What functional brain studies have revealed about face and facial expression perception?

916

Abstract

The models of face perception mechanisms have been substantially extended recently by the results obtained with functional brain mapping studies. The current paper reviews the studies that help to define more precisely the functional organization of the distributed facial system. We explore the issue of independence versus interrelation of face identification and expression recognition; compare the mechanisms of static and dynamic faces perception, as well as face-in-context perception. We emphasize the importance of higher ecological validity of face perception and its brain mechanisms.

General Information

Keywords: fMRI, face perception, facial expressions, dynamic expression, face in context, FFA, STS, OFA, distributed brain system for face perception

Journal rubric: Neurosciences and Cognitive Studies

DOI: https://doi.org/10.17759/jmfp.2016050404

For citation: Korolkova O.A. What functional brain studies have revealed about face and facial expression perception? [Elektronnyi resurs]. Sovremennaia zarubezhnaia psikhologiia = Journal of Modern Foreign Psychology, 2016. Vol. 5, no. 4, pp. 36–49. DOI: 10.17759/jmfp.2016050404. (In Russ., аbstr. in Engl.)

References

  1. Bruyer R. et al. A case of prosopagnosia with some preserved covert remembrance of familiar faces. Brain and cognition, 1983. Vol. 2, no. 3, pp. 257–284. doi: 10.1016/0278-2626(83)90014-3
  2. Steeves J. et al. Abnormal face identity coding in the middle fusiform gyrus of two brain-damaged prosopagnosic patients. Neuropsychologia, 2009. Vol. 47, no. 12, pp. 2584–2592. doi: 10.1016/j.neuropsychologia.2009.05.005
  3. Adams R.B. et al. Amygdala responses to averted vs direct gaze fear vary as a function of presentation speed. Social Cognitive and Affective Neuroscience, 2012. Vol. 7, no. 5, pp. 568–577. doi: 10.1093/scan/nsr038
  4. Andrews T.J., Ewbank M.P. Distinct representations for facial identity and changeable aspects of faces in the human temporal lobe. NeuroImage, 2004. Vol. 23, no. 3, pp. 905–913. doi: 10.1016/j.neuroimage.2004.07.060
  5. Riddoch M.J. et al. Are faces special? A case of pure prosopagnosia. Cognitive Neuropsychology, 2008. Vol. 25, no. 1, pp. 3–26. doi: 10.1080/02643290801920113
  6. Barton J.J.S. Structure and function in acquired prosopagnosia: Lessons from a series of 10 patients with brain damage. Journal of Neuropsychology, 2008. Vol. 2, no. 1, pp. 197–225. doi: 10.1348/174866407X214172
  7. Bate S., Bennetts R. The independence of expression and identity in face-processing: evidence from neuropsychological case studies. Frontiers in Psychology, 2015. Vol. 6, pp. 1–7. doi: 10.3389/fpsyg.2015.00770
  8. Bernstein M., Yovel G. Two neural pathways of face processing: A critical evaluation of current models. Neuroscience & Biobehavioral Reviews, 2015. Vol. 55, pp. 536–546. doi: 10.1016/j.neubiorev.2015.06.010
  9. de Gelder B. et al. Beyond the face: exploring rapid influences of context on face processing. Progress in Brain Research, 2006. Vol, part B. 155, pp. 37–48. doi: 10.1016/S0079-6123(06)55003-4
  10. Ferri F. et al. Binding action and emotion in social understanding. PloS one, 2013. Vol. 8, no. 1, pp. e54091. doi: 10.1371/journal.pone.0054091
  11. Bouvier S.E. Behavioral Deficits and Cortical Damage Loci in Cerebral Achromatopsia. Cerebral Cortex, 2005. Vol. 16, no. 2, pp. 183–191. doi: 10.1093/cercor/bhi096
  12. Bruce V., Young A. Understanding face recognition. British Journal of Psychology, 1986. Vol. 77, no. 3, pp. 305–327. doi: 10.1111/j.2044-8295.1986.tb02199.x
  13. Calder A.J., Young A.W. Understanding the recognition of facial identity and facial expression. Nature reviews. Neuroscience, 2005. Vol. 6, no. 8, pp. 641–651. doi: 10.1038/nrn1724
  14. Bate S. et al. Covert face recognition relies on affective valence in congenital prosopagnosia. Cognitive Neuropsychology, 2009. Vol. 26, no. 4, pp. 391–411. doi: 10.1080/02643290903175004
  15. Pitcher D. et al. Differential selectivity for dynamic versus static information in face-selective cortical regions. NeuroImage, 2011. Vol. 56, no. 4, pp. 2356–2363. doi: 10.1016/j.neuroimage.2011.03.067
  16. Kilts C.D. et al. Dissociable Neural Pathways Are Involved in the Recognition of Emotion in Static and Dynamic Facial Expressions. NeuroImage, 2003. Vol. 18, no. 1, pp. 156–168. doi: 10.1006/nimg.2002.1323
  17. Pourtois G. et al. Dissociable roles of the human somatosensory and superior temporal cortices for processing social face signals.Neuroscience, 2004. Vol. 20, no. 12, pp. 3507–3515. doi: 10.1111/j.1460-9568.2004.03794.x
  18. Duchaine B., Germine L., Nakayama K. Family resemblance: Ten family members with prosopagnosia and within-class object agnosia. Cognitive Neuropsychology, 2007. Vol. 24, no. 4, pp. 419–430. doi: 10.1080/02643290701380491
  19. Duchaine B.C., Parker H., Nakayama K. Normal recognition of emotion in a prosopagnosic. Perception, 2003. Vol. 32, no. 7, pp. 827–38.
  20. Curio C. et al. Dynamic Faces: Insights from Experiments and Computation. Cambridge, MA: MIT Press, 2010. 288 p.
  21. Foley E. et al. Dynamic Facial Expressions Evoke Distinct Activation in the Face Perception Network: A Connectivity Analysis Study. Journal of Cognitive Neuroscience, 2012. Vol. 24, no. 2, pp. 507–520. doi: 10.1162/jocn_a_00120
  22. Sauer A. et al. Effects of gaze direction, head orientation and valence of facial expression on amygdala activity. Social Cognitive and Affective Neuroscience, 2014. Vol. 9, no. 8, pp. 1246–1252. doi: 10.1093/scan/nst100
  23. Brierley B. et al. Emotional memory and perception in temporal lobectomy patients with amygdala damage.Journal of Neurology, Neurosurgery & Psychiatry, 2004. Vol. 75, no. 4, pp. 593–599. doi: 10.1136/jnnp.2002.006403
  24. Sato W. et al. Enhanced neural activity in response to dynamic facial expressions of emotion: an fMRI study. Cognitive Brain Research, 2004. Vol. 20, no. 1, pp. 81–91. doi: 10.1016/j.cogbrainres.2004.01.008
  25. Minnebusch D.A. et al. Event-related potentials reflect heterogeneity of developmental prosopagnosia. European Journal of Neuroscience, 2007. Vol. 25, no. 7, pp. 2234–2247. doi: 10.1111/j.1460-9568.2007.05451.x
  26. Pyles J.A. et al. Explicating the Face Perception Network with White Matter Connectivity. PLoS ONE, 2013. Vol. 8, no. 4. doi: 10.1371/journal.pone.0061611
  27. Young A.W. et al Face perception after brain injury. Selective impairments affecting identity and expression. Brain, 1993. Vol. 116, no. 4, pp. 941–959. doi: 10.1093/brain/116.4.941
  28. Susilo T. et al. Face perception is category-specific: Evidence from normal body perception in acquired prosopagnosia. Cognition, 2013. Vol. 129, no. 1, pp. 88–94. doi: 10.1016/j.cognition.2013.06.004
  29. Winston J.S. et al. fMRI-adaptation reveals dissociable neural representations of identity and expression in face perception. Journal of neurophysiology, 2004. Vol. 92, no. 3, pp. 1830–1839. doi: 10.1152/jn.00155.2004
  30. Fox C.J., Iaria G., Barton J.J.S. Defining the face processing network: Optimization of the functional localizer in fMRI. Human Brain Mapping, 2009. Vol. 30, no. 5, pp. 1637–1651. doi: 10.1002/hbm.20630
  31. Girges C., O’Brien J., Spencer J. Neural correlates of facial motion perception. Social Neuroscience, 2016. Vol. 11, no. 3, pp. 311–316. doi: 10.1080/17470919.2015.1061689
  32. Harris R.J., Young A.W., Andrews T.J. Dynamic stimuli demonstrate a categorical representation of facial expression in the amygdale. Neuropsychologia, 2014. Vol. 56, pp. 47–52. doi: 10.1016/j.neuropsychologia.2014.01.005
  33. Haxby J. V., Hoffman E.A., Gobbini M.I. The distributed human neural system for face perception. Trends in Cognitive Sciences, 2000. Vol. 4, no. 6, pp. 223–233. doi: 10.1016/S1364-6613(00)01482-0
  34. Haxby J.V., Gobbini M.I. Distributed neural systems for face perception. Oxford Handbook of Face Perception. Ed. A.J. Calder et al. Oxford: Oxford University Press Oxford, UK, 2011. P. 93–109
  35. Hoffman E.A., Haxby J.V. Distinct representations of eye gaze and identity in the distributed human neural system for face perception. Nature neuroscience, 2000. Vol. 3, no. 1, pp. 80–84. doi: 10.1038/71152
  36. Hornak J., Rolls E.T., Wade D. Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage. Neuropsychologia, 1996. Vol. 34, no. 4, pp. 247–261. doi: 10.1016/0028-3932(95)00106-9
  37. Humphreys K., Avidan G., Behrmann M. A detailed investigation of facial expression processing in congenital prosopagnosia as compared to acquired prosopagnosia. Experimental Brain Research, 2007. Vol. 176, no. 2, pp. 356–373. doi: 10.1007/s00221-006-0621-5
  38. Schiltz C. et al. Impaired face discrimination in acquired prosopagnosia is associated with abnormal response to individual faces in the right middle fusiform gyrus. Cerebral cortex, 2006. Vol. 16, no. 4, pp. 574–586. doi: 10.1093/cercor/bhj005
  39. Ishai A. Let’s face it: It’s a cortical network. NeuroImage, 2008. Vol. 40, no. 2, pp. 415–419. doi: 10.1016/j.neuroimage.2007.10.040
  40. Lander K., Butcher N. Independence of face identity and expression processing: exploring the role of motion. Frontiers in Psychology, 2015. Vol. 6, pp. 1–6. doi: 10.3389/fpsyg.2015.00255
  41. Yarkoni T. et al. Large-scale automated synthesis of human functional neuroimaging data. Nature Methods, 2011. Vol. 8, no. 8, pp. 665–670. doi: 10.1038/nmeth.1635
  42. Longmore C.A., Tree J.J. Motion as a cue to face recognition: Evidence from congenital prosopagnosia. Neuropsychologia, 2013. Vol. 51, no. 5, pp. 864–875. doi: 10.1016/j.neuropsychologia.2013.01.022
  43. Mazard A., Schiltz C., Rossion B. Recovery from adaptation to facial identity is larger for upright than inverted faces in the human occipito-temporal cortex. Neuropsychologia, 2006. Vol. 44, no. 6, pp. 912–922. doi: 10.1016/j.neuropsychologia.2005.08.015
  44. Meeren H.K.M., Heijnsbergen C.C.R.J. van, Gelder B. de. Rapid perceptual integration of facial expression and emotional body language. Proceedings of the National Academy of Sciences, 2005. Vol. 102, no. 45, pp. 16518–16523. doi: 10.1073/pnas.0507650102
  45. Rotshtein P. et al. Morphing Marilyn into Maggie dissociates physical and identity face representations in the brain. Nature Neuroscience, 2005. Vol. 8, pp. 107–113. doi: 10.1038/nn1370
  46. Bennetts R.J. et al. Movement cues aid face recognition in developmental prosopagnosia. Neuropsychology, 2015. Vol. 29, no. 6, pp. 855–860. doi: 10.1037/neu0000187
  47. N’Diaye K., Sander D., Vuilleumier P. Self-relevance processing in the human amygdala: Gaze direction, facial expression, and emotion intensity. Emotion, 2009. Vol. 9, no. 6, pp. 798–806. doi: 10.1037/a0017845
  48. O’Toole A.J., Roark D.A., Abdi H. Recognizing moving faces: a psychological and neural synthesis. Trends in Cognitive Sciences, 2002. Vol. 6, no. 6, pp. 261–266. doi: 10.1016/S1364-6613(02)01908-3
  49. Peelen M. V, Downing P.E. Selectivity for the human b ody in the fusiform gyrus. Journal of neurophysiology, 2005. Vol. 93, no. 1, pp. 603–608. doi: 10.1152/jn.00513.2004
  50. Fox C.J. et al. Perceptual and anatomic patterns of selective deficits in facial identity and expression processing. Neuropsychologia, 2011. Vol. 49, no. 12, pp. 3188–3200. doi: 10.1016/j.neuropsychologia.2011.07.018
  51. Pitcher D., Duchaine B., Walsh V. Combined TMS and FMRI reveal dissociable cortical pathways for dynamic and static face perception. Current biology, 2014. Vol. 24, no. 17, pp. 2066–2070. doi: 10.1016/j.cub.2014.07.060
  52. Pitcher D., Walsh V., Duchaine B. Transcranial Magnetic Stimulation Studies of Face Processing // Oxford Handbook of Face Perception. G. Rhodes [et al.] Oxford: Oxford University Press, 2011. P. 367–385. doi: 10.1093/oxfordhb/9780199559053.013.0019
  53. Duchaine B.C. et al. Prosopagnosia as an impairment to face-specific mechanisms: Elimination of the alternative hypotheses in a developmental case. Cognitive Neuropsychology, 2006. Vol. 23, no. 5, pp. 714–747. doi: 10.1080/02643290500441296
  54. Richoz A.-R. et al. Reconstructing dynamic mental models of facial expressions in prosopagnosia reveals distinct representations for identity and expression. Cortex, 2015. Vol. 65, pp. 50–64. doi: 10.1016/j.cortex.2014.11.015
  55. Reinl M., Bartels A. Face processing regions are sensitive to distinct aspects of temporal sequence in facial dynamics. NeuroImage, 2014. Vol. 102, pp. 407–415. doi: 10.1016/j.neuroimage.2014.08.011
  56. Rossion B. A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain, 2003. Vol. 126, no. 11, pp. 2381–2395. doi: 10.1093/brain/awg241
  57. Said C.P., Haxby J. V., Todorov A. Brain systems for assessing the affective value of faces. Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 2011. Vol. 366, no. 1571, pp. 1660–1670. doi: 10.1098/rstb.2010.0351
  58. Sato W., Kochiyama T., Uono S. Spatiotemporal neural network dynamics for the processing of dynamic facial expressions. Nature Publishing Group, 2015. Vol. 5, article number: 12432, pp. 1–13. doi: 10.1038/srep12432
  59. Schmalzl L., Zopf R., Williams M.A. From head to toe: evidence for selective brain activation reflecting visual perception of whole individuals. Frontiers in human neuroscience, 2012. Vol. 6, pp. 108. doi: 10.3389/fnhum.2012.00108
  60. Schultz J., Pilz K.S. Natural facial motion enhances cortical responses to faces. Experimental Brain Research, 2009. Vol. 194, no. 3. P. 465–475. doi: 10.1007/s00221-009-1721-9
  61. Schwarzlose R.F., Baker C.I., Kanwisher N. Separate face and body selectivity on the fusiform gyrus. The Journal of neuroscience, 2005. Vol. 25, no. 47, pp. 11055–11059. doi: 10.1523/JNEUROSCI.2621-05.2005
  62. Kret M.E. et al. Similarities and differences in perceiving threat from dynamic faces and bodies. An fMRI study. NeuroImage, 2011. Vol. 54, no. 2, pp. 1755–1762. doi: 10.1016/j.neuroimage.2010.08.012
  63. Solomon-Harris L.M. Remote effects of OFA disruption on the face perception network revealed by consecutive TMS-fMRI. Toronto, Canada: York University, 2014. 66 p.
  64. de Gelder B. et al. Standing up for the body. Recent progress in uncovering the networks involved in the perception of bodies and bodily expressions. Neuroscience & Biobehavioral Reviews, 2010. Vol. 34, no. 4, pp. 513–527.doi: 10.1016/j.neubiorev.2009.10.008
  65. Fox C.J. et al. The correlates of subjective perception of identity and expression in the face network: An fMRI adaptation study. NeuroImage, 2009. Vol. 44, no. 2, pp. 569–580. doi: 10.1016/j.neuroimage.2008.09.011
  66. Steeves J.K.E. et al. The fusiform face area is not sufficient for face recognition: Evidence from a patient with dense prosopagnosia and no occipital face area. Neuropsychologia, 2006. Vol. 44, no. 4, pp. 594–609. doi: 10.1016/j.neuropsychologia.2005.06.013
  67. Ganel T. et al. The involvement of the “fusiform face area” in processing facial expression. Neuropsychologia, 2005. Vol. 43, no. 11, pp. 1645–1654. doi: 10.1016/j.neuropsychologia.2005.01.012
  68. Pitcher D. et al. TMS Evidence for the Involvement of the Right Occipital Face Area in Early Face Processing. Current Biology, 2007. Vol. 17, no. 18, pp. 1568–1573. doi: 10.1016/j.cub.2007.07.063
  69. Furl N. et al. Top-Down Control of Visual Responses to Fear by the Amygdala. Journal of Neuroscience, 2013. Vol. 33, no. 44, pp. 17435–17443. doi: 10.1523/JNEUROSCI.2992-13.2013
  70. Tranel D., Damasio A.R., Damasio H. Intact recognition of facial expression, gender, and age in patients with impaired recognition of face identity. Neurology, 1988. Vol. 38, no. 5, pp. 690–696. doi: 10.1212/WNL.38.5.690
  71. Pitcher D. et al. Transcranial magnetic stimulation disrupts the perception and embodiment of facial expressions. The Journal of Neuroscience, 2008. Vol. 28, no. 36, pp. 8929–8933. doi: 10.1523/JNEUROSCI.1450-08.2008
  72. Trautmann S.A., Fehr T., Herrmann M. Emotions in motion: dynamic compared to static facial expressions of disgust and happiness reveal more widespread emotion-specific activations. Brain research, 2009. Vol. 1284, pp. 100–115. doi: 10.1016/j.brainres.2009.05.075
  73. Pitcher D. et al. Triple Dissociation of Faces, Bodies, and Objects in Extrastriate Cortex. Current Biology, 2009. Vol. 19, no. 4, pp. 319–324. doi: 10.1016/j.cub.2009.01.007
  74. Pitcher D. et al. Two critical and functionally distinct stages of face and body perception. The Journal of neuroscience, 2012. Vol. 32, no. 45, pp. 15877–15885. doi: 10.1523/JNEUROSCI.2624-12.2012
  75. Candidi M. et al. Virtual lesion of right posterior superior temporal sulcus modulates conscious visual perception of fearful expressions in faces and bodies. Cortex, 2015. Vol. 65, pp. 184–194. doi: 10.1016/j.cortex.2015.01.012
  76. Schultz J. et al. What the Human Brain Likes About Facial Motion. Cerebral Cortex, 2013. Vol. 23, no. 5, pp. 1167–1178. doi: 10.1093/cercor/bhs106
  77. Gschwind M. et al.White-Matter Connectivity between Face-Responsive Regions in the Human Brain. Cerebral Cortex, 2012. Vol. 22, no. 7, pp. 1564–1576. doi: 10.1093/cercor/bhr226
  78. Wieser M.J., Brosch T. Faces in Context: A Review and Systematization of Contextual Influences on Affective Face Processing. Frontiers in Psychology, 2012. Vol. 3, pp. 471. doi: 10.3389/fpsyg.2012.00471
  79. Xu X., Biederman I. Loci of the release from fMRI adaptation for changes in facial expression, identity, and viewpoint. Journal of Vision, 2010. Vol. 10, no. 14, pp. 1–36. doi: 10.1167/10.14.36
  80. Yang J., Andric M., Mathew M.M. The neural basis of hand gesture comprehension: A meta-analysis of functional magnetic resonance imaging studies. Neuroscience & Biobehavioral Reviews, 2015. Vol. 57, pp. 88–104. doi: 10.1016/j.neubiorev.2015.08.006

Information About the Authors

Olga A. Korolkova, PhD in Psychology, professor, Leading Research Associate, Institute of Experimental Psychology, Moscow State University of Psychology & Education, Moscow, Russia, ORCID: https://orcid.org/0000-0003-4814-7266, e-mail: olga.kurakova@gmail.com

Metrics

Views

Total: 1876
Previous month: 21
Current month: 7

Downloads

Total: 916
Previous month: 6
Current month: 1