Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Tuning the developing brain to social signals of emotions

Nature Reviews Neuroscience volume 10, pages 37–47 (2009)Cite this article

Key Points

  • Most humans develop a capacity to recognize the emotional signals of different facial expressions. This capacity is mediated by a brain network that involves emotion-related brain circuits (including the amygdala and the orbitofrontal cortex) and higher-level visual representation areas (the fusiform gyrus and the superior temporal sulcus).

  • Human infants start to discriminate facial expressions by the second half of their first year. At approximately the same age, they begin to exhibit adult-like attentional bias towards certain salient facial expressions (such as expressions of fear), as well as enhanced vision- and attention-related event-related brain potentials to fearful facial expressions.

  • These findings, together with experimental lesion and anatomical tracing studies in other species, suggest that the key components of the emotion-processing network and their interconnections are established and become functional early in postnatal life.

  • Developmental studies in humans and monkeys have further shown that face-processing mechanisms are initially broadly tuned (activated by a broad range of stimuli, such as human and monkey faces) but narrow and become more specialized for specific types of perceptual discriminations with experience (discrimination of information in human faces).

  • Collectively, these data suggest that the acquisition of representations of facial expressions may reflect the functional emergence of an experience-expectant mechanism by the second half of the first year and rapid experience-driven attunement of this mechanism to species-typical facial expressions.

  • Specifically, components of the emotion-processing network (such as the amygdala) may be to a limited extent prepared for processing and storing information about biologically salient cues, but they require exposure to facial expressions at a specific developmental time point ('expected experience') in order to be refined and develop towards more mature forms.

  • Although the basic organization of the emotion-recognition networks is specified by an experience-expectant neural circuitry that emerges during a sensitive period, representations of facial expressions are likely to be continually fine-tuned by individual-specific experiences (reflecting the experience-dependent development of facial-expression processing).

  • Genetically driven differences in the reactivity of emotion-related brain circuits (for example, polymorphisms that affect serotonin transmission and amygdala reactivity) might, in combination with environmental factors (such as exposure to negative emotions), bias the developmental process towards heightened sensitivity to signals of certain negative emotions.

Abstract

Humans in different cultures develop a similar capacity to recognize the emotional signals of diverse facial expressions. This capacity is mediated by a brain network that involves emotion-related brain circuits and higher-level visual-representation areas. Recent studies suggest that the key components of this network begin to emerge early in life. The studies also suggest that initial biases in emotion-related brain circuits and the early coupling of these circuits and cortical perceptual areas provide a foundation for a rapid acquisition of representations of those facial features that denote specific emotions.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: An emotion-processing network in the brain.
Figure 2: Development of facial-emotion discrimination in infancy.
Figure 3: Emotional influences on attention and perception in infants.
Figure 4: A proposed model of the development of emotion-recognition mechanisms.

Similar content being viewed by others

References

  1. Ekman, P., Sorenson, E. R. & Friesen, W. V. Pan-cultural elements in facial displays of emotion. Science 164, 86–88 (1969).

    CAS  PubMed  Google Scholar 

  2. Ekman, P. & Friesen, W. V. A new pan-cultural facial expression of emotion. Motiv. Emot. 10, 159–168 (1986).

    Google Scholar 

  3. Levenson, R. W. in Handbook of Affective Sciences (eds Davidson, R. J., Scherer, K. R. & Goldsmith, H. H.) 212–224 (Oxford Univ. Press, New York, 2003).

    Google Scholar 

  4. Vuilleumier, P. How brains beware: neural mechanisms of emotional attention. Trends Cogn. Sci. 9, 585–594 (2005). Presents an overview of studies showing that the respective influences of voluntary attention (task relevance) and affective significance on sensory processing are dissociable and mediated by distinct neural mechanisms.

    PubMed  Google Scholar 

  5. Pourtois, G., Grandjean, D., Sander, D. & Vuilleumier, P. Electrophysiological correlates of rapid spatial orienting towards fearful faces. Cereb. Cortex 14, 619–633 (2004).

    PubMed  Google Scholar 

  6. Milders, M., Sahraie, A., Logan, S. & Donnellon, N. Awareness of faces is modulated by their emotional meaning. Emotion 6, 10–17 (2006).

    PubMed  Google Scholar 

  7. Yang, E., Zald, D. H. & Blake, R. Fearful expressions gain preferential access to awareness during continuous flash suppression. Emotion 7, 882–886 (2007).

    PubMed  PubMed Central  Google Scholar 

  8. Georgiou, G. A. et al. Focusing on fear: attentional disengagement from emotional faces. Vis. Cogn. 12, 145–158 (2005).

    PubMed  PubMed Central  Google Scholar 

  9. Leppänen, J. M., Hietanen, J. K. & Koskinen, K. Differential early ERPs to fearful versus neutral facial expressions: a response to the salience of the eyes? Biol. Psychol. 78, 150–158 (2008).

    PubMed  Google Scholar 

  10. Batty, M. & Taylor, M. J. Early processing of the six basic facial emotional expressions. Cogn. Brain Res. 17, 613–620 (2003).

    Google Scholar 

  11. Morris, J. S. et al. A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain 121, 47–57 (1998).

    PubMed  Google Scholar 

  12. Hadj-Bouziane, F., Bell, A. H., Knusten, T. A., Ungerleider, L. G. & Tootell, R. B. H. Perception of emotional expressions is independent of face selectivity in monkey inferior temporal cortex. Proc. Natl Acad. Sci. USA 105, 5591–5596 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Hooker, C. I., Germine, L. T., Knight, R. T. & D'Esposito, M. Amygdala response to facial expressions reflects emotional learning. J. Neurosci. 26, 8915–8922 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Adolphs, R. Neural systems for recognizing emotion. Curr. Opin. Neurobiol. 12, 169–177 (2002).

    CAS  PubMed  Google Scholar 

  15. Luo, Q., Holroyd, T., Jones, M., Hendler, T. & Blair, J. Neural dynamics for facial threat processing as revealed by gamma band synchronization using MEG. Neuroimage 34, 839–847 (2007).

    PubMed  Google Scholar 

  16. Vuilleumier, P., Armony, J. L., Driver, J. & Dolan, R. J. Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nature Neurosci. 6, 624–631 (2003).

    CAS  PubMed  Google Scholar 

  17. Vuilleumier, P., Richardson, M. P., Armony, J. L., Driver, J. & Dolan, R. J. Distant influences of amygdala lesion on visual cortical activation during emotional face processing. Nature Neurosci. 7, 1271–1278 (2004). Showed that the amygdala is critically involved in enhanced perceptual processing of emotionally expressive faces.

    CAS  PubMed  Google Scholar 

  18. Anderson, A. K. & Phelps, E. A. Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature 411, 305–309 (2001).

    CAS  PubMed  Google Scholar 

  19. Freese, J. L. & Amaral, D. G. The organization of projections from the amygdala to visual cortical areas TE and V1 in the macaque monkey. J. Comp. Neurol. 486, 295–317 (2005).

    PubMed  Google Scholar 

  20. Freese, J. L. & Amaral, D. G. Synaptic organization of projections from the amygdala to visual cortical areas TE and V1 in the macaque monkey. J. Comp. Neurol. 496, 655–667 (2006).

    PubMed  PubMed Central  Google Scholar 

  21. Amaral, D. G., Behniea, H. & Kelly, J. L. Topographic organization of projections from the amygdala to the visual cortex in the macaque monkey. Neuroscience 118, 1099–1120 (2003).

    CAS  PubMed  Google Scholar 

  22. Kapp, B. S., Supple, W. F. & Whalen, P. J. Effects of electrical stimulation of the amygdaloid central nucleus on neocortical arousal in the rabbit. Behav. Neurosci. 108, 81–93 (1994).

    CAS  PubMed  Google Scholar 

  23. Bentley, P., Vuilleumier, P., Thiel, C. M., Driver, J. & Dolan, R. J. Cholinergic enhancement modulates neural correlates of selective attention and emotional processing. Neuroimage 20, 58–70 (2003).

    PubMed  Google Scholar 

  24. Whalen, P. J. Fear, vigilance, and ambiguity: initial neuroimaging studies of the human amygdala. Curr. Dir. Psychol. Sci. 7, 177–188 (1998).

    Google Scholar 

  25. Adolphs, R. Fear, faces, and the human amygdala. Curr. Opin. Neurobiol. 18, 166–172 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Paton, J. J., Belova, M. A., Morrison, S. E. & Salzman, C. D. The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 439, 865–870 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Hornak, J. et al. Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices. Brain 126, 1691–1712 (2003).

    CAS  PubMed  Google Scholar 

  28. O'Doherty, J. et al. Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness. Neuropsychologia 41, 147–155 (2003).

    CAS  PubMed  Google Scholar 

  29. Blair, R. J. R., Morris, J. S., Frith, C. D., Perrett, D. I. & Dolan, R. J. Dissociable neural responses to facial expressions of sadness and anger. Brain 122, 883–893 (1999).

    PubMed  Google Scholar 

  30. Rolls, E. T. The representation of information about faces in the temporal and frontal lobes. Neuropsychologia 45, 124–143 (2007).

    PubMed  Google Scholar 

  31. Hooker, C. I., Verosky, S. C., Miyakawa, A., Knight, R. T. & D'Esposito, M. The influence of personality on neural mechanisms of observational fear and reward learning. Neuropsychologia 46, 2709–2724 (2008).

    PubMed  PubMed Central  Google Scholar 

  32. Cavada, C., Company, T., Tejedor, J., Cruz-Rizzolo, R. J. & Reinoso-Suarez, F. The anatomical connections of the macaque monkey orbitofrontal cortex: a review. Cereb. Cortex 10, 220–242 (2000).

    CAS  PubMed  Google Scholar 

  33. Bar, M. et al. Top-down facilitation of visual recognition. Proc. Natl Acad. Sci. USA 103, 449–454 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Kringelbach, M. L. et al. A specific and rapid neural signature for parental instinct. PLoS ONE 3, e1664 (2008).

    PubMed  PubMed Central  Google Scholar 

  35. Canli, T. Toward a neurogenetic theory of neuroticism. Ann. NY Acad. Sci. 1129, 153–174 (2008).

    PubMed  Google Scholar 

  36. Fox, E., Mathews, A., Calder, A. J. & Yiend, J. Anxiety and sensitivity to gaze direction in emotionally expressive faces. Emotion 7, 478–486 (2007).

    PubMed  PubMed Central  Google Scholar 

  37. Etkin, A. et al. Individual differences in trait anxiety predict the response of the basolateral amygdala to unconsciously processed fearful faces. Neuron 44, 1043–1055 (2004).

    CAS  PubMed  Google Scholar 

  38. Stein, M. B., Simmons, A. N., Feinstein, J. S. & Paulus, M. P. Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. Am. J. Psychiatry 164, 318–327 (2007).

    PubMed  Google Scholar 

  39. Hare, T. A. et al. Biological substrates of emotional reactivity and regulation in adolescence during an emotional go-nogo task. Biol. Psychiatry 63, 927–934 (2008).

    PubMed  PubMed Central  Google Scholar 

  40. Sorce, F. F., Emde, R. N., Campos, J. J. & Klinnert, M. D. Maternal emotional signaling: its effect on the visual cliff behavior of 1-year-olds. Dev. Psychol. 21, 195–200 (1985).

    Google Scholar 

  41. Johnson, M. H. Subcortical face processing. Nature Rev. Neurosci. 6, 766–774 (2005).

    CAS  Google Scholar 

  42. Banks, M. S. & Salapatek, P. in Handbook of Child Psychology (eds Haith, M. M. & Campos, J. J.) 435–571 (Wiley, New York, 1983).

    Google Scholar 

  43. Bushnell, I. W. R. Modification of the externality effect in young infants. J. Exp. Child Psychol. 28, 211–229 (1979).

    CAS  PubMed  Google Scholar 

  44. Maurer, D. & Salapatek, P. Developmental changes in the scanning of faces by young infants. Child Dev. 47, 523–527 (1976).

    CAS  PubMed  Google Scholar 

  45. Field, T. M., Woodson, R. W., Greenberg, R. & Cohen, C. Discrimination and imitation of facial expressions by neonates. Science 218, 179–181 (1982).

    CAS  PubMed  Google Scholar 

  46. Kestenbaum, R. & Nelson, C. A. The recognition and categorization of upright and inverted emotional expressions by 7-month-old infants. Infant Behav. Dev. 13, 497–511 (1990).

    Google Scholar 

  47. Bornstein, M. H. & Arterberry, M. E. Recognition, discrimination and categorization of smiling by 5-month-old infants. Dev. Sci. 6, 585–599 (2003).

    Google Scholar 

  48. Ludemann, P. M. & Nelson, C. A. Categorical representation of facial expressions by 7-month-old infants. Dev. Psychol. 24, 492–501 (1988).

    Google Scholar 

  49. Nelson, C. A., Morse, P. A. & Leavitt, L. A. Recognition of facial expressions by 7-month-old infants. Child Dev. 50, 1239–1242 (1979). One of the first papers to report that infants can perceptually discriminate certain facial expressions from one another (specifically, happy and fearful expressions) and prefer to look longer at fearful faces than happy faces.

    CAS  PubMed  Google Scholar 

  50. Bahrick, L. E., Lickliter, R. & Flom, R. Intersensory redundancy guides the development of selective attention, perception, and cognition. Curr. Dir. Psychol. Sci. 13, 99–102 (2004).

    Google Scholar 

  51. Flom, R. & Bahrick, L. E. The development of infant discrimination of affect in multimodal and unimodal stimulation: the role of intersensory redundancy. Dev. Psychol. 43, 238–252 (2007).

    PubMed  PubMed Central  Google Scholar 

  52. Walker-Andrews, A. S. Infants' perception of expressive behaviors: differentiation of multimodal information. Psychol. Bull. 121, 437–456 (1997).

    CAS  PubMed  Google Scholar 

  53. Kotsoni, E., de Haan, M. & Johnson, M. H. Categorical perception of facial expressions by 7-month-old infants. Perception 30, 1115–1125 (2001).

    CAS  PubMed  Google Scholar 

  54. Nelson, C. A. & Dolgin, K. The generalized discrimination of facial expressions by 7-month-old infants. Child Dev. 56, 58–61 (1985).

    CAS  PubMed  Google Scholar 

  55. Peltola, M. J., Leppänen, J. M., Palokangas, T. & Hietanen, J. K. Fearful faces modulate looking duration and attention disengagement in 7-month-old infants. Dev. Sci. 11, 60–68 (2008). Provided evidence for adult-like emotion–attention interactions in infants and showed that the influence of fearful faces on attention in infants is not simply attributable to the novelty of these faces.

    PubMed  Google Scholar 

  56. de Haan, M., Johnson, M. H. & Halit, H. Development of face-sensitive event-related potentials during infancy: a review. Int. J. Psychophysiol. 51, 45–58 (2003).

    PubMed  Google Scholar 

  57. de Haan, M. & Nelson, C. A. Brain activity differentiates face and object processing in 6-month-old infants. Dev. Psychol. 35, 1113–1121 (1999). Provided electrophysiological evidence that the brain of the typically developing 6-month-old infant distinguishes between faces and non-face objects.

    CAS  PubMed  Google Scholar 

  58. de Haan, M., Pascalis, O. & Johnson, M. H. Specialization of neural mechanisms underlying face recognition in human infants. J. Cogn. Neurosci. 14, 199–209 (2002).

    PubMed  Google Scholar 

  59. Halit, H., Csibra, G., Volein, Á . & Johnson, M. H. Face-sensitive cortical processing in early infancy. J. Child Psychol. Psychiatry 45, 1228–1234 (2004).

    PubMed  Google Scholar 

  60. Halit, H., de Haan, M. & Johnson, M. H. Cortical specialization for face processing: face-sensitive event-related potential components in 3- and 12-month-old infants. Neuroimage 19, 1180–1193 (2003).

    CAS  PubMed  Google Scholar 

  61. Tzourio-Mazoyer, N. et al. Neural correlates of woman face processing by 2-month-old infants. Neuroimage 15, 454–461 (2002).

    PubMed  Google Scholar 

  62. Otsuka, Y. et al. Neural activation to upright and inverted faces in infants measured by near infrared spectroscopy. Neuroimage 34, 399–406 (2007).

    PubMed  Google Scholar 

  63. Amaral, D. G. & Bennett, J. Development of amygdalo-cortical connection in the macaque monkey. Soc. Neurosci. Abstr. 26, 17–26 (2000).

    Google Scholar 

  64. Machado, C. J. & Bachevalier, J. Non-human primate models of childhood psychopathology: the promise and the limitations. J. Child Psychol. Psychiatry 44, 64–87 (2003).

    PubMed  Google Scholar 

  65. Minagawa-Kawai, Y. et al. Prefrontal activation associated with social attachment: facial emotion recognition in mothers and infants. Cereb. Cortex 30 May 2008 (doi:10.1093/cercor/bhn081). Reported an optical-imaging study which showed that the orbitofrontal cortex is involved in processing happy facial expressions in infants.

    PubMed  Google Scholar 

  66. Leppänen, J. M., Moulson, M. C., Vogel-Farley, V. K. & Nelson, C. A. An ERP study of emotional face processing in the adult and infant brain. Child Dev. 78, 232–245 (2007). Reported evidence that affective significance modulates the early stages of cortical face processing in adults and 7-month-old infants.

    PubMed  PubMed Central  Google Scholar 

  67. Nelson, C. A. & de Haan, M. Neural correlates of infants' visual responsiveness to facial expressions of emotions. Dev. Psychobiol. 29, 577–595 (1996). Examined the neural correlates of infants' ability to discriminate facial expressions of emotion.

    CAS  PubMed  Google Scholar 

  68. de Haan, M. in Infant EEG and event-related potentials (ed. de Haan, M.) 101–143 (Psychology Press, New York, 2007).

    Google Scholar 

  69. Nelson, C. A. in Human Behavior and the Developing Brain (eds Dawson, G. & Fischer, K.) 269–313 (Guilford Press, New York, 1994).

    Google Scholar 

  70. Reynolds, G. D. & Richards, J. E. Familiarization, attention, and recognition memory in infancy: an event-related-potential and cortical source localization study. Dev. Psychol. 41, 598–615 (2005).

    PubMed  PubMed Central  Google Scholar 

  71. Bush, G., Luu, P. & Posner, M. I. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 4, 215–222 (2000).

    CAS  PubMed  Google Scholar 

  72. Hoehl, S., Palumbo, L., Heinisch, C. & Striano, T. Infants' attention is biased by emotional expressions and eye gaze direction. Neuroreport 19, 579–582 (2008).

    PubMed  Google Scholar 

  73. Hoehl, S., Wiese, L. & Striano, T. Young infants' neural processing of objects is affected by eye gaze direction and emotional expression. PLoS ONE 3, e2389 (2008). Provided evidence that infants use information from adults gaze direction and emotional expression to enhance attention towards certain objects.

    PubMed  PubMed Central  Google Scholar 

  74. Bauman, M. D., Lavenex, P., Mason, W. A., Capitanio, J. P. & Amaral, D. G. The development of social behavior following neonatal amygdala lesions in rhesus monkeys. J. Cogn. Neurosci. 16, 1388–1411 (2004).

    CAS  PubMed  Google Scholar 

  75. Moriceau, S. & Sullivan, R. M. Maternal presence serves as a switch between learning fear and attraction in infancy. Nature Neurosci. 9, 1004–1006 (2004).

    Google Scholar 

  76. Thompson, J. V., Sullivan, R. M. & Wilson, D. A. Developmental emergence of fear learning corresponds with changes in amygdala synaptic plasticity. Brain Res. 1200, 58–65 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Farroni, T., Menon, E., Rigato, S. & Johnson, M. H. The perception of facial expressions in newborns. Eur. J. Dev. Psychol. 4, 2–13 (2007).

    PubMed  PubMed Central  Google Scholar 

  78. Greenough, W. T., Black, J. E. & Wallace, C. S. Experience and brain development. Child Dev. 58, 539–559 (1987). A theoretical review that illustrates the differences between experience-expectant and experience-dependent plasticity and learning.

    CAS  PubMed  Google Scholar 

  79. Pascalis, O., de Haan, M. & Nelson, C. A. Is face processing species-specific during the first year of life? Science 296, 1321–1323 (2002). The first study to show that face-processing mechanisms are initially broadly tuned but narrow with experience.

    CAS  PubMed  Google Scholar 

  80. Pascalis, O. et al. Plasticity of face processing in infancy. Proc. Natl Acad. Sci. USA 102, 5297–5300 (2005). Demonstrated that one can rescue the sensitive period for discriminating monkey faces by providing infants with distributed exposure to monkey faces.

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Lewkowicz, D. J. & Ghazanfar, A. A. The decline of cross-species intersensory perception in human infants. Proc. Natl Acad. Sci. USA 103, 6771–6774 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Weikum, W. M. et al. Visual language discrimination in infancy. Science 316, 1159 (2007).

    CAS  PubMed  Google Scholar 

  83. Scott, L. S., Pascalis, O. & Nelson, C. A. A domain general theory of the development of perceptual discrimination. Curr. Dir. Psychol. Sci. 16, 197–201 (2007).

    PubMed  PubMed Central  Google Scholar 

  84. Sugita, Y. Face perception in monkeys reared with no exposure to faces. Proc. Natl Acad. Sci. USA 105, 394–398 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Pollak, S. D., Cicchetti, D., Hornung, K. & Reed, A. Recognizing emotion in faces: developmental effects of child abuse and neglect. Dev. Psychol. 36, 679–688 (2000).

    PubMed  Google Scholar 

  86. Pollak, S. D. & Kistler, D. J. Early experience is associated with the development of categorical representations for facial expression of emotions. Proc. Natl Acad. Sci. USA 88, 7572–7575 (2002). Reported evidence of experience-dependent plasticity in brain networks underlying perception of universal facial expressions.

    Google Scholar 

  87. Pollak, S. D., Klorman, R., Thatcher, J. E. & Cicchetti, D. P3b reflects maltreated children's reactions to facial displays of emotion. Psychophysiology 38, 264–274 (2001).

    Google Scholar 

  88. Pollak, S. D. & Sinha, P. Effects of early experience on children's recognition of facial displays of emotion. Dev. Psychol. 38, 784–791 (2002).

    PubMed  Google Scholar 

  89. Pollak, S. D. & Tolley-Schell, S. A. Selective attention to facial emotion in physically abused children. J. Abnorm. Psychol. 112, 323–338 (2003).

    PubMed  Google Scholar 

  90. Salzman, C. D., Paton, J. J., Belova, M. A. & Morrison, S. E. Flexible neural representations of value in the primate brain. Ann. NY Acad. Sci. 1121, 336–354 (2007).

    PubMed  Google Scholar 

  91. Weinberger, N. M. Specific long-term memory traces in primary auditory cortex. Nature Rev. Neurosci. 5, 279–290 (2004).

    CAS  Google Scholar 

  92. Keil, A., Stolarova, M., Moratti, S. & Ray, W. J. Adaptation in human visual cortex as a mechanism for rapid discrimination of aversive stimuli. Neuroimage 36, 472–479 (2007).

    PubMed  Google Scholar 

  93. Lim, S. L. & Pessoa, L. Affective learning increases sensitivity to graded emotional faces. Emotion 8, 96–103 (2008).

    PubMed  Google Scholar 

  94. Pizzagalli, D. A., Greischar, L. L. & Davidson, R. J. Spatio-temporal dynamics of brain mechanisms in aversive classical conditioning: high-density event-related potential and brain electrical tomography analyses. Neuropsychologia 41, 184–194 (2003).

    PubMed  Google Scholar 

  95. Olsson, A. & Phelps, E. A. Social learning of fear. Nature Neurosci. 10, 1095–1102 (2007).

    CAS  PubMed  Google Scholar 

  96. Mathews, A. & MacLeod, C. Cognitive vulnerability to emotional disorders. Annu. Rev. Clin. Psychol. 1, 167–195 (2005).

    PubMed  Google Scholar 

  97. Hariri, A. R. et al. Serotonin transporter genetic variation and the response of the human amygdala. Science 297, 400–403 (2002).

    CAS  PubMed  Google Scholar 

  98. Caspi, A. et al. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301, 386–389 (2003).

    CAS  PubMed  Google Scholar 

  99. Hariri, A. R. & Holmes, A. Genetics of emotional regulation: the role of the serotonin transporter in neural function. Trends Cogn. Sci. 10, 182–191 (2006).

    PubMed  Google Scholar 

  100. Lakatos, K. et al. Association of D4 dopamine receptor gene and serotonin transporter promoter polymorphisms with infants' response to novelty. Mol. Psychiatry 8, 90–97 (2003).

    CAS  PubMed  Google Scholar 

  101. Bishop, S. J. Neurocognitive mechanisms of anxiety: an integrative account. Trends Cogn. Sci. 11, 307–317 (2007).

    PubMed  Google Scholar 

  102. Moulson, M. C. & Nelson, C. A. Early adverse experiences and the neurobiology of facial emotion processing. Dev. Psychol. (in the press).

  103. Nelson, C. A., Parker, S. W. & Guthrie, D. The discrimination of facial expressions by typically developing infants and toddlers and those experiencing early institutional care. Infant Behav. Dev. 29, 210–219 (2006).

    PubMed  Google Scholar 

  104. Widen, S. C. & Russell, J. A. A closer look at preschoolers' freely produced labels for facial expressions. Dev. Psychol. 39, 114–128 (2003).

    PubMed  Google Scholar 

  105. Cunningham, M. G., Bhattacharyya, S. & Benes, F. M. Amygdalo-cortical sprouting continues into early adulthood: implications for the development of normal and abnormal function during adolescence. J. Comp. Neurol. 453, 116–130 (2002).

    PubMed  Google Scholar 

  106. Hariri, A. R., Bookheimer, S. Y. & Mazziotta, J. C. Modulating emotional responses: effects of a neocortical network on the limbic system. Neuroreport 11, 43–48 (2000).

    CAS  PubMed  Google Scholar 

  107. Kim, H. et al. Contextual modulation of amygdala responsivity to surprised faces. J. Cogn. Neurosci. 16, 1730–1743 (2004).

    PubMed  Google Scholar 

  108. Cohen Kadosh, K. & Johnson, M. H. Developing a cortex specialized for face perception. Trends Cogn. Sci. 11, 367–369 (2007).

    PubMed  Google Scholar 

  109. Humphrey, T. The development of the human amygdala during early embryonic life. J. Comp. Neurol. 132, 135–165 (1968).

    CAS  PubMed  Google Scholar 

  110. Kordower, J. H., Piecinski, P. & Rakic, P. Neurogenesis of the amygdaloid nuclear complex in the rhesus monkey. Brain Res. Dev. Brain Res. 68, 9–15 (1992).

    CAS  PubMed  Google Scholar 

  111. Nikolic, I. & Kostovic, I. Development of the lateral amygdaloid nucleus in the human fetus: transient presence of discrete cytoarchitectonic units. Anat. Embryol. (Berl.) 174, 355–360 (1986).

    CAS  Google Scholar 

  112. Bachevalier, J., Ungerleider, L. G., O'Neill, J. B. & Friedman, D. P. Regional distribution of [3H] naloxone binding in the brain of a newborn rhesus monkey. Brain Res. 390, 302–308 (1986).

    CAS  PubMed  Google Scholar 

  113. Berger, B., Febvret, A., Greengard, P. & Goldman-Rakic, P. S. DARPP-32, a phosphoprotein enriched in dopaminoceptive neurons bearing dopamine D1 receptors: distribution in the cerebral cortex of the newborn and adult rhesus monkey. J. Comp. Neurol. 299, 327–348 (1990).

    CAS  PubMed  Google Scholar 

  114. Prather, M. D. & Amaral, D. G. The development and distribution of serotonergic fibers in the macaque monkey amygdala. Soc. Neurosci. Abstr. 26, 1727 (2000).

    Google Scholar 

  115. Webster, M. J., Bachevalier, J. & Ungerleider, L. G. Connections of inferior temporal area TEO and TE with parietal and frontal cortex in macaque monkeys. Cereb. Cortex 5, 470–483 (1994).

    Google Scholar 

  116. Webster, M. J., Ungerleider, L. G. & Bachevalier, J. Connections of inferior temporal areas TE and TEO with medial temporal-lobe structures in infant and adult monkeys. J. Neurosci. 11, 1095–1116 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  117. Rodman, H. R. & Consuelos, M. J. Cortical projections to anterior inferior temporal cortex in infant macaque monkeys. Vis. Neurosci. 11, 119–133 (1994).

    CAS  PubMed  Google Scholar 

  118. Afraz, S.-R., Kiani, R. & Esteky, H. Microstimulation of inferotemporal cortex influences face categorization. Nature 442, 692–695 (2006).

    CAS  PubMed  Google Scholar 

  119. Hasselmo, M. E., Rolls, E. T. & Baylis, G. C. The role of expression and identity in the face-selective responses of neurons in the temporal visual cortex of the monkey. Behav. Brain Res. 32, 203–218 (1989).

    CAS  PubMed  Google Scholar 

  120. Sugase, Y., Yamane, S., Ueno, S. & Kawano, K. Global and fine information coded by single neurons in the temporal visual cortex. Nature 400, 869–873 (1999).

    Google Scholar 

  121. Tsao, D. Y., Freiwald, W. A., Tootell, R. B. H. & Livingstone, M. S. A cortical region consisting entirely of face-selective cells. Science 311, 670–674 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  122. Bentin, S., Allison, T., Puce, A., Perez, E. & McCarthy, G. Electrophysiological studies of face perception in humans. J. Cogn. Neurosci. 8, 551–565 (1996).

    PubMed  PubMed Central  Google Scholar 

  123. Hoffman, E. A. & Haxby, J. V. Distinct representations of eye gaze and identity in the distributed human neural system for face perception. Nature Neurosci. 3, 80–84 (2000).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  125. LaBar, K. S., Crupain, M. J., Voyvodic, J. T. & McCarthy, G. Dynamic perception of facial affect and identity in the human brain. Cereb. Cortex 13, 1023–1033 (2003).

    PubMed  Google Scholar 

  126. Engell, A. D. & Haxby, J. V. Facial expression and gaze-direction in human superior temporal sulcus. Neuropsychologia 45, 3234–3241 (2007).

    PubMed  Google Scholar 

  127. Haxby, J. V., Hoffman, E. A. & Gobbini, M. I. Human neural systems for face recognition and social communication. Biol. Psychiatry 15, 59–67 (2002).

    Google Scholar 

  128. Calder, A. J. & Young, A. W. Understanding the recognition of facial identity and facial expression. Nature Rev. Neurosci. 6, 641–651 (2005).

    CAS  Google Scholar 

  129. Calder, A. J., Young, A. W., Keane, J. & Dean, M. Configural information in facial expression perception. J. Exp. Psychol. Hum. Percept. Perform. 26, 527–551 (2000).

    CAS  PubMed  Google Scholar 

  130. Ambadar, Z., Schooler, J. W. & Cohn, J. F. Deciphering the enigmatic face: the importance of facial dynamics in interpreting subtle facial expressions. Psychol. Sci. 16, 403–410 (2005).

    PubMed  Google Scholar 

  131. Adams, R. B. J. & Kleck, R. E. Perceived gaze direction and the processing of facial displays of emotion. Psychol. Sci. 14, 644–647 (2003).

    PubMed  Google Scholar 

  132. Campanella, S. & Belin, P. Integrating face and voice in person perception. Trends Cogn. Sci. 11, 535–543 (2007).

    PubMed  Google Scholar 

  133. Kreifelts, B., Ethofer, T., Grodd, W., Erb, M. & Wildgruber, D. Audiovisual integration of emotional signals in voice and face: an event-related fMRI study. Neuroimage 37, 1445–1456 (2007).

    PubMed  Google Scholar 

  134. Puce, A. & Perrett, D. Electrophysiology and brain imaging of biological motion. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 435–445 (2003).

    PubMed  PubMed Central  Google Scholar 

  135. Möttönen, R. et al. Perceiving identical sounds as speech or non-speech modulates activity in the left posterior superior temporal sulcus. Neuroimage 30, 563–569 (2006).

    PubMed  Google Scholar 

  136. Hein, G. & Knight, R. T. Superior temporal sulcus - it's my area: or is it? J. Cogn. Neurosci. 20, 1–12 (2008).

    Google Scholar 

  137. Redcay, E. The superior temporal sulcus performs a common function for social and speech perception: implications for the emergence of autism. Neurosci. Biobehav. Rev. 32, 123–142 (2008).

    PubMed  Google Scholar 

  138. Phelps, E. A., Ling, S. & Carrasco, M. Emotion facilitates perception and potentiates the perceptual benefits of attention. Psychol. Sci. 17, 292–299 (2006).

    PubMed  Google Scholar 

Download references

Acknowledgements

C.A.N. gratefully acknowledges support from the US National Institutes of Health (MH078829) and the Richard David Scott endowment; J.M.L. acknowledges financial support from the Academy of Finland (grant number 1115536). The authors thank J. Kagan for his comments on an earlier draft of this article.

Author information

Authors and Affiliations

  1. Department of Psychology, University of Tampere, Tampere, Finland

    Jukka M. Leppänen

  2. Children's Hospital Boston/Harvard Medical School, Developmental Medicine Center Laboratories of Cognitive Neuroscience, 1 Autumn Street, Office AU621, Mailbox 713, Boston, 021155365, Massachusetts, USA

    Charles A. Nelson

Authors
  1. Jukka M. Leppänen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Charles A. Nelson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Charles A. Nelson.

Related links

Related links

FURTHER INFORMATION

Charles Nelson's homepage

Glossary

Universal facial expressions

A limited set of emotional facial expressions that seem to be recognized universally (by members of different cultures).

Magnocellular pathway

A system of vision-responsive cells that are characterized by large axons and the rapid transmission of nerve impulses.

Near-infra-red spectroscopy

A technique used for measuring changes in haemoglobin concentrations and oxygenation levels that can be used to study changes in brain activity in localized cortical regions.

Experience-expectant mechanisms

Evolved neural mechanisms and plasticity for processing and storing information that is expected to be common to all members of the species; for example, patterned light, faces, speech and language.

Experience-dependent mechanisms

Neural mechanisms and plasticity for processing information that is unique to the individual; for example, individual differences in processing cognitive, linguistic or social challenges. In the cognitive sphere, for example, learning and memory reflect an experience-dependent process.

Perceptual narrowing

A developmental process in which discrimination of frequently encountered stimulus features is maintained and improved whereas discrimination of less frequently encountered stimulus features is diminished or lost; for example, the gradual loss of the ability to discriminate non-native speech contrasts while retaining the ability to discriminate native speech contrasts.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Leppänen, J., Nelson, C. Tuning the developing brain to social signals of emotions. Nat Rev Neurosci 10, 37–47 (2009). https://doi.org/10.1038/nrn2554

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrn2554

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing