The social motivation theory of autism

doi:10.1016/j.tics.2012.02.007

Trends in Cognitive Sciences

Volume 16, Issue 4, April 2012, Pages 231-239

https://doi.org/10.1016/j.tics.2012.02.007 Get rights and content

The idea that social motivation deficits play a central role in Autism Spectrum Disorders (ASD) has recently gained increased interest. This constitutes a shift in autism research, which has traditionally focused more intensely on cognitive impairments, such as theory-of-mind deficits or executive dysfunction, and has granted comparatively less attention to motivational factors. This review delineates the concept of social motivation and capitalizes on recent findings in several research areas to provide an integrated account of social motivation at the behavioral, biological and evolutionary levels. We conclude that ASD can be construed as an extreme case of diminished social motivation and, as such, provides a powerful model to understand humans’ intrinsic drive to seek acceptance and avoid rejection.

Section snippets

Social motivation and social cognition: two competing accounts of autism

Over the past three decades, a number of theories have been put forward to account for the pervasive social impairments found in Autism Spectrum Disorders (ASD). Among the various attempts, the idea of a core deficit in social cognition (theory of mind, or ToM, in particular; see Glossary) has become one of the most prominent accounts of ASD. Concomitantly, the impact of motivational factors on the development of social skills and social cognition has received little attention. Recently,

Behavioral level

Behavioral manifestations of humans’ social interest are of at least three kinds: (i) objects with social importance are prioritized by attention; (ii) social interactions are rewarding; (iii) interpersonal behaviors are influenced by the desire to maintain and enhance relationships. We now review interdisciplinary evidence supportive of this three-tiered disposition.

Social orienting. In very much the same way that negative signals (e.g. threats) capture attention, potentially beneficial or

Behavioral level

Social motivation models of ASD posit that early-onset impairments in social attention set in motion developmental processes that ultimately deprive the child of adequate social learning experiences, and that the resulting imbalance in attending to social and non-social stimuli further disrupts social skill and social cognitive development 46, 47, 48. As discussed in detail below, recent evidence demonstrates that social orienting, social seeking and liking, and social maintaining are all

What is the scope of the social motivation theory?

Although many questions remain (Box 3), the research reviewed here suggests that the social motivation theory provides a credible framework to account for social impairments in ASD. However, by concentrating on social deficits, the social motivation account faces similar shortcomings as the ToM account. Unlike non-social accounts (e.g. executive dysfunction or weak central coherence), both of these social theories indeed fall short of explaining non-social deficits in ASD, such as repetitive

Concluding remarks

The social world summons our attention like no other domain: social signals are prioritized by attention, interactions are intrinsically rewarding, and social maintaining permeates interpersonal behaviors. Social motivation is subserved by dedicated biological mechanisms and can be seen as an evolutionary adaptation to humans’ highly collaborative environment: by enhancing attention to social information, by rewarding social interactions, and by promoting the desire to effectively maintain

Acknowledgments

This work was supported by the National Institute of Health NIMH R01MH073084 (R.T.S.) and R01MH080718 (E.S.B.), by the Robert Wood Johnson Foundation #66727 (R.T.S., G.K.), by the Pennsylvania Department of Health SAP # 4100042728 (R.T.S., C.C.) and 4100047863 (R.T.S., E.S.B.), and by a National Science Foundation Graduate Fellowship (V.T.). The authors wish to thank Nicolas Baumard, Francesca Happé and Hugo Mercier for stimulating discussion and debate on the ideas presented here.

Glossary

Audience effect: refers to the influence of the presence of a spectator on a subject's performance or decisions. This classic effect in social psychology has received robust experimental support. Behavioral economists have demonstrated that the presence of others enhances participants’ generosity in a range of games, such as the dictator game, the ultimatum game, and the public good game.
Overjustification effect: refers to the fact that extrinsic incentives, such as money, can undermine

References (107)

A. Senju et al.
The eye contact effect: mechanisms and development
Trends Cogn. Sci.
(2009)
T. Stein
Eye contact facilitates awareness of faces during interocular suppression
Cognition
(2011)
K.C. Berridge
Dissecting components of reward: ‘liking’, ‘wanting’, and learning
Curr. Opin. Pharmacol.
(2009)
E. Fehr et al.
Social neuroeconomics: the neural circuitry of social preferences
Trends Cogn. Sci.
(2007)
Y. Rekers
Children, but not chimpanzees, prefer to collaborate
Curr. Biol.
(2011)
R. Adolphs et al.
Role of the amygdala in processing visual social stimuli
Prog. Brain Res.
(2006)
J.T. Klein
Social attention and the brain
Curr. Biol.
(2009)
H. Ghashghaei
Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala
Neuroimage
(2007)
A. Schirmer
When vocal processing gets emotional: on the role of social orientation in relevance detection by the human amygdala
Neuroimage
(2008)
J.K. Rilling
Neural correlates of social cooperation and non-cooperation as a function of psychopathy
Biol. Psychiatry
(2007)

J.A. Bartz

Social effects of oxytocin in humans: context and person matter

Trends Cogn. Sci.

(2011)

V. Trezza

The pleasures of play: pharmacological insights into social reward mechanisms

Trends Pharmacol. Sci.

(2010)

R. Schultz

Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area

Int. J. Dev. Neurosci.

(2005)

D.M. Riby et al.

Viewing it differently: social scene perception in Williams syndrome and autism

Neuropsychologia

(2008)

M. Elsabbagh

Infant neural sensitivity to dynamic eye gaze is associated with later emerging autism

Curr. Biol.

(2012)

J. Bachevalier et al.

The orbitofrontal-amygdala circuit and self-regulation of social-emotional behavior in autism

Neurosci. Biobehav. Rev.

(2006)

C.L. Masten

An fMRI Investigation of responses to peer rejection in adolescents with Autism Spectrum Disorders

Dev. Cogn. Neurosci.

(2011)

S. Jacob

Association of the oxytocin receptor gene (OXTR) in Caucasian children and adolescents with autism

Neurosci. Lett.

(2007)

P. Mehzabin et al.

Self-assessed sexuality in young adults with High-Functioning Autism

Res. Autism Spectr. Dis.

(2011)

R. Baillargeon

False-belief understanding in infants

Trends Cogn. Sci.

(2010)

J.T. Cacioppo et al.

Perceived social isolation and cognition

Trends Cogn. Sci.

(2009)

S. Fletcher-Watson

Rapid detection of person information in a naturalistic scene

Perception

(2008)

Y. Kikuchi

Faces do not capture special attention in children with autism spectrum disorder: a change blindness study

Child Dev.

(2009)

T. Ro

Changing faces: a detection advantage in the flicker paradigm

Psychol. Sci.

(2001)

D.G. Purcell et al.

The face-detection effect: configuration enhances detection

Atten. Percept. Psychophys.

(1988)

T. Gliga

Faces attract infants’ attention in complex displays

Infancy

(2009)

O. Rosa Salva

The evolution of social orienting: evidence from chicks (gallus gallus) and human newborns

PLoS ONE

(2011)

Y. Jiang

Processing of invisible stimuli: advantage of upright faces and recognizable words in overcoming interocular suppression

Psychol. Sci.

(2007)

B.Y. Hayden

Economic principles motivating social attention in humans

Proc. R. Soc. B: Biol. Sci.

(2007)

S. Bowles

Policies designed for self-interested citizens may undermine ‘the moral sentiments’: evidence from economic experiments

Science

(2008)

F. Warneken et al.

Extrinsic rewards undermine altruistic tendencies in 20-month-olds

Dev. Psychol.

(2008)

M.R. Leary et al.

Belonging motivation: establishing, maintaining, and repairing relational value

C. Higgins

Influence tactics and work outcomes: a meta analysis

J. Organ. Behav.

(2003)

V. Talwar

White lie-telling in children for politeness purposes

Int. J. Behav. Dev.

(2007)

G. Fu et al.

Social grooming in the kindergarten: the emergence of flattery behavior

Dev. Sci.

(2007)

H. Ross

Shading the truth: self-serving biases in children's reports of sibling conflicts

Merrill-Palmer Q.

(2004)

J.L. Lakin

The chameleon effect as social glue: evidence for the evolutionary significance of nonconscious mimicry

J. Nonverbal Behav.

(2003)

T.L. Chartrand et al.

The chameleon effect: the perception–behavior link and social interaction

J. Pers. Soc. Psychol.

(1999)

J.L. Lakin et al.

Using nonconscious behavioral mimicry to create affiliation and rapport

Psychol. Sci.

(2003)

A. Lin

Social and monetary reward learning engage overlapping neural substrates

Soc. Cogn. Affect. Neurosci.

(2011)

G. Tabibnia et al.

Fairness and cooperation are rewarding

Ann. N. Y. Acad. Sci.

(2007)

K. Izuma

Processing of the incentive for social approval in the ventral striatum during charitable donation

J. Cogn. Neurosci.

(2010)

J. Rilling

Opposing BOLD responses to reciprocated and unreciprocated altruism in putative reward pathways

Neuroreport

(2004)

A.E. Guyer

Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety

Arch. Gen. Psychiatry

(2008)

D.P. Kennedy

Personal space regulation by the human amygdala

Nat. Neurosci.

(2009)

M.L. Spezio

Amygdala damage impairs eye contact during conversations with real people

J. Neurosci.

(2007)

J. Hornak

Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices

Brain

(2003)

Y. Takayanagi

Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice

Proc. Natl. Acad. Sci. U.S.A.

(2005)

M.E. Avale

Prefrontal nicotinic receptors control novel social interaction between mice

FASEB J.

(2011)

M. Tomasello

Human culture in evolutionary perspective

Adv. Cult. Psychol.

(2010)

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Trends in Cognitive Sciences

ReviewThe social motivation theory of autism

Section snippets

Social motivation and social cognition: two competing accounts of autism

Behavioral level

Behavioral level

What is the scope of the social motivation theory?

Concluding remarks

Acknowledgments

Glossary

Trends Cogn. Sci.

Cognition

Curr. Opin. Pharmacol.

Trends Cogn. Sci.

Curr. Biol.

Prog. Brain Res.

Curr. Biol.

Neuroimage

Neuroimage

Biol. Psychiatry

Trends Cogn. Sci.

Trends Pharmacol. Sci.

Int. J. Dev. Neurosci.

Neuropsychologia

Curr. Biol.

Neurosci. Biobehav. Rev.

Dev. Cogn. Neurosci.

Neurosci. Lett.

Res. Autism Spectr. Dis.

Trends Cogn. Sci.

Trends Cogn. Sci.

Rapid detection of person information in a naturalistic scene

Perception

Faces do not capture special attention in children with autism spectrum disorder: a change blindness study

Child Dev.

Changing faces: a detection advantage in the flicker paradigm

Psychol. Sci.

The face-detection effect: configuration enhances detection

Atten. Percept. Psychophys.

Faces attract infants’ attention in complex displays

Infancy

The evolution of social orienting: evidence from chicks (gallus gallus) and human newborns

PLoS ONE

Processing of invisible stimuli: advantage of upright faces and recognizable words in overcoming interocular suppression

Psychol. Sci.

Economic principles motivating social attention in humans

Proc. R. Soc. B: Biol. Sci.

Policies designed for self-interested citizens may undermine ‘the moral sentiments’: evidence from economic experiments

Science

Extrinsic rewards undermine altruistic tendencies in 20-month-olds

Dev. Psychol.

Belonging motivation: establishing, maintaining, and repairing relational value

Influence tactics and work outcomes: a meta analysis

J. Organ. Behav.

White lie-telling in children for politeness purposes

Int. J. Behav. Dev.

Social grooming in the kindergarten: the emergence of flattery behavior

Dev. Sci.

Shading the truth: self-serving biases in children's reports of sibling conflicts

Merrill-Palmer Q.

The chameleon effect as social glue: evidence for the evolutionary significance of nonconscious mimicry

J. Nonverbal Behav.

The chameleon effect: the perception–behavior link and social interaction

J. Pers. Soc. Psychol.

Using nonconscious behavioral mimicry to create affiliation and rapport

Psychol. Sci.

Social and monetary reward learning engage overlapping neural substrates

Soc. Cogn. Affect. Neurosci.

Fairness and cooperation are rewarding

Ann. N. Y. Acad. Sci.

Processing of the incentive for social approval in the ventral striatum during charitable donation

J. Cogn. Neurosci.

Opposing BOLD responses to reciprocated and unreciprocated altruism in putative reward pathways

Neuroreport

Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety

Arch. Gen. Psychiatry

Personal space regulation by the human amygdala

Nat. Neurosci.

Amygdala damage impairs eye contact during conversations with real people

J. Neurosci.

Review
The social motivation theory of autism