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Heritability of reflexive social attention triggered by eye gaze and walking direction: common and unique genetic underpinnings

Published online by Cambridge University Press:  04 March 2019

Li Wang Open the ORCID record for Li Wang [Opens in a new window] ,
Ying Wang ,
Qian Xu ,
Dong Liu ,
Haoyue Ji ,
Yiwen Yu ,
Zhaoqi Hu ,
Peijun Yuan  and
Yi Jiang
Li Wang
Affiliation:
State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Psychology, Chinese Academy of Sciences, 16 Lincui Road, Beijing100101, P. R. China Department of Psychology, University of Chinese Academy of Sciences, 19A Yuquan Road, Beijing100049, P. R. China
Ying Wang
Affiliation:
State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Psychology, Chinese Academy of Sciences, 16 Lincui Road, Beijing100101, P. R. China Department of Psychology, University of Chinese Academy of Sciences, 19A Yuquan Road, Beijing100049, P. R. China
Qian Xu
Affiliation:
State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Psychology, Chinese Academy of Sciences, 16 Lincui Road, Beijing100101, P. R. China Department of Psychology, University of Chinese Academy of Sciences, 19A Yuquan Road, Beijing100049, P. R. China
Dong Liu
Affiliation:
State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Psychology, Chinese Academy of Sciences, 16 Lincui Road, Beijing100101, P. R. China Department of Psychology, University of Chinese Academy of Sciences, 19A Yuquan Road, Beijing100049, P. R. China
Haoyue Ji
Affiliation:
State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Psychology, Chinese Academy of Sciences, 16 Lincui Road, Beijing100101, P. R. China Department of Psychology, University of Chinese Academy of Sciences, 19A Yuquan Road, Beijing100049, P. R. China
Yiwen Yu
Affiliation:
State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Psychology, Chinese Academy of Sciences, 16 Lincui Road, Beijing100101, P. R. China Department of Psychology, University of Chinese Academy of Sciences, 19A Yuquan Road, Beijing100049, P. R. China
Zhaoqi Hu
Affiliation:
State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Psychology, Chinese Academy of Sciences, 16 Lincui Road, Beijing100101, P. R. China Department of Psychology, University of Chinese Academy of Sciences, 19A Yuquan Road, Beijing100049, P. R. China
Peijun Yuan
Affiliation:
State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Psychology, Chinese Academy of Sciences, 16 Lincui Road, Beijing100101, P. R. China Department of Psychology, University of Chinese Academy of Sciences, 19A Yuquan Road, Beijing100049, P. R. China
Yi Jiang*
Affiliation:
State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Psychology, Chinese Academy of Sciences, 16 Lincui Road, Beijing100101, P. R. China Department of Psychology, University of Chinese Academy of Sciences, 19A Yuquan Road, Beijing100049, P. R. China
*
Author for correspondence: Yi Jiang, E-mail: [email protected]
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Abstract

Background

Social attention ability is crucial for human adaptive social behaviors and interpersonal communications, and the malfunction of which has been implicated in autism spectrum disorder (ASD), a highly genetic neurodevelopmental disorder marked by striking social deficits.

Methods

Using a classical twin design, the current study investigated the genetic contribution to individual variation in social and non-social attention abilities, and further probed their potential genetic linkage. Moreover, individual autistic traits were further measured in an independent group of non-twin participants to examine the hypothetical link between the core social attention ability and ASD.

Results

We found reliable genetic influences on the social attentional effects induced by two distinct cues (eye gaze and walking direction), with 91% of their covariance accounted for by common genetic effects. However, no evidence of heritability or shared genetic effects was observed for the attentional effect directed by a non-social cue (i.e. arrow direction) and its correlation with the social attention ability. Remarkably, one's autistic traits could well predict his/her heritable core social attention ability extracted from the conventional social attentional effect.

Conclusions

These findings together suggest that human social attention ability is supported by unique genetic mechanisms that can be shared across different social, but not non-social, processing. Moreover, they also encourage the identification of ‘social attention genes’ and highlight the critical role of the core human social attention ability in seeking the endophenotypes of social cognitive disorders including ASD.

Keywords

Behavioral geneticsbiological motioneye gazesocial cognitiontwin study
Type
Original Articles
Information
Psychological Medicine , Volume 50 , Issue 3 , February 2020 , pp. 475 - 483
Copyright
Copyright © Cambridge University Press 2019

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References

Bardi, L, Di Giorgio, E, Lunghi, M, Troje, NF and Simion, F (2015) Walking direction triggers visuo-spatial orienting in 6-month-old infants and adults: an eye tracking study. Cognition 141, 112–120.CrossRefGoogle Scholar
Baron-Cohen, S (1995) The eye direction detector (EDD) and the shared attention mechanism (SAM): two cases for evolutionary psychology. In Joint Attention: its Origins and Role in Development. Hillsdale, NJ: Erlbaum, pp. 41–59.Google Scholar
Baron-Cohen, S, Wheelwright, S, Skinner, R, Martin, J and Clubley, E (2001) The autism-spectrum quotient (AQ): evidence from asperger syndrome/high-functioning autism, malesand females, scientists and mathematicians. Journal of Autism and Developmental Disorders 31, 5–17.CrossRefGoogle Scholar
Bayliss, AP, di Pellegrino, G and Tipper, SP (2005) Sex differences in eye gaze and symbolic cueing of attention. The Quarterly Journal of Experimental Psychology Section A 58, 631–650.CrossRefGoogle Scholar
Birmingham, E and Kingstone, A (2009) Human social attention. Annals of the New York Academy of Sciences 1156, 118–140.CrossRefGoogle ScholarPubMed
Bruinsma, Y, Koegel, RL and Koegel, LK (2004) Joint attention and children with autism: a review of the literature. Mental Retardation and Developmental Disabilities Research Reviews 10, 169–175.CrossRefGoogle ScholarPubMed
Chen, J, Li, X, Zhang, J, Natsuaki, MN, Leve, LD, Harold, GT, Chen, Z, Yang, X, Guo, F and Zhang, J (2013) The Beijing Twin Study (BeTwiSt): a longitudinal study of child and adolescent development. Twin Research and Human Genetics 16, 91–97.CrossRefGoogle ScholarPubMed
Dawson, G, Bernier, R and Ring, RH (2012) Social attention: a possible early indicator of efficacy in autism clinical trials. Journal of Neurodevelopmental Disorders 4, 1–12.CrossRefGoogle ScholarPubMed
Deaner, RO and Platt, ML (2003) Reflexive social attention in monkeys and humans. Current Biology 13, 1609–1613.CrossRefGoogle ScholarPubMed
Driver, J, Davis, G, Ricciardelli, P, Kidd, P, Maxwell, E and Baron-Cohen, S (1999) Gaze perception triggers reflexive visuospatial orienting. Visual Cognition 6, 509–540.CrossRefGoogle Scholar
Ekman, P and Friesen, WV (1976) Pictures of facial affect. Consulting psychologists: Palo Alto, CA.Google Scholar
Engell, AD, Nummenmaa, L, Oosterhof, NN, Henson, RN, Haxby, JV and Calder, AJ (2010) Differential activation of frontoparietal attention networks by social and symbolic spatial cues. Social Cognitive and Affective Neuroscience 5, 432–440.CrossRefGoogle ScholarPubMed
Fan, J, Wu, Y, Fossella, JA and Posner, MI (2001) Assessing the heritability of attentional networks. BMC Neuroscience 2, 14.CrossRefGoogle ScholarPubMed
Farroni, T, Massaccesi, S, Pividori, D and Johnson, MH (2004) Gaze following in newborns. Infancy 5, 39–60.CrossRefGoogle Scholar
Feng, Q, Zheng, Y, Zhang, X, Song, Y, Luo, Y-j, Li, Y and Talhelm, T (2011) Gender differences in visual reflexive attention shifting: evidence from an ERP study. Brain Research 1401, 59–65.CrossRefGoogle ScholarPubMed
Friesen, CK and Kingstone, A (1998) The eyes have it! Reflexive orienting is triggered by nonpredictive gaze. Psychonomic Bulletin and Review 5, 490–495.CrossRefGoogle Scholar
Friesen, CK and Kingstone, A (2003) Abrupt onsets and gaze direction cues trigger independent reflexive attentional effects. Cognition 87, B1–B10.CrossRefGoogle ScholarPubMed
Friesen, CK, Ristic, J and Kingstone, A (2004) Attentional effects of counterpredictive gaze and arrow cues. Journal of Experimental Psychology: Human Perception and Performance 30, 319–329.Google ScholarPubMed
Frischen, A, Bayliss, AP and Tipper, SP (2007) Gaze cueing of attention: visual attention, social cognition, and individual differences. Psychological Bulletin 133, 694–724.CrossRefGoogle ScholarPubMed
Goldberg, MC, Mostow, AJ, Vecera, SP, Larson, JCG, Mostofsky, SH, Mahone, EM and Denckla, MB (2008) Evidence for impairments in using static line drawings of eye gaze cues to orient visual-spatial attention in children with high functioning autism. Journal of Autism and Developmental Disorders 38, 1405–1413.CrossRefGoogle ScholarPubMed
Hirai, M, Saunders, DR and Troje, NF (2011) Allocation of attention to biological motion: local motion dominates global shape. Journal of Vision 11, 1–11.CrossRefGoogle ScholarPubMed
Hood, BM, Willen, JD and Driver, J (1998) Adult's eyes trigger shifts of visual attention in human infants. Psychological Science 9, 131–134.CrossRefGoogle Scholar
Itier, RJ and Batty, M (2009) Neural bases of eye and gaze processing: the core of social cognition. Neuroscience & Biobehavioral Reviews 33, 843–863.CrossRefGoogle ScholarPubMed
Johnson, MH (2006) Biological motion: a perceptual life detector? Current Biology 16, R376–R377.CrossRefGoogle ScholarPubMed
Joseph, RM, Fricker, Z and Keehn, B (2015) Activation of frontoparietal attention networks by non-predictive gaze and arrow cues. Social Cognitive and Affective Neuroscience 10, 294–301.CrossRefGoogle ScholarPubMed
Kingstone, A, Tipper, C, Ristic, J and Ngan, E (2004) The eyes have it!: an fMRI investigation. Brain and Cognition 55, 269–271.CrossRefGoogle ScholarPubMed
Koster, EH, Leyman, L, De Raedt, R and Crombez, G (2006) Cueing of visual attention by emotional facial expressions: the influence of individual differences in anxiety and depression. Personality and Individual Differences 41, 329–339.CrossRefGoogle Scholar
Koster, EH, Crombez, G, Verschuere, B, Vanvolsem, P and De Houwer, J (2007) A time-course analysis of attentional cueing by threatening scenes. Experimental Psychology 54, 161–171.CrossRefGoogle ScholarPubMed
Kylliäinen, A and Hietanen, JK (2004) Attention orienting by another's gaze direction in children with autism. Journal of Child Psychology and Psychiatry 45, 435–444.CrossRefGoogle ScholarPubMed
Jakobsen, KV, Frick, JE and Simpson, EA (2013) Look here! The development of attentional orienting to symbolic cues. Journal of Cognition and Development 14, 229–249.CrossRefGoogle Scholar
Langton, SR and Bruce, V (1999) Reflexive visual orienting in response to the social attention of others. Visual Cognition 6, 541–567.CrossRefGoogle Scholar
Langton, SR, Watt, RJ and Bruce, V (2000) Do the eyes have it? Cues to the direction of social attention. Trends in Cognitive Sciences 4, 50–59.CrossRefGoogle ScholarPubMed
Maestro, S, Muratori, F, Cavallaro, MC, Pei, F, Stern, D, Golse, B and Palacio-Espasa, F (2002) Attentional skills during the first 6 months of age in autism spectrum disorder. Journal of the American Academy of Child & Adolescent Psychiatry 41, 1239–1245.CrossRefGoogle ScholarPubMed
Nuku, P and Bekkering, H (2008) Joint attention: inferring what others perceive (and don't perceive). Consciousness and Cognition 17, 339–349.CrossRefGoogle Scholar
Nummenmaa, L and Hietanen, JK (2009) How attentional systems process conflicting cues. The superiority of social over symbolic orienting revisited. Journal of Experimental Psychology: Human Perception and Performance 35, 1738–1754.Google ScholarPubMed
Okada, T, Sato, W, Murai, T, Kubota, Y and Toichi, M (2003) Eye gaze triggers visuospatial attentional shift in individuals with autism. Psychologia 46, 246–254.CrossRefGoogle Scholar
Perrett, D and Emery, N (1994) Understanding the intentions of others from visual signals: neurophysiological evidence. Cahiers de Psychologie Cognitive 13, 683–694.Google Scholar
Perrett, D, Hietanen, J, Oram, M, Benson, P and Rolls, E (1992) Organization and functions of cells responsive to faces in the temporal cortex [and discussion]. Philosophical Transactions: Biological Sciences 335, 23–30.Google Scholar
Posner, MI (1980) Orienting of attention. Quarterly Journal of Experimental Psychology 32, 3–25.CrossRefGoogle ScholarPubMed
Richardson, DC and Gobel, MS (2015) Social attention. In Fawcett, JM, Risko, EF and Kingstone, A (eds), The Handbook of Attention. Cambridge: MIT Press, pp. 349–367.Google Scholar
Risko, EF, Richardson, DC and Kingstone, A (2016) Breaking the fourth wall of cognitive science: real-world social attention and the dual function of gaze. Current Directions in Psychological Science 25, 70–74.CrossRefGoogle Scholar
Ristic, J, Friesen, CK and Kingstone, A (2002) Are eyes special? It depends on how you look at it. Psychonomic Bulletin & Review 9, 507–513.CrossRefGoogle Scholar
Ristic, J, Wright, A and Kingstone, A (2007) Attentional control and reflexive orienting to gaze and arrow cues. Psychonomic Bulletin & Review 14, 964–969.CrossRefGoogle ScholarPubMed
Rutherford, M and Krysko, KM (2008) Eye direction, not movement direction, predicts attention shifts in those with autism spectrum disorders. Journal of Autism and Developmental Disorders 38, 1958–1965.CrossRefGoogle Scholar
Sato, W, Kochiyama, T, Uono, S and Yoshikawa, S (2009) Commonalities in the neural mechanisms underlying automatic attentional shifts by gaze, gestures, and symbols. NeuroImage 45, 984–992.CrossRefGoogle ScholarPubMed
Shane, MS and Peterson, JB (2007) An evaluation of early and late stage attentional processing of positive and negative information in dysphoria. Cognition and Emotion 21, 789–815.CrossRefGoogle Scholar
Shi, J, Weng, X, He, S and Jiang, Y (2010) Biological motion cues trigger reflexive attentional orienting. Cognition 117, 348–354.CrossRefGoogle ScholarPubMed
Thornton, IM and Vuong, QC (2004) Incidental processing of biological motion. Current Biology 14, 1084–1089.CrossRefGoogle ScholarPubMed
Tipples, J (2002) Eye gaze is not unique: automatic orienting in response to uninformative arrows. Psychonomic Bulletin & Review 9, 314–318.CrossRefGoogle Scholar
Tipples, J (2008) Orienting to counterpredictive gaze and arrow cues. Perception & Psychophysics 70, 77–87.CrossRefGoogle ScholarPubMed
Troje, NF and Westhoff, C (2006) The inversion effect in biological motion perception: evidence for a ‘life detector’? Current Biology 16, 821–824.CrossRefGoogle Scholar
Uono, S, Sato, W and Kochiyama, T (2014) Commonalities and differences in the spatiotemporal neural dynamics associated with automatic attentional shifts induced by gaze and arrows. Neuroscience Research 87, 56–65.CrossRefGoogle Scholar
Vanrie, J and Verfaillie, K (2004) Perception of biological motion: a stimulus set of human point-light actions. Behavior Research Methods, Instruments, & Computers 36, 625–629.CrossRefGoogle ScholarPubMed
Wang, L and Jiang, Y (2012) Life motion signals lengthen perceived temporal duration. Proceedings of the National Academy of Sciences 109, E673–E677.CrossRefGoogle ScholarPubMed
Wang, L, Yang, X, Shi, J and Jiang, Y (2014) The feet have it: local biological motion cues trigger reflexive attentional orienting in the brain. NeuroImage 84, 217–224.CrossRefGoogle Scholar
Zhang, L, Sun, Y, Chen, F, Wu, D, Tang, J, Han, X, Ye, J and Wang, K (2016) Psychometric properties of the Autism-Spectrum quotient in both clinical and non-clinical samples: Chinese version for mainland China. BMC Psychiatry 16, 213.CrossRefGoogle ScholarPubMed
Zhao, J, Wang, L, Wang, Y, Weng, X, Li, S and Jiang, Y (2014) Developmental tuning of reflexive attentional effect to biological motion cues. Scientific Reports 4, 55–58.Google ScholarPubMed
Zwaigenbaum, L, Bryson, S, Rogers, T, Roberts, W, Brian, J and Szatmari, P (2005) Behavioral manifestations of autism in the first year of life. International Journal of Developmental Neuroscience 23, 143–152.CrossRefGoogle ScholarPubMed
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