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Contrast polarity and face recognition in the human fusiform gyrus

Abstract

Functional imaging has revealed face-responsive visual areas in the human fusiform gyrus, but their role in recognizing familiar individuals remains controversial. Face recognition is particularly impaired by reversing contrast polarity of the image, even though this preserves all edges and spatial frequencies. Here, combined influences of familiarity and priming on face processing were examined as contrast polarity was manipulated. Our fMRI results show that bilateral posterior areas in fusiform gyrus responded more strongly for faces with positive than with negative contrast polarity. An anterior, right-lateralized fusiform region is activated when a given face stimulus becomes recognizable as a well-known individual.

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Figure 1: Four example face stimuli, each illustrating one condition.
Figure 2: The same four faces as in Fig.1 with reversed contrast polarity.
Figure 3: Activation for all face conditions versus the fixation baseline.
Figure 4: Activations for the main effect of positive versus negative face stimuli, pooling over fame.
Figure 5: Activation produced by the interaction between fame and contrast polarity (specifically, voxels with a larger positive versus negative difference for famous than unknown faces).
Figure 6: The effect of previous exposure to the corresponding positive on the fMRI response to famous face negatives.

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References

  1. Bruce, V. & Humphreys, G. W. Recognizing objects and faces. Visual Cognition 1, 141– 180 (1994).

    Article  Google Scholar 

  2. Damasio, A. R., Damasio, H. & Van Hoesen, G. W. Prosopagnosia: anatomic basis and behavioral mechanisms. Neurology 32, 331–341 (1982).

    Article  CAS  Google Scholar 

  3. de Renzi, E. in Handbook of Research on Face Processing (eds. Young, A. W. & Ellis H. D.) 27–35 (Elsevier, Amsterdam, 1989).

    Book  Google Scholar 

  4. de Renzi, E., Perani, D., Carlesimo, G. A., Silveri, M. C. & Fazio, F. Prosopagnosia can be associated with damage confined to the right hemisphere—An MRI and PET study and a review of the literature. Neuropsychologia 32, 893–902 (1994).

    Article  Google Scholar 

  5. Ettlin, T. M. et al. Prosopagnosia: a bihemispheric disorder. Cortex 28, 129–134 ( 1992).

    Article  CAS  Google Scholar 

  6. Meadows, J. C. The anotomical basis of prosopagnosia. J. Neurol. Neurosurg. Psychiatry 37, 489–501 ( 1974).

    Article  CAS  Google Scholar 

  7. Warrington, E. K. & James, M. An experimental investigation of facial recognition in patients with unilateral cerebral lesions. Cortex 3, 317–326 (1967).

    Article  Google Scholar 

  8. Desimone, R., Albright, T. D., Gross, C. G. & Bruce, C. Stimulus-selective properties of inferior temporal neurons in the macaque. J. Neurosci. 4, 2051–2062 (1984).

    Article  CAS  Google Scholar 

  9. Harries, M. H. & Perrett, D. I. Visual processing of faces in the temporal cortex: physiological evidence for a modular organization and possible anatomical correlates. J. Cogn. Neurosci. 3, 9–24 (1991).

    Article  CAS  Google Scholar 

  10. Rolls, E. T. & Baylis, G. C. Size and contrast have only small effects on the responses to faces of neurons in the cortex of the superior temporal sulcus of the monkey. Exp. Brain Res. 65, 38–48 (1986).

    Article  CAS  Google Scholar 

  11. Grady, C. L. et al. Age-related reductions in human recognition memory due to impaired encoding. Science 269, 218– 221 (1995).

    Article  CAS  Google Scholar 

  12. Haxby, J. V. et al. Face encoding and recognition in the human brain. Proc. Natl. Acad. Sci. USA 93, 922– 927 (1996).

    Article  CAS  Google Scholar 

  13. Haxby, J. V. et al. Dissociation of object and spatial visual processing pathways in human extrastriate cortex. Proc. Natl. Acad. Sci. USA 88, 1621–1625 (1991).

    Article  CAS  Google Scholar 

  14. Clark, V. P., Maisog, J. M. & Haxby, J. V. fMRI study of face perception and memory using random stimulus sequences. J. Neurophysiol. 79, 3257–3265 (1998).

    Article  CAS  Google Scholar 

  15. Kanwisher, N., McDermott, J. M. & Chun, M. The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 17, 4302–4311 (1997).

    Article  CAS  Google Scholar 

  16. McCarthy, G., Puce, A., Gore, J. C. & Allison, T. Face-specific processing in the human fusiform gyrus. J. Cogn. Neurosci. 9, 605–610 (1997).

    Article  CAS  Google Scholar 

  17. Puce, A., Allison, T., Asgari, M., Gore, J. C. & McCarthy, G. Differential sensitivity of human visual cortex to faces, letterstrings, and textures: a functional magnetic resonance imaging study. J. Neurosci. 16, 5205– 5215 (1996).

    Article  CAS  Google Scholar 

  18. Kanwisher, N., Tong, F. & Nakayama, K. The effect of face inversion on the human fusiform face area. Cognition (in press).

  19. Tempini, M. L. et al. The neural systems sustaining face and proper-name processing. Brain 121, 2103–2118 (1998).

    Article  Google Scholar 

  20. Davies, G., Ellis, H. & Shepherd, J. Face recognition accuracy as a function of mode of representation. J. Appl. Psychol. 63, 180– 187 (1978).

    Article  Google Scholar 

  21. Kemp, R., Pike, G., White, P. & Musselman, A. Perception and recognition of normal and negative faces - the role of shape from shading and pigmentation cues. Perception 25, 37 –52 (1996).

    Article  CAS  Google Scholar 

  22. Cavanagh, P. & Leclerc, Y. G. Shape from shadows. J. Exp. Psychol. Hum. Percept. Perform. 15, 3– 27 (1989).

    Article  CAS  Google Scholar 

  23. Johnston, A., Hill, H. & Carman, N. Recognizing faces: effects of lighting direction, inversion, and brightness reversal. Perception 21, 365–375 (1992).

    Article  CAS  Google Scholar 

  24. Bruce, V. & Langton, S. The use of pigmentation and shading information in recognizing the sex and identities of faces. Perception 23, 803–822 ( 1994).

    Article  CAS  Google Scholar 

  25. Biederman, I. & Kalocsai, P. Neurocomputational bases of object and face recognition. Phil. Trans. R. Soc. Lond. B Biol. Sci. 352, 1203–1219 (1997).

    Article  CAS  Google Scholar 

  26. Wiskott, L. & von der Malsburg, C. Recognizing face by dynamic link matching. Neuroimage 4, S14–S18 ( 1996).

    Article  CAS  Google Scholar 

  27. Sinha, P. & Poggio, T. Role of learning in three-dimensional form perception. Nature 384, 460– 463 (1996).

    Article  CAS  Google Scholar 

  28. Brunas-Wagstaff, J., Young, A. W. & Ellis, A. W. Repetition priming follows spontaneous but not prompted recognition of familiar faces. Q. J. Exp. Psychol. [A] 44, 423–454 (1992).

    Article  CAS  Google Scholar 

  29. Ellis, A. W., Young, A. W. & Flude, B. M. Repetition priming and face processing: priming occurs within the system that responds to the identity of a face. Q. J. Exp. Psychol. [A] 42, 495–512 (1990).

    Article  CAS  Google Scholar 

  30. Young, A. W., Flude, B. M., Hellawell, D. J. & Ellis, A. W. The nature of semantic priming effects in the recognition of familiar people. Br. J. Psychol. 85, 393– 411 (1994).

    Article  Google Scholar 

  31. Andreasen N. C. et al. Neural substrates of facial recognition. J. Neuropsychiatry Clin. Neurosci. 8, 139–146 (1996).

    Article  CAS  Google Scholar 

  32. Kapur, N., Friston, K. J., Young, A., Frith, C. D. & Frackowiak, R. S. Activation of human hippocampal formation during memory for faces: a PET study. Cortex 31, 99–108 (1995).

    Article  CAS  Google Scholar 

  33. Sergent, J., Ohta, S. & MacDonald, B. Functional neuroanatomy of face and object processing. A positron emission tomography study. Brain 1, 15–36 (1992).

    Article  Google Scholar 

  34. Perrett, D. I. et al. Neurones responsive to faces in the temporal cortex: studies of functional organization, sensitivity to identity and relation to perception. Hum. Neurobiol. 3, 197– 208 (1984).

    CAS  PubMed  Google Scholar 

  35. Courtney, S. M., Ungerleider, L. G., Keil, K. & Haxby, J. V. Transient and sustained activity in a distributed neural system for human working memory. Nature 386, 608– 611 (1997).

    Article  CAS  Google Scholar 

  36. Damasio, A. R., Tranel, D. & Damasio, H. Face agnosia and the neural substrates of memory. Annu. Rev. Neurosci. 13, 89–109 (1990).

    Article  CAS  Google Scholar 

  37. Haxby, J. V. et al. The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and location. J. Neurosci. 14, 6336–6353 (1994).

    Article  CAS  Google Scholar 

  38. Ungerleider, L. G. Functional brain imaging studies of cortical mechanisms for memory. Science 270, 769–775 ( 1995).

    Article  CAS  Google Scholar 

  39. Sergent, J. in Handbook of Research on Face Processing (eds. Young, A. W. & Ellis, H. D.) 77–84 (Elsevier, Amsterdam, 1989).

    Google Scholar 

  40. Subramanian, S. & Biederman, I. Does contrast reversal affect object identification? Investigative Ophthalmol. Visual Sci. 38, 998 (1997).

    Google Scholar 

  41. Gauthier, I., Anderson, A. W., Tarr, M. J., Skudlarski, P. & Gore, J. C. Levels of categorization in visual recognition studied using functional magnetic resonance imaging. Curr. Biol. 7, 645–651 ( 1997).

    Article  CAS  Google Scholar 

  42. Rizzo, M., Hurtig, R. & Damasio, A. R. The role of scanpaths in facial recognition and learning. Ann. Neurol. 22, 41–45 (1987).

    Article  CAS  Google Scholar 

  43. Buckner R. L. et al. Functional-anatomic correlates of object priming in humans revealed by rapid presentation event-related fMRI. Neuron 20, 285–296 (1998).

    Article  CAS  Google Scholar 

  44. Buckner, R. L. et al. Functional anatomical studies of explicit and implicit memory retrieval tasks. J. Neurosci. 15, 12– 29 (1995).

    Article  CAS  Google Scholar 

  45. Raichle, M. E. et al. Practice-related changes in human brain functional anatomy during nonmotor learning. Cereb. Cortex 4, 8–26 (1994).

    Article  CAS  Google Scholar 

  46. Schacter, D. L. & Buckner, R. L. Priming and the brain. Neuron 20, 185– 195 (1998).

    Article  CAS  Google Scholar 

  47. Squire, L. R. et al. Activation of the hippocampus in normal humans: a functional anatomical study of memory. Proc. Natl. Acad. Sci. USA 89, 1837–1841 (1992).

    Article  CAS  Google Scholar 

  48. Dolan, R. J. et al. How the brain learns to see objects and faces in an impoverished context. Nature 389, 596– 599 (1997).

    Article  CAS  Google Scholar 

  49. Schacter, D. L. et al. Brain regions associated with retrieval of structurally coherent visual information. Nature 376, 587– 590 (1995).

    Article  CAS  Google Scholar 

  50. Morton, J. Interaction of information in word recognition. Psychol. Rev. 76, 165–178 (1969).

    Article  Google Scholar 

Download references

Acknowledgements

The functional imaging laboratory and R.J.D. were supported by the Wellcome Trust, N.G. by the Fyssen Foundation, G.C.B. by the National Science Foundation, and J.D. by the Human Frontiers Science Program.

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Correspondence to Raymond J. Dolan.

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George, N., Dolan, R., Fink, G. et al. Contrast polarity and face recognition in the human fusiform gyrus . Nat Neurosci 2, 574–580 (1999). https://doi.org/10.1038/9230

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