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Neurophysiological correlates of visuospatial attention and the social dynamics of gaze processing

  • Grace WeiEmail author
  • Jacqueline A. Rushby
  • Frances M. De Blasio
Article

Abstract

The reflexive orienting response triggered by nonpredictive gaze cues is thought to be driven by a dedicated social neural network responsible for directing attention toward socially salient information. However, atypical processing of eye gaze using concomitant perceptual features has been proposed to underlie attentional orienting in groups with impairments in social cognition. Here, we examined the neurophysiological indices of visuospatial attention during a spatial cueing task, considering individual variability in social cognition in typically developing individuals, and the relative salience of social gaze and perceptual motion cues. We found enhanced neural activation to incongruent cues, wherein modulation of the N2b serves as a marker of the allocation of attention in the spatial domain. Our findings suggest the social gaze cue is less salient for those with greater autistic traits. An attentional bias toward perceptual motion cues correlated with greater social anxiety and alexithymia, and thus may reflect reduced sensitivity to social stimuli. These results provide evidence for likely neurophysiological mechanisms underlying gaze cueing and offer insight into the use of qualitatively different cognitive mechanisms used to access social information. Such paradigms provide potential insight into normative orienting responses reported in atypical groups and would benefit investigations of gaze following abilities in clinical populations.

Keywords

EEG ERP Gaze cueing PCA Social cognition Spatial attention 

Notes

Acknowledgements

We thank Christopher Sufani for his assistance with stimulus development and data processing and Rebecca El Helou for her assistance in data collection. J.R. was supported by a National Health and Medical Research Council of Australia Project Grant (1081923).

Supplementary material

13415_2019_728_MOESM1_ESM.pdf (55 kb)
Fig. S1 Participant scores across measures of social functioning. Coloured and patterned data points reflect high individual participant scores across multiple measures. Mean scores are represented by the solid black line. Dotted lines indicate cutoffs: highest quartile (AQ; Baron-Cohen, Wheelwright, Skinner, Martin, & Clubley, 2001), marked and above social anxiety (LSAS-SR; Liebowitz, 1987), possible alexithymia (TAS-20; Bagby, Taylor, & Parker, 1994). (PDF 55 kb)

References

  1. American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Washington, DC: Author.Google Scholar
  2. Bagby, R. M., Taylor, G. J. & Parker, J. D. (1994). The Twenty-Item Toronto Alexithymia Scale-II. Convergent, discriminant, and concurrent validity. Journal of Psychosomatic of Research, 38(1), 33–40.Google Scholar
  3. Baron-Cohen, S. (1995). Mindblindness: An essay on autism and theory of mind. Learning, development, and conceptual change. Cambridge, MA: MIT Press.Google Scholar
  4. Baron-Cohen, S. (2003). The essential difference: Men, women and the extreme male brain. London, UK: Penguin Books.Google Scholar
  5. Barry, R. J., Clarke, A. R., Johnstone, S. J., & Rushby, J. A. (2008). Timing of caffeine’s impact on autonomic and central nervous system measures: Clarification of arousal effects. Biological Psychology, 77(3), 304–316.Google Scholar
  6. Barry, R. J., & De Blasio, F. M. (2015). Performance and ERP components in the equiprobable go/no-go task: Inhibition in children. Psychophysiology, 52(9), 1228–1237.Google Scholar
  7. Barry, R. J., De Blasio, F. M., Fogarty, J. S., & Karamacoska, D. (2016). ERP go/no-go condition effects are better detected with separate PCAs. International Journal of Psychophysiology, 106, 50–64.Google Scholar
  8. Barry, R. J., Rushby, J. A., Wallace, M. J., Clarke, A. R., Johnstone, S. J., & Zlojutro, I. (2005). Caffeine effects on resting-state arousal. Clinical Neurophysiology, 116(11), 2693–2700.Google Scholar
  9. Bayliss, A. P., Murphy, E., Naughtin, C. K., Kritikos, A., Schilbach, L., & Becker, S. I. (2013). “Gaze leading”: Initiating simulated joint attention influences eye movements and choice behavior. Journal of Experimental Psychology: General, 142(1), 76–92.Google Scholar
  10. Bender, R., & Lange, S. (2001). Adjusting for multiple testing-when and how? Journal of Clinical Epidemiology, 54(4), 343–349.Google Scholar
  11. Berthoz, S., & Hill, E. L. (2005). The validity of using self-reports to assess emotion regulation abilities in adults with autism spectrum disorder. European Psychiatry, 20(3), 291–298.Google Scholar
  12. Bird, G., Press, C., & Richardson, D. C. (2011). The role of alexithymia in reduced eye-fixation in autism spectrum conditions. Journal of Autism and Developmental Disorders, 41(11), 1156–1164.Google Scholar
  13. Birmingham, E., & Kingstone, A. (2009). Human social attention: A new look at past, present, and future investigations. Annals of the New York Academy of Sciences, 1156, 118–140.Google Scholar
  14. Brothers, L. (1990). The social brain: A project for integrating primate behaviour and neurophysiology in a new domain. Concepts in Neuroscience, 1, 27–51.Google Scholar
  15. Bruin, K. J., & Wijers, A. A. (2002). Inhibition, response mode, and stimulus probability: A comparative event-related potential study. Clinical Neurophysiology, 113(7), 1172–1182.Google Scholar
  16. Buodo, G., Sarlo, M., & Munafò, M. (2010). The neural correlates of attentional bias in blood phobia as revealed by the N2pc. Social Cognitive and Affective Neuroscience, 5, 29–38.Google Scholar
  17. Calder, A. J., Lawrence, A. D., Keane, J., Scott, S. K., Owen, A. M., Christoeffels, I., & Young, A. W. (2002). Reading the mind from eye gaze. Neuropsychologia, 40(8), 1129–1138.Google Scholar
  18. Castelli, F., Frith, C., Happe, F., & Frith, U. (2002). Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. Brain, 125, 1839–1849.Google Scholar
  19. Conty, L., N’Diaye, K., Tijus, C., & George, N. (2007). When eye creates the contact! ERP evidence for early dissociation between direct and averted gaze motion processing. Neuropsychologia, 45, 3024–3037.Google Scholar
  20. Dell’Acqua, R., Sessa, P., Jolicoeur, P., & Robitaille, N. (2006). Spatial attention freezes during the attentional blink. Psychophysiology, 43, 394–400.Google Scholar
  21. Dien, J. (2010). The ERP PCA Toolkit: An open source program for advanced statistical analysis of event-related potential data. Journal of Neuroscience Methods, 187(1), 138–145.Google Scholar
  22. Driver, J., Davis, G., Ricciardelli, P., Kidd, P., Maxwell, E., & Baron-Cohen, S. (1999). Gaze perception triggers reflexive visuospatial orienting. Visual Cognition, 6(5), 509–540.Google Scholar
  23. Eimer, M. (1996). The N2pc component as an indicator of attentional selectivity. Electroencephalography & Clinical Neurophysiology, 99(3), 225–234.Google Scholar
  24. Emery, N. J. (2000). The eyes have it: The neuroethology, function and evolution of social gaze. Neuroscience and Biobehavioral Reviews, 24(6), 581–604.Google Scholar
  25. Farroni, T., Csibra, G., Simion, F., & Johnson, M. H. (2002). Eye contact detection in humans from birth. Proceedings of the National Academy of Sciences of the United States of America, 99(14), 9602–9605.Google Scholar
  26. Folstein, J. R., & Van Petten, C. (2008). Influence of cognitive control and mismatch on the N2 component of the ERP: A review. Psychophysiology, 45(1), 152–170.Google Scholar
  27. Fresco, D. M., Coles, M. E., Heimberg, R. G., Liebowitz, M. R., Hami, S., Stein, M. B., & Goetz, D. (2001). The Liebowitz Social Anxiety Scale: A comparison of the psychometric properties of self-report and clinician-administered formats. Psychological Medicine, 31(6), 1025–1035.Google Scholar
  28. Friesen, C. K., & Kingstone, A. (1998). The eyes have it! Reflexive orienting is triggered by nonpredictive gaze. Psychonomic Bulletin & Review, 5(3), 490–495.Google Scholar
  29. Frith, C. D., & Frith, U. (2006). The neural basis of mentalizing. Neuron, 50(4), 531–534.Google Scholar
  30. Galfano, G., Sarlo, M., Sassi, F., Munafò, M., Fuentes, L. J., & Umiltà, C. (2011). Reorienting of spatial attention in gaze cuing is reflected in N2pc. Social Neuroscience, 6(3), 257–269.Google Scholar
  31. Goff, W. R., Allison, T., & Vaughan, H. G. J. (1978). The functional neuroanatomy of event-related potentials. New York, NY: Academic Press.Google Scholar
  32. Halladay, A. K., Bishop, S., Constantino, J. N., Daniels, A. M., Koenig, K., Palmer, K., . . . Szatmari, P. (2015). Sex and gender differences in autism spectrum disorder: Summarizing evidence gaps and identifying emerging areas of priority. Molecular Autism, 6, 36.Google Scholar
  33. Hayward, D. A., & Ristic, J. (2017). Feature and motion-based gaze cuing is linked with reduced social competence. Scientific Reports, 7, 44221.Google Scholar
  34. Hietanen, J. K., Nummenmaa, L., Nyman, M. J., Parkkola, R., & Hämäläinen, H. (2006). Automatic attention orienting by social and symbolic cues activates different neural networks: An fMRI study. NeuroImage, 33, 406–413.Google Scholar
  35. Hillyard, S. A., & Kutas, M. (1983). Electrophysiology of cognitive processing. Annual Review of Psychology, 34, 33–61.Google Scholar
  36. Holmes, A., Bradley, B. P., Kragh Nielsen, M., & Mogg, K. (2009). Attentional selectivity for emotional faces: Evidence from human electrophysiology. Psychophysiology, 46, 62–68.Google Scholar
  37. Hommel, B., Pratt, J., Colzato, L., & Godijn, R. (2001). Symbolic control of visual attention. Psychological Science, 12, 360–365.Google Scholar
  38. Horley, K., Williams, L. M., Gonsalvez, C., & Gordon, E. (2003). Social phobics do not see eye to eye: A visual scanpath study of emotional expression processing. Journal of Anxiety Disorders, 17(1), 33–44.Google Scholar
  39. Horley, K., Williams, L. M., Gonsalvez, C., & Gordon, E. (2004). Face to face: Visual scanpath evidence for abnormal processing of facial expressions in social phobia. Psychiatry Research, 127(1/2), 43–53.Google Scholar
  40. Jarick, M., & Kingstone, A. (2015). The duality of gaze: Eyes extract and signal social information during sustained cooperative and competitive dyadic gaze. Frontiers in Psychology, 6, 1423.Google Scholar
  41. Johnson, M. H., Griffin, R., Csibra, G., Halit, H., Farroni, T., De Haan, M., . . . . Richards, J. (2005). The emergence of the social brain network: Evidence from typical and atypical development. Development and Psychopathology, 17(3), 599–619.Google Scholar
  42. Kayser, J., & Tenke, C. E. (2003). Optimizing PCA methodology for ERP component identification and measurement: Theoretical rationale and empirical evaluation. Clinical Neurophysiology, 114(12), 2307–2325.Google Scholar
  43. Klein, R. M. (2000). Inhibition of return. Trends in Cognitive Sciences, 4(4), 138–147.Google Scholar
  44. Kobayashi, H., & Kohshima, S. (1997). Unique morphology of the human eye. Nature, 387, 767–768.Google Scholar
  45. Lasaponara, S., D’Onofrio, M., Pinto, M., Dragone, A., Menicagli, D., Bueti, D., . . . Doricchi, F. (2018). EEG correlates of preparatory orienting, contextual updating and inhibition of sensory processing in left spatial neglect. Journal of Neuroscience, 38(15), 3792–3808.Google Scholar
  46. Leekam, S., Baron-Cohen, S., Perrett, D., Milders, M., & Brown, S. (1997). Eye-direction detection: A dissociation between geometric and joint attention skills in autism. British Journal of Developmental Psychology, 15, 77–95.Google Scholar
  47. Liebowitz, M. R. (1987). Social phobia. Modern Problems in Pharmacopsychiatry, 22, 141–173.Google Scholar
  48. Lorenzo-Seva, U., & ten Berge, J. M. F. (2006). Tucker’s congruence coefficient as a meaningful index of factor similarity. Methodology: European Journal of Research Methods for the Behavioral and Social Sciences, 2, 57–64.Google Scholar
  49. Luck, S. J., & Hillyard, S. A. (1994). Electrophysiological correlates of feature analysis during visual search. Psychophysiology, 31(3), 291–308.Google Scholar
  50. Moukheiber, A., Rautureau, G., Perez-Diaz, F., Soussignan, R., Dubal, S., Jouvent, R., & Pelissolo A. (2010). Gaze avoidance in social phobia: Objective measure and correlates. Behaviour Research and Therapy, 48(2), 147–151.Google Scholar
  51. Mundy, P. (1995). Joint attention and social-emotional approach behavior in children with autism. Development and Psychopathology, 7(1), 63–82.Google Scholar
  52. Murray, A. M., Nobre, A. C., & Stokes, M. G. (2011). Markers of preparatory attention predict visual short-term memory performance. Neuropsychologia, 49(6), 1458–1465.Google Scholar
  53. Näätänen, R., Gaillard, A. W., & Mantysalo, S. (1978). Early selective-attention effect on evoked potential reinterpreted. Acta Psychologica, 42(4), 313–329.Google Scholar
  54. Näätänen, R., & Michie, P. T. (1979). Early selective-attention effects on the evoked potential: A critical review and reinterpretation. Biological Psychology, 8(2), 81–136.Google Scholar
  55. Nation, K., & Penny, S. (2008). Sensitivity to eye gaze in autism: Is it normal? Is it automatic? Is it social? Development and Psychopathology, 20, 79–97.Google Scholar
  56. Nixima, K., Fujimori, M., & Okanoya, K. (2013). An ERP study of autistic traits and emotional recognition in non-clinical adolescence. Scientific Research Psychology, 4, 515–519.Google Scholar
  57. Okada, T., Sato, W., Murai, T., Kubota, Y., & Toichi, M. (2003). Eye gaze triggers visuospatial attentional shifts in individuals with autism. Psychologia, 46, 246–254.Google Scholar
  58. Pfefferbaum, A., Ford, J. M., Weller, B. J., & Kopell, B. S. (1985). ERPs to response production and inhibition. Electroencephalography and Clinical Neurophysiology, 60(5), 423–434.Google Scholar
  59. Posner, M. I. (1980). Orienting of attention. The Quarterly Journal of Experimental Psychology, 32(1), 3–25.Google Scholar
  60. Pritchard, W. S., Shappell, S. A., & Brandt, M. E. (1991). Psychophysiology of N200/N400: A review and classification scheme. London, UK: Jessica Kingsley.Google Scholar
  61. Ristic, J., & Kingstone, A. (2012). A new form of human spatial attention: Automated symbolic orienting. Visual Cognition, 20(3), 244–264.Google Scholar
  62. Ristic, J., & Landry, M. (2015). Combining attention: A novel way of conceptualizing the links between attention, sensory processing, and behavior. Attention, Perception, & Psychophysics, 77(1), 36–49.Google Scholar
  63. Ristic, J., Mottron, L., Friesen, C. K., Iarocci, G., Burack, J. A., & Kingstone, A. (2005). Eyes are special but not for everyone: The case of autism. Cognitive Brain Research, 24(3), 715–718.Google Scholar
  64. Seiss, E., Gherri, E., Eardley, A. F., & Eimer, M. (2007). Do ERP components triggered during attentional orienting represent supramodal attentional control? Psychophysiology, 44(6), 987–990.Google Scholar
  65. Semlitsch, H. V., Anderer, P., Schuster, P., & Presslich, O. (1986). A solution for reliable and valid reduction of ocular artifacts, applied to the P300 ERP. Psychophysiology, 23(6), 695–703.Google Scholar
  66. Senju, A., Tojo, Y., Dairoku, H., & Hasegawa, T. (2004). Reflexive orienting in response to eye gaze and an arrow in children with and without autism. Journal of Child Psychology and Psychiatry, 45(3), 445–458.Google Scholar
  67. Strom, J. C., & Buck, R. W. (1979). Staring and participants’ sex: Physiological and subjective reactions. Personality and Social Psychology Bulletin, 5(1), 114–117.Google Scholar
  68. Suwazono, S., Machado, L., & Knight, R. T. (2000). Predictive value of novel stimuli modifies visual event-related potentials and behavior. Clinical Neurophysiology, 111(1), 29–39.Google Scholar
  69. Swettenham, J., Condie, S., Campbell, R., Milne, E., & Coleman, M. (2003). Does the perception of moving eyes trigger reflexive visual orienting in autism? Autism: Mind and brain (pp. 89–107). New York, NY: Oxford University Press.Google Scholar
  70. Tabachnik, B. G., & Fidell, L. S. (2013). Using multivariate statistics (6th ed.). Boston, MA: Pearson.Google Scholar
  71. Timoney, L. R., & Holder, M. D. (2013). Emotional processing deficits and happiness. Dordrecht, Netherlands: Springer.Google Scholar
  72. Tipples, J. (2002). Eye gaze is not unique: Automatic orienting in response to uninformative arrows. Psychonomic Bulletin & Review, 9(2), 314–318.Google Scholar
  73. Tucker, L. R. (1951). A method for synthesis of factor analysis studies (Personnel Research Section Report No. 984), Washington, DC: Department of the Army.Google Scholar
  74. Vaughan, H. G. J., & Arezzo, J. C. (1998). The neural basis of event-related potentials (Vol. 3, pp. 45–96). New York, NY: Elsevier.Google Scholar
  75. Werling, D. M., & Geschwind, D. H. (2013). Sex differences in autism spectrum disorders. Current Opinion in Neurology, 26(2), 146–153.Google Scholar
  76. Woodman, G. F. (2010). A brief introduction to the use of event-related potentials in studies of perception and attention. Attention, Perception, & Psychophysics, 72(8), 2031–2046.Google Scholar

Copyright information

© The Psychonomic Society, Inc. 2019

Authors and Affiliations

  • Grace Wei
    • 1
    • 2
    Email author
  • Jacqueline A. Rushby
    • 1
  • Frances M. De Blasio
    • 1
  1. 1.School of PsychologyThe University of New South WalesSydneyAustralia
  2. 2.Brain and Mind CentreUniversity of SydneyCamperdownAustralia

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