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Social attention: Developmental foundations and relevance for autism spectrum disorder

  • Terje Falck-Ytter
    Correspondence
    corresponding authors (; )
    Affiliations
    Development and Neurodiversity Lab, Department of Psychology, Uppsala University, Uppsala, Sweden

    Center of Neurodevelopmental Disorders (KIND), Centre for Psychiatry Research, Department of Women’s and Children’s Health, Karolinska Institutet & Stockholm Health Care Services, Region Stockholm, Stockholm, Sweden

    The Swedish Collegium for Advanced Study (SCAS), Uppsala, Sweden
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  • Johan Lundin Kleberg
    Affiliations
    Rare Diseases Research Group, Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden

    Center for Psychiatry Research, Department of Clinical Neuroscience, Karolinska Institutet & Stockholm Health Care Services, Region Stockholm, Stockholm, Sweden

    Department of Psychology, Stockholm University, Stockholm, Sweden
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  • Ana Maria Portugal
    Affiliations
    Development and Neurodiversity Lab, Department of Psychology, Uppsala University, Uppsala, Sweden

    Center of Neurodevelopmental Disorders (KIND), Centre for Psychiatry Research, Department of Women’s and Children’s Health, Karolinska Institutet & Stockholm Health Care Services, Region Stockholm, Stockholm, Sweden
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  • Emilia Thorup
    Correspondence
    corresponding authors (; )
    Affiliations
    Development and Neurodiversity Lab, Department of Psychology, Uppsala University, Uppsala, Sweden

    Department of Psychology, Lund University, Lund, Sweden
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Open AccessPublished:October 19, 2022DOI:https://doi.org/10.1016/j.biopsych.2022.09.035

      ABSTRACT

      The use of the term Social Attention (SA) in the cognitive neuroscience and developmental psychopathology literature has increased exponentially in recent years, in part motivated by the aim to understand the early development of autism spectrum disorder (ASD). Unfortunately, theoretical discussions around the term have lagged behind its various uses. Here, we evaluate SA through a review of key candidate SA phenotypes emerging early in life, from newborn gaze cueing and preference for face-like configurations to later emerging skills such as joint attention. We argue that most of the considered SA phenotypes are unlikely to represent unique socio-attentional processes but have to be understood in the broader context of bottom-up and emerging top-down (domain-general) attention. Some types of SA behaviors (e.g., initiation of joint attention) are linked to the early development of ASD, but this may reflect differences in social motivation rather than attention per se. Several SA candidates are not linked to ASD early in life, including the ones that may represent uniquely socio-attentional processes (e.g., orienting to faces, predicting others’ manual action goals). Although SA may be a useful super-ordinate category under which one can organize certain research questions, the widespread use of the term without proper definition is problematic. Characterizing gaze patterns and visual attention in infants at elevated likelihood for ASD in social contexts may facilitate early detection, but conceptual clarity regarding the underlying processes at play are needed to sharpen research questions and identify potential targets for early intervention.

      Keywords

      Looking at Hugues Merle’s painting Contes Enfantines (Figure 1), few would disagree that “social attention” occurs in the scene. The younger children look at the older girl’s face with a magnetic intensity, completely absorbed by the words coming from her mouth, her gaze, and her facial expressions. The term Social Attention (SA) is typically used to describe phenomena linked to selective attention to eyes and faces, non-verbal social communication, and joint attention. The term is also commonly used when describing differences in looking behaviors in people with Autism Spectrum Disorder (ASD) (
      • Frazier T.W.
      • Strauss M.
      • Klingemier E.W.
      • Zetzer E.E.
      • Hardan A.Y.
      • Eng C.
      • et al.
      A meta-analysis of gaze differences to social and nonsocial information between individuals with and without autism.
      ), and atypical SA has been suggested to represent a potential biomarker for the condition (
      • Murias M.
      • Major S.
      • Davlantis K.
      • Franz L.
      • Harris A.
      • Rardin B.
      • et al.
      Validation of eye‐tracking measures of social attention as a potential biomarker for autism clinical trials.
      ). A common assumption is that atypicalities in SA very early in life may be central for understanding early developmental trajectories in children with ASD (
      • Klin A.
      • Lin D.J.
      • Gorrindo P.
      • Ramsay G.
      • Jones W.
      Two-year-olds with autism orient to non-social contingencies rather than biological motion.
      ). Potentially, while looking in social contexts could be facilitated by automatized SA processes in typical development, it may draw on different processes in ASD. This potential fundamental link to ASD and the general use of eye tracking technology in (social) cognitive developmental neuroscience may explain why the use of the term SA appears to be increasing exponentially in the literature (
      • Salley B.
      • Colombo J.
      Conceptualizing social attention in developmental research.
      ).
      Figure thumbnail gr1
      Figure 1Contes Enfantines, by Hugues Merle (1823-1881)
      Although theoretical discussions of the SA term are scarce (
      • Salley B.
      • Colombo J.
      Conceptualizing social attention in developmental research.
      ), two distinct views regarding the nature of SA can be identified in the existing literature:
      A. SA is a domain specific attentional process, distinct from other attentional processes. This view is implicated by research suggesting that it builds on highly specialized brain circuits (
      • Salley B.
      • Colombo J.
      Conceptualizing social attention in developmental research.
      ,
      • Nummenmaa L.
      • Calder A.J.
      Neural mechanisms of social attention.
      ), i.e., as a social parallel to the domain general attentional networks identified over the last decades (
      • Petersen S.E.
      • Posner M.I.
      The Attention System of the Human Brain: 20 Years After.
      ,
      • Posner M.I.
      Attention as a cognitive and neural system.
      ). A more extreme version of this hypothesis is that SA is both domain specific and unitary (across many ostensibly different SA phenotypes) (
      • Salley B.
      • Colombo J.
      Conceptualizing social attention in developmental research.
      ), a possibility we will return to in the Discussion.
      B. Attention allocation to social objects, events and scenes can be explained by general attentional processes (Figure 2). These involve two interlinked types: exogenous (stimulus driven, reflexive) and endogenous (goal-directed, voluntary) orienting (
      • Corbetta M.
      • Shulman G.L.
      Control of goal-directed and stimulus-driven attention in the brain.
      ). Further, attentional mechanisms that are spatially unselective (the alerting network) can be differentiated from visuospatial orienting (
      • Petersen S.E.
      • Posner M.I.
      The Attention System of the Human Brain: 20 Years After.
      ). In infancy, many looking behaviors reflect a blend of exogenous and emerging endogenous processes (
      • Amso D.
      • Scerif G.
      The attentive brain: insights from developmental cognitive neuroscience.
      ).
      Figure thumbnail gr2
      Figure 2How social is social attention? The use of the term in the developmental and ASD literature often implies a specialized process for social attention in the brain (central dashed box). According to an alternative view, behavioral instances of SA (rightmost box) can be explained by domain-general attentional processes (bottom, top). The figure provides a simplified overview of the main factors behind SA behaviors. It is not intended to provide a full overview of all possible links (e.g., bidirectional).
      These two views represent the extreme ends of a spectrum of possibilities, including that SA becomes distinct from other attentional processes over time, driven by experience and interaction with social stimuli (
      • Salley B.
      • Colombo J.
      Conceptualizing social attention in developmental research.
      ,
      • Posner M.I.
      • Rothbart M.K.
      • Sheese B.E.
      • Voelker P.
      Control networks and neuromodulators of early development.
      ).
      In order to improve clarity around these contrasting views on SA, this review presents and discusses specific phenotypes that have been termed SA in the past (hereafter candidate SA phenotypes), while briefly considering available evidence supporting either A or B above for the phenotype in question. The candidates are selected based on their prevalence in the ASD and developmental cognitive neuroscience literature. Because SA is thought to be tightly linked to ASD, which develops early in childhood, our focus is on developmental data from the first years of life. We also summarize the link, or lack thereof, to ASD early in life for each candidate SA phenotype. Whether a single SA candidate is affected in ASD is not in itself informative for evaluating A versus B. However, looking at the emerging pattern across several SA candidates could be informative for understanding the nature of SA (e.g., its unity) and ASD. If ASD is fundamentally linked to SA, we expect the candidate SA phenotypes with most support for hypothesis A above to be particularly affected in infants who develop ASD symptoms.
      Studies of SA have been criticized for their reliance on 2D stimuli shown on a computer screen (
      • Schilbach L.
      • Timmermans B.
      • Reddy V.
      • Costall A.
      • Bente G.
      • Schlicht T.
      A second-person neuroscience in interaction.
      ,
      • Redcay E.
      • Schilbach L.
      Using second-person neuroscience to elucidate the mechanisms of social interaction.
      ,
      • Pfeiffer U.J.
      • Vogeley K.
      • Schilbach L.
      From gaze cueing to dual eye-tracking: novel approaches to investigate the neural correlates of gaze in social interaction.
      ). In this review we also illustrate how researchers are increasingly using modern technology for assessing infants in more ecologically valid settings to try to circumvent this limitation (
      • Valtakari N.V.
      • Hooge I.T.C.
      • Viktorsson C.
      • Nystrom P.
      • Falck-Ytter T.
      • Hessels R.S.
      Eye tracking in human interaction: Possibilities and limitations.
      ).

      SOCIAL ATTENTION: THE CANDIDATES

      Orienting to faces and preference for social information
      Frequently, the term SA is used when describing how individuals distribute their gaze to social versus non-social stimuli. Given our focus on early development in ASD, we have selected looking to faces, eyes, and mouths, but there are other examples of stimuli that belong to this category, including preferential looking to biological motion (for which the link to ASD below age 2 years is largely unexplored, see references 3, 18, 19) and the actions of others (
      • Shic F.
      • Bradshaw J.
      • Klin A.
      • Scassellati B.
      • Chawarska K.
      Limited activity monitoring in toddlers with autism spectrum disorder.
      ).

      Candidate 1: Basic orienting to face-like patterns

      There is a robust body of evidence demonstrating a fast capture of attention by face-like patterns (Figure 3a) at birth and throughout the lifespan (e.g., (
      • Morton J.
      • Johnson M.H.
      CONSPEC and CONLERN: a two-process theory of infant face recognition.
      ,
      • Farroni T.
      • Johnson M.H.
      • Menon E.
      • Zulian L.
      • Faraguna D.
      • Csibra G.
      Newborns' preference for face-relevant stimuli: Effects of contrast polarity.
      ,
      • Shah P.
      • Gaule A.
      • Bird G.
      • Cook R.
      Robust orienting to protofacial stimuli in autism.
      ,
      • Hirai M.
      • Muramatsu Y.
      • Nakamura M.
      Developmental changes in orienting towards faces: A behavioral and eye-tracking study.
      ,

      Johnson M, Morton J (1991): Biology and Cognitive Development: The Case of Face Recognition. Oxford: Blackwell.

      )). Such face orienting is reflexive and exogenously driven (
      • Shah P.
      • Gaule A.
      • Bird G.
      • Cook R.
      Robust orienting to protofacial stimuli in autism.
      ,
      • Hirai M.
      • Muramatsu Y.
      • Nakamura M.
      Developmental changes in orienting towards faces: A behavioral and eye-tracking study.
      ) and is thought to have a canalizing role in cortical specialization and perceptual narrowing (
      • Amso D.
      • Scerif G.
      The attentive brain: insights from developmental cognitive neuroscience.
      ,
      • Reynolds G.D.
      • Roth K.C.
      The development of attentional biases for faces in infancy: A developmental systems perspective.
      ,
      • Johnson M.H.
      • Senju A.
      • Tomalski P.
      The two-process theory of face processing: modifications based on two decades of data from infants and adults.
      ,
      • Simion F.
      • Giorgio E.D.
      Face perception and processing in early infancy: inborn predispositions and developmental changes.
      ).
      Figure thumbnail gr3
      Figure 3The many faces of Social Attention A) Human newborns prefer to look at stimuli with patterns resembling the basic configuration of high-contrast areas of a face (left). Whether newborns with later ASD display similar attentional patterns is not yet known. B) Responding to and initiating joint attention, assessed in a live eye tracking paradigm (reproduced from (
      • Nystrom P.
      • Thorup E.
      • Bolte S.
      • Falck-Ytter T.
      Joint Attention in Infancy and the Emergence of Autism.
      )). While children with ASD showed atypicalities in initiating joint attention (IJA), their tendency to follow gaze was like typical infant performance (Responding to joint attention; RJA). C) Predictive eye movements used in action observation. When observing a model moving objects to a container, 6-month-olds reactively track the moving object/hand. In contrast, 12-month-olds and adults, who are able to perform such actions themselves, use goal-directed predictive eye movements, which is believed to tax their own motor system and representations of similar actions (
      • Elsner C.
      • D'Ausilio A.
      • Gredeback G.
      • Falck-Ytter T.
      • Fadiga L.
      The motor cortex is causally related to predictive eye movements during action observation.
      ). The colored lines show the direction of eye movements when leaving the object area (right) and entering the goal area (left), respectively, illustrating the striking similarity between 12-month-olds and adults, who do not follow the moving hand/object, but move gaze towards the goal area (bucket). Most data indicate that this basic predictive ability is intact in children with ASD (
      • Falck-Ytter T.
      Young children with autism spectrum disorder use predictive eye movements in action observation.
      ). Data are replotted based on ref (
      • Falck-Ytter T.
      • Gredebäck G.
      • von Hofsten C.
      Infants predict other people's action goals.
      ). D) Attending to complex and dynamic social scenes involving a non-verbal video-recorded interaction between two children. In the video, the girl refuses to give the object to the boy, despite his request. The top row shows the full stimuli, and the bottom row shows how typically developing 6-year-olds tend to attend to this scene. The final frame (D3) illustrates how virtually all typically developing children quickly moved their gaze to the face of the girl after the boy’s (neglected) request. The tendency to do so was significantly weaker in ASD (AUC>.85; reproduced and adapted from ref (
      • Falck-Ytter T.
      • von Hofsten C.
      • Gillberg C.
      • Fernell E.
      Visualization and Analysis of Eye Movement Data from Children with Typical and Atypical Development.
      )). This result indicates that analyses that take the timing of gaze shifts into account may provide insights that are not captured by aggregated looking time measures.
      It has been argued that newborn face orienting is the product of a domain-general process based on low-level stimulus characteristics (e.g., (
      • Reynolds G.D.
      • Roth K.C.
      The development of attentional biases for faces in infancy: A developmental systems perspective.
      ,
      • Nelson C.A.
      The development and neural bases of face recognition.
      ,
      • Simion F.
      • Macchi Cassia V.
      • Turati C.
      • Valenza E.
      The origins of face perception: specific versus non‐specific mechanisms.
      ,
      • Wilkinson N.
      • Paikan A.
      • Gredebäck G.
      • Rea F.
      • Metta G.
      Staring us in the face? An embodied theory of innate face preference.
      ,
      • Guillon Q.
      • Rogé B.
      • Afzali M.H.
      • Baduel S.
      • Kruck J.
      • Hadjikhani N.
      Intact perception but abnormal orientation towards face-like objects in young children with ASD.
      ,
      • Turati C.
      Why faces are not special to newborns: An alternative account of the face preference.
      )), yet, the prevailing view is that it represents a domain-specific social bias (e.g., (
      • Johnson M.H.
      • Senju A.
      • Tomalski P.
      The two-process theory of face processing: modifications based on two decades of data from infants and adults.
      ,
      • Farroni T.
      • Menon E.
      • Johnson M.H.
      Factors influencing newborns’ preference for faces with eye contact.
      ) hypothesized to be generated by a subcortical processing route including the superior colliculus, pulvinar, and amygdala complex (
      • Johnson M.H.
      • Senju A.
      • Tomalski P.
      The two-process theory of face processing: modifications based on two decades of data from infants and adults.
      ). The existence of a specialized and very early emerging face orienting mechanism is supported by one report of preferential head turns to face-like stimuli in fetuses during the third trimester (
      • Reid V.M.
      • Dunn K.
      • Young R.J.
      • Amu J.
      • Donovan T.
      • Reissland N.
      The human fetus preferentially engages with face-like visual stimuli.
      ) and a recent finding that newborn brain responses to face-like patterns recruit an adult-like face-specific cortical circuit (
      • Buiatti M.
      • Di Giorgio E.
      • Piazza M.
      • Polloni C.
      • Menna G.
      • Taddei F.
      • et al.
      Cortical route for facelike pattern processing in human newborns.
      ).
      Available evidence suggests that this basic face bias is no different in infants with a later ASD diagnosis (
      • Elsabbagh M.
      • Gliga T.
      • Pickles A.
      • Hudry K.
      • Charman T.
      • Johnson M.H.
      • et al.
      The development of face orienting mechanisms in infants at-risk for autism.
      ) or in autistic adult individuals (
      • Shah P.
      • Gaule A.
      • Bird G.
      • Cook R.
      Robust orienting to protofacial stimuli in autism.
      ), although one study found that it was decreased in preschoolers with ASD (
      • Falck-Ytter T.
      • Nyström P.
      • Gredebäck G.
      • Gliga T.
      • Bölte S.
      • the Et
      Reduced orienting to audiovisual synchrony in infancy predicts autism diagnosis at 3 years of age.
      ). In the infant study, Elsabbagh and colleagues (
      • Elsabbagh M.
      • Gliga T.
      • Pickles A.
      • Hudry K.
      • Charman T.
      • Johnson M.H.
      • et al.
      The development of face orienting mechanisms in infants at-risk for autism.
      ) measured 6-10 month-old infants’ tendency to orient to faces among non-face distractors presented on a computer screen. All groups, including infants who later met the criteria for an ASD diagnosis, tended to move their gaze to faces on about 50% of trials, high above the level expected by random gaze allocation (20%). Notably, no study has examined whether face orienting is typical in newborns with later ASD.

      Candidate 2: Preferential looking to naturalistic faces in more complex visual displays

      From around 4-6 months of age, infants’ sustained face preference also reflects top-down control (
      • Elsabbagh M.
      • Gliga T.
      • Pickles A.
      • Hudry K.
      • Charman T.
      • Johnson M.H.
      • et al.
      The development of face orienting mechanisms in infants at-risk for autism.
      ,
      • Di Giorgio E.
      • Turati C.
      • Altoè G.
      • Simion F.
      Face detection in complex visual displays: An eye-tracking study with 3-and 6-month-old infants and adults.
      ,
      • Gliga T.
      • Elsabbagh M.
      • Andravizou A.
      • Johnson M.
      Faces attract infants' attention in complex displays.
      ,
      • Frank M.C.
      • Vul E.
      • Johnson S.P.
      Development of infants’ attention to faces during the first year.
      ). Thus, older infants’ face preference and consequential emerging face expertise are the products of both unique SA orienting biases, and multiple other attentional and executive abilities (
      • Johnson M.H.
      • Senju A.
      • Tomalski P.
      The two-process theory of face processing: modifications based on two decades of data from infants and adults.
      ,
      • Nelson C.A.
      The development and neural bases of face recognition.
      ,
      • Simion F.
      • Macchi Cassia V.
      • Turati C.
      • Valenza E.
      The origins of face perception: specific versus non‐specific mechanisms.
      ,

      Johnson MH, Karmiloff-Smith A (2004): Perspectives on Infant Development. Theories of infant development.121.

      ). Face preference (when in competition with non-social objects) has a substantial contribution from genetic factors already at 5 months (heritability of .46, (

      Portugal AM, Viktorsson C, Taylor M, Mason L, Tammimies K, Ronald A, et al. (in preparation): Infants’ looking preferences for social versus non-social objects reflect genetic variation and are linked to later language development. OSF Preprints

      )), implying that infants select social versus non-social input partly due to their genetic predispositions (
      • Kennedy D.P.
      • D’Onofrio B.M.
      • Quinn P.D.
      • Bölte S.
      • Lichtenstein P.
      • Falck-Ytter T.
      Genetic Influence on Eye Movements to Complex Scenes at Short Timescales.
      ).
      Looking at non-facial body parts and non-social objects and events represents adaptive behaviors that are expected to dominate in certain age periods (
      • Falck-Ytter T.
      • Nyström P.
      • Gredebäck G.
      • Gliga T.
      • Bölte S.
      • the Et
      Reduced orienting to audiovisual synchrony in infancy predicts autism diagnosis at 3 years of age.
      ,

      Bertenthal BI, Boyer TW (2015): The development of social attention in human infants. The many faces of social attention: Springer, pp 21-65.

      ). This complexity may explain the mixed findings with regards to face preference in ASD. Some studies have shown that infants and toddlers later diagnosed with ASD look longer at faces than control groups (
      • Elsabbagh M.
      • Gliga T.
      • Pickles A.
      • Hudry K.
      • Charman T.
      • Johnson M.H.
      • et al.
      The development of face orienting mechanisms in infants at-risk for autism.
      ,
      • Webb S.J.
      • Jones E.J.
      • Merkle K.
      • Namkung J.
      • Toth K.
      • Greenson J.
      • et al.
      Toddlers with elevated autism symptoms show slowed habituation to faces.
      ,
      • Hendry A.
      • Jones E.J.
      • Bedford R.
      • Gliga T.
      • Charman T.
      • Johnson M.H.
      Developmental change in look durations predicts later effortful control in toddlers at familial risk for ASD.
      ), hypothesizing that this indicates slower maturation of attention control in ASD. Other studies based on screen-based eye tracking and video recordings from homes (
      • Chawarska K.
      • Macari S.
      • Shic F.
      Decreased Spontaneous Attention to Social Scenes in 6-Month-Old Infants Later Diagnosed with Autism Spectrum Disorders.
      ,
      • Saint-Georges C.
      • Cassel R.S.
      • Cohen D.
      • Chetouani M.
      • Laznik M.-C.
      • Maestro S.
      • et al.
      What studies of family home movies can teach us about autistic infants: A literature review.
      ) have suggested shorter looking time to faces in the first two years of life in infants with later ASD, while a recent live eye tracking study found no clear group differences in terms of face preference (
      • Nystrom P.
      • Thorup E.
      • Bolte S.
      • Falck-Ytter T.
      Joint Attention in Infancy and the Emergence of Autism.
      ).

      Candidate 3: Preference for specific facial parts (eyes and mouth)

      A bias to attend to faces with direct as compared to averted gaze is seen already shortly after
      birth (
      • Farroni T.
      • Johnson M.H.
      • Menon E.
      • Zulian L.
      • Faraguna D.
      • Csibra G.
      Newborns' preference for face-relevant stimuli: Effects of contrast polarity.
      ), and preferential looking to the eyes over other facial features is seen throughout the first half of the first year (
      • Oakes L.M.
      • Ellis A.E.
      An eye‐tracking investigation of developmental changes in infants’ exploration of upright and inverted human faces.
      ,
      • Lewkowicz D.J.
      • Hansen-Tift A.M.
      Infants deploy selective attention to the mouth of a talking face when learning speech.
      ,

      Viktorsson C, Portugal AM, Li D, Rudling M, Tammimies K, Taylor M, et al. (2021): Infants’ attention to eyes is an independent, heritable trait predicting later verbal competence.

      ). Neurophysiological responses from infants elicited during the earliest time stages of visual attention which are sensitive to the presence of whole faces are equally, or even more strongly, elicited by images of eyes alone or among non-social objects (
      • Itier R.J.
      • Batty M.
      Neural bases of eye and gaze processing: the core of social cognition.
      ,
      • Hoehl S.
      How do neural responses to eyes contribute to face-sensitive ERP components in young infants? A rapid repetition study.
      ). While these results demonstrate that eyes are prioritized during visual processing, it is not clear whether this effect is driven by unique attentional mechanisms underlying attention to eyes rather than orienting to faces per se (i.e., Candidate 1).
      Towards the end of their first year, when infants are in an intense phase of language learning, they tend to increase their looking to the mouth (vs. eyes), which provides rich audio-visual speech information (
      • Oakes L.M.
      • Ellis A.E.
      An eye‐tracking investigation of developmental changes in infants’ exploration of upright and inverted human faces.
      ,
      • Lewkowicz D.J.
      • Hansen-Tift A.M.
      Infants deploy selective attention to the mouth of a talking face when learning speech.
      ,
      • Tenenbaum E.J.
      • Shah R.J.
      • Sobel D.M.
      • Malle B.F.
      • Morgan J.L.
      Increased focus on the mouth among infants in the first year of life: A longitudinal eye-tracking study.
      ,
      • Hillairet de Boisferon A.
      • Tift A.H.
      • Minar N.J.
      • Lewkowicz D.J.
      Selective attention to a talker's mouth in infancy: role of audiovisual temporal synchrony and linguistic experience.
      ). During the second year of life, when infants have gained some native language experience and narrowed their perceptual expertise, their preference for eyes increases again. Individual differences in mouth (vs. eyes) preference are substantial, and recent twin data suggest that this variability has a moderate-to-high contribution from genetic influences at 5 months (

      Viktorsson C, Portugal AM, Li D, Rudling M, Tammimies K, Taylor M, et al. (2021): Infants’ attention to eyes is an independent, heritable trait predicting later verbal competence.

      ) and at 21 months (

      Constantino JN, Kennon-McGill S, Weichselbaum C, Marrus N, Haider A, Glowinski AL, et al. (2017): Infant viewing of social scenes is under genetic control and is atypical in autism. Nature. 547:nature22999.

      ).
      Regarding infants with later ASD, results are mixed, probably reflecting age differences as well as other study-specific factors (
      • Chawarska K.
      • Macari S.
      • Shic F.
      Decreased Spontaneous Attention to Social Scenes in 6-Month-Old Infants Later Diagnosed with Autism Spectrum Disorders.
      ,
      • Jones W.
      • Klin A.
      Attention to eyes is present but in decline in 2-6-month-old infants later diagnosed with autism.
      ). A small effect of decreased looking to the mouth has been found in a meta-analysis of attention in children with diagnosed ASD (
      • Chita-Tegmark M.
      Social attention in ASD: A review and meta-analysis of eye-tracking studies.
      ). Eye versus mouth looking has not been evaluated in an ecologically valid context in infants at elevated likelihood for ASD (but see ref (
      • Falck-Ytter T.
      • Carlström C.
      • Johansson M.
      Eye Contact Modulates Cognitive Processing Differently in Children With Autism.
      ) for a study of school aged children).

      Phenotypes linked to Joint Attention

      Joint attention refers to the triadic sharing of attention between two individuals towards a common object or event (
      • Bruner J.S.
      From communication to language—A psychological perspective.
      ,
      • Scaife M.
      • Bruner J.S.
      The capacity for joint visual attention in the infant.
      ). Here we review three SA candidates of increasing complexity linked to this concept.

      Candidate 4: Gaze cueing

      Gaze cueing refers to the tendency to orient faster to peripheral stimuli appearing in locations previously cued by other people’s eyes. Gaze cueing is present across the lifespan (including in newborns) (
      • Friesen C.K.
      • Kingstone A.
      The eyes have it! Reflexive orienting is triggered by nonpredictive gaze.
      ,
      • Ristic J.
      • Friesen C.K.
      • Kingstone A.
      Are eyes special? It depends on how you look at it.
      ,
      • Farroni T.
      • Johnson M.H.
      • Brockbank M.
      • Simion F.
      Infants' use of gaze direction to cue attention: The importance of perceived motion.
      ,
      • Farroni T.
      • Massaccesi S.
      • Pividori D.
      • Johnson M.H.
      Gaze following in newborns.
      ) and is typically seen as an exogenous form of attention cueing subserved by activity in the anterior superior temporal sulcus (STS; (
      • Calder A.J.
      • Beaver J.D.
      • Winston J.S.
      • Dolan R.J.
      • Jenkins R.
      • Eger E.
      • et al.
      Separate coding of different gaze directions in the superior temporal sulcus and inferior parietal lobule.
      )). Gaze cueing has been suggested to indicate the presence of a specific sensitivity to spatial information conveyed by eyes (
      • Friesen C.K.
      • Kingstone A.
      The eyes have it! Reflexive orienting is triggered by nonpredictive gaze.
      ). This view was challenged by the finding that arrows produce a similar cueing effect (
      • Tipples J.
      Eye gaze is not unique: Automatic orienting in response to uninformative arrows.
      ). However, later studies have indicated that attention cued by gaze is more strongly reflexive (and less amenable to top-down processes) than attention cued by arrows (
      • Friesen C.K.
      • Ristic J.
      • Kingstone A.
      Attentional effects of counterpredictive gaze and arrow cues.
      ,
      • Langdon R.
      • Smith P.
      Spatial cueing by social versus nonsocial directional signals.
      ,
      • Ristic J.
      • Wright A.
      • Kingstone A.
      Attentional control and reflexive orienting to gaze and arrow cues.
      ), thus supporting the hypothesis of eye gaze having a special status compared to non-biological cues, and potentially being supported by a distinct neural network (
      • Hietanen J.K.
      • Leppanen J.M.
      • Peltola M.J.
      • Linna-Aho K.
      • Ruuhiala H.J.
      Seeing direct and averted gaze activates the approach-avoidance motivational brain systems.
      ).
      To our knowledge, gaze cueing in infants who later receive an ASD diagnosis has not yet been investigated. In children with a confirmed ASD diagnosis, results are mixed (
      • Kylliäinen A.
      • Hietanen J.K.
      Attention orienting by another's gaze direction in children with autism.
      ,
      • Rombough A.
      • Iarocci G.
      Orienting in response to gaze and the social use of gaze among children with autism spectrum disorder.
      ,
      • Gillespie-Lynch K.
      • Elias R.
      • Escudero P.
      • Hutman T.
      • Johnson S.P.
      Atypical gaze following in autism: A comparison of three potential mechanisms.
      ,
      • Goldberg M.C.
      • Mostow A.J.
      • Vecera S.P.
      • Larson J.C.G.
      • Mostofsky S.H.
      • Mahone E.M.
      • et al.
      Evidence for impairments in using static line drawings of eye gaze cues to orient visual-spatial attention in children with high functioning autism.
      ,
      • Pruett J.R.
      • LaMacchia A.
      • Hoertel S.
      • Squire E.
      • McVey K.
      • Todd R.D.
      • et al.
      Social and non-social cueing of visuospatial attention in autism and typical development.
      ,
      • Swettenham J.
      • Condie S.
      • Campbell R.
      • Milne E.
      • Coleman M.
      Does the perception of moving eyes trigger reflexive visual orienting in autism?.
      ,
      • Johnson M.H.
      • Griffin R.
      • Csibra G.
      • Halit H.
      • Farroni T.
      • De Haan M.
      • et al.
      The emergence of the social brain network: Evidence from typical and atypical development.
      ). Senju et al. (
      • Senju A.
      • Tojo Y.
      • Dairoku H.
      • Hasegawa T.
      Reflexive orienting in response to eye gaze and an arrow in children with and without autism.
      ) and Chawarska et al. (
      • Chawarska K.
      • Klin A.
      • Volkmar F.
      Automatic attention cueing through eye movement in 2-year-old children with autism.
      ) both found typical gaze cuing in autistic children, but reported more subtle differences between these children and typically developing controls in terms of their responses to gaze cues vs. non-biological cues (e.g. arrows). This may reflect dissociable underlying processes (
      • Nation K.
      • Penny S.
      Sensitivity to eye gaze in autism: Is it normal? Is it automatic? Is it social?.
      ), a view supported by a functional magnetic resonance imaging study (
      • Greene D.J.
      • Colich N.
      • Iacoboni M.
      • Zaidel E.
      • Bookheimer S.Y.
      • Dapretto M.
      Atypical neural networks for social orienting in autism spectrum disorders.
      ).

      Candidate 5: Gaze following

      Gaze following refers to the tendency to respond to changes in others’ gaze by looking in the same direction. In contrast to gaze cueing, gaze following is not exogenously triggered by changes in peripheral stimulation. Gaze following emerges around 3-4 months (
      • D'Entremont B.
      • Hains S.M.
      • Muir D.W.
      A demonstration of gaze following in 3-to 6-month-olds.
      ), coinciding with a period of intense development of cortical control over eye movements (
      • Klin A.
      • Shultz S.
      • Jones W.
      Social visual engagement in infants and toddlers with autism: early developmental transitions and a model of pathogenesis.
      ). Gaze following then gradually becomes faster (
      • Gredebäck G.
      • Fikke L.
      • Melinder A.
      The development of joint visual attention: a longitudinal study of gaze following during interactions with mothers and strangers.
      ) and more accurate (
      • Nystrom P.
      • Thorup E.
      • Bolte S.
      • Falck-Ytter T.
      Joint Attention in Infancy and the Emergence of Autism.
      ) during infancy and early childhood. Gaze following plays an important role in language development and learning (
      • Baldwin D.A.
      INFANTS CONTRIBUTION TO THE ACHIEVEMENT OF JOINT REFERENCE.
      ,
      • Beuker K.T.
      • Rommelse N.N.
      • Donders R.
      • Buitelaar J.K.
      Development of early communication skills in the first two years of life.
      ,
      • Van Hecke A.V.
      • Mundy P.
      • Block J.J.
      • Delgado C.E.
      • Parlade M.V.
      • Pomares Y.B.
      • et al.
      Infant responding to joint attention, executive processes, and self-regulation in preschool children.
      ). In adulthood, gaze following is associated with activity in several areas of the medial prefrontal cortex as well as the right posterior temporal sulcus (
      • Caruana N.
      • Brock J.
      • Woolgar A.
      A frontotemporoparietal network common to initiating and responding to joint attention bids.
      ,
      • Redcay E.
      • Kleiner M.
      • Saxe R.
      Look at this: the neural correlates of initiating and responding to bids for joint attention.
      ,
      • Schilbach L.
      • Wilms M.
      • Eickhoff S.B.
      • Romanzetti S.
      • Tepest R.
      • Bente G.
      Minds made for sharing: initiating joint attention recruits reward-related neurocircuitry.
      ). Gaze following in infancy is associated with partly similar brain activation patterns (
      • Elison J.T.
      • Wolff J.J.
      • Heimer D.C.
      • Paterson S.J.
      • Gu H.
      • Hazlett H.C.
      • et al.
      Frontolimbic neural circuitry at 6 months predicts individual differences in joint attention at 9 months.
      ,
      • Grossmann T.
      • Johnson M.H.
      Selective prefrontal cortex responses to joint attention in early infancy.
      ).
      The ability to follow gaze reflects several processes, such as attention to eyes and faces and the ability to disengage attention. It has been argued that gaze following in very young infants may rely on the perceived motion of the head or pupils (e.g. (
      • Farroni T.
      • Massaccesi S.
      • Pividori D.
      • Johnson M.H.
      Gaze following in newborns.
      ,

      Deák GO (2015): When and where do infants follow gaze? 2015 Joint IEEE international conference on development and learning and epigenetic robotics (ICDL-EpiRob): IEEE, pp 182-187.

      ), and that non-biological moving objects may evoke a similar response (
      • Deligianni F.
      • Senju A.
      • Gergely G.
      • Csibra G.
      Automated gaze-contingent objects elicit orientation following in 8-month-old infants.
      ). One recent study indicated that young infants’ gaze following is affected by both social cues (direction of looking) and non-social cues (general movement), but that gaze following comes to rely more on social cues with increasing age (
      • Astor K.
      • Thiele M.
      • Gredebäck G.
      Gaze following emergence relies on both perceptual cues and social awareness.
      ).
      Live observational studies of gaze following early in life in ASD tend to find group differences (
      • Chiang C.-H.
      • Soong W.-T.
      • Lin T.-L.
      • Rogers S.J.
      Nonverbal communication skills in young children with autism.
      ,
      • Dawson G.
      • Toth K.
      • Abbott R.
      • Osterling J.
      • Munson J.
      • Estes A.
      • et al.
      Early social attention impairments in autism: social orienting, joint attention, and attention to distress.
      ,
      • Landa R.J.
      • Holman K.C.
      • Garrett-Mayer E.
      Social and communication development in toddlers with early and later diagnosis of autism spectrum disorders.
      ,
      • Rozga A.
      • Hutman T.
      • Young G.S.
      • Rogers S.J.
      • Ozonoff S.
      • Dapretto M.
      • et al.
      Behavioral profiles of affected and unaffected siblings of children with autism: Contribution of measures of mother–infant interaction and nonverbal communication.
      ), but these findings are not replicated in eye tracking studies using pre-recorded stimuli (
      • Akechi H.
      • Senju A.
      • Kikuchi Y.
      • Tojo Y.
      • Osanai H.
      • Hasegawa T.
      Do children with ASD use referential gaze to learn the name of an object? An eye-tracking study.
      ,
      • Falck-Ytter T.
      • Thorup E.
      • Bolte S.
      Brief report: Lack of processing bias for the objects other people attend to in 3-year-olds with autism.
      ,
      • Bedford R.
      • Elsabbagh M.
      • Gliga T.
      • Pickles A.
      • Senju A.
      • Charman T.
      Precursors to social and communication difficulties in infants at-risk for autism: gaze following and attentional engagement.
      ,
      • Parsons J.P.
      • Bedford R.
      • Jones E.J.
      • Charman T.
      • Johnson M.H.
      • Gliga T.
      Gaze following and attention to objects in infants at familial risk for ASD.
      ). This suggests that screen-based methods could fail to capture some important element of the interaction (
      • Stallworthy I.C.
      • Lasch C.
      • Berry D.
      • Wolff J.J.
      • Pruett Jr., J.R.
      • Marrus N.
      • et al.
      Variability in responding to joint attention cues in the first year is associated with autism outcome.
      ). However, using a live eye tracking approach (i.e., real interaction with another person; Figure 3B), Nyström et al. (
      • Nystrom P.
      • Thorup E.
      • Bolte S.
      • Falck-Ytter T.
      Joint Attention in Infancy and the Emergence of Autism.
      ) recently found that 10-month-old infants with later ASD were equally likely to follow gaze as infants without subsequent ASD. Thus, impaired gaze following per se does not stand out as a clear early marker of ASD.

      Candidate 6: Initiation of joint attention

      Infants’ gaze is not only an “information gathering device”. Because eye movements are visible to others, the use of gaze is also a key component of their non-verbal communication, e.g., with parents (
      • Kennedy D.P.
      • D’Onofrio B.M.
      • Quinn P.D.
      • Bölte S.
      • Lichtenstein P.
      • Falck-Ytter T.
      Genetic Influence on Eye Movements to Complex Scenes at Short Timescales.
      ,
      • Nystrom P.
      • Thorup E.
      • Bolte S.
      • Falck-Ytter T.
      Joint Attention in Infancy and the Emergence of Autism.
      ,

      Nasiopoulos E, Risko EF, Kingstone A (2015): Social attention, social presence, and the dual function of gaze. The many faces of social attention: Springer, pp 129-155.

      ). Towards the end of the first year, infants begin to use gaze behaviors that can initiate joint attention episodes with others (
      • Nystrom P.
      • Thorup E.
      • Bolte S.
      • Falck-Ytter T.
      Joint Attention in Infancy and the Emergence of Autism.
      ). Specifically, around 8-9 months of age, infants start looking back and forth between an object that has caught their attention and another person, a behavior referred to as alternating gaze (
      • Beuker K.T.
      • Rommelse N.N.
      • Donders R.
      • Buitelaar J.K.
      Development of early communication skills in the first two years of life.
      ). At 10-13 months, more overt behaviors, such as pointing, start to emerge (
      • Beuker K.T.
      • Rommelse N.N.
      • Donders R.
      • Buitelaar J.K.
      Development of early communication skills in the first two years of life.
      ,

      Carpenter M, Nagell K, Tomasello M, Butterworth G, Moore C (1998): Social cognition, joint attention, and communicative competence from 9 to 15 months of age. Monographs of the society for research in child development.i-174.

      ). Initiation of joint attention (at least in adulthood) specifically recruits reward-related brain areas linked to social motivation, such as the ventral striatum, suggesting involvement of top-down attentional control (
      • Schilbach L.
      • Wilms M.
      • Eickhoff S.B.
      • Romanzetti S.
      • Tepest R.
      • Bente G.
      Minds made for sharing: initiating joint attention recruits reward-related neurocircuitry.
      ). The same brain areas are not typically activated during more reactive gaze following.
      Children with ASD use gestures such as pointing and showing less than typically developing children (e.g. (
      • Chiang C.-H.
      • Soong W.-T.
      • Lin T.-L.
      • Rogers S.J.
      Nonverbal communication skills in young children with autism.
      )), and infants later diagnosed with ASD have been shown to engage less in alternating gaze than typically developing infants already at 8-10 months of age (
      • Nystrom P.
      • Thorup E.
      • Bolte S.
      • Falck-Ytter T.
      Joint Attention in Infancy and the Emergence of Autism.
      ,
      • Ibanez L.V.
      • Grantz C.J.
      • Messinger D.S.
      The development of referential communication and autism symptomatology in high‐risk infants.
      ). Compared to gaze following, impairment in initiation of joint attention in autistic children appears to be both more pronounced and longer-lasting (
      • Gotham K.
      • Risi S.
      • Pickles A.
      • Lord C.
      The autism diagnostic observation schedule: Revised algorithms for improved diagnostic validity.
      ).
      Attention during observation of other people’s manual actions
      Although gaze performance during action observation in part can be seen as a special case of preferential looking to social information (similar to preference for faces, above), evidence suggests that manual actions give rise to a special type of eye movements that deserve a separate discussion.

      Candidate 7: Predictive, goal-directed eye movements

      Real time, predictive eye movements to goals during action observation emerge towards the end of the first year in infancy (
      • Falck-Ytter T.
      • Gredebäck G.
      • von Hofsten C.
      Infants predict other people's action goals.
      ,
      • Rosander K.
      • von Hofsten C.
      Predictive gaze shifts elicited during observed and performed actions in 10-month-old infants and adults.
      ) (Figure 3C) and, at least in adults, depend on a somatotopic recruitment of the observer's motor system (
      • Elsner C.
      • D'Ausilio A.
      • Gredeback G.
      • Falck-Ytter T.
      • Fadiga L.
      The motor cortex is causally related to predictive eye movements during action observation.
      ). It is believed that observers recruit their own action plans during action observation to predict other people’s action goals (
      • Flanagan J.R.
      • Johansson R.S.
      Action plans used in action observation.
      ). According to one interpretation of the literature, this action mirroring is a highly automatic process (“direct matching”), not requiring top-down control (

      Csibra G (2007): Action mirroring and action interpretation: An alternative account. In: Haggard P, Rosetti Y, Kawato M, editors. Sensorimotor Foundations of Higher Cognition Attention and Performance XXII Oxford: Oxford University Press, pp 435-459.

      ,
      • Gredebäck G.
      • Falck-Ytter T.
      Eye movements during action observation.
      ). If correct, these eye movements may reflect low-level SA processes, triggered specifically by hand-object interactions. According to an alternative “re-enactment” view, motor recruitment happens after the observer has understood an agent’s intention (

      Csibra G (2007): Action mirroring and action interpretation: An alternative account. In: Haggard P, Rosetti Y, Kawato M, editors. Sensorimotor Foundations of Higher Cognition Attention and Performance XXII Oxford: Oxford University Press, pp 435-459.

      ). The latter view however, cannot explain why predictive eye movements are typically not observed when infants look at self-propelled objects moving towards target objects, even though they do attribute goals to such events (
      • Gredebäck G.
      • Falck-Ytter T.
      Eye movements during action observation.
      ). Although both predictive abilities in general and perception-action mirroring have been proposed to be atypical in ASD (
      • Iacoboni M.
      • Dapretto M.
      The mirror neuron system and the consequences of its dysfunction.
      ,
      • Van de Cruys S.
      • Evers K.
      • Van der Hallen R.
      • Van Eylen L.
      • Boets B.
      • de-Wit L.
      • et al.
      Precise minds in uncertain worlds: predictive coding in autism.
      ), the available data from young children and infants at elevated likelihood do not indicate substantial group differences, if any (
      • Falck-Ytter T.
      Young children with autism spectrum disorder use predictive eye movements in action observation.
      ,
      • Braukmann R.
      • Ward E.
      • Hessels R.S.
      • Bekkering H.
      • Buitelaar J.K.
      • Hunnius S.
      Action prediction in 10-month-old infants at high and low familial risk for Autism Spectrum Disorder.
      ,
      • Krogh‐Jespersen S.
      • Kaldy Z.
      • Valadez A.G.
      • Carter A.S.
      • Woodward A.L.
      Goal prediction in 2‐year‐old children with and without autism spectrum disorder: An eye‐tracking study.
      ). It appears as the distinction between live versus screen-based eye tracking is not crucial for this phenotype, as it is observable in both contexts in infancy and adulthood (
      • Falck-Ytter T.
      • Gredebäck G.
      • von Hofsten C.
      Infants predict other people's action goals.
      ,
      • Rosander K.
      • von Hofsten C.
      Predictive gaze shifts elicited during observed and performed actions in 10-month-old infants and adults.
      ,
      • Flanagan J.R.
      • Johansson R.S.
      Action plans used in action observation.
      ).

      DISCUSSION

      In the literature on basic attentional processes, careful experimentation over many years indicate that the underlying neural systems are anatomically separate from other information processing systems, and that multiple distinct attentional systems exist (
      • Petersen S.E.
      • Posner M.I.
      The Attention System of the Human Brain: 20 Years After.
      ). How SA fits into this picture has not been altogether clear. Our review indicates that for none of the SA candidates, there is unequivocal support for the involvement of unique socio-attentional processes (Hypothesis A in Introduction; Table 1). For example, there is no consensus in the field that joint attention behaviors such as gaze following and alternating gaze (Figure 3B), very often referred to as reflecting SA in the literature, involve distinct social attention processes in this sense. In fact, during joint attention, and when looking at complex social scenes more generally (e.g., Figure 3D), top-down influences (reflecting past experiences, social motivation, mentalizing and other forms of social cognition) are likely to play a major role in moment-to-moment gaze allocation. This may explain why visual saliency models (
      • Itti L.
      • Koch C.
      Computational modelling of visual attention.
      ) tend to fail to predict attention in such contexts (
      • Birmingham E.
      • Bischof W.F.
      • Kingstone A.
      Saliency does not account for fixations to eyes within social scenes.
      ). However, for some SA behaviors there is partial support for domain specificity and uniqueness at a mechanistic level. Prediction of other people’s action goals (Figure 3B) appears to reflect a unique (at both behavioral and brain levels (
      • Elsner C.
      • D'Ausilio A.
      • Gredeback G.
      • Falck-Ytter T.
      • Fadiga L.
      The motor cortex is causally related to predictive eye movements during action observation.
      )) process linked to perceptual selection and which requires social input to be triggered (
      • Falck-Ytter T.
      • Gredebäck G.
      • von Hofsten C.
      Infants predict other people's action goals.
      ,
      • Flanagan J.R.
      • Johansson R.S.
      Action plans used in action observation.
      ). Similarly, newborn orienting to face-like configurations (Figure 3A) is considered by many (but not all (
      • Reynolds G.D.
      • Roth K.C.
      The development of attentional biases for faces in infancy: A developmental systems perspective.
      ,
      • Nelson C.A.
      The development and neural bases of face recognition.
      ,
      • Simion F.
      • Macchi Cassia V.
      • Turati C.
      • Valenza E.
      The origins of face perception: specific versus non‐specific mechanisms.
      ,
      • Wilkinson N.
      • Paikan A.
      • Gredebäck G.
      • Rea F.
      • Metta G.
      Staring us in the face? An embodied theory of innate face preference.
      ,
      • Guillon Q.
      • Rogé B.
      • Afzali M.H.
      • Baduel S.
      • Kruck J.
      • Hadjikhani N.
      Intact perception but abnormal orientation towards face-like objects in young children with ASD.
      ,
      • Turati C.
      Why faces are not special to newborns: An alternative account of the face preference.
      )) to constitute a uniquely social attentional process operating early in life (
      • Johnson M.H.
      • Senju A.
      • Tomalski P.
      The two-process theory of face processing: modifications based on two decades of data from infants and adults.
      ,
      • Farroni T.
      • Menon E.
      • Johnson M.H.
      Factors influencing newborns’ preference for faces with eye contact.
      ).
      Table 1Overview of reviewed Social Attention phenotypes
      CandidateSupport for hypothesis A versus BAtypical in infants with later ASD?
      1) Basic orienting to face-like patternsLeaning ANo (but not yet studied in newborns)
      2) Preferential looking to naturalistic faces in more complex visual displaysLeaning BMixed findings
      3) Preference for specific facial parts (eyes and mouth)Leaning BMixed findings (age dependent)
      4) Gaze cueingInconclusiveNot yet studied in infancy
      5) Gaze followingInconclusiveMixed findings (methods dependent)
      6) Initiation of joint attentionLeaning BYes
      7) Predictive, goal-directed eye movementsLeaning ANo
      How fundamental are SA differences in the development of ASD? Currently, there is no evidence available to suggest that SA behaviors that may be considered “strong candidates” in a mechanistic sense, like action prediction (
      • Gredebäck G.
      • Falck-Ytter T.
      Eye movements during action observation.
      ) or orienting to faces (
      • Elsabbagh M.
      • Gliga T.
      • Pickles A.
      • Hudry K.
      • Charman T.
      • Johnson M.H.
      • et al.
      The development of face orienting mechanisms in infants at-risk for autism.
      ), are atypical in infants with emerging ASD. In fact, the relatively few studies that have reported evidence in support for atypical SA behaviors (other than initiation of joint attention; Candidate 6) during the first year of life in infants later diagnosed with ASD tend to have modest effect sizes or small sample sizes (
      • Chawarska K.
      • Macari S.
      • Shic F.
      Decreased Spontaneous Attention to Social Scenes in 6-Month-Old Infants Later Diagnosed with Autism Spectrum Disorders.
      ,
      • Jones W.
      • Klin A.
      Attention to eyes is present but in decline in 2-6-month-old infants later diagnosed with autism.
      ,
      • Macari S.
      • Milgramm A.
      • Reed J.
      • Shic F.
      • Powell K.K.
      • Macris D.
      • et al.
      Context-specific dyadic attention vulnerabilities during the first year in infants later developing autism spectrum disorder.
      ). However, it is worth noting that some SA behaviors, such as gaze cueing, orienting to biological motion, and orienting to faces, have not yet been probed in relation to ASD in the first months of life. That initiation of joint attention in infancy shows a relatively strong relation to later ASD could be consistent with the social motivation theory of ASD which states that interaction and communication impairments in ASD stem from a reduced intrinsic reward value of social interaction for autistic as compared to typically developing individuals (
      • Chevallier C.
      • Kohls G.
      • Troiani V.
      • Brodkin E.S.
      • Schultz R.T.
      The social motivation theory of autism.
      ). Although it is questionable if atypical gaze behaviors during social interaction in ASD reflect differences in domain specific attentional functions per se, they may still be important as they could potentially alter child-parent interaction dynamics and developmental trajectories.
      We have focused our review mainly on the question of whether specific SA behaviors reflect unique socio-attentional processes, i.e., distinct from general attention and from “non-attentional” processes such as social motivation and social cognition (Figure 2). An arguably more extreme interpretation of SA is that it is also unitary (
      • Salley B.
      • Colombo J.
      Conceptualizing social attention in developmental research.
      ). The wide range of behaviors referred to as SA (ranging from basic biases (present at or even before birth (
      • Reid V.M.
      • Dunn K.
      • Young R.J.
      • Amu J.
      • Donovan T.
      • Reissland N.
      The human fetus preferentially engages with face-like visual stimuli.
      )) to highly dynamic gaze behaviors (Figure 3)), their different developmental trajectories, and their differential links to ASD speak against strong claims of unity (but notably, a differential link to ASD for early versus later emerging SA behaviors does not per se exclude the possibility that SA is unitary, as it could be linked to the timing of gene expression in children with the condition). It is likely that correlations across different SA phenotypes would emerge due to them being similarly modulated by the social context in the same individual – e.g., via social motivation or general attention.
      Despite the above reservations regarding the SA category, one could argue that it is a useful umbrella term under which one can organize a set of related research questions. For example, some types of early SA phenotypes are associated with later social developmental outcomes (

      Portugal AM, Viktorsson C, Taylor M, Mason L, Tammimies K, Ronald A, et al. (in preparation): Infants’ looking preferences for social versus non-social objects reflect genetic variation and are linked to later language development. OSF Preprints

      ,
      • Nystrom P.
      • Thorup E.
      • Bolte S.
      • Falck-Ytter T.
      Joint Attention in Infancy and the Emergence of Autism.
      ), and thus important to study irrespective of the exact biological/psychological underpinnings. However, more conceptual and methodological clarity is needed for progress both at a basic and applied level. Studying looking at social objects and events with an eye tracker does not necessarily entail that what has been measured is best described as social attention.
      It is likely that differences in infants’ gaze behaviors in social settings partly reflect genetic differences in the population (

      Portugal AM, Viktorsson C, Taylor M, Mason L, Tammimies K, Ronald A, et al. (in preparation): Infants’ looking preferences for social versus non-social objects reflect genetic variation and are linked to later language development. OSF Preprints

      ,
      • Kennedy D.P.
      • D’Onofrio B.M.
      • Quinn P.D.
      • Bölte S.
      • Lichtenstein P.
      • Falck-Ytter T.
      Genetic Influence on Eye Movements to Complex Scenes at Short Timescales.
      ,

      Viktorsson C, Portugal AM, Li D, Rudling M, Tammimies K, Taylor M, et al. (2021): Infants’ attention to eyes is an independent, heritable trait predicting later verbal competence.

      ,

      Constantino JN, Kennon-McGill S, Weichselbaum C, Marrus N, Haider A, Glowinski AL, et al. (2017): Infant viewing of social scenes is under genetic control and is atypical in autism. Nature. 547:nature22999.

      ), meaning that selection of visual input to some extent is rooted in genetics (active gene-environment correlation). Further, because the eyes are visible to others’, these differences could in turn affect caregiver responses toward their offspring (evocative gene-environment interplay).
      Lately, interest in SA has spread to many other neurodevelopmental and child psychiatric disorders partly phenotypically overlapping with ASD, including social anxiety disorder (SAD) (
      • Chen J.
      • van den Bos E.
      • Westenberg P.M.
      A systematic review of visual avoidance of faces in socially anxious individuals: Influence of severity, type of social situation, and development.
      ,
      • Kleberg J.L.
      • Högström J.
      • Sundström K.
      • Frick A.
      • Serlachius E.
      Delayed gaze shifts away from others’ eyes in children and adolescents with social anxiety disorder.
      ), attention deficit/hyperactivity disorder (ADHD) (
      • Ioannou C.
      • Seernani D.
      • Stefanou M.E.
      • Riedel A.
      • van Elst L.T.
      • Smyrnis N.
      • et al.
      Comorbidity Matters: Social Visual Attention in a Comparative Study of Autism Spectrum Disorder, Attention-Deficit/Hyperactivity Disorder and Their Comorbidity.
      ), and even anorexia nervosa (
      • Kerr-Gaffney J.
      • Jones E.
      • Mason L.
      • Hayward H.
      • Murphy D.
      • Loth E.
      • et al.
      Social attention in anorexia nervosa and autism spectrum disorder: Role of social motivation.
      ). Behavioral inhibition (BI) is a temperamental precursor of social anxiety which can be detected already in infancy (
      • Tang A.
      • Crawford H.
      • Morales S.
      • Degnan K.A.
      • Pine D.S.
      • Fox N.A.
      Infant behavioral inhibition predicts personality and social outcomes three decades later.
      ). Longitudinal studies of SA behaviors in infants with BI could be informative about the role of emotional reactivity and regulation in relation to specific SA behaviors. Similarly, studies of different SA behaviors may compare developmental trajectories in infants with (later) autism versus ADHD (
      • Braithwaite E.K.
      • Gui A.
      • Jones E.J.
      Social attention: What is it, how can we measure it, and what can it tell us about autism and ADHD?.
      ), to understand the role of more general attentional atypicalities. Further, studying SA behaviors in disorders with a known genetic cause can inform us about the underlying biological mechanisms and hence potentially identify stratification markers for ASD. Infants with Fragile X syndrome look less at other’s faces than typically developing infants, mirroring the adult literature from the condition (
      • Black C.J.
      • Hogan A.L.
      • Smith K.D.
      • Roberts J.E.
      Early behavioral and physiological markers of social anxiety in infants with fragile X syndrome.
      ), and also seemingly consistent with the high prevalence of ASD in the condition (
      • McDuffie A.
      • Thurman A.J.
      • Hagerman R.J.
      • Abbeduto L.
      Symptoms of autism in males with fragile X syndrome: A comparison to nonsyndromic ASD using current ADI-R scores.
      ). In contrast, although between 70 and 90% of children with Smith-Magenis syndrome (SMS) have symptoms consistent with an ASD diagnosis (

      Laje G, Morse R, Richter W, Ball J, Pao M, Smith AC (2010): Autism spectrum features in Smith–Magenis syndrome. American journal of medical genetics part C: Seminars in medical genetics: Wiley Online Library, pp 456-462.

      ,
      • Nag H.E.
      • Nordgren A.
      • Anderlid B.-M.
      • Nærland T.
      Reversed gender ratio of autism spectrum disorder in Smith-Magenis syndrome.
      ) preliminary evidence suggests that SA is relatively spared in infants with SMS (
      • Wolters P.L.
      • Gropman A.L.
      • Martin S.C.
      • Smith M.R.
      • Hildenbrand H.L.
      • Brewer C.C.
      • et al.
      Neurodevelopment of children under 3 years of age with Smith-Magenis syndrome.
      ) and even enhanced at school-age (
      • Wilde L.
      • Silva D.
      • Oliver C.
      The nature of social preference and interactions in Smith–Magenis syndrome.
      ). Infants with Williams syndrome (whose personality later in life is often described as hyper-social) have atypically high levels of attention to faces (
      • Mervis C.B.
      • Morris C.A.
      • Klein-Tasman B.P.
      • Bertrand J.
      • Kwitny S.
      • Appelbaum L.G.
      • et al.
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      ).
      Ecologically valid studies of SA phenotypes have been mostly conducted in older individuals, but distinct processing during passive social observation versus reciprocal interaction could emerge early (
      • Redcay E.
      • Schilbach L.
      Using second-person neuroscience to elucidate the mechanisms of social interaction.
      ) (but see Candidate 7). As such, and as exemplified by the recent “live” joint attention eye-tracking study of Nyström et al (
      • Nystrom P.
      • Thorup E.
      • Bolte S.
      • Falck-Ytter T.
      Joint Attention in Infancy and the Emergence of Autism.
      ), more work needs to be done in order to characterize and validate SA behaviors (and potential atypicalities in ASD) in real life contexts early in life (

      Nasiopoulos E, Risko EF, Kingstone A (2015): Social attention, social presence, and the dual function of gaze. The many faces of social attention: Springer, pp 129-155.

      ). New analytic approaches which take into account the dynamic and bidirectional nature of everyday social stimuli and contexts may reveal more distinct underlying processes than aggregated looking time measures based on passive viewing (Figure 3C, D).
      Most studies aiming to measure SA have focused on visual attention. This has also been the focus in this review, but it is important that future research expands to include non-visual modalities. Experiments specifically addressing attention to social auditory cues in ASD early in life are few (but see (
      • Rudling M.
      • Nystrom P.
      • Bolte S.
      • Falck-Ytter T.
      Larger pupil dilation to nonsocial sounds in infants with subsequent autism diagnosis.
      ,
      • Čeponienė R.
      • Lepistö T.
      • Shestakova A.
      • Vanhala R.
      • Alku P.
      • Näätänen R.
      • et al.
      Speech–sound-selective auditory impairment in children with autism: they can perceive but do not attend.
      ) ).
      To comprehensively address the questions of SA domain specificity and unity from a developmental perspective, it would be important to collect multiple SA candidate measures together with carefully assessed contrast phenotypes longitudinally over time. Furthermore, studies which compare different types of attentional functions (e.g., orienting and disengagement of attention) during processing of social and non-social stimuli, beyond examining gaze allocation, are likely to provide more definitive answers that advance the field forward. It is important to keep in mind that although a phenotype may recruit a domain specific process at the group level, individual differences in this phenotype (or case control differences for ASD) may reflect other processes influencing the phenotype in question. In terms of intervention research for ASD, a better understanding of the nature of social attention atypicalities is needed in order to develop better support and intervention programs (
      • Green J.
      • Charman T.
      • Pickles A.
      • Wan M.W.
      • Elsabbagh M.
      • Slonims V.
      • et al.
      Parent-mediated intervention versus no intervention for infants at high risk of autism: a parallel, single-blind, randomised trial.
      ,
      • Walsh P.
      • Elsabbagh M.
      • Bolton P.
      • Singh I.
      In search of biomarkers for autism: scientific, social and ethical challenges.
      ). These will necessarily differ depending on whether atypicalities are reflected in social understanding, in social motivation or in lower-level attention (Figure 2). Relatedly, because gaze atypicalities may be adaptive responses to other, more fundamental information processing or motivational biases (
      • Johnson M.H.
      • Charman T.
      • Pickles A.
      • Jones E.J.
      Annual Research Review: Anterior Modifiers in the Emergence of Neurodevelopmental Disorders (AMEND)—a systems neuroscience approach to common developmental disorders.
      ), it is not self-evident that it is meaningful, or even ethical, to target such behaviors in intervention trials.

      FINANCIAL DISCLOSURES

      All authors report no biomedical financial interests or potential conflicts of interest.

      Uncited reference

      Puce A, Bertenthal BI (2015): The Many Faces of Social Attention: Behavioral and Neural Measures. Springer.

      ,
      • Mason L.
      • Shic F.
      • Falck-Ytter T.
      • Chakrabarti B.
      • Charman T.
      • Loth E.
      • et al.
      Preference for biological motion is reduced in ASD: implications for clinical trials and the search for biomarkers.
      ,
      • Jones E.J.H.
      • Gliga T.
      • Bedford R.
      • Charman T.
      • Johnson M.H.
      Developmental pathways to autism: a review of prospective studies of infants at risk.
      ,
      • Schultz R.T.
      Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area.
      ,
      • Johnson M.H.
      Subcortical face processing.
      ,
      • Dawson G.
      Early behavioral intervention, brain plasticity, and the prevention of autism spectrum disorder.
      .

      ACKNOWLEDGEMENTS

      We thank Kim Astor, Christine Fawcet and Gustaf Gredebäck for valuable comments on an earlier version of this manuscript. The work leading to these results was supported by grants from Riksbankens Jubileumsfond, Knut and Alice Wallenberg Foundation, and Innovative Medicines Initiative 2 Joint Undertaking under grant agreement No 777394. This Joint Undertaking receives support from the European Union’s Horizon 2020 research and innovation program and EFPIA and AUTISM SPEAKS, Autistica, SFARI. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

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