Social, reward, and attention brain networks are involved when online bids for joint attention are met with congruent versus incongruent responses

Joint attention (JA) is a cornerstone of adaptive human social functioning. Little functional magnetic resonance imaging (fMRI) research has examined, in interactive paradigms, neural activation underlying bids for JA, met with a congruent or an incongruent social response. We developed a highly naturalistic fMRI paradigm utilizing eye-tracking to create real-time, contingent social responses to participant-initiated JA. During congruent responses to JA bids, we observed increased activation in the right amygdala, the right fusiform gyrus, anterior and dorsal anterior cingulate cortices, striatum, ventral tegmental area, and posterior parietal cortices. Incongruent responses to JA bids elicited increased activity localized to the right temporoparietal junction (TPJ) and bilateral cerebellum. No differences in eye-gaze patterns were observed during congruent or incongruent trials. Our results highlight the importance of utilizing interactive fMRI paradigms in social neuroscience and the impact of congruency in recruiting integrated social, reward, and attention circuits for processing JA.

[1]  Emery N. Brown,et al.  Distinct Regions of Right Temporo-Parietal Junction Are Selective for Theory of Mind and Exogenous Attention , 2009, PloS one.

[2]  Jason P. Mitchell Activity in right temporo-parietal junction is not selective for theory-of-mind. , 2008, Cerebral cortex.

[3]  Talma Hendler,et al.  Vase or face? A neural correlate of shape-selective grouping processes in the human brain , 2001, NeuroImage.

[4]  Timothy E. J. Behrens,et al.  Optimal decision making and the anterior cingulate cortex , 2006, Nature Neuroscience.

[5]  D. Perrett,et al.  A region of right posterior superior temporal sulcus responds to observed intentional actions , 2004, Neuropsychologia.

[6]  Susan Whitfield-Gabrieli,et al.  Brain regions for perceiving and reasoning about other people in school-aged children. , 2009, Child development.

[7]  Nadim Joni Shah,et al.  Minds Made for Sharing: Initiating Joint Attention Recruits Reward-related Neurocircuitry , 2010, Journal of Cognitive Neuroscience.

[8]  G. McCarthy,et al.  Neural basis of eye gaze processing deficits in autism. , 2005, Brain : a journal of neurology.

[9]  Rebecca Saxe,et al.  Live face-to-face interaction during fMRI: A new tool for social cognitive neuroscience , 2010, NeuroImage.

[10]  J. O'Doherty,et al.  Decoding the neural substrates of reward-related decision making with functional MRI , 2007, Proceedings of the National Academy of Sciences.

[11]  Joseph Piven,et al.  Journal of Neurodevelopmental Disorders is now a fully open access journal , 2012, Journal of Neurodevelopmental Disorders.

[12]  Penelope L. Mavros,et al.  Atypical brain activation patterns during a face‐to‐face joint attention game in adults with autism spectrum disorder , 2013, Human brain mapping.

[13]  K. Zilles,et al.  The neural correlates of person familiarity. A functional magnetic resonance imaging study with clinical implications. , 2001, Brain : a journal of neurology.

[14]  David M. Sobel,et al.  Action Understanding in the Superior Temporal Sulcus Region , 2009, Psychological science.

[15]  A. Mastergeorge,et al.  A parallel and distributed‐processing model of joint attention, social cognition and autism , 2009, Autism research : official journal of the International Society for Autism Research.

[16]  Talma Hendler,et al.  Vase or face? A neural correlate of shape-selective grouping processes in the human brain , 2001, NeuroImage.

[17]  R. Adolphs,et al.  Annals of the New York Academy of Sciences What Does the Amygdala Contribute to Social Cognition? , 2022 .

[18]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[19]  P. Frankland,et al.  Shifting to Automatic , 2010, Front. Integr. Neurosci..

[20]  S. Gallagher Direct perception in the intersubjective context , 2008, Consciousness and Cognition.

[21]  G. Fink,et al.  Being with virtual others: Neural correlates of social interaction , 2006, Neuropsychologia.

[22]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[23]  Edward T. Bullmore,et al.  Specialization of right temporo-parietal junction for mentalizing and its relation to social impairments in autism , 2011, NeuroImage.

[24]  M. Roesch,et al.  Neural structures underlying set-shifting: Roles of medial prefrontal cortex and anterior cingulate cortex , 2013, Behavioural Brain Research.

[25]  T. Allison,et al.  Face-Specific Processing in the Human Fusiform Gyrus , 1997, Journal of Cognitive Neuroscience.

[26]  M. Tomasello Joint attention as social cognition. , 1995 .

[27]  Masamichi J. Hayashi,et al.  “Stay Tuned”: Inter-Individual Neural Synchronization During Mutual Gaze and Joint Attention , 2010, Front. Integr. Neurosci..

[28]  David I. Perrett,et al.  An fMRI study of joint attention experience , 2005, NeuroImage.

[29]  Kevin A. Pelphrey,et al.  Action representation in the superior temporal sulcus in children and adults: An fMRI study , 2012, Developmental Cognitive Neuroscience.

[30]  S. Haber,et al.  The Reward Circuit: Linking Primate Anatomy and Human Imaging , 2010, Neuropsychopharmacology.

[31]  C. Frith,et al.  Functional imaging of ‘theory of mind’ , 2003, Trends in Cognitive Sciences.

[32]  S. Kennerley,et al.  Contrasting reward signals in the orbitofrontal cortex and anterior cingulate cortex , 2011, Annals of the New York Academy of Sciences.

[33]  R. Schultz,et al.  Social ‘wanting’ dysfunction in autism: neurobiological underpinnings and treatment implications , 2012, Journal of Neurodevelopmental Disorders.

[34]  R Saxe,et al.  People thinking about thinking people The role of the temporo-parietal junction in “theory of mind” , 2003, NeuroImage.

[35]  J. Decety,et al.  The Role of the Right Temporoparietal Junction in Social Interaction: How Low-Level Computational Processes Contribute to Meta-Cognition , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[36]  S. Itakura,et al.  Origins of the Social Mind , 2008 .

[37]  P. Mundy Annotation: the neural basis of social impairments in autism: the role of the dorsal medial-frontal cortex and anterior cingulate system. , 2003, Journal of child psychology and psychiatry, and allied disciplines.

[38]  K. Berridge,et al.  Parsing reward , 2003, Trends in Neurosciences.

[39]  P. Mundy,et al.  CURRENT DIRECTIONS IN PSYCHOLOGICAL SCIENCE Attention, Joint Attention, and Social Cognition , 2022 .

[40]  R. Saxe,et al.  Look at this: the neural correlates of initiating and responding to bids for joint attention , 2012, Front. Hum. Neurosci..

[41]  W. Gehring,et al.  More attention must be paid: The neurobiology of attentional effort , 2006, Brain Research Reviews.

[42]  S. Zeki,et al.  The neural basis of romantic love , 2000, Neuroreport.

[43]  Mark H. Johnson,et al.  The eye contact effect: mechanisms and development , 2009, Trends in Cognitive Sciences.

[44]  R. Saxe,et al.  What gets the attention of the temporo-parietal junction? An fMRI investigation of attention and theory of mind , 2010, Neuropsychologia.

[45]  Tony Charman,et al.  Why is joint attention a pivotal skill in autism? , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[46]  M. Posner,et al.  The attention system of the human brain: 20 years after. , 2012, Annual review of neuroscience.

[47]  C. Moore,et al.  Joint attention : its origins and role in development , 1995 .

[48]  M. Tomasello,et al.  Understanding and sharing intentions: The origins of cultural cognition , 2005, Behavioral and Brain Sciences.

[49]  Rainer Goebel,et al.  Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: From single‐subject to cortically aligned group general linear model analysis and self‐organizing group independent component analysis , 2006, Human brain mapping.

[50]  M. Seghier,et al.  A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. , 2003, Brain : a journal of neurology.

[51]  Rebecca Saxe,et al.  The neural basis of belief encoding and integration in moral judgment , 2008, NeuroImage.