school of education, department of psychiatry and the m.i ... · the approach also emphasizes a...

Infant Joint Attention, Neural Networks and Social Cognition

Peter Mundy and William JarroldSchool of Education, Department of Psychiatry and the M.I.N.D. Institute, University of California atDavis, 2315 Stockton Blvd., Sacramento, CA, 95817-9956, 916-702-0310

AbstractNeural network models of attention can provide a unifying approach to the study of human cognitiveand emotional development (Posner & Rothbart, 2007). This paper we argue that a neural networksapproach to the infant development of joint attention can inform our understanding of the nature ofhuman social learning, symbolic thought process and social cognition. At its most basic, jointattention involves the capacity to coordinate one’s own visual attention with that of another person.We propose that joint attention development involves increments in the capacity to engage insimultaneous or parallel processing of information about one’s own attention and the attention ofother people. Infant practice with joint attention is both a consequence and organizer of thedevelopment of a distributed and integrated brain network involving frontal and parietal corticalsystems. This executive distributed network first serves to regulate the capacity of infants to respondto and direct the overt behavior of other people in order to share experience with others through thesocial coordination of visual attention. In this paper we describe this parallel and distributed neuralnetwork model of joint attention development and discuss two hypotheses that stem from this model.One is that activation of this distributed network during coordinated attention enhances to depth ofinformation processing and encoding beginning in the first year of life. We also propose that withdevelopment joint attention becomes internalized as the capacity to socially coordinate mentalattention to internal representations. As this occurs the executive joint attention network makes vitalcontributions to the development of human symbolic thinking and social cognition.

In this paper we provide an overview of theory and research on how a neural networks outlookon joint attention assists in our understanding of the mechanisms that support human sociallearning, symbolic thinking and social cognition. This theory and research has stemmed inlarge part from the contemporary pursuit of the question; how do people become capable ofsharing information with one another? One immediate answer is that it has a lot to do with thephylogeny and ontogeny of bio-behavioral systems specific to language. However, in the laterpart of the 20th century it became clear that vital elements of the cognitive foundations forinformation sharing develop before the onset of language in human infancy (Bates, et al.1979; Bruner, 1975; Werner & Kaplan, 1963). One especially pertinent observation was thatby 6 to 9 months infants become increasingly capable of sharing experience about objects andevents by directing or following the visual gaze of social partners (Bakeman & Adamson,1984; Bates et al., 1979; Scaife & Bruner, 1975, see Figure 1). Bruner (1975) referred to thistype of preverbal referential behavior as joint attention. He suggested that joint attention

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Published in final edited form as:Neural Netw. 2010 ; 23(8-9): 985–997. doi:10.1016/j.neunet.2010.08.009.

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behaviors reflect the early onset of psychological processes that are specific to social referencebut are distinct from, albeit necessary to the ontogeny of language.

By and large research over the past 30 years has supported Bruner’s hypothesis about thedistinct nature of communication versus language development and the primacy of infant jointattention development with regard to the former. For example, Willems, Boerl, Ruiter Noordziget al. (2009) have recently reported evidence for two distinct but interacting neurocognitivesystems in adults, one unique to communication processes and one unique to languageprocesses. Studies and theory also suggest that joint attention is pivotal to the development ofthe human neurocognitive communication functions (Mundy 1995; 2003; Mundy, Sullivan &Mastergeorge, 2009) and that the neurocognitive joint attention functions are integral to thesubsequent development of social cognition, as well as language (e.g. Baldwin, 1995; Charmanet al. 2000; Hirotani et al. 2009; Kasari et al. 2008; Kwisthout et al. 2009; Meltzoff & Brooks,2008; Mundy, Fox & Card et al. 2003). More to the point of this article recent theory suggeststhat neurocognitive joint attention development is supported by a distributed neural networkthat that synthesizes multiple sources of information in real time in social interactions and,though not necessarily species specific, contributes to a unique constellation of cognitivecapacities in human beings (Mundy et al. 2009).

Bruner (1995) characterized a principal approach to research on joint attention as one that isfocused on the “epistemological question”. That is to say, much of the research has beenconcerned with describing what the development of joint attention behaviors reveals aboutchange in the stages of knowledge infants possess about other people’s minds, or reveals aboutthe nature of cognitive modules that may be dedicated to knowledge about people’s minds(e.g., Baron-Cohen, 1995; Tomasello et al., 2005). This “social cognitive” paradigmemphasizes the comparison of the types of joint attention infants are capable of at differentages. These comparisons have provided grounds for numerous experimentally controlledinferences and insights about age-related changes in infant’s knowledge about the intentionsof other people (e.g., Baron-Cohen, 1995; Carpenter, Nagell & Tomasello, 1998; Meltzoff &Brooks, 2008). The emphasis on knowledge has become so strong in this paradigm that in someopinions joint attention, per se, is not thought to be achievable until a critical module or stageof social cognitive development is reached. Social cognitive theory argues that this point indevelopment is heralded by signs of “intentional” joint attention inferred from the emergenceof infants’ tendency to acknowledge shared experience with the use of spontaneous gazealternation between objects and people by about 12 to 15 months of age (Baron-Cohen,1995, Tomasello et al. 2005; see Fig. 1).

A complimentary but alternative approach to the social cognitive paradigm is exemplified bythe question of; does joint attention lead to social knowledge acquisition (learning) and thecapacity to share knowledge with others, and if so, how? This question was part of Bruner’s(1975) original motivation for the study of joint attention. He thought of joint attention as anearly onset interactive key to social learning and, therefore, a potentially informative naturalexample to emulate in curriculum design (Bruner, 1995).

A critical difference between these two views that joint attention ostensibly follows from andis defined by social knowledge development in the social cognitive paradigm, but is conceivedof as leading to knowledge development and sharing information in the alternative paradigm.Our research and theory on joint attention development has been guided by this alternativeapproach for quite some time. A maxim of this approach is that cognitive and psychologicaldevelopment is not only effectively modeled in terms of relatively discontinuous changes inknowledge or modules, but also in terms of changes and continuities in the speed, efficiency,and combinations of information processing that give rise to knowledge or psychologicalphenomenon (Hunt, 1999).

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The approach also emphasizes a constructivist view of cognitive and neurocognitivedevelopment in which infants learn as much about the minds of other people from their ownactions in episodes of joint attention, as they do from the perceptions of others behavior(Mareschal, Johnson, Sirois, Spratling et al. 2007; Mundy, 2003; Mundy & Newell, 2007;Piaget, 1952). Indeed, this paradigm is associated with a model that describes joint attentiondevelopment in terms of advances in the parallel processing of three sources of informationillustrated in Figure 2. When people interact in joint attention they actively engage in: 1) self-referenced processing of information about actions they generate (e.g. movement andorientation of one’s own eyes or control of visual attention), and about bodily state (e.g. affectand spatial position relative to a referent), 2) processing information about another person’sattention and behavior, as well as, 3) integrating those strands of input with processinginformation about a commonly referenced object or event (e.g., Mundy, Kasari & Sigman,1993; Mundy & Newell, 2007; Mundy, Sullivan & Mastergeorge, 2009).

We assume the early development of this type of parallel processing involves a transactionalor dynamic interplay between neural, psychological and behavioral development. That is tosay, practice with parallel self-referenced, other-referenced, and object/event-referencedinformation processing during joint attention in infancy is both a consequence and an epigeneticorganizational impetus related to the establishment of distributed neural processing networkthat involves the flow of information across distal frontal, temporal and parietal cortical systems(provided below). With maturation and experience, this distributed neural network comes toserve a social-executive function that enables infants to engage in increasingly effortless social-coordination of attention to internal information, external social, and external objects/eventinformation in social interactions. With development the overt operations of sociallycoordinating visual attention to external references become internalized as cognitive operationsthat allow for the joint coordination of mental attention to common representations. Thisinternalization of joint attention process contributes to the neurocognitive foundation for socialcognition, symbolic thought, and self awareness (Mundy et al. 2009). We refer to this as theparallel and distributed processing model (PDPM) of joint attention development. Thefollowing provides a more details related to this synopsis of this model and a review of researchon the distributed neural networks involved in joint attention development.

THE DEVELOPMENT AND DISSOCIATION OF JOINT ATTENTIONThere are two main functional categories of joint-attention behaviors in infancy. Respondingto joint attention (RJA) refers to measures of infants’ ability to follow the direction of the gazeand gestures of others in order to share a common point of reference. RJA functions as anautomatic reaction to the potential that others’ gaze signifies an important source of informationin the environment. Alternatively, initiating joint attention (IJA) involves infants’ generationof gestures and eye contact to direct others’ attention to objects, to events, and to themselves.The prototypical function of IJA is to “show” or spontaneously seek to share interests orpleasurable experience with others (Fig. 2). Just as speech comprehension and expressiondissociate in early language development (Bates, 1993) one important characteristic of theontogeny of human joint attention is that IJA and RJA also dissociate in development.

Several independent studies indicate that the cross dimension correlations between thefrequency or consistency of IJA and RJA (i.e. internal consistency of measures of a commoncontruct) are weak to non-significant concurrently and predictively in samples of 9, 12, 15 and18-month-old infants (e.g. Meltzoff & Brooks, 2008; Mundy et al., 2007; Sheinkopf et al.,2004; Slaughter & McDonald, 2003). In contrast, within dimension correlations of thefrequency of infant IJA and RJA across age (i.e., test-retest reliability) has been shown to besignificant in a large sample of infants from 9 to 12, 12 to 15, and 15 to 18 months, and even9 to 18 months for IJA (Mundy et al. 2007). Moreover, although both infant IJA and RJA

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measures correlate with or predict learning and cognitive development, these measures alsoexhibit different patterns of correlations with childhood IQ (Ulvund & Smith, 1998), frontalbrain activity (Caplan, Chugani, Messa, Guthrie, et al., 1993; Mundy et al.,, 2000); rewardbased behavioral goal-inhibition and self-monitoring behaviors (Nichols et al., 2005), attentionrelated self-regulation (Morales et al., 2005), and attachment (Claussen et al., 2002).

Results from clinical and comparative research also provided evidence for the dissociation ofIJA and RJA development. Indeed, this dissociation may have first been noted in research onautism. Both RJA and IJA are useful in the early identification and diagnosis of autismchildhood (e.g. Lord, et al., 2000; Stone, Counrod & Ousley, 1997). RJA impairments,however, become less evident among children with autism after they achieve a cognitivedevelopmental level of approximately 30 to 36 months (Mundy et al., 1994). Subsequentresearch has indicated that there is inconsistent evidence of a robust syndrome specificimpairment in the ability to process gaze or respond to joint attention in school age childrenor older people with autism (Nation & Penny, 2008). On the other hand, IJA deficits areobserved in children with autism from preschool through adolescence (e.g. Charman, 2004;Dawson et al., 2004; Hobson & Hobson, 2007; Mundy et al., 1986; Sigman & Ruskin, 1999).

The relative centrality of initiating rather than responding to joint attention impairments ishighlighted in the current nosology where ‘a lack of spontaneous seeking to shareenjoyment, interests, or achievements with other people, (e.g., by a lack of showing, bringing,or pointing out objects of interest to other people)’ is described as one of the four primary socialsymptoms of autism (APA, 1994). Furthermore, in the “gold standard” diagnostic observationinstrument, the Autism Diagnostic Observation Schedule (ADOS), both IJA and RJA are usedin Module 1 diagnostic algorithms for the youngest children. However, for older childrenModule 2 only includes IJA measures in its diagnostic criteria (Lord et al., 2000) because thediagnostic value of RJA for autism is recognized to diminish with age.

The correlates of IJA and RJA also diverge as much as they converge in studies of autism.Both IJA and RJA are related to executive inhibition and language development in autism,although RJA may be the more robust correlate of language development (Bono et al., 2004;Dawson et al., 2002, 2004; Griffith et al., 1999; Sigman & McGovern, 2005). However, to ourknowledge, only IJA has been observed to be significantly associated with differences in socialand affective symptom presentation in autism (Charman 2004; Kasari et al., 1990; Kasari etal., 2007; Lord et al., 2003; Mundy et al., 1994; Naber et al., 2008; Sigman & Ruskin, 1999).

Comparative research also suggests that there are important distinctions to be understoodbetween IJA and RJA development. Chimpanzees reportedly show the capacity for RJA.Indeed, gaze tracking is common to a variety of animals and even observed in the neonatalperiod of development (Jaime, Lopez, & Lickliter, 2009). However, animals and primates otherthan humans display little evidence of IJA or spontaneous attempts to convey informationsingularly for the social sharing or experiences with members of their own species (Tomasello& Carpenter, 2005). This suggests that basic information processing systems that enableadaptive responding to the perception of gaze direction as manifested in RJA might be commonto many animals. However, a second processing system involved the spontaneous generationof a joint attention to initiate experience sharing with others may be a unique and defining facetof human nature (Tomasello & Carpenter, 2005).

Why do different types of joint attention behaviors appear to be dissociated in typicaldevelopment, in neurodevelopmental disorders such as autism, and phylogenetically acrosshuman and non-human primates? One plausible hypothesis that was first raised several yearsago is that IJA and RJA reflect overlapping but substantially different types of socialinformation processing that occur in both shared and unique neural systems (Mundy, 1995;

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Mundy 2003; Mundy & Newell, 2007). Research that informs and in some cases tests thisproposition is described in the following review of the two neural systems of joint attention.

The Two Neural Systems of Joint Attention and Social CognitionElectroencephalography and Positron Tomography data from studies of infants have indicatedthat during early development IJA is associated with frontal-cortical activity (Caplan et al.,1993; Henderson et al., 2002; Mundy et al., 2000; Torkildsen et al., 2008), while RJA andrelated behaviors are more closely tied to parietal and temporal cortical processes (e.g.Frieschen, Bayliss, & Tipper, 2007; Materna, Dicke & Thern, 2008; Mundy et al., 2000). Oneinterpretation of these data (Mundy et al. 2000) is that early in development IJA and RJArespectively involve functions of the anterior and posterior cortical attention networks that havebeen described by Michael Posner and others (Posner & Peterson, 1990; Posner & Rothbart,2007). The functions of the posterior attention network are common to many primates, but theanterior attention network is not well represented in primates other than humans (Astafiev,Shulman, Stanley & Snyder et al., 2003; Emery, 2000; Jellema, Baker, Wicker, & Perrett,2000).

RJA appears to be most closely associated with the posterior system, which regulates relativelyrapid, involuntary attention orienting to perceived objects/events. The posterior attentionsystem begins to develop in the first 3 months of life, and prioritizes orienting to biologicallymeaningful stimuli (Posner & Rothbart; 2007). It is supported by neural networks of theparietal/precuneous and superior temporal cortices (Figure 3). These neural networks are activein the perception of the eye and head orientations of others, as well as the perception of spatialrelations between self, other and the environment (Frieschen, Bayliss, & Tipper, 2007). Inparticular, the recent work of Materna, Dieke, & Their (2009) suggests that the posterior partof the STS region and adjacent regions of the precuneous are specifically involved in extractingand using detailed directional information from the eyes of another person to redirect one’sown gaze and establish joint attention. On the other hand regions of the intraparietal sulcusmay contribute more generic encoding of spatial direction and mediate shifts of spatial attentionindependent of the type of cue that triggers this process (Materna et al. 2009). The posteriorsystem is also involved in the development of cognitive representations about the world builtfrom information acquired through external senses (Dosenbach et al., 2007; Fuster, 2006;Cavana & Trimble, 2006).

Processes associated with initiating joint attention may reasonably be expected to be supportedby the later developing anterior network involved in the regulation of more volitional, self-initiated, goal directed attention deployment. The anterior network includes elements of theanterior cingulate, medial superior frontal cortex including the frontal eye fields, anteriorprefrontal cortex and orbital frontal cortex (e.g. Dosenbach et al., 2007; Fuster, 2006). Thedevelopment of the intentional control of visual attention begins at about 3 to 4 months of age,when a pathway from the frontal eye fields (BA 8/9) that releases the superior colliculus frominhibition begins to be actively involved in the prospective control of saccades and visualattention (Canfield & Kirkham, 2001; Johnson, 1990). The function of this pathway mayunderlie four-month-old infants’ ability to suppress automatic visual saccades in order torespond to a second, more attractive stimulus (Johnson, 1995), and six month olds’ ability torespond to a peripheral target when central, competing stimuli are present (Atkinson, Hood,Wattam-Bell, & Braddick, 1992). We assume that the functions of this pathway also enablethe type of IJA behavior that involves intentional gaze alternation between interesting eventsand social partners (Mundy, 2003, see Fig. 1).

In summary, volitional or intentional control of attention is one of the primary features thoughtto distinguish IJA and RJA development. We are relatively compelled to engage RJA to lookwhere others look, but we choose to spontaneously engage in IJA to affect others attention to

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share experience. This conceptualization lead to a corollary assumption that variability in thetendency to engage in IJA behaviors among individuals or groups may involve motivationprocesses and sensitivity to the reward value of social engagement (Dawson et al. 2004; Mundy,1995). One specific suggestion is that frontal networks involved the Behavioral ActivationSystem (BAS) and reward sensitive activation of appetitive, approach behavior may beinvolved to a greater degree in IJA and RJA (Mundy, 1995). The BAS is thought to involvenetworks of the ventromedial frontal cortex, striatum, and amygdala (Davidson & Irwin,1999). In a related vein, Tomasello et al. (2005) suggested that constitutional processesassociated with a species-unique motivation to share emotions, experience, and activities withother persons may critical to IJA and part of what differentiate human and other primatecommunicative and social cognitive development. A third idea is that frontal mediation ofmotivation is thought to be a vital component of resolving conflict between goal relatedbehavior alternative. Research on the neural networks involved in the latter suggest thatfunctions of the anterior cingulate may play a vital role IJA development and individualdifferences (Mundy, 2003).

Theoretically, the differences in the functions, developmental timing, and the neural networksinvolved in the anterior and posterior attention systems outlined in the proceeding paragraphscontribute to the developmental dissociation of IJA and RJA in typical, atypical and primatedevelopment (Mundy et al., 2000, 2007; Mundy & Newell, 2007). However, although IJA andRJA appear to follow distinct bio-behavioral paths of development it is also likely that theyintegrate in development. For example, although predominantly associated with frontal activityEEG data also indicates that activation of a distributed anterior and posterior cortical systemat 14 months predicts IJA development at 18 months in infancy (Henderson et al., 2002). Hence,what we observe as the neural correlates of joint attention in infants may be only a part of thepicture of the mature, fully integrated mature human joint attention network. Two recent fMRIstudies have significantly advanced our understanding of the distributed anterior-posteriorcortical network that is associated with joint attention processes in adults.

Williams, Waiter, Perra, Perrett, et al. (2005) presented 12 right handed male participants withcongruent and incongruent responding to joint attention stimuli during fMRI data acquisition.The task for the participants was to track a red ball that appeared and then disappeared indifferent regions of the perimeter of a video screen. A video image of an adult male face wasvisible in the middle of the screen. On Congruent RJA trials the visual gaze of the male stimulusface shifted to the region of the screen prior to and predicting the correct location of theappearance of the red ball. In the Incongruent RJA trials the visual gaze of the male stimulusface shifted to a region of the screen that did not predict the correct location of the appearanceof the ball. In the former gaze tracking benefited correct and rapid responding and in the secondcondition inhibition of gaze tracking benefited optimal responding. The methods and resultsof this study are depicted in Figure 4. Contrasts associated with task performance in theCongruent and Incongruent RJA revealed neural activation across a neural network thatincluded the caudate, medial frontal cortex (BA 9,10), cingulate and anterior cingulate andparietal- precuneous cortex (Williams et al. 2005).

In another study Schilbach, Wilms, Eickhoff, Romanzetti et al. (in press) employed aninnovative paradigm to test the hypothesis that initiating and responding to joint attentionreflected activation of partially dissociated or independent neural networks. In particular, theytested the hypothesis that initiating of joint attention recruited activation of neural systemsinvolved in motivation and reward to a greater extent than did responding to joint attention(Mundy, 1995; Mundy & Newell, 2007). To do so Schibach’s research team collected 3 TelsafMRI data from 21 participants who were presented with a task with four conditions.

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During neuroimaging trials participants were instructed to look at one of three object thatappeared on a video monitor. A face created by virtual reality methods also appeared at thecenter of the video stimuli. On some trials the gaze of the virtual face was made to be responsiveto the participant’s gaze. The gaze of the virtual face either followed the participants correctlyin the joint attention condition (JA) emulating the experience of successfully initiating jointattention, or looked elsewhere in the non-joint attention condition (NOJA) emulating theexperience of unsuccessfully initiating joint attention. On other trials participants experiencedfollowing the gaze of the virtual other person to one of three objects to emulate the experienceof Responding to Joint attention (RJA). On some trials the gaze of the virtual other personpredicted the correct region to look for the object (joint attention condition, JA) and on sometrials the gaze of the virtual others failed to predict the correct region to look for objects (non-joint attention condition, NOJA). This resulted in a 2×2 factorial design comparing IJA andRJA and JA and NOJA conditions.

The a-priori comparison of IJA-JA + RJA-JA > IJA-NOJA + RJA-NOJA indicated a uniquepattern of activation for joint attention in a distributed neural network involving the regions ofthe dorsal and ventral medial prefrontal cortex, medial orbital frontal cortex, posterior cingulatecortex, subgenual cingulate and ventral striatum, right hippocampus and anterior temporalcortex (Figure 5). The interaction of IJA, RJA, and condition such that (IJA-JA > RJA-JA) >(IJA-NOJA > RJA-NOJA) revealed activity in a network of regions in the inferior and superiorparietal cortex, middle cingulate cortex and insular cortex specific to IJA-JA versus all otherbehaviors. RJA-JA versus all other behaviors was associated with specific recruitment of theleft superior frontal lobe. Finally, IJA-JA versus RJA-JA revealed unique activation for IJA inthe ventral striatum bilaterally for Initiating Joint Attention and activation of the ventral medialprefrontal cortex for Responding to Joint Attention.

Schilbach et al. (in press) provide a cogent interpretation of their seminal data. Among thepoints they innumerate three stand out in terms of their relevance to hypotheses related to thePDP model of joint attention. First their data are consistent with the hypothesis that jointattention involves a distally distributed neural network of frontal temporal and parietal corticaland subcortical neural activity (Mundy, 2003). Second, RJA and IJA reflect functions ofpartially independent sub-units of this neural network, and these may be differentiated on thebasis of the latter’s association with motivation, striatal, dopaminergic functions (Mundy,1995; 2003). Finally, joint attention may involve self referenced processing and the corticalsystems that support proprioception and interoceptive, such as the insular cortex (Mundy,Gwaltney & Sullivan, in press). We now turn to a more detailed consideration of this idea.

Self-Referenced Processing and Joint AttentionRecall that joint attention involves a tripartite deployment of attention and triadic informationprocessing (Fig. 2). When we engage in joint attention we attend to and process informationabout: 1) an object or event, 2) another person’s attention and behavior related to the object,and 3) self-reference information about our own attention to, and experience of the object andthe situation.

Self-referenced processing refers to implicit, subjective, and pre-reflective processing andintegration of information from one’s own body (e.g. heart rate, volitional muscle movement)with perceptual and cognitive activity such as representations in working or long term memory(Northoff et al., 2006). It involves at least two types of information. Interoception describessensitivity to physiological information originating within the body, such as heart rate,respiration, autonomic arousal, respiration, and emotional states. Proprioception involvessensitivity to the position, location, orientation, and movement of the body. Research suggeststhat specific, distributed neural systems may be involved in processing interoceptiveinformation (anterior insula) and proprioceptive information about movement and orientation

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(anterior cingulate and parietal cortices). Robust connectivity between these associativecortical systems also likely allows for a fundamental integration of these two dimensions ofself-referenced information (Craig, 2009; Balslev & Miall, 2008; Uddin & Menon, 2009).Indeed, comparative research suggests that interoception and its integration withproprioception may be more elaborated in humans via Von Economo neurons of the anteriorcingulate than in other primates and mammals (Allman, Watson, Tetreault, & Hakeem,2005; Craig, 2003).

In the past discussions, the first author naively described self-referenced informationprocessing in joint attention singularly in terms of the proprioceptive functions that wereattributed to functions of medial frontal structures, such as the anterior cingulate (Mundy,2003). This was an important oversight because it conflated interoceptive self referencedprocessing with goal related proprioceptive processing. Recently we have attempted to bringgreater clarity to putative nature of self-referenced processing in joint attention (Mundy, et al.in press). The dual nature of self-referenced information processing in joint attention may bebetter described in terms of: a) proprioception, such as feedback from ocular muscle controland the vestibular system related to the spatial direction of one’s own visual attention and headposture (see Butterworth & Jarrett, 1991 for related discussion), and b) interoception includingbut not limited to information about arousal and the positive (rewarding), neutral or negativevalence of self perception of the object or event, as well as the valence of sharing attentionwith a social partner. The latter conjecture now finds some substantiation in the observationsof insular cortical activity associated with adult’s experience of initiating joint attention(Schilbach et al. In press).

The capacity to meet the demands of multiple target, self-other-object attention deploymentand information processing in joint attention is only gradually acquired. Facility with thedemands of social attention coordination emerges in infancy as a function of the interactionbetween frequent, incremental practice with joint attention behaviors (e.g. gaze following orgaze alternating, Fig. 1) and neurocognitive maturation. Daily if not hourly practice with jointattention typically begins by three months of age and continues through at least the second year(D’Entremont et al., 1997;Carpenter et al., 1998).

Hypothetically practice with management of multiple sources of information processing injoint attention contributes to the developmental articulation of self- and other-referenced neuralprocessing networks, which aid the psychological differentiation of self from other in earlydevelopment (c.f. Decety & Sommerville, 2003; Northoff et al., 2006). This hypothesis isconsistent with a school of thought that human self-awareness does not simply rest uponadvances in self-reference proprioception and interoception. Rather, self-awareness is anincrementally achieved property of social relational processing that involves the analogous,parallel processing of self-and other- referenced information (Chen, Boucher, & Parker Tapias,2006; Piaget, 1952; Vygotsky, 1962). Typical human conscious self-awareness may not arisein social isolation because its development requires a deep and prolonged synthesis of self-referenced information processing (proprioceptive/interoceptive) and other referencedinformation processing (e.g. Piaget, 1952). Neurocognitive research suggests that this synthesisoccurs by way of the repeated social experiences of infants interacting with the maturation ofa distributed frontal, temporal and parietal cortical system (Decety & Sommerville, 2003;Keysers & Perret, 2004).

Keysers and Perret (2004), for example, propose that the relational processing of self-referenced and other-referenced information in infancy may be thought of in terms of a formof Hebbian learning that facilitates social-cognitive development. Hebb (1949) proposed thatlearning is supported by a basic neural function. Neural networks that are repeatedly active atthe same time become associated, such that specific activity [e.g. re-presentations] in one

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network triggers activity in the other (Hebb, 1949). Keysers and Perrett suggest that co-activation of neural networks for processing self-generated information and information aboutpeople is fundamental to the development of representations and knowledge about self andothers. We are inclined to agree with Hebbian model proposed by Keysers & Perrett, but wouldadd that rostral-medial-frontal processing of information about self-produced visual attentionand integrated with posterior processing of the attention of others is primary to the Hebbianmapping involved in social-cognitive development.

In this regard we conceptualize the development of joint attention in terms of an executivefunction. One definition of executive functions is that they involve the transmission of biassignals throughout neural networks to selectively inhibit comparatively automatic behavioralresponses in favor of more volitional, planned and goal-directed ideation and action in problemsolving contexts (Miller & Cohen, 2001). The aggregate effect of these bias signals is to guidethe flow of neural activity along pathways that establish the proper mappings between inputs,internal states, and outputs needed to perform a given task more efficiently (Miller & Cohen,2001).

With this definition in mind we propose that the incremental practice of joint attention inapproximately the 3- to 15-month period is both a cause and an experience-expectant organizerof the emergence of frontal bias signals. These signals facilitate adaptive mappings acrossoutside-in posterior cortical {temporal-precuneous} processing of exteroceptive informationabout the attention behaviors of other people, and the inside-out medial-frontal and insular-cortical proprioceptive and interoceptive processing of internal states, as well as informationrelated to the intentional control of visual attention. This mapping results in the integrateddevelopment of a distributed anterior and posterior cortical joint attention system (Fig. 3;Mundy, 2003;Mundy et al., 2009).

In our view, the early establishment of this cortical mapping of a joint processing system isformative with respect to the development of the shared neural network of representations ofself and others that have been described as driving the developmental progression of self-awareness social-cognition in infancy through adulthood (e.g. Decety & Grezes, 2006; Keysers& Perrett, 2004; Vanderwal, Hunyadi, Grupe, Conners, & Schultz, 2008). That is to say theHebbian mapping associated with social-cognition which Keysers and Perrett(2004) have solucidly described begins, with the integrated anterior cortical processing of information aboutself-produced visual attention and posterior cortical processing of the visual attention of others(Mundy et al., 2009). With sufficient practice and experience, the capacity for the jointprocessing of self-other attention information begins to consolidate and require less mentaleffort. As basic joint attention processes are mastered and require less effort it becomes a socialexecutive function that contributes to the development and efficiency of social learning,symbolic thinking and social-cognitive problem solving and development. How this model ofneural network mapping helps us to better understand the connection between and jointattention and development each of these domains will next be considered in turn.

Joint Attention and Social LearningDuring language learning how do infants correctly associate their parents’ vocal labels to thecorrect distal object or event in the midst of an environment flush with a myriad of potentialreferents? Baldwin (1995) suggested that they use RJA and the direction of gaze of their parentto guide them to the correct area of the distal environment, thereby reducing the potential for‘referential’ mapping errors. Infants’ can also use IJA to denote something of immediateinterest. This assists parents to provide new information in context when the child’s interestand attention is optimal for learning and the reduction of referential mapping errors learning(Tomasello & Farrar, 1986). Hence, joint attention may be conceived of as a self-organizingsystem that facilitates information processing in support of social-learning (Mundy, 2003).

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This ‘learning function’ is fundamental to the nature of joint attention (Bruner, 1975) andcontinues to operate throughout our lives (e.g., Bayliss et al., 2006; Nathan et al., 2007). Forexample, imagine the school readiness problems of a five-year-old who enters kindergartenbut is not facile with, and/or sufficiently motivated to coordinate attention with the teacher.

Another viewpoint on the links between joint attention and early learning is provided by therecent research of Striano and her colleagues (Hirotani, Stets, Striano, & Friedman, 2009;Striano, Chen, Cleveland, & Bradshaw, 2006a; Striano, Reid & Hoel, 2006b). Striano et al.(2006a,b) compared the visual recognition memory of 9-month-old infants who studiedpictures in one of two conditions. In the active joint attention condition each infant’s mothermade eye contact with their child and then turned to look at the pictures their infant studied.In passive joint attention condition the mother’s did not make eye contact but simply lookedat pictures in parallel with their infants. The results indicated that the 9-month-olds in the activejoint attention condition displayed EEG evidence of enhanced neural activity associated withgreater depth of processing and behavioral evidence of better recognition memory. Morerecently Hirotani et al. 2009 report EEG evidence of widespread frontal, central, parietal neuralnetwork activity and better depth of processing among 18 month olds during a word learningtask in joint attention versus non-joint attention conditions. The authors note that Joint attentionmay not only serve to referentially map new word object associations but somehow also enforcethe relation between the two.

One mechanism of enhanced depth of processing during joint attention may involve a role ofneural networks in learning. Parallel and distributed cognitive theory suggests that depth ofencoding is optimized by the simultaneous activation of multiple neural networks duringinformation processing (e.g., Munakata & McClelland, 2003; Otten et al., 2001). Jointattention, we assume, engages the activation of a distributed neural network comprised of nodesinvolved in the frontal processing of self-referenced attention related information and posteriorcortical processing of information related to the attention of another person (see Figure 6).Research suggests that activation of such a distributed network occurs in infants (Hendersonet al. 2002) just as it does in adults (e.g. Schilbach et al. in press). Therefore, it is plausible thatprocessing information during joint attention enhances learning by embedding semantic orlexical encoding in association with the parallel activation of a distributed, neural networkengaged in processing of information pertaining to the attention of self and the attention ofothers. This suggests that neural network activation during joint attention may be one principalmechanism of our advanced human capacity for social-learning.

Joint Attention and Symbolic ThinkingTomasello et al., (2005) have provided perhaps the most well articulated model of jointattention development in terms of three stages of what infants know about other people. In thefirst Understanding Animate Action stage, 3- to 8-month-old infants can perceive contingenciesbetween their own animate actions and emotions relative to the animate actions and affect ofothers. However, they cannot represent the internal mental goals of others that are associatedwith these actions. In the next Understanding of Pursuit of Goals stage 9-month-olds becomecapable of shared action and attention on objects (e.g. building a block tower with parents).Tomasello et al., 2005 suggest this involves joint perception, rather than joint attention, becausethe social-cognitive capacity to represent others internal mental representations necessary fortrue joint attention is not yet available. The latter emerges between 12-15 months in theUnderstanding Choice of Plans stage. This stage is heralded when infants become truly activein initiating episodes of joint engagement by alternating their eye-contact between interestingsights and caregivers (Tomasello et al., 2005, also see Fig. 1c1,2,3). This shift to activealternating gaze indicates infants’ appreciation that others make mental choices aboutalternative actions that affect their attention. Infants also now know themselves as agents that

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initiate collaborative activity based on their own goals. Hence, the development of “true” jointattention at this stage is revealed in the capacity to adopt two perspectives analogous to speaker-listener.

The capacity to adopt two perspectives is also assumed to be an intrinsic characteristic ofsymbolic representations. In this regard, Tomasello et al., (2005) raise a seminal hypothesisthat symbolic thought is a transformation of joint attention. They argue that symbolsthemselves serve to socially coordinate attention so that the intentions of the listener align withthose of the speaker. In other words linguistic symbols both lead to and are dependent uponthe efficient social coordination of covert mental attention to common abstract representationsamong people. This hypothesis fits well with the parallel and distributed processing model ofjoint attention, but the perspective of the PDP MODEL places it in a substantially differentdevelopmental and neural networks framework.

As previously noted the notion that true joint attention does not emerge until requisite social-cognitive awareness or modules emerges in the latter part of the first year (Baron-Cohen,1995; Tomasello et al., 2005) is not germane to the PDP MODEL. Rather, the PDP Modelholds that joint attention is defined in terms of the multiple level attention deployment andsocial information processing which begins to be practiced by infants by three to four monthsof age (D‘Entremont, Hains, & Muir, 1997; Farroni, Massuccessi, & Francesca, 2002; Hood,Willen, & Driver, 1998, Morales et al., 1998, Striano & Reed, 2006; Striano & Stahl, 2005).Indeed, even the types of active alternating gaze thought to mark the onset of true joint at 12-15months (Tomasello et al., 2005) develops no later than at 8-9 months of life, and quite possiblyearlier (Mundy et al., 2007; Venezia et al., 2004).

The PDP Model also includes the proposition that with practice, the operations of joint attentionto external objects or events become internalized to form cognitive operations that enable usto socially coordinate mental attention to representations (Mundy et al. 2009). This ability tosocially coordinate mental attention across people to common cognitive representations isessential to the development and use of symbolic thinking throughout the life span (Werner &Kaplan, 1963). Thus, in addition to conceiving of linguistic symbols as enabling the socialcoordination of covert attention to common mental representations across people (Tomasello,et al. 2005), it is equally plausible to conceive of internalized joint attention processes as thebasis of social coordination of covert attention to common mental representations that enablesthe symbolic development. Thus, the activation of the distributed joint attention neural networkalways occurs in the course of initial symbolic development, and in subsequent symbolicthinking throughout the life span. It is possible to have joint attention without symbolicthinking, but the converse seems unlikely.

Only indirect support exists for this hypothesis at this time. Theory and data suggest thatsymbolic representations are often initially encoded during the joint processing of informationabout the overt attention of self and of others directed toward some third object or event(Adamson et al., 2004; Baldwin, 1995; Kasari et al., 2007; Wener & Kaplan, 1963).Experimental studies of intervention with autism suggest that improvement of joint attentiondevelopment has a positive effect on symbolic behavior development and visa versa (Kasariet al. 2007).

A most useful test of the joint attention hypothesis of symbolic thought would be to useimagining methods to examine the expectation that there is the expected overlap betweennetwork brain activity associated with symbol acquisition or symbolic thought process, andthe network brain activity associated with joint attention. Although such a comparison has yetto be conducted two studies do bear on this prediction. German et al. (2004) and Whitehead etal. (2009) have reported that observations of the pretend rather than conventional object (e.g.

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tennis racket as guitar) elicits activation in a distributed neural network involving systems ofthe medial prefrontal areas (Brodmann’s areas [BA] 9/6/32, 9, and 10), inferior frontal gyrus(BA 44, 47), temporo-parietal regions (BA 21 and 22), and parahippocampal areas, includingthe amygdale (German et al. 2004; Whitehead et al. 2009). These studies were interpreted tosuggest that there is a strong association between neural networks that support symbolic pretendcognitive functions and “mentalizing” social cognitive processes (e.g. Whitehead et al.2009). We would suggest though that it is equally possible that any such association is at leastpartially mediated by the role the neural network for internalized joint attention processes playsin both symbolic processes and social cognition (Mundy et al. 2009; Tomasello et al. 2005).Let us finally consider the latter in more detail.

The Joint Attention Foundations of Social CognitionIn considering how the PDP model represents the contribution of joint attention to socialcognitive development it is useful to recall that PDP perspective gives equal footing to thesignificance of infants’ development of their own intentional visual behavior in modeling jointattention and social cognitive development (Mundy et al., 1993). The assumption here is thatneonates and young infants receive greater quantities and fidelity of information about self-intended actions, such as active control of visual attention, through proprioception andinteroception than they receive about other’s intended actions through exteroceptiveinformation processing. Thus, infants have the opportunity to learn as much or more aboutintentionality from their own actions as from observing the actions of others. The developmentof joint attention and social cognition are constructivist process that involves self-perceptionas a foundation for the attribution of meaning to the perception of others behaviors. We havereferred to this as the “inside out” processing assumption of the PDP model (Mundy &Vaughan, 2008).

Accordingly, the PDP Model suggests that, while IJA and RJA reflect distinct functions ininfancy, the interaction of information processing associated with each type of joint attentionplays is vital to social-cognitive development. As previously noted the dissociative butinteractive development of IJA and RJA may be similar to the dissociative but interactive pathsof early receptive and expressive language development. The former is supported in part byposterior cortical systems of the temporal and (Wernicke’s area) as well as parietal cortex, andthe latter by dorsolateral frontal systems of Broca’s area. The distinct nature of these neuralsystems may help to explain why receptive and expressive language expression is notnecessarily highly correlated in the early period of language development (Bates, 1993).However, the distributed neural networks for language interact via massive connectivitysupported by associative fibers (arcurate faciculus). Theoretically, more optimal languagerelated development is associated with greater coherent activity across the distributed neuralnetwork systems of expressive and receptive language development (Mundy et al. 2003;Salmelin & Kujala, 2006).

Similarly the manifest effect of joint attention on social cognition can be conceptualized interms of a synthesis of information processing output from the distributed neural networks forRJA and IJA (Mundy & Newell, 2007). With regard to the former Jellema, Baker, Wicker &Perrett (2000) epitomized the goal related neurocognitive output for the RJA system in primatesterms of the “concept” that that “where others’ eyes go, their behavior follows”. Mundy andNewell (2007) went on to suggest that, if part of the cognitive output from the posterior RJAsystem can be characterized as “where others’ eyes go, their behavior follows”, then a parallelpart of the cognitive output of the anterior system IJA could be characterized as “where myeye’s go, my [own] behaviors follows.”

The interaction and juxtaposition of information and concept formation from these two systemsis posited to serve as an important engine of cognitive development. It enhances the

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developmental differentiation of awareness of self-agency with respect to the control ofattention versus others’ agency and attention control. Moreover, the same integration of theanterior and posterior attention system that enables the comparative monitoring of overtattention (looking behavior) ultimately plays the same role when individuals begin to be ableto attend to internal representations about the behavior of self and representations of thebehavior of others. They (we) can begin to impute the conditional proposition that if selfreferenced-control of attention relates to one’s own goal-directed behavior representations thengoal related behavior in others must follow from their self-control of attention (see top “thoughtballoon” in Fig. 2). As this integrative anterior–posterior capacity to attend to overt or covertinformation about self and others matures with advances in representational abilities, a fullyfunctional, adaptive, human social-cognitive system emerges.

Another perspective on the developmental outcome of the integration of IJA and RJA issuggested by the description Keysers and Perrett (2004) provide of the role of Hebbian learningin social-cognitive development. Neural networks that are repeatedly active at the same timebecome associated, such that activity [e.g. “re-presentations”] in one network triggers activityin the other (Hebb, 1949). Keysers and Perrett suggest that frequent early experience with thecommon activation of neural networks for processing self-generated information whileprocessing information about conspecifics leads to an automatic reciprocal activation of selfreferenced information when thinking about others later in development. They suggest thisreciprocal Hebbian activation of information learned about self and other is fundamental to thecapacity to understand the actions and intentions of others. It seems likely that the longstandingnotions of Hebbian learning process invoked by Keysers and Perrettis have much in commonthe new labels for related constructs such as simulation (Gordon, 1986) and mirror neurons(i.e., Decety & Summerville, 2003; Williams, 2008) that are commonly invoked in currentmodels of social-cognitive development.

Recall that the PDP MODEL accommodates these interrelated ideas/constructs and suggeststhat one fundamental domain of relevant Hebbian mapping for social-cognitive developmentbegins with integrated frontal processing of information about self produced visual attentionand posterior processing of the attention of others. The PDP also suggests that once wellpracticed the joint processing of attention information requires less mental effort. Once themental effort to engage in joint attention decreases, it becomes possible for infants to learnfrom combined self and other referenced information processing in new ways. This is a criticalassumption of the PDP assumes and referred to as the “learning to do” and “learning from”phases of joint attention (Mundy & Vaughan, 2008).

A useful analogy to consider here may be learning to ride a bicycle. At first the demands ofcoordinating the processing of motor movement information, vestibular information and visualinformation are so high that it is difficult to attend to one’s surrounding when first learning toride. However, once some mastery of coordinating information processing and motor outputis achieved we begin to experience the mental capacity to focus our attention on oursurroundings and enjoy, if not learn from the information about the world that flows by as wecycle. We imagine it’s much the same course of development for infants with respect to jointattention. At first the process is difficult to manage, but with practice effort decreases and mostinfants begin to be able to process and learn from the rich array of social comparativeinformation available during joint attention (Mundy et al. 1993).

Recall the assertion that the co-active system of joint attention begins synergize as frontalexecutive bias signals (Miller & Cohen, 2001) that increasingly enable attending to multiplesources of information during infancy. Accordingly, the “learning to” phase of joint attentiondevelopment may be thought of as reflecting the emergence of frontal bias signals that establishthe proper mappings across: 1) outside-in posterior cortical {temporal-precuneous} processing

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of inputs about the attention behaviors of other people and, 2) inside-out rostral-medial frontalcortical {dorsal frontal medial cortex (BA 8-9), anterior cingulate, insular cortex} processingof internal states and outputs related to active vision. We imagine this mapping is influence byHebbian learning processes (Keysers & Perrett, 2004), genetic and especially activitydependent genetic processes (Mundy et al. 2009) and environmental processes (e.g. Claussenet al. 2002). The mapping ultimately results in the [more or less] functional, integrateddevelopment of a distributed anterior and posterior cortical joint attention system.

As basic joint attention process is mastered and becomes an executive function its ‘effort toengage’ goes down. As effort decreases joint attention development has the potential to shiftto a “learning from ” phase of development. In the learning from phase the capacity to attendto and learn from the integration of multiple sources of information in “triadic attention”deployment becomes more common (Scaife & Bruner, 1975). Triadic attention contextsprovide infants with rich opportunities to compare information gleaned through processinginternal states associated with volitional visual attention deployment and the processing of thevisual attention of others in reference to a common third object or event. Through somethingakin to cognitive simulation (Gordon, 1986) infants may begin to impute that others haveintentional control over their looking behavior that is similar to their own.

The role of simulation in the learning from phase of joint attention development is powerfullyillustrated by a recent sequence of elegant experimental studies (e.g. Brooks & Meltzoff,2002, Meltzoff & Brooks, 2008). Twelve-month-olds often follow the head turn and “gazedirection” of testers, even if their eyes are closed. After 12 months, though, infants discriminateand only follow the head turn and gaze of testers whose eyes are open. This suggests thatinfants’ understanding of the meaning of the eye gaze of others may improve after about 12months leading many older infants to inhibit looking in the “eyes closed” condition (Brooks& Meltzoff, 2002).

To examine this interpretation Meltzoff and Brooks (2008) manipulated the informationprocessing of infants in joint attention. They provided 12-month-old infants with the experienceof blindfolds that occluded their own looking behavior. After gaining that experience, 12-month-olds acted like older infants in so far as they did not follow the head-turn of blindfoldedtesters, but did follow the head-turn and gaze of non-blindfolded testers. Meltzoff and Brooksalso cleverly provided 18-month-olds with experience with blindfolds that looked opaque, butwere actually transparent when worn. After this experience in this condition the 18-month-oldsreverted to following the gaze of blindfolded social partners. These data strongly suggest thatthe infants demonstrated inside-out learning and constructed social-cognitive awareness aboutothers’ gaze based on the experience of the effects of blindfolds on their own active vision.

Lest we fall into the constraints of a stage model we would like to emphasize that the learningto and learning from phases of joint attention development are conceptualized as overlappingrather than sequential. Although more of one than the other may occur at a particular age from3 months on, examples of both are likely to be observed across many ages. For example,although Meltzoff and Brooks (2008) have provided a seminal example of learning from jointattention in the second year of life the PDP Model holds that some learning from joint attentionlikely has its onset early in the first year.

One of the first and most vitally informative types of constructivist actions infants take involvesthe self-control of their looking behaviors, or “active vision”. The science of vision has movedaway from the study of “seeing” or passive visual perception, to the study of “looking” orintentional, active-vision and attention deployment (Findlay & Gilchrist, 2003). Active visionin infancy begins to develop at 3-4 months (e.g. Canfield & Kirkham, 2001; Johnson, 1990;1995).

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The human eye is thought to have unique spatially signifying characteristics, such ashighlighted contrast between the dark coloration of the pupil and iris versus the light to whitecoloration of the sclera. This has lead to the suggests that human eyes that provide a potentsource of information to infants about other people’s attention that promotes social cognitivedevelopment (e.g., Baron-Cohen, 1995; Tomasello, Hare, Lehman, & Call, 2006). However,the same spatial characteristics of eye that provide information about other people to infantsalso likely allows the saccades of infants to be readily observed by other people and,consequently, act as elicitors of contingent social feedback. When infants shift attention to anobject their parents may pick-up and show them the object. When infants shift attention to theirparents’ eyes they may also receive a vocal or physical parental response. Thus, just as thecharacteristics of eyes make it easier for infants to perceive the attention of others, the signalvalue of eyes makes the active control of vision a likely nexus of information about infants’own developing intentional agency. Active vision is one of the first domains that enable infantsto experience goal directed selection of information to attend to, and a behavior that elicitcontingent social behavior responses from other people, such as parental smiles, vocalizationsor gaze shifts. It also is one of the first types of volitional actions that infants use to controlstimulation in order to self-regulate arousal and affect (Posner & Rothbart, 2007).

The contemporary literature on social-cognitive development often validly but, singularlynotes the potential importance of the information infants gather from processing the visualattention of others (e.g. Johnson et al., 2005). It neglects the potential importance of theinformation infants’ process about their own active vision, and socially contingent responses.The PDP MODEL alternatively also notes the potential for inside-out processing,constructivism and the role of active vision in the development of joint attention and socialcognition. Indeed, this aspect of the PDP MODEL offers one explanation for why activationof the frontal eye-fields (a cortical area involved in volitional saccadic control) is a consistentcomponent of the brain activation network observed to correlate with social-cognition inimaging studies (Mundy, 2003). This is because the volitional control of active vision, via thefrontal eye fields, may be central to developing an integrated sense of the relations betweenself-attention and other-attention, which is fundamental to joint attention and social cognition.

The PDP MODEL emphasizes inside-out processing, constructivism and the role of activevision in the development of joint attention. However, it does not maintain that the inside-outprocessing of self-attention is more important for social-cognitive development than out-sidein processing of other’s-attention. This is because, as previously noted the PDP MODEL holdsthat social meaning, and even conscious self-awareness, cannot be derived from processingeither self-attention or other’s-attention in isolation (cf. Decety & Sommerville, 2003; Keyser& Perret, 2004; Vygotsky, 1962). Ontogeny and phylogeny may be best viewed as a dynamicsystem that, through interactions of multiple factors over time and experience, coalesce intohigher order integrations, structures and skills (e.g. Smith & Thelen, 2003). Joint attention, orthe joint processing of the attention of self and other, is such a dynamic system. Its pertinencefor human development derives from the unique synthesis of the rapid parallel processing ofself attention and other attention across distributed neural networks. Consequently, it is notpossible to comprehensively account for the role of joint attention in typical or atypicaldevelopment with research or theory that focuses on only one of its elements in isolation.

Summary and ConclusionsPosner and Rothbart (2007) have cogently revived the notion that neural network models ofattention can provide a common, unifying approach to theory and research on many aspects ofhuman cognitive and emotional development. We resonate with this perspective and suggestthat the study of joint attention from a neural networks PDP model helps us understandcommonalities among developmental processes associated social learning, symbolic thinking,

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social cognition and social motivation. In this view joint attention is conceptualized as socialexecutive function of a frontal-parietal neural network, which constitutes a unique and discretedomain of human cognition that has a vital functional impact on social-communicativecompetence throughout the life span. The joint attention executive function serves to enablethe rapid, parallel and comparative processing of information about one’s own attention andthe attention of other people in social interactions. This executive function emerges as withactive behavioral practice in the first year of life and is both a cause and consequence of thedevelopment of a parallel and distributed neural network of primarily frontal and parietalcortical and sub-cortical systems. Once codified this parallel and distributed processing systemcontributes to the human capacity for increased depth of processing in social learning situations,mental coordination of attention to socially common reference of abstract representations(symbolic thought) and the capacity to mentally represent the attention of self and others. Thelatter is integral to social cognition. This perspective suggests that we may have as much tolearn about human cognition and development through the study of joint attention as anexecutive attention neutral network, as we do from conceptualizing joint attention as a vitalbyproduct of development of social-cognitive knowledge.

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Figure 1.Illustrations of different types of infant social attention coordination behaviors: a) Respondingto Joint Attention-RJA involving following another person’s gaze and pointing gesture; b)Initiating Joint Attention-IJA involving a conventional gesture ‘pointing’ to share attentionregarding a poster on the wall, c1,2,3) IJA involving alternating eye contact to share attentionwith respect to a toy, d) Initiating Behavior Request involving pointing to elicit aid in obtainingan out of reach object, and e) Responding to Behavior Requests involving following an adult’sopen-palm “give it to me” gesture.

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Figure 2.An illustration of integrated triadic information processing during joint attention. In the lowerpart of the figure the arrows depict “person B’s” integration of: 1) processing her own visualinformation about an object (arrow from person B to apple); 2) processing information aboutthe visual attention of person A (arrow from person B to person A), and 3) processing selfreferenced information about her attention to the apple and person B, including feedback fromeye muscles, affect or arousal (e.g. heart rate) associated with information processing of theevent, reward value of self generated goal directed behavior in the context of the event, etc.,(also see Figure 1c1,2,3). The top portion of the figure illustrates the developmentalinternalization of operations of joint attention. The behavioral operations once first involvedin the social coordination of attention and information processing with respect to and externalreferent becomes re-described as a social executive system that contributes to the humancapacity to socially coordinate mental attention to a representation of shared experience.

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Figure 3.Illustration from Mundy & Newell (2007) depicting the lateral (top) and medial (bottom)illustrations of the distributed system of Brodmann’s cytoarchitectonic areas of the cerebralcortex associated with Initiating Joint Attention and the anterior attention system, as well asRJA and the posterior attention systems. The former include areas 8 (frontal eye fields) 9(prefrontal association cortex), 24 (anterior cingulate), 47 and 43 (orbital prefrontal and insulaassociative cortices). The latter include areas 7 (precuneous, posterior parietal associationarea), 22, 41, and 42 (superior temporal cortex) and 39 and 40 (parietal, temporal, occipitalassociation cortex).

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Figure 4.Illustration of the face/gaze direction stimuli that preceded the appearance of the ball stimulifor congruent (joint attention) and non-congruent (non-joint attention) conditions in Williamset al. (2005). Illustration of regions of cortical activation uniquely associated with the jointattention condition (red), the non-joint attention condition (green) and both (green on red).

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Figure 5.Illustrations of facial stimuli observed by participants in the self initiated joint attentioncondition and other initiated joint attention conditions in the study of Schilbach et al. (Inpress). Composite brain images can also be seen for frontal-parietal activation associated withthe joint attention condition; parietal central activation associated with the non joint attentioncondition, and ventral striatum activation associated with self initiated joint attention versusprefrontal activation associated with other initiated joint attention condition.

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Figure 6.An estimation of the distributed neural network activated in joint attention, and its commonalitywith the network of brain regions active only in self processing (self > other) and co-active inboth self and other information processing. Estimation of the former was derived from dataavailable in Schilbach et al. (In press) and Williams et al. 2005. Estimation of the latter wasbased on data available from Northoff et al. (2006) and Lombardo et al. (2007). Note activationassociated with the insular cortex is not illustrated in this figure.

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school of education, department of psychiatry and the m.i ... · the approach also emphasizes a...

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