that contribute to cogni-tive functioning.

Critically important in psychiatric disorders, executive attention hasbeen implicated in a wide range of disorders, including borderline per-sonality and schizophrenia (Posner, 2012a). Such transdiagnosticapproaches, congruent with the advent of the RDoC, may prove essentialto the development of a scientific basis for psychiatry that is grounded incognitive neuroscience.

The Functional Anatomy and Genetics of Attention Systems

In summary, recent research has mapped the functional anatomy ofmultiple systems in the brain. Event-related fMRI studies have identifiedbrain areas or networks associated with alerting, orienting, and executiveattention (Fan, McCandliss, Fossella, Flombaum, & Posner, 2005).Research on the effects of warning signals (e.g., alerting or expectationof when a target will occur) have shown that, while sustained vigilanceinvolves mainly areas of the right cerebral hemisphere, phasic changes inalertness following warning signals tend to operate through left hemi-sphere sites (Coull, Nobre, & Frith, 2001). Event-related fMRI studies oforienting (cf. Corbetta & Shulman, 2002) identify a dorsal system thatincludes the interparietal sulcus and frontal eye fields as key sites trig-gered by volitional shifts of attention. A more ventral parietal-frontalnetwork serves as a “circuit breaker” leading to shifts of attention, par-ticularly to novel stimuli. The more ventral system has been identified asa major site where cortical lesions produce attentional neglect. There isconsiderable agreement on which cortical areas orchestrate shifts ofattention toward sensory information, but the subcortical areas are stilllargely unclear (Posner, 2004; Posner, 2012a).

Much effort has been given to determining the exact role of specificareas, including the ACC and lateral prefrontal cortex. Several research-ers have argued that the cingulate involves a monitoring function,whereas lateral prefrontal areas act more directly to suppress neuralactivity in unselected areas (e.g., Cohen, Aston-Jones, & Gilzenrat,2004). Although consensus on the sites involved in executive attention



exists, active debates continue on whether these brain areas operate as awhole or via local, specific operations (Posner, 2004, Posner, 2012a).

Initial work on the molecular genetics of attention provided evidenceon the roles that MAOA, COMT, DRD4, and DAT1 genes play inmeasures of attention control (Fossella et al., 2002), and major studiesfrom a large group at NIH have confirmed the role of COMT inattention (Blasi et al., 2005). In addition, researchers have identifiedtwo cholinergic genes that influence individual differences in theorienting network (Parasuraman, Greenwood, Kumar, & Fossella,2005). Neuroimaging has been used to further explore the anatomy ofthese genetic differences (Egan et al., 2003; Fan et al., 2003). The areaof cognitive genetics has become a large field, allowing the study ofindividual differences in attention at the molecular level (Goldberg &Weinberger, 2004). As findings from this field accumulate, we maysoon have refined biological correlates of psychiatric distress that canguide the development of clinical interventions based on cultivating ourattentional capacities.

Neurodevelopment of Attention

The field of developmental cognitive neuroscience has traced the devel-opment of the attention systems in some detail (e.g., Posner, 2012a;Posner, Rothbart, Sheese, & Voelker, 2014; Rothbart, Posner, & Kieras,2006). Not only is this field of particular importance for understandingneurodevelopmental disorders such as ADHD, but it also sheds light onthe impact of environmental factors on attention (Posner, 2012a).

In adults, most cognitive and emotional self-regulation involves anetwork of brain regions drawing on structures such as the ACC, theinsula, and areas of the basal ganglia related to executive attention.During infancy and throughout early development, however, controlsystems depend primarily on a brain network involved in orienting tosensory events that includes areas of the parietal lobe and frontal eyefields (Posner, 2012a).

Over the first few years of life, emotion regulation is a major aspect ofdevelopment. fMRI studies on newborns and infants up to a year old(Gao et al., 2009), as well as on children and adolescents (Fair et al.,2009; Fair, Dosenbach, Petersen, & Schlaggar, 2012; Fransson et al.,2007), have provided data on two attention networks related to controlsystems: the frontoparietal network and the cingulo-opercular network.During early development the two networks cooperate closely together,while in adulthood the cingulo-opercular network becomes independentfrom the frontoparietal network. Drawing on the neural substrates of



the orienting network, the frontoparietal network is important for rapidadaptive control on shorter timescales, whereas the cingulo-opercularnetwork draws on the executive network’s neural infrastructure to main-tain stable attentional sets over longer timescales.

These patterns of connectivity suggest that the control structuresinvolved in executive attention – including structures on the medialaspect of the frontal lobe (e.g., ACC) and parietal lobe (e.g., opercu-lum) – are active during early development, maturing to wield fullercontrol only later in life. The parallels identified by studies of brainnetworks of attention in adults (e.g., Posner & Fan, 2008) and develop-mental studies of resting fMRI connectivity (e.g., Fair et al., 2009; Fairet al., 2012) may help unravel the story of the development of attention ininfants and young children.

Researchers, including Posner and others, have pursued the study ofchanges in control in early life, from orienting to executive attention,showing increased frontoparietal (i.e., orienting) resting network activityand reduced cingulo-cuneus (i.e., executive) activity during infancy(Posner, Rothbart, Sheese, & Voelker, 2012). As children develop,executive functioning increases, as indexed by both behavioral measuresand neural correlates.

During infancy, orienting serves as the primary control system; later inchildhood, effortful control becomes dominant. Control during infancymay be mainly in relation to emotion and only later related to executivefunctioning. Parents and caregivers probably propel the development ofself-regulation and exercise executive systems by presenting novel stimuli(e.g., new objects or people). Reading to the child may be anotherform of this type of stimulation. Some cultures make “active watching”(e.g., observation and imitation) the main learning venue of the develop-ing young. “High motivation to learn” among the children of Aka andBofi foragers in the Congo Basin rainforest “occurs early and often.Infants climb into their parents’ laps to watch them cook, play an instru-ment or make a net” (B. S. Hewlett, Fouts, Boyette, & B. L Hewlett,2011). Such cultures may prepare the executive attention network ofinfants by orienting to novel stimuli. The cingulate system appears tofunction, at least for the detection of errors, as early as seven months ofage (Berger, Tzur, & Posner, 2006; cf. Ketay, Aron, & Hedden, 2009;Boduroglu et al., 2009); with epigenetic and environmental interactionsshaping the development of the networks in later life (Sheese et al., 2007;Voelker, Sheese, Rothbart, & Posner, 2009), training can increase theefficiency of white matter connections, even in adults (Tang et al., 2010).Therefore, assuming that infants and adults share similar mechanismswith regard to novelty, cingulate activity may forge connections found in



later life. Better understanding of the development of attention systemswill have implications for child-rearing, pedagogy, and treating attention-related disorders.

Attention Training: Meditation and Hypnosis

Learning shapes attention systems well into adulthood. Attentional cap-acities are malleable, and attention can be trained in a number of ways.Michael Posner and colleagues, for example, have tried to distinguishattention training (e.g., conflict-related tasks) from attention statetraining (e.g., meditative practices accompanied by changes in mind/body states; 2009). Furthermore, they have demonstrated alterations inwhite matter connectivity in critical areas related to the ACC afterattention state training (Tang et al., 2010). Attention state training canimprove attention performance and response to stress, and measures ofattention have been used with individuals as young as four years old.

The potential clinical value of forms of attentional training such asmeditation and hypnosis is apparent from research on pain regulation(Holroyd, 1996); modulation of the immune system (Kiecolt-Glaser,Marucha, Atkinson, & Glaser, 2001); and treatment effectiveness(Kirsch, Montgomery, & Sapirstein, 1995).

Clinical hypnosis involves the deliberate use of attentional capacities tomanage symptoms, change behaviors, and produce other helpful out-comes (Nash & Barnier, 2012). During a hypnotherapy session, a ther-apist uses suggestion in the form of hypnotic instruction to bring aboutsuch outcomes in a client. Individuals vary widely in their ability torespond to hypnotic instructions and suggestions. We can measure thisindividual trait, which is known as hypnotizability, via the use of scales;but no biological marker currently exists for indexing either hypnotiz-ability or the hypnotic experience. In other words, neither a brain scannor a blood test can determine if a person is highly hypnotizable or ifsomeone is currently experiencing hypnotically induced alterations oreffects. In fact, most children are highly hypnotizable, with an age peak ofabout eleven to twelve years, but hypnotizability seems to graduallydiminish for many people thereafter; and adult hypnotizability is a rela-tively stable characteristic that is normally distributed in the population(Kohen & Olness, 2011; Raz, 2012). A few studies, however, have foundthat individuals can increase their hypnotic responsiveness throughtraining (Gorassini et al., 1999). Although it is controversial, hypnotiz-ability training aims to teach individuals to direct their attention in aspecific fashion to achieve a hypnotic experience (Spanos et al., 1989; cf.Rabipour & Raz, 2012). Although critics argue that the observed



responses may result from a combination of factors, including training-to-task and a certain measure of theatrics and self-deception, little researchhas examined hypnotic training in depth. It would be interesting to know,for example, whether people with low hypnotizability who undergotraining can achieve the ability of highly hypnotizable but untrainedpeople to override automatic effects such as those measured by executivetasks (Lifshitz et al., 2013). Attention training is a form of cognitiveintervention, similar to hypnotic training, that is aimed at exercisingspecific control networks (Rabipour & Raz, 2012). Behavioral programs,including attention training, have become ubiquitous; proponents claimthat they can be valuable adjuncts, if not rivals, to conventional pharma-cotherapy for certain disorders (e.g., Tourette syndrome), especially inchildren (Piacentini et al., 2010; Steeves et al., 2012). Finding nondrugtreatments for mental and neurological disorders might help patientsavoid or limit the side effects of medication; however, this nascent fieldis still in its infancy (cf Rabipour & Raz, 2012).

Tourette Syndrome: Intervening through the FunctionalSystem of Attention

Tourette syndrome (TS) is a neuropsychiatric condition marked bycompulsive, habitual movements and vocalizations. Individuals with TSfrequently report that these tics are preceded by physical sensations orurges to tic. These proceeding sensations and urges, known as premoni-tory urges, resemble the sensations and desires to blink that one may getwhen holding their eyes open for too long. Researchers often considerpremonitory urges to be “semivoluntary” since, as with blinking, they canbe suppressed only with a great deal of effort and discomfort. Moreover,many individuals with TS find that their tics ameliorate during times ofdeep mental focus.

Because of its close relationship to other diagnoses, we will use TS asan illustration of how to apply findings from attention research to thestudy and treatment of clinical populations. Although some may con-strue TS as a neurological condition, a strong psychological componenthas been noted for well over a century (Kushner, 1999), and the pastdecade has seen a revival of behavioral interventions that exploit top-down control (Wile & Pringsheim, 2013). Furthermore, TS symptomsoverlap with other conditions, including Obsessive Compulsive Disorder(OCD) and Attention Deficit Hyperactivity Disorder (ADHD). “Pure”TS is hard to find and usually occurs alongside multiple co-morbiditiesof attention and emotional regulation (Freeman et al., 2000). Hence,



some researchers have characterized TS as an impulse-control disorderrelated to ADHD and OCD.

Following the logic of RDoC, models of attention would unite TS withimpulse-control disorders on the basis of putatively shared neurobio-logical substrates, as suggested by studies of individuals who have comor-bid TS (Freeman et al., 2000) or experience urges (Blumberg et al.,2003; Bush, 2008; Raz et al., 2009; Shafritz, Collins, & Blumberg, 2006;Sowell et al., 2008). In a large-scale study, Freeman et al. (2000)sampled thousands of individuals with TS from twenty-two countries.ADHD and OCD formed the bulk of TS-comorbid diagnoses, contrib-uting to 60 and 27 percent, respectively, of all TS cases. Impairment ofthe attention system responsible for emotional and behavioral regulationis likely central to these disorders (Raz & Buhle, 2006; Raz et al., 2009).These results highlight the potential for attention research to elucidateboth the neurobiological substrate of psychopathology and the mechan-isms underlying the clinical effects of current therapies.

Whereas TS was once thought to result from an oversensitivity todopamine in the basal ganglia, the neurobiological mechanisms appearto be more complex (Felling & Singer, 2011; Leckman, Bloch, Smith,Larabi, & Hampson, 2010). Therefore, pharmacological dopamineblockers, the standard treatment for TS, have fallen short in successfullyameliorating tics for many patients (Peterson & Cohen, 1998; Phelps,2008; Pringsheim & Pearce, 2010). These drugs frequently induceintolerable side effects, including sedation, parkinsonism, cognitivedulling, dry mouth, fatigue, dizziness, weight gain, and metabolic syn-drome (Swain, Scahill, Lombroso, King, & Leckman, 2007). In light ofsuch challenges with pharmacotherapy, efforts have been redoubled todevelop cognitive-behavioral interventions for TS (Piacentini et al.,2010), whereas others have examined TS biology more closely (Leckmanet al., 2010).

A shared neural circuitry among TS, ADHD, and OCD is consistentwith findings that approximately 90 percent of individuals with TSqualify for multiple diagnoses (Freeman, 2007; Robertson, 2006; Scahill,Bitsko, Visser, & Blumberg, 2009). TS, ADHD, and OCD all involveirregularities in the internal neural circuitry that modulate impulsecontrol and in executive attention (Eddy, Rickards, & Cavanna, 2012;Willcutt, Doyle, Nigg, Faraone, & Pennington, 2005). TS research hasfocused on cortico-striatal-thalamo-cortical (CSTC) loops involved inhabit formation and information transmission between the basal gangliaand the cortex (Alexander, DeLong, & Strick, 1986; Graybiel & Canales,2000; Leckman et al., 2010). Decreased volume of the caudate nucleus(part of the basal ganglia) in childhood is a predictor of tic severity in



adulthood (Bloch, Leckman, Zhu, & Peterson, 2005); and frontostriatalloop activation, particularly in subcortical structures, influences ticsymptom severity (Peterson et al., 1998). Cognitive neuroscientists havefurther elucidated these subcortical structures as key nodes in the atten-tional system that may contribute to ADHD (Casey et al., 1997). BothOCD and TS involve include dysfunction of CSTC loops (Harrisonet al., 2009); and novel findings from deep brain stimulation suggest thatdirect modulation of basal ganglia activity can improve OCD symptoms(Welter et al., 2011). Taken together, the neurobiology of comorbid TSblur the distinction between “compulsion” and “tic” and implicateattention as a central component of the condition.

Cognitive-behavioral therapies, which train attention, have been foundto surpass pharmacological treatments as effective therapies for TS (Pia-centini et al., 2010; Steeves et al., 2012). In response to the considerableempirical evidence supporting habit reversal training (Feldman, Storch,& Murphy, 2011) and comprehensive behavioral intervention for tics(CBIT; Piacentini et al., 2010), recent Canadian guidelines forevidence-based treatment of TS identify cognitive-behavioral approachesas first line treatments for TS (Steeves et al., 2012). These therapiesemploy classic tools of attention training (AT; Rabipour & Raz, 2012) inthat they require sustained attention, awareness, and focus.

Attention may play a key role in tic disorders. When tested with theStroop task, for instance, groups with TS demonstrate poorer inhibitoryfunction compared to control groups (Eddy et al., 2012; Raz et al.,2009). In addition, tic suppression reduces cognitive performance(Conelea & Woods, 2008), and stress induction raises tic frequency(Conelea, Woods, & Brandt, 2011). We have found preliminary evidencethat attention training is effective at reducing tic expression, and six-month follow up data suggest long-term efficacy and increased qualityof life (Rabipour & Raz, 2012).

Additional research avenues remain to be explored. For example,using combinations of attention training and neuroimaging techniques,it may be possible to probe the relationships between executive attentiontraining, the unusual ACC patterns in OCD (Freeman et al., 2000), andthe abnormal ACC anatomy in adults with TS (Müller-Vahl et al., 2009).Moreover, TS is a unique context for studying impulse control becausethe overt behavioral expression of tics lends itself to quantitative meas-urement, even during novel experimental paradigms.

There is evidence that hypnotic suggestion can override processespreviously believed to be impermeable to top-down influences (Lifshitzet al., 2013; Raz, Kirsch, Pollard, & Nitkin-Kaner, 2006; Raz, Moreno-Íniguez, Martin, & Zhu, 2007; Raz, Shapiro, Fan, & Posner, 2002);



and hypnosis has been shown to modulate tic expression (Kushner,1999; Raz, Keller, Norman, & Senechal, 2007). Interestingly, like sug-gestibility, tic severity peaks during childhood development (Leckmanet al., 1998). Because of its ability to bridge controlled and seeminglyautomatic processes, hypnosis may be an effective tool for attention andTS research alike (Raz, Moreno-Íniguez, et al., 2007). For example,hypnosis can be used to empower individuals to exert executive controlover an otherwise involuntary tic. Hypnosis can alter the voluntariness ofthe semivoluntary tics characteristic of TS in ways that may be similar toattention training, CBIT, or habit reversal training (HRT; Feldmanet al., 2011). With regard to HRT and CBIT, hypnosis may have poten-tial as a useful adjunct to attention training. In these training programs,individuals with TS engage in behaviors called “competing responses”when they feel the urge to tic. These competing responses are incompat-ible with the motions and vocalizations of the tic. Because it can helpmake voluntary behaviors more automatic, hypnosis may simultaneouslyincrease the elements of suggestion in CBIT and HRT and decrease thedifficulty of employing competing responses. Furthermore, hypnosishas proven itself a powerful analgesic (Montgomery, DuHamel, &Redd, 2000), and may provide new ways of reducing the sensory dis-comfort associated with the premonitory urges that individuals with TSoften suffer.

Another approach to clinical intervention has proposed using medita-tion to improve attention, self-regulation, and emotional control(Perlman, Salomons, Davidson, & Lutz, 2010; Tang et al., 2007;Zeidan, Johnson, Diamond, David, & Goolkasian, 2010). Studies havereported that expert meditators show significant alterations in ACCactivity and effortless control over previously challenging and effortfulmodes of attention (Tang, Rothbart, & Posner, 2012). Such approacheshave yet to be applied to conditions such as TS, but there is enoughevidence to encourage further investigation.

As research on neural functioning in psychiatric disorders moves frombiological reductionism to an integration of neurobiology and psych-ology, with social science clarifying the contexts of functioning andadaptation, the clinical importance of attention as a mediator of ticsand other impulse-related problems suggests the utility of transdiagnosticresearch frameworks, such as RDoC. The history of approaches toTS shows how the psychiatric pendulum has swung from completelypsychological to extremely biological explanations, and then, mostrecently, back to a more balanced perspective, in which neurobiology,psychology, and social interactional processes all contribute to symptomproduction. This interactional perspective supports the search for



cognitive-behavioral interventions (Kirmayer & Crafa, 2014; Raz,Keller, et al., 2007).

Although TS represents a particularly interesting condition for thestudy of attention, it is but one example of how findings on attentionsystems might be applied to psychiatry. Similar approaches may be usefulto help ADHD patients build sustained attention and to help OCDpatients alleviate compulsions.

Conclusion

In this chapter, we have emphasized the importance of development inthe study of attention as a functional system. Studies conducted over thelast decade have revealed key aspects of the neurodevelopment of atten-tion networks. This research shapes our efforts to understand howexperience and genetics interact to produce the executive attentionnetwork, with possible consequences for developmental problems ofchildren and adults (Posner, 2012a; Posner & Rothbart, 2005).

Approaching attention as a functional organ system – with specificcontrol networks carrying its basic functions – provides a useful directionfor psychiatry (Posner & Fan, 2008). Setting aside diagnostic criteria fordiscrete disorders (as in the DSM), the framework we have presentedshows how molecular, neural network, and cognitive studies can beintegrated to provide a view of attention that illuminates its role inthe development of children and the everyday performance of adults.Disorders of attention comprise an important subset of the problemsaddressed by modern psychiatry. Attention systems also play a role inadapting to many conditions. Attention training, therefore, can be apowerful tool to influence behavior and modulate cognition, affect, andaction in a wide range of problems. As we have shown, linking clinicalsymptomatology to functional systems through the behavioral and brainsciences breaks down the functional/organic distinction and actuallysupports the use of psychological and psychosocial interventions for awide range of putatively “biological” disorders.

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