Advertisement

Brain Imaging and Behavior

, Volume 4, Issue 1, pp 55–67 | Cite as

Gender Differences in Brain Activation During Encoding and Recognition of Male and Female Faces

  • Tadashi InoEmail author
  • Ryusuke Nakai
  • Takashi Azuma
  • Toru Kimura
  • Hidenao Fukuyama
Article

Abstract

Although behavioral studies have suggested that there are gender differences regarding facial recognition, the neural substrates of these differences have not been fully examined. In order to clarify them, we performed a functional magnetic resonance imaging (fMRI) experiment in which participants encoded and recognized male and female faces. Behaviorally, the facial recognition ability of men and women was similar, and was superior for female faces compared to male faces. At the neural level, widespread areas showed greater responses for men vs. women during the encoding and recognition phase, and several areas, including the hippocampal region, showed greater responses to female vs. male faces during recognition. The reduced activation of women’s brains during encoding and recognition suggests that the relevant neural systems were more efficiently recruited in women than in men.

Keywords

Functional magnetic resonance imaging Gender Face Recognition Encoding 

References

  1. Aleman, A., & Swart, M. (2008). Sex differences in neural activation to facial expressions denoting contempt and disgust. PLoS ONE, 3, e3622.CrossRefPubMedGoogle Scholar
  2. Armony, J. L., & Sergerie, K. (2007). Own-sex effects in emotional memory for faces. Neuroscience Letters, 426, 1–5.CrossRefPubMedGoogle Scholar
  3. Breiter, H. C., Etcoff, N. L., Whalen, P. J., Kennedy, W. A., Rauch, S. L., Buckner, R. L., et al. (1996). Response and habituation of the human amygdala during visual processing of facial expression. Neuron, 17, 875–887.CrossRefPubMedGoogle Scholar
  4. Burton, A. M., Bruce, V., & Dench, N. (1993). What’s the difference between men and women? Evidence from facial measurement. Perception, 22, 153–176.CrossRefPubMedGoogle Scholar
  5. Callan, D. E., Jones, J. A., Callan, A. M., & Akahane-Yamada, R. (2004). Phonetic perceptual identification by native- and second-language speakers differentially activates brain regions involved with acoustic phonetic processing and those involved with articulatory-auditory/orosensory internal models. NeuroImage, 22, 1182–1194.CrossRefPubMedGoogle Scholar
  6. Cross, J. F., Cross, J., & Daly, J. (1971). Sex, race, age and beauty as factors in recognition of faces. Perception & Psychophysics, 10, 393–396.Google Scholar
  7. Duzel, E., Cabeza, R., Picton, T. W., Yonelinas, A. P., Scheich, H., Heinze, H.-J., et al. (1999). Task-related and item-related brain processes of memory retrieval. Proceedings of the National Academy of Science USA, 96, 1794–1799.CrossRefGoogle Scholar
  8. Ellis, H. D., Shepherd, J. W., & Bruce, A. (1973). The effects of age and sex upon adolescents’ recognition of faces. The Journal of Genetic Psychology, 123, 173–174.PubMedGoogle Scholar
  9. Feinman, S., & Entwisle, D. R. (1976). Children’s ability to recognize other children’s faces. Child Development, 47, 506–510.CrossRefPubMedGoogle Scholar
  10. Fischer, H., Sandblom, J., Herlitz, A., Fransson, P., Wright, C. I., & Bäckman, L. (2004). Sex-differential brain activation during exposure to female and male faces. NeuroReport, 15, 235–238.CrossRefPubMedGoogle Scholar
  11. Fischer, H., Sandblom, J., Nyberg, L., Herlitz, A., & Bäckman, L. (2007). Brain activation while forming memories of fearful and neutral faces in women and men. Emotion, 7, 767–773.CrossRefPubMedGoogle Scholar
  12. Fox, C. J., Moon, S. Y., Iaria, G., & Barton, J. J. (2009). The correlates of subjective perception of identity and expression in the face network: an fMRI adaptation study. NeuroImage, 44, 569–580.CrossRefPubMedGoogle Scholar
  13. Gobbini, M. I., & Haxby, J. V. (2007). Neural systems for recognition of familiar faces. Neuropsychologia, 45, 32–41.CrossRefPubMedGoogle Scholar
  14. Habel, U., Windischberger, C., Derntl, B., Robinson, S., Kryspin-Exner, I., Gur, R. C., et al. (2007). Amygdala activation and facial expressions: explicit emotion discrimination versus implicit emotion processing. Neuropsychologia, 45, 2369–2377.CrossRefPubMedGoogle Scholar
  15. Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2000). The distributed human neural system for face perception. Trends in Cognitive Science, 46, 223–233.CrossRefGoogle Scholar
  16. Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2002). Human systems for face recognition and social communication. Biological Psychiatry, 51, 59–67.CrossRefPubMedGoogle Scholar
  17. Hennenlotter, A., Schroeder, U., Erhard, P., Castrop, F., Haslinger, B., Stoecker, D., et al. (2005). A common neural basis for receptive and expressive communication of pleasant facial affect. NeuroImage, 26, 581–591.CrossRefPubMedGoogle Scholar
  18. Herlitz, A., & Yonker, J. E. (2002). Sex differences in episodic memory: the impact of intelligence. Journal of Clinical and Experimental Neuropsychology, 24, 107–114.CrossRefPubMedGoogle Scholar
  19. Herlitz, A., Nilsson, L. G., & Bäckman, L. (1997). Gender differences in episodic memory. Memory & Cognition, 25, 801–811.Google Scholar
  20. Hill, R. D., Grut, M., Wahlin, Å., Herlitz, A., Winblad, B., & Bäckman, L. (1995). Predicting memory performance in optimally healthy very old adults. Journal of Mental Health and Aging, 1, 55–65.Google Scholar
  21. Hochhaus, L. (1972). A table for the calculation of d′ and BETA. Psychological Bulletin, 77, 375–376.CrossRefGoogle Scholar
  22. Hoffman, E. A., & Haxby, J. V. (2000). Distinct representation of eye gaze and identity in the distributed human neural system for face perception. Nature Neuroscience, 3, 80–84.CrossRefPubMedGoogle Scholar
  23. Ishai, A. (2007). Sex, beauty and the orbitofrontal cortex. International Journal of Psychophysiology, 63, 181–185.CrossRefPubMedGoogle Scholar
  24. Ishai, A. (2008). Let’s face it: it’s a cortical network. NeuroImage, 40, 415–419.CrossRefPubMedGoogle Scholar
  25. Ishai, A., Pessoa, L., Bikle, P. C., & Ungerleider, L. G. (2004). Repetition suppression of faces is modulated by emotion. Proceedings of the National Academy of Science USA, 101, 9827–9832.CrossRefGoogle Scholar
  26. Ishai, A., Schmidt, C. F., & Boesiger, P. (2005). Face perception is mediated by a distributed cortical network. Brain Research Bulletin, 67, 87–93.CrossRefPubMedGoogle Scholar
  27. Kaplan, H. B. (1978). Sex differences in social interest. Journal of Individual Psychology, 34, 206–209.Google Scholar
  28. Killgore, W. D. S., & Yurgelun-Todd, D. A. (2001). Sex differences in amygdala activation during the perception of facial affect. NeuroReport, 12, 2543–2547.CrossRefPubMedGoogle Scholar
  29. Kranz, F., & Ishai, A. (2006). Face perception is modulated by sexual preference. Current Biology, 16, 63–68.CrossRefPubMedGoogle Scholar
  30. Lepage, M., Ghaffar, O., Nyberg, L., & Tulving, E. (2000). Prefrontal cortex and episodic memory retrieval mode. Proceedings of the National Academy of Science USA, 97, 506–511.CrossRefGoogle Scholar
  31. Lepsien, J., & Pollmann, S. (2002). Covert reorienting and inhibition of return: an event-related fMRI study. Journal of Cognitive Neuroscience, 14, 127–144.CrossRefPubMedGoogle Scholar
  32. Lewin, C., & Herlitz, A. (2002). Sex differences in face recognition: women’s faces make the difference. Brain and Cognition, 50, 121–128.CrossRefPubMedGoogle Scholar
  33. Mayer, R., Dorflinger, J. M., Rao, S. M., & Seidenberg, M. (2004). Neural networks underlying endogenous and exogenous visual-spatial orienting. NeuroImage, 23, 534–541.CrossRefPubMedGoogle Scholar
  34. McKelvie, S. J., Standing, L., St. Jean, D., & Law, J. (1993). Gender differences in recognition memory for faces and cars: evidence for the interest hypothesis. Bulletin of the Psychonomic Society, 31, 353–421.Google Scholar
  35. Morin, O., & Grèzes, J. (2008). What is “mirror” in the premotor cortex? A review. Clinical Neurophysiology, 38, 189–195.CrossRefPubMedGoogle Scholar
  36. Morris, J. S., Frith, C. D., Perrett, D. I., Rowland, D., Young, A. W., Calder, A. J., et al. (1996). A differential neural response in the human amygdala to fearful and happy facial expressions. Nature, 383, 812–815.CrossRefPubMedGoogle Scholar
  37. Oldfield, R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychology, 9, 97–113.CrossRefGoogle Scholar
  38. Palermo, R., & Rhodes, G. (2007). Are you always on my mind? A review of how face perception and attention interact. Neuropsychologia, 45, 75–92.CrossRefPubMedGoogle Scholar
  39. Pelphrey, K. A., Singerman, J. D., Allison, T., & McCarthy, G. (2003). Brain activation evoked by perception of gaze shifts: the influence of context. Neuropsychologia, 41, 156–170.CrossRefPubMedGoogle Scholar
  40. Phillips, M. L., Young, A. W., Senior, C., Brammer, M., Andrew, C., Calder, A. J., et al. (1997). A specific neural substrate for perceiving facial expressions of disgust. Nature, 389, 495–498.CrossRefPubMedGoogle Scholar
  41. Puce, A., Allison, T., Bentin, S., Gore, J. C., & McCarthy, G. (1998). Temporal cortex activation in humans viewing eye and mouth movements. Journal of Neuroscience, 18, 2188–2199.PubMedGoogle Scholar
  42. Rehnman, J., & Herlitz, A. (2006). Higher face recognition ability in girls: magnified by own-sex and own-ethnicity bias. Memory, 14, 289–296.CrossRefPubMedGoogle Scholar
  43. Rehnman, J., & Herlitz, A. (2007). Women remember more faces than men do. Acta Psychologica, 124, 344–355.CrossRefPubMedGoogle Scholar
  44. Rosas, A., & Bastir, M. (2002). Thin-plate spline analysis of allometry and sexual dimorphism in the human craniofacial complex. American Journal of Physical Anthropology, 117, 236–245.CrossRefPubMedGoogle Scholar
  45. Rotshtein, P., Henson, R. N., Treves, A., Driver, J., & Dolan, R. J. (2005). Morphing Marilyn into Maggie dissociates physical and identity face representations in the brain. Nature Neuroscience, 8, 107–113.CrossRefPubMedGoogle Scholar
  46. Schacter, D. L., Buckner, R. L., Koutstaal, W., Dale, A. M., & Rosen, B. R. (1997). Late onset of anterior prefrontal activity during true and false recognition: an event-related fMRI study. NeuroImage, 6, 259–269.CrossRefPubMedGoogle Scholar
  47. Schulte-Rüther, M., Markowitsch, H. J., Shah, N. J., Fink, G. R., & Piefke, M. (2008). Gender differences in brain networks supporting empathy. NeuroImage, 42, 393–403.CrossRefPubMedGoogle Scholar
  48. Sergerie, K., Lepage, M., & Armony, J. L. (2006). A process-specific functional dissociation of the amygdala in emotional memory. Journal of Cognitive Neuroscience, 18, 1359–1367.CrossRefPubMedGoogle Scholar
  49. Shapiro, P. N., & Penrod, S. (1986). Meta-analysis of facial identification studies. Psychological Bulletin, 100, 139–156.CrossRefGoogle Scholar
  50. Shaw, J. I., & Skolnick, P. (1994). Sex-differences, weapon focus, and eyewitness reliability. Journal of Social Psychology, 134, 413–420.PubMedGoogle Scholar
  51. Shaw, J. I., & Skolnick, P. (1999). Weapon focus and gender differences in eyewitness accuracy: arousal versus salience. Journal of Applied Social Psychology, 29, 2328–2341.CrossRefGoogle Scholar
  52. Somerville, L. H., Kim, H., Johnstone, T., Alexander, A. L., & Whalen, P. J. (2004). Human amygdala responses during presentation of happy and neutral faces: correlations with state anxiety. Biological Psychiatry, 55, 897–903.CrossRefPubMedGoogle Scholar
  53. Tulving, E., Kapur, S., Markowitsch, H. J., Craik, F. I., Habib, R., & Houle, S. (1994). Neuroanatomical correlates of retrieval in episodic memory: auditory sentence recognition. Proceedings of the National Academy of Science U.S.A., 91, 2012–2015.CrossRefGoogle Scholar
  54. Vuilleumier, P., Armony, J. L., Driver, J., & Dolan, R. J. (2001). Effects of attention and emotion on face processing in the human brain: an event-related fMRI study. Neuron, 30, 829–841.CrossRefPubMedGoogle Scholar
  55. Vuilleumier, P., George, N., Lister, V., Armony, J. L., & Driver, J. (2005). Effects of perceived mutual gaze and gender on face processing and recognition memory. Visual Cognition, 12, 85–101.CrossRefGoogle Scholar
  56. Wahlin, Å., Bäckman, L., Mäntylä, T., Herlitz, A., Viitanen, M., & Winblad, B. (1993). Prior knowledge and face recognition in a community-based sample of healthy, very old adults. Journal of Gerontology, 48, 54–61.Google Scholar
  57. Winston, J. S., O’Doherty, J., & Dolan, R. J. (2003). Common and distinct neural responses during direct and incidental processing of multiple facial emotions. NeuroImage, 20, 84–97.CrossRefPubMedGoogle Scholar
  58. Wright, D. B., & Sladden, B. (2003). An own gender bias and the importance of hair in face recognition. Acta Psychologica, 114, 101–114.CrossRefPubMedGoogle Scholar
  59. Yang, T. T., Menon, V., Eliez, S., Blasey, C., White, C. D., Reid, A. J., et al. (2002). Amygdalar activation associated with positive and negative facial expressions. NeuroReport, 13, 1737–1741.CrossRefPubMedGoogle Scholar
  60. Zhouand, X., & Chen, Q. (2008). Neural correlates of spatial and non-spatial inhibition of return (IOR) in attentional orienting. Neuropsychologia, 46, 2766–2775.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Tadashi Ino
    • 1
    Email author
  • Ryusuke Nakai
    • 2
  • Takashi Azuma
    • 2
  • Toru Kimura
    • 1
  • Hidenao Fukuyama
    • 3
  1. 1.Department of NeurologyRakuwakai-Otowa HospitalKyotoJapan
  2. 2.Research Center for Nano Medical Engineering, Institute for Frontier Medical SciencesKyoto UniversityKyotoJapan
  3. 3.Department of Brain Pathophysiology, Human Brain Research Center, Graduate School of MedicineKyoto UniversityKyotoJapan

Personalised recommendations