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The emergence of the social brain network: Evidence from typical and atypical development

Published online by Cambridge University Press:  01 November 2005

MARK H. JOHNSON ,
RICHARD GRIFFIN ,
GERGELY CSIBRA ,
HANIFE HALIT ,
TERESA FARRONI ,
MICHELLE DE HAAN ,
LESLIE A. TUCKER ,
SIMON BARON–COHEN  and
JOHN RICHARDS
MARK H. JOHNSON
Affiliation:
Birkbeck, University of London
RICHARD GRIFFIN
Affiliation:
Cambridge University
GERGELY CSIBRA
Affiliation:
Birkbeck, University of London
HANIFE HALIT
Affiliation:
Birkbeck, University of London
TERESA FARRONI
Affiliation:
Birkbeck, University of London
MICHELLE DE HAAN
Affiliation:
University College London
LESLIE A. TUCKER
Affiliation:
Birkbeck, University of London
SIMON BARON–COHEN
Affiliation:
Cambridge University
JOHN RICHARDS
Affiliation:
University of South Carolina
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Abstract

Several research groups have identified a network of regions of the adult cortex that are activated during social perception and cognition tasks. In this paper we focus on the development of components of this social brain network during early childhood and test aspects of a particular viewpoint on human functional brain development: “interactive specialization.” Specifically, we apply new data analysis techniques to a previously published data set of event-related potential (ERP) studies involving 3-, 4-, and 12-month-old infants viewing faces of different orientation and direction of eye gaze. Using source separation and localization methods, several likely generators of scalp recorded ERP are identified, and we describe how they are modulated by stimulus characteristics. We then review the results of a series of experiments concerned with perceiving and acting on eye gaze, before reporting on a new experiment involving young children with autism. Finally, we discuss predictions based on the atypical emergence of the social brain network.This work was funded by UK Medical Research Council Programme Grants (G9901005 and G9715587) to M.H.J. and S.B.C. T.F. was supported by a Wellcome Trust Research Fellowship (073985/Z/03/Z).

Type
Research Article
Information
Development and Psychopathology , Volume 17 , Issue 3 , September 2005 , pp. 599 - 619
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Adolphs, R. (2003a). Cognitive neuroscience of human social behaviour. Nature Reviews: Neuroscience 4, 165–178.Google Scholar
Adolphs, R. (2003b). Investigating the cognitive neuroscience of social behavior. Neuropsychologia 41, 119–126.Google Scholar
Allen, G., & Courchesne, E. (2001). Attention function and dysfunction in autism. Frontiers in Bioscience 6, 105–119.Google Scholar
Allison, T., Puce, A., & McCarthy, G. (2000). Social perception from visual cues: Role of STS region. Trends in Cognitive Sciences 4, 267–278.Google Scholar
Baron–Cohen, S. (1989). Joint attention deficits in autism: Towards a cognitive analysis. Development and Psychopathology 1, 185–189.Google Scholar
Baron–Cohen, S. (1995). Mindblindness: An essay on autism and theory of mind. Cambridge, MA: MIT Press.
Baron–Cohen, S., Jolliffe, T., Mortimore, C., & Robertson, M. (1997). Another advanced test of theory of mind: Evidence from very high functioning adults with autism or Asperger syndrome. Journal of Child Psychology and Psychiatry 38, 813–822.Google Scholar
Baron–Cohen, S., Leslie, A. M., & Frith, U. (1985). Does the autistic child have a “theory of mind”? Cognition 21, 37–46.Google Scholar
Baron–Cohen, S., O'Riordan, M., Jones, R., Stone, V., & Plaisted, K. (1999). A new test of social sensitivity: Detection of faux pas in normal children and children with Asperger syndrome. Journal of Autism and Developmental Disorders 29, 407–418.Google Scholar
Bentin, S., Allison, T., Puce, A., Perez, E., & McCarthy, G. (1996). Electrophysiological studies of face perception in humans. Journal of Cognitive Neuroscience 8, 551–565.Google Scholar
Butterworth, G., & Jarrett, N. (1991). What minds have in common is space: Spatial mechanisms serving joint visual attention in infancy. British Journal of Developmental Psychology 9, 55–72.Google Scholar
Carpenter, P. A., Just, M. A., Keller, T., Cherkassky, V., Roth, J. K., & Minshew, N. (2001). Dynamic cortical systems subserving cognition: fMRI studies with typical and atypical individuals. In J. L. McClelland & R. S. Siegler (Eds.), Mechanisms of cognitive development (pp. 353–386). Mahwah, NJ: Erlbaum.
Charman, T., Baron–Cohen, S., Swettenham, J., Cox, A., Baird, G., & Drew, A. (1998). An experimental investigation of social–cognitive abilities in infants with autism: Clinical implications. Infant Mental Health Journal 19, 260–275.Google Scholar
Chawarska, K., Klin, A., & Volkmar, F. (2003). Automatic attention cueing through eye movement in 2-year-old children with autism. Child Development 74, 1108–1122.Google Scholar
Cicchetti, D. (1984). The emergence of developmental psychopathology. Child Development 55, 1–7.Google Scholar
Cicchetti, D. (1991). Fractures in the crystal: Developmental psychopathology and the emergence of the self. Developmental Review 11, 271–287.Google Scholar
de Haan, M., Johnson, M. H., & Halit, H. (2003). Development of face-sensitive event-related potential components during infancy. International Journal of Psychophysiology 51, 45–58.Google Scholar
de Haan, M., Pascalis, O., & Johnson, M. H. (2002). Specialization of neural mechanisms underlying face recognition in human infants. Journal of Cognitive Neuroscience 14, 199–209.Google Scholar
Dehaene–Lambertz, G., Dehaene, S., & Hertz–Pannier, L. (2002). Functional neuroimaging of speech perception in infants. Science 298, 2013–2015.Google Scholar
DeLorme, A., Makeig, S., Fabre–Thorpe, M., & Sejnowski, T. (2002). From single-trial EEG to brain area dynamics. Neurocomputing 44–46, 1057–1064.Google Scholar
Driver, J., Davis, G., Ricciardelli, P., Kidd, P., Maxwell, E., & Baron–Cohen, S. (1999). Gaze perception triggers reflexive visuo-spatial orienting. Visual Cognition 6, 509–540.Google Scholar
Eimer, M. (2000). Effects of face inversion on the structural encoding and recognition of faces: Evidence from event-related brain potentials. Cognitive Brain Research 10, 145–158.Google Scholar
Elman, J., Bates, E., Johnson, M. H., Karmiloff–Smith, A., Parisi, D., & Plunkett, K. (1996). Rethinking innateness: A connectionist perspective on development. Cambridge, MA: MIT Press.
Farroni, T., Csibra, G., Simion, F., & Johnson, M. H. (2002). Eye contact detection in humans from birth. Proceedings of the National Academy of Sciences USA 99, 9602–9605.Google Scholar
Farroni, T., Johnson, M. H., Brockbank, M., & Simion, F. (2000). Infant's use of gaze direction to cue attention: The importance of perceived motion. Visual Cognition 7, 705–718.Google Scholar
Farroni, T., Mansfield, E. M., Lai, C., & Johnson, M. H. (2003). Motion and mutual gaze in directing infants' spatial attention. Journal of Experimental Child Psychology 85, 199–212.Google Scholar
Friesen, C. K., & Kingstone, A. (1998). The eyes have it! Reflexive orienting is triggered by nonpredictive gaze. Psychonomic Bulletin and Review 5, 490–495.Google Scholar
Friston, K. J., & Price, C. J. (2001). Dynamic representation and generative models of brain function. Brain Research Bulletin 54, 275–285.Google Scholar
Frith, U. (2003). Autism: Explaining the Enigma (2nd ed.). Oxford: Blackwell.
Gauthier, I., Tarr, M. J., Anderson, A. W., Skudlarski, P., & Gore, J. C. (1999). Activation of the middle fusiform “face area” increases with expertise in recognizing novel objects. Nature Neuroscience 2, 568–573.Google Scholar
George, N., Evans, J., Fiori, N., Davidoff, J., & Renault, B. (1996). Brain events related to normal and moderately scrambled faces. Cognitive Brain Research 4, 65–76.Google Scholar
Gottlieb, G. (1992). Individual development and evolution. New York: Oxford University Press.
Grice, S. J., Halit, H., Farroni, T., Baron–Cohen, S., Bolton, P., & Johnson, M. H. (2005). Neural correlates of eye-gaze detection in young children with autism. Cortex 41, 342–353.Google Scholar
Halit, H., Csibra, G., Volein, Á., & Johnson, M. H. (2004). Face-sensitive cortical processing in early infancy. Journal of Child Psychology and Psychiatry 45, 1228–1234.Google Scholar
Halit, H., de Haan, M., & Johnson, M. H. (2003). Cortical specialisation for face processing: Face-sensitive event-related potential components in 3 and 12 month-old infants. NeuroImage 19, 1180–1193.Google Scholar
Hamilton, A., Plunkett, K., & Schafer, G. (2000). Infant vocabulary development assessed with a British Communicative Development Inventory: Lower score in the UK than in the USA. Journal of Child Language 27, 689–705.Google Scholar
Happe, F. (1994). Autism: An introduction to psychological theory. London: UCL Press.
Haxby, J. V., Gobbini, M. I., Furey, M. L., Ishai, A., Schouten, J. L., & Pietrini, P. (2001). Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science 293, 2425–2430.Google Scholar
Hood, B. M., Willen, J. D., & Driver, J. (1998). Adult's eyes trigger shifts of visual attention in human infants. Psychological Science 9, 131–134.Google Scholar
Ishai, A., Ungerleider, L. G., Martin, A., Schouten, J. L., & Haxby, J. V. (1999). Distributed representation of objects in the human ventral visual pathway. Proceedings of the National Academy of Science USA 96, 9379–9384.Google Scholar
Johnson, M. H. (2000). Functional brain development in infants: Elements of an interactive specialization framework. Child Development 71, 75–81.Google Scholar
Johnson, M. H. (2001). Functional brain development in humans. Nature Reviews: Neuroscience 2, 475–483.Google Scholar
Johnson, M. H. (2005). Developmental cognitive neuroscience: An introduction (2nd ed.). Oxford: Blackwell.
Johnson, M. H., de Haan, M., Oliver, A., Smith, W., Hatzakis, H., Tucker, L. A., Csibra, G. (2001). Recording and analyzing high-density event-related potentials with infants using the Geodesic Sensor Net. Developmental Neuropsychology 19, 295–323.Google Scholar
Johnson, M. H., & Farroni, T. (2003). Perceiving and acting on the eyes: The development and neural basis of eye gaze perception. In O. Pascalis & A. Slater (Eds.), The development of face processing in infancy and early childhood: Current perspectives (pp. 155–168). New York: Nova Science Publishers.
Johnson, M. H., Halit, H., Grice, S., & Karmiloff–Smith, A. (2002). Neuroimaging of typical and atypical development: A perspective from multiple levels of analysis. Development and Psychopathology 14, 521–536.Google Scholar
Jung, T.-P., Makeig, S., Westerfield, M., Townsend, J., Courchesne, E., & Sejnowski, T. (2001). Analysis and visualization of single-trial event-related potentials. Human Brain Mapping 14, 166–185.Google Scholar
Kanwisher, N., McDermott, J., & Chun, M. M. (1997). The fusiform face area: A module in human extrastriate cortex specialized for face perception. The Journal of Neuroscience 17, 4302–4311.Google Scholar
Kylliäinen, A., & Hietanen, J. K. (2004). Attention orienting by another's gaze direction in children with autism. Journal of Child Psychology and Psychiatry, 45, 435.Google Scholar
Landry, R., & Bryson, S. E. (2004). Impaired disengagement of attention in young children with autism. Journal of Child Psychology and Psychiatry 45, 1115–1122.Google Scholar
Langton, S. R. H., & Bruce, V. (1999). Reflexive visual orienting in response to the social attention of others. Visual Cognition 6, 541–567.Google Scholar
Lavie, N., Ro, T., & Russell, C. (2003). The role of perceptual load in processing distractor faces. Psychological Science 14, 510–515.Google Scholar
Lee, T.-W., Girolami, M., & Sejnowski, T. J. (1999). Independent component analysis using an extended infomax algorithm for mixed sub-Gaussian and super-Gaussian Sources. Neural Computation 11, 417–441.Google Scholar
Leekam, S. R., Lopez, B., & Moore, C. (2000). Attention and joint attention in preschool children with autism. Developmental Psychology 36, 261–273.Google Scholar
Luna, B., Thulborn, K. R., Munoz, D. P., Merriam, E. P., Garver, K. E., Minshew, N. J., Keshavan, M. S., Genovese, C. R., Eddy, W. F., & Sweeney, J. A. (2001). Maturation of widely distributed brain function subserves cognitive development. NeuroImage 13, 786–793.Google Scholar
Makeig, S., Bell, A. J., Jung, T.-P., & Sejnowski, T. (1996). Independent component analysis of electroencephalographic data. Advances in Neural Information Processing Systems 8, 145–151.Google Scholar
Makeig, S., Jung, T.-P., Bell, A. J., Ghahremani, D., & Sejnowski, T. J. (1997). Blind separation of event-related brain responses into independent components. Proceedings of the National Academy of Sciences USA 94, 10979–10984.Google Scholar
Moore, R. J., Vadeyar, S. H., Fulford, J., Tyler, D. J., Gribben, C., Baker, P. N., James, D. K., & Gowland, P. A. (2001). Antenatal determination of fetal brain activity in response to an acoustic stimulus using functional magnetic resonance imaging. Human Brain Mapping 12, 94–99.Google Scholar
Passarotti, A. M., Paul, B. M., Bussiere, J. R., Buxton, R. B., Wong, E. C., & Stiles, J. (2003). The development of face and location processing: An fMRI study. Developmental Science 6, 100–117.Google Scholar
Perrin, F., Bertrand, O., & Pernier, J. (1987). Scalp current density mapping: Value and estimation from potential data. IEEE Transactions on Biomedical Engineering 34, 283–288.Google Scholar
Perrin, F., Pernier, J., Bertrand, O., & Echallier, J. F. (1989). Spherical splines for scalp potential and current density mapping. Electroencephalography and Clinical Neurophysiology 72, 184–187.Google Scholar
Posner, M. I. (1980). Orienting of attention. Quarterly Journal of Experimental Psychology 32, 3–25.Google Scholar
Puce, A., Allison, T., Bentin, S., Gore, J. C., & McCarthy, G. (1998). Temporal cortex activation in human viewing eye and mouth movements. Journal of Neuroscience 18, 2188–2199.Google Scholar
Rebai, M., Poiroux, S., Bernard, C., & Lalonde, R. (2001). Event-related potentials for category-specific information during passive viewing of faces and objects. International Journal of Neuroscience 106, 209–226.Google Scholar
Reynolds, G. D., & Richards, J. E. (in press). Familiarization, attention, and recognition memory in infancy: An ERP and cortical source localization study. Developmental Psychology.
Richards, J. E. (2004). Recovering cortical dipole sources from scalp-recorded event-related-potentials using component analysis: Principal component analysis and independent component analysis. International Journal of Psychophysiology 54, 201–220.Google Scholar
Richards, J. E. (2005). Localizing cortical sources of event-related potentials in infants' covert orienting. Developmental Science 8, 255–278.Google Scholar
Rossion, B., Gauthier, I., Tarr, M. J., Despland, P., Bruyer, R., Linotte, S., & Crommelinck, M. (2000). The N170 occipito-temporal component is delayed and enhanced to inverted faces but not to inverted objects: An electrophysiological account of face-specific processes in the human brain. NeuroReport 11, 69–74.Google Scholar
Scherg, M. (1992). Functional imaging and localization of electromagnetic brain activity. Brain Topography 5, 103–111.Google Scholar
Scherg, M., & Picton, T. W. (1991). Separation and identification of event-related potential components by brain electric source analysis. Electroencephalography & Clinical Neurophysiology, 42(Suppl.), 24–37.Google Scholar
Schuller, A. M., & Rossion, B. (2001). Spatial attention triggered by eye gaze increases and speeds up early visual activity. NeuroReport 12, 2381–2386.Google Scholar
Senju, A., Tojo, Y., Dairoku, H., & Hasegawa, T. (2003). Reflexive orienting in response to eye gaze and an arrow in children with and without autism. Journal of Child Psychology and Psychiatry 44, 1–14.Google Scholar
Sigman, M., Mundy, P., Sherman, T., & Ungerer, J. (1986). Social interactions of autistic, mentally retarded and normal children and their caregivers. Journal of Child Psychology and Psychiatry 5, 647–655.Google Scholar
Sparrow, S., Balla, D., & Cicchetti, D. (1984). Vineland Adaptive Behavior Scales (interview edition). Circle Pines, MN: American Guidance Service.
Spiridon, M., & Kanwisher, N. (2002). How distributed is visual category information in human occipital–temporal cortex? An fMRI study. Neuron 35, 1157–1165.Google Scholar
Talairach, J., & Tournoux, P. (1988). Co-planar stereotactic atlas of the human brain. New York: Thieme Medical Publishers.
Taylor, M. J., Edmonds, G. E., McCarthy, G., & Allison, T. (2001). Eyes first! Eye processing develops before face processing in children. NeuroReport 12, 1671–1676.Google Scholar
Taylor, M. J., McCarthy, G., Saliba, E., & DeGiovanni, E. (1999). ERP evidence of developmental changes in processing of faces. Clinical Neurophysiology 110, 910–915.Google Scholar
Tzourio–Mazoyer, N., de Schonen, S., Crivello, F., Reutter, B., Aujard, Y., & Mazoyer, B. (2002). Neural correlates of woman face processing by 2-month-old infants. NeuroImage 15, 454–461.Google Scholar
Urban, J., Carlson, E. A., Egeland, B., & Sroufe, L. A. (1991). Patterns of individual adaptation across childhood. Development and Psychopathology 3, 445–560.Google Scholar
Vecera, S. P., & Johnson, M. H. (1995). Eye gaze detection and the cortical processing of faces: Evidence from infants and adults. Visual Cognition 2, 101–129.Google Scholar
Watanabe, S., Kakigi, R., & Puce, A. (2001). Occipitotemporal activity elicited by viewing eye movements: A magnetoencephalographic study. NeuroImage 13, 351–363.Google Scholar
Wicker, B., Michel, F., Henaff, M. A., & Decety, J. (1998). Brain regions involved in the perception of gaze: A PET study. NeuroImage 8, 221–227.Google Scholar
Yin, R. K. (1969). Looking at upside down faces. Journal of Experimental Psychology 81, 141–145.Google Scholar