Location via proxy:   [ UP ]  
[Report a bug]   [Manage cookies]                
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:

Neural bases of the non-conscious perception of emotional signals

Nature Reviews Neuroscience volume 11, pages 697–709 (2010)Cite this article

Subjects

Key Points

  • Many emotional signals are processed without being consciously perceived.

  • Non-conscious perception of emotional stimuli is present in both healthy observers, as a consequence of experimental manipulation, and in neurological conditions resulting from focal brain damage, such as hemispatial neglect and cortical blindness.

  • An emotional stimulus can be perceived non-consciously because it falls outside the focus of attention (a phenomenon referred to as attentional unawareness) or because its sensory analysis is hampered (a phenomenon referred to as sensory unawareness). Although both phenomena render the observer unaware of the stimulus, they involve different neural processes.

  • Non-conscious perception of emotional stimuli involves a neural system that is composed of subcortical structures, such as the superior colliculus, the visual pulvinar and the amygdala. This neural system receives visual information directly from the retina — thus bypassing the visual cortex — and has an old evolutionary origin, being present in other species like birds, rats and monkeys.

  • The function of this subcortical system is to provide a rapid, but coarse, analysis of the visual stimuli in order to provide reflex-like responses to emotional signals in the environment. Neurophysiological changes and expressive reactions associated with non-conscious perception of emotional stimuli are consistently more rapid and more intense than responses associated with conscious perception of the same stimuli.

  • The subcortical system for emotion processing influences cortical activity in several direct and indirect ways. The extent of this cortico–subcortical integration is a crucial factor in affecting visual awareness.

Abstract

Many emotional stimuli are processed without being consciously perceived. Recent evidence indicates that subcortical structures have a substantial role in this processing. These structures are part of a phylogenetically ancient pathway that has specific functional properties and that interacts with cortical processes. There is now increasing evidence that non-consciously perceived emotional stimuli induce distinct neurophysiological changes and influence behaviour towards the consciously perceived world. Understanding the neural bases of the non-conscious perception of emotional signals will clarify the phylogenetic continuity of emotion systems across species and the integration of cortical and subcortical activity in the human brain.

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: Cortical and subcortical pathways for vision and emotion.
Figure 2: Subcortical pathway for processing emotional signals in the animal brain.
Figure 3: Expressive and autonomic changes induced by non-conscious perception of emotional stimuli.
Figure 4: Circuits for subcortical modulation of cortical activity.

Similar content being viewed by others

References

  1. de Gelder, B., de Haan, E. & Heywood, C. Out of Mind. Varieties of Unconscious Processes (Oxford Univ. Press, 2001).

    Google Scholar 

  2. de Gelder, B., Vroomen, J., Pourtois, G. & Weiskrantz, L. Non-conscious recognition of affect in the absence of striate cortex. Neuroreport 10, 3759–3763 (1999). This study provided the first demonstration that patients with cortical blindness can perceive emotions non-consciously and can correctly guess the emotion displayed in facial expressions presented in the blind portion of their visual field.

    CAS  PubMed  Google Scholar 

  3. Esteves, F., Dimberg, U. & Ohman, A. Automatically elicited fear: conditioned skin conductance responses to masked facial expressions. Cogn. Emot. 8, 99–108 (1994). One of the earliest studies showing that conscious perception of emotional faces can be blocked in healthy observers by backward masking, whereas non-conscious perception is still indexed by physiological changes in skin conductance (indicative of autonomic arousal).

    Google Scholar 

  4. Kunst-Wilson, W. R. & Zajonc, R. B. Affective discrimination of stimuli that cannot be recognized. Science 207, 557–558 (1980).

    CAS  PubMed  Google Scholar 

  5. LeDoux, J. E. The Emotional Brain (Simon & Shuster, New York, 1996). A very influential book summarizing evidence from the author's studies in animals indicating the existence of a direct subcortical pathway to the amygdala bypassing the primary sensory cortex in the rat brain. This book also fostered an evolution-inspired approach to non-conscious perception of emotions in neuroscience research.

    Google Scholar 

  6. Morris, J. S., Ohman, A. & Dolan, R. J. Conscious and unconscious emotional learning in the human amygdala. Nature 393, 467–470 (1998).

    CAS  PubMed  Google Scholar 

  7. Whalen, P. J. et al. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J. Neurosci. 18, 411–418 (1998). The first study reporting that fearful facial expressions that are masked still induce amygdala activity while activity in emotion-related cortical areas is suppressed.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Panksepp, J. Affective Neuroscience (Oxford Univ. Press, New York, 1998).

    Google Scholar 

  9. Williams, L. M. An integrative neuroscience model of 'significance' processing. J. Integr. Neurosci. 5, 1–47 (2006).

    PubMed  Google Scholar 

  10. Posner, M. I. Attention: the mechanisms of consciousness. Proc. Natl Acad. Sci. USA 91, 7398–7403 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Kentridge, R. W., Heywood, C. A. & Weiskrantz, L. Spatial attention speeds discrimination without awareness in blindsight. Neuropsychologia 42, 831–835 (2004).

    CAS  PubMed  Google Scholar 

  12. Dehaene, S., Changeux, J. P., Naccache, L., Sackur, J. & Sergent, C. Conscious, preconscious, and subliminal processing: a testable taxonomy. Trends Cogn. Sci. 10, 204–211 (2006).

    PubMed  Google Scholar 

  13. Savazzi, S. & Marzi, C. A. Speeding up reaction time with invisible stimuli. Curr. Biol. 12, 403–407 (2002).

    CAS  PubMed  Google Scholar 

  14. Koch, C. & Tsuchiya, N. Attention and consciousness: two distinct brain processes. Trends Cogn. Sci. 11, 16–22 (2007).

    PubMed  Google Scholar 

  15. Mack, A. & Rock, I. Inattentional Blindness (MIT Press, Cambridge, Massachusetts, 1998).

    Google Scholar 

  16. Beck, D. M., Rees, G., Frith, C. D. & Lavie, N. Neural correlates of change detection and change blindness. Nature Neurosci. 4, 645–650 (2001).

    CAS  PubMed  Google Scholar 

  17. Vuilleumier, P. How brains beware: neural mechanisms of emotional attention. Trends Cogn. Sci. 9, 585–594 (2005).

    PubMed  Google Scholar 

  18. Eastwood, J. D., Smilek, D. & Merikle, P. M. Negative facial expression captures attention and disrupts performance. Percept. Psychophys. 65, 352–358 (2003).

    PubMed  Google Scholar 

  19. Hart, S. J., Green, S. R., Casp, M. & Belger, A. Emotional priming effects during Stroop task performance. Neuroimage 49, 2662–2670 (2010).

    PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  21. Hansen, C. H. & Hansen, R. D. Finding the face in the crowd: an anger superiority effect. J. Pers. Soc. Psychol. 54, 917–924 (1988).

    CAS  PubMed  Google Scholar 

  22. Ohman, A., Flykt, A. & Esteves, F. Emotion drives attention: detecting the snake in the grass. J. Exp. Psychol. Gen. 130, 466–478 (2001).

    CAS  PubMed  Google Scholar 

  23. Anderson, A. K. Affective influences on the attentional dynamics supporting awareness. J. Exp. Psychol. Gen. 134, 258–281 (2005).

    PubMed  Google Scholar 

  24. Anderson, A. K. & Phelps, E. A. Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature 411, 305–309 (2001). This study shows that enhanced processing of emotional signals under conditions of limited attention due to attentional blink is abolished in patients with amygdala lesions.

    CAS  PubMed  Google Scholar 

  25. Anderson, A. K., Christoff, K., Panitz, D., De Rosa, E. & Gabrieli, J. D. Neural correlates of the automatic processing of threat facial signals. J. Neurosci. 23, 5627–5633 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Bishop, S. J., Duncan, J. & Lawrence, A. D. State anxiety modulation of the amygdala response to unattended threat-related stimuli. J. Neurosci. 24, 10364–10368 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Vuilleumier, P., Armony, J. L., Driver, J. & Dolan, R. J. Effects of attention and emotion on face processing in the human brain: an event-related fMRI study. Neuron 30, 829–841 (2001). This study used a dual-task design to induce attentional unawareness of facial expressions. The amygdala responded to fearful expressions regardless of the allocation of spatial attention, whereas the fusiform face areas showed additive effects of attention and emotion, being more active when faces occurred at attended locations but always more activated by fearful than neutral faces even when faces were task-irrelevant and produced reduced cortical activity overall (see also reference 30 for contrasting results).

    CAS  PubMed  Google Scholar 

  28. Williams, M. A., McGlone, F., Abbott, D. F. & Mattingley, J. B. Differential amygdala responses to happy and fearful facial expressions depend on selective attention. Neuroimage 24, 417–425 (2005).

    PubMed  Google Scholar 

  29. Pessoa, L. To what extent are emotional visual stimuli processed without attention and awareness? Curr. Opin. Neurobiol. 15, 188–196 (2005).

    CAS  PubMed  Google Scholar 

  30. Pessoa, L., McKenna, M., Gutierrez, E. & Ungerleider, L. G. Neural processing of emotional faces requires attention. Proc. Natl Acad. Sci. USA 99, 11458–11463 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Pessoa, L., Padmala, S. & Morland, T. Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation. Neuroimage 28, 249–255 (2005).

    PubMed  Google Scholar 

  32. Silvert, L. et al. Influence of attentional demands on the processing of emotional facial expressions in the amygdala. Neuroimage 38, 357–366 (2007).

    PubMed  Google Scholar 

  33. Vuilleumier, P. et al. Neural response to emotional faces with and without awareness: event-related fMRI in a parietal patient with visual extinction and spatial neglect. Neuropsychologia 40, 2156–2166 (2002).

    CAS  PubMed  Google Scholar 

  34. Tamietto, M., Geminiani, G., Genero, R. & de Gelder, B. Seeing fearful body language overcomes attentional deficits in patients with neglect. J. Cogn. Neurosci. 19, 445–454 (2007). This study showed that fearful body expressions can be processed pre-attentively in patients with hemispatial neglect, thereby reducing the attentional bias and increasing perceptual sensitivity to stimuli presented in the left side of the space. Similar effects were previously reported for schematic facial expressions and spiders (see also references 36 and 37).

    PubMed  Google Scholar 

  35. Tamietto, M. et al. Effects of emotional face cueing on line bisection in neglect: a single case study. Neurocase 11, 399–404 (2005).

    PubMed  Google Scholar 

  36. Vuilleumier, P. & Schwartz, S. Emotional facial expressions capture attention. Neurology 56, 153–158 (2001).

    CAS  PubMed  Google Scholar 

  37. Vuilleumier, P. & Schwartz, S. Beware and be aware: capture of spatial attention by fear-related stimuli in neglect. Neuroreport 12, 1119–1122 (2001).

    CAS  PubMed  Google Scholar 

  38. Williams, M. A. & Mattingley, J. B. Unconscious perception of non-threatening facial emotion in parietal extinction. Exp. Brain Res. 154, 403–406 (2004).

    PubMed  Google Scholar 

  39. Macknik, S. L. & Livingstone, M. S. Neuronal correlates of visibility and invisibility in the primate visual system. Nature Neurosci. 1, 144–149 (1998).

    CAS  PubMed  Google Scholar 

  40. Tong, F., Meng, M. & Blake, R. Neural bases of binocular rivalry. Trends Cogn. Sci. 10, 502–511 (2006).

    PubMed  Google Scholar 

  41. Glascher, J. & Adolphs, R. Processing of the arousal of subliminal and supraliminal emotional stimuli by the human amygdala. J. Neurosci. 23, 10274–10282 (2003).

    PubMed  PubMed Central  Google Scholar 

  42. Williams, L. M. et al. Mapping the time course of nonconscious and conscious perception of fear: an integration of central and peripheral measures. Hum. Brain Mapp. 21, 64–74 (2004).

    PubMed  Google Scholar 

  43. Liddell, B. J., Williams, L. M., Rathjen, J., Shevrin, H. & Gordon, E. A temporal dissociation of subliminal versus supraliminal fear perception: an event-related potential study. J. Cogn. Neurosci. 16, 479–486 (2004).

    PubMed  Google Scholar 

  44. Dimberg, U., Thunberg, M. & Elmehed, K. Unconscious facial reactions to emotional facial expressions. Psychol. Sci. 11, 86–89 (2000).

    CAS  PubMed  Google Scholar 

  45. Tamietto, M. & de Gelder, B. Emotional contagion for unseen bodily expressions: evidence from facial EMG. Automatic Face and Gesture Recognition (8th IEEE Int. Conference, Amsterdam, 2008).

  46. Carlson, J. M., Reinke, K. S. & Habib, R. A left amygdala mediated network for rapid orienting to masked fearful faces. Neuropsychologia 47, 1386–1389 (2009).

    PubMed  Google Scholar 

  47. Critchley, H. D., Mathias, C. J. & Dolan, R. J. Fear conditioning in humans: the influence of awareness and autonomic arousal on functional neuroanatomy. Neuron 33, 653–663 (2002).

    CAS  PubMed  Google Scholar 

  48. Juruena, M. F. et al. Amygdala activation to masked happy facial expressions. J. Int. Neuropsychol. Soc. 16, 383–387 (2010).

    PubMed  Google Scholar 

  49. Killgore, W. D. & Yurgelun-Todd, D. A. Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces. Neuroimage 21, 1215–1223 (2004).

    PubMed  Google Scholar 

  50. Liddell, B. J. et al. A direct brainstem–amygdala–cortical 'alarm' system for subliminal signals of fear. Neuroimage 24, 235–243 (2005).

    PubMed  Google Scholar 

  51. Morris, J. S., Ohman, A. & Dolan, R. J. A subcortical pathway to the right amygdala mediating 'unseen' fear. Proc. Natl Acad. Sci. USA 96, 1680–1685 (1999). This study showed for the first time that non-conscious perception of emotions due to backward masking in healthy observers engages a subcortical pathway involving the superior colliculus, the pulvinar and the amygdala.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Whalen, P. J. et al. Human amygdala responsivity to masked fearful eye whites. Science 306, 2061 (2004).

    CAS  PubMed  Google Scholar 

  53. Williams, L. M. et al. Mode of functional connectivity in amygdala pathways dissociates level of awareness for signals of fear. J. Neurosci. 26, 9264–9271 (2006). This study showed that the conscious versus non-conscious perception of fearful facial expressions is associated with distinct patterns of functional connectivity. Conscious perception of fearful facial expressions was associated with negative functional connectivity between the amygdala and related cortical and subcortical areas, whereas non-conscious perception was supported by positive functional connectivity between the superior colliculus, the pulvinar and amygdala.

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Williams, L. M. et al. Amygdala-prefrontal dissociation of subliminal and supraliminal fear. Hum. Brain Mapp. 27, 652–661 (2006).

    PubMed  Google Scholar 

  55. Pasley, B. N., Mayes, L. C. & Schultz, R. T. Subcortical discrimination of unperceived objects during binocular rivalry. Neuron 42, 163–172 (2004).

    CAS  PubMed  Google Scholar 

  56. Williams, M. A., Morris, A. P., McGlone, F., Abbott, D. F. & Mattingley, J. B. Amygdala responses to fearful and happy facial expressions under conditions of binocular suppression. J. Neurosci. 24, 2898–2904 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Yoon, K. L., Hong, S. W., Joormann, J. & Kang, P. Perception of facial expressions of emotion during binocular rivalry. Emotion 9, 172–182 (2009).

    PubMed  Google Scholar 

  58. Pessoa, L., Japee, S., Sturman, D. & Ungerleider, L. G. Target visibility and visual awareness modulate amygdala responses to fearful faces. Cereb. Cortex 16, 366–375 (2006).

    PubMed  Google Scholar 

  59. Pessoa, L., Japee, S. & Ungerleider, L. G. Visual awareness and the detection of fearful faces. Emotion 5, 243–247 (2005).

    PubMed  Google Scholar 

  60. Tamietto, M. & de Gelder, B. Affective blindsight in the intact brain: neural interhemispheric summation for unseen fearful expressions. Neuropsychologia 46, 820–828 (2008).

    PubMed  Google Scholar 

  61. Kim, M. J. et al. Behind the mask: the influence of mask-type on amygdala response to fearful faces. Soc. Cogn. Affect. Neurosci. 10 Feb 2010 (doi:10.1093/scan/nsq014).

    PubMed  PubMed Central  Google Scholar 

  62. de Gelder, B. et al. Intact navigation skills after bilateral loss of striate cortex. Curr. Biol. 18, R1128–R1129 (2008).

    CAS  PubMed  Google Scholar 

  63. de Gelder, B. Uncanny sight in the blind. Sci. Am. 302, 60–65 (2010).

    PubMed  Google Scholar 

  64. de Gelder, B. & Hadjikhani, N. Non-conscious recognition of emotional body language. Neuroreport 17, 583–586 (2006).

    PubMed  Google Scholar 

  65. Hamm, A. O. et al. Affective blindsight: intact fear conditioning to a visual cue in a cortically blind patient. Brain 126, 267–275 (2003).

    PubMed  Google Scholar 

  66. Morris, J. S., de Gelder, B., Weiskrantz, L. & Dolan, R. J. Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. Brain 124, 1241–1252 (2001).

    CAS  PubMed  Google Scholar 

  67. Pegna, A. J., Khateb, A., Lazeyras, F. & Seghier, M. L. Discriminating emotional faces without primary visual cortices involves the right amygdala. Nature Neurosci. 8, 24–25 (2005).

    CAS  PubMed  Google Scholar 

  68. Tamietto, M. et al. Unseen facial and bodily expressions trigger fast emotional reactions. Proc. Natl Acad. Sci. USA 106, 17661–17666 (2009). This study showed that spontaneous facial and pupillary reactions can be triggered by passive exposure to consciously and non-consciously perceived expressions of fear and happiness in patients with cortical blindness. Facial reactions were shown to be faster and pupil dilation higher for non-consciously than for consciously perceived facial and bodily expressions, whereas there was no difference between face and body stimuli.

    CAS  PubMed  PubMed Central  Google Scholar 

  69. de Gelder, B., Pourtois, G., van Raamsdonk, M., Vroomen, J. & Weiskrantz, L. Unseen stimuli modulate conscious visual experience: evidence from inter-hemispheric summation. Neuroreport 12, 385–391 (2001).

    CAS  PubMed  Google Scholar 

  70. Ro, T., Shelton, D., Lee, O. L. & Chang, E. Extrageniculate mediation of unconscious vision in transcranial magnetic stimulation-induced blindsight. Proc. Natl Acad. Sci. USA 101, 9933–9935 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Jolij, J. & Lamme, V. A. Repression of unconscious information by conscious processing: evidence from affective blindsight induced by transcranial magnetic stimulation. Proc. Natl Acad. Sci. USA 102, 10747–10751 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Hendler, T. et al. Sensing the invisible: differential sensitivity of visual cortex and amygdala to traumatic context. Neuroimage 19, 587–600 (2003).

    PubMed  Google Scholar 

  73. Schiller, P. H. & Malpeli, J. G. Properties and tectal projections of monkey retinal ganglion cells. J. Neurophysiol. 40, 428–445 (1977).

    CAS  PubMed  Google Scholar 

  74. Tamietto, M. et al. Collicular vision guides nonconscious behavior. J. Cogn. Neurosci. 22, 888–902 (2010).

    PubMed  Google Scholar 

  75. de Gelder, B., Morris, J. S. & Dolan, R. J. Unconscious fear influences emotional awareness of faces and voices. Proc. Natl Acad. Sci. USA 102, 18682–18687 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Lyon, D. C., Nassi, J. J. & Callaway, E. M. A disynaptic relay from superior colliculus to dorsal stream visual cortex in macaque monkey. Neuron 65, 270–279 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Ward, R., Danziger, S. & Bamford, S. Response to visual threat following damage to the pulvinar. Curr. Biol. 15, 571–573 (2005).

    CAS  PubMed  Google Scholar 

  78. Romanski, L. M., Giguere, M., Bates, J. F. & Goldman-Rakic, P. S. Topographic organization of medial pulvinar connections with the prefrontal cortex in the rhesus monkey. J. Comp. Neurol. 379, 313–332 (1997).

    CAS  PubMed  Google Scholar 

  79. Phelps, E. A. & LeDoux, J. E. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48, 175–187 (2005).

    CAS  PubMed  Google Scholar 

  80. Whalen, P. J. & Phelps, E. A. (eds) The Human Amygdala (Guilford Press, New York, 2009).

    Google Scholar 

  81. Sergerie, K., Chochol, C. & Armony, J. L. The role of the amygdala in emotional processing: a quantitative meta-analysis of functional neuroimaging studies. Neurosci. Biobehav. Rev. 32, 811–830 (2008).

    PubMed  Google Scholar 

  82. Somerville, L. H., Kim, H., Johnstone, T., Alexander, A. L. & Whalen, P. J. Human amygdala responses during presentation of happy and neutral faces: correlations with state anxiety. Biol. Psychiatry 55, 897–903 (2004).

    PubMed  Google Scholar 

  83. Jolkkonen, E., Pikkarainen, M., Kemppainen, S. & Pitkanen, A. Interconnectivity between the amygdaloid complex and the amygdalostriatal transition area: a PHA-L study in rat. J. Comp. Neurol. 431, 39–58 (2001).

    CAS  PubMed  Google Scholar 

  84. Whalen, P. J. et al. A functional MRI study of human amygdala responses to facial expressions of fear versus anger. Emotion 1, 70–83 (2001).

    CAS  PubMed  Google Scholar 

  85. Whalen, P. J., Kapp, B. S. & Pascoe, J. P. Neuronal activity within the nucleus basalis and conditioned neocortical electroencephalographic activation. J. Neurosci. 14, 1623–1633 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Breiter, H. C. et al. Response and habituation of the human amygdala during visual processing of facial expression. Neuron 17, 875–887 (1996).

    CAS  PubMed  Google Scholar 

  87. Berns, G. S., Cohen, J. D. & Mintun, M. A. Brain regions responsive to novelty in the absence of awareness. Science 276, 1272–1275 (1997).

    CAS  PubMed  Google Scholar 

  88. McHaffie, J. G., Stanford, T. R., Stein, B. E., Coizet, V. & Redgrave, P. Subcortical loops through the basal ganglia. Trends Neurosci. 28, 401–407 (2005).

    CAS  PubMed  Google Scholar 

  89. Cauda, F. et al. in XIX Symposium Neuroradiologicum. Neuroradiol. J. (Centauro, Italy, 2010).

    Google Scholar 

  90. Mobbs, D. et al. When fear is near: threat imminence elicits prefrontal-periaqueductal gray shifts in humans. Science 317, 1079–1083 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Aston-Jones, G., Chiang, C. & Alexinsky, T. Discharge of noradrenergic locus coeruleus neurons in behaving rats and monkeys suggests a role in vigilance. Prog. Brain Res. 88, 501–520 (1991).

    CAS  PubMed  Google Scholar 

  92. Bentley, P., Vuilleumier, P., Thiel, C. M., Driver, J. & Dolan, R. J. Effects of attention and emotion on repetition priming and their modulation by cholinergic enhancement. J. Neurophysiol. 90, 1171–1181 (2003).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  94. Calder, A. J., Lawrence, A. D. & Young, A. W. Neuropsychology of fear and loathing. Nature Rev. Neurosci. 2, 352–363 (2001).

    CAS  Google Scholar 

  95. Phillips, M. L. et al. Differential neural responses to overt and covert presentations of facial expressions of fear and disgust. Neuroimage 21, 1484–1496 (2004).

    PubMed  Google Scholar 

  96. Nakamura, K. & Ono, T. Lateral hypothalamus neuron involvement in integration of natural and artificial rewards and cue signals. J. Neurophysiol. 55, 163–181 (1986).

    CAS  PubMed  Google Scholar 

  97. Tamietto, M., Pullens, P., Weiskrantz, L., Goebel, R. & de Gelder, B. in Second Meeting of the Federation of the European Societies of Neuropsychology (ESN, The Netherlands, 2010).

    Google Scholar 

  98. Krolak-Salmon, P., Henaff, M. A., Vighetto, A., Bertrand, O. & Mauguiere, F. Early amygdala reaction to fear spreading in occipital, temporal, and frontal cortex: a depth electrode ERP study in human. Neuron 42, 665–676 (2004).

    CAS  PubMed  Google Scholar 

  99. Leppanen, 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).

    PubMed  PubMed Central  Google Scholar 

  100. Holmes, A., Vuilleumier, P. & Eimer, M. The processing of emotional facial expression is gated by spatial attention: evidence from event-related brain potentials. Brain Res. Cogn. Brain Res. 16, 174–184 (2003).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  102. Livingstone, M. & Hubel, D. Segregation of form, color, movement, and depth: anatomy, physiology, and perception. Science 240, 740–749 (1988).

    CAS  PubMed  Google Scholar 

  103. 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 

  104. Jarvis, E. D. et al. Avian brains and a new understanding of vertebrate brain evolution. Nature Rev. Neurosci. 6, 151–159 (2005).

    CAS  Google Scholar 

  105. Andrew, R. J. Changes in visual responsiveness following intercollicular lesions and their effects on avoidance and attack. Brain Behav. Evol. 10, 400–424 (1975).

    CAS  PubMed  Google Scholar 

  106. Linke, R., De Lima, A. D., Schwegler, H. & Pape, H. C. Direct synaptic connections of axons from superior colliculus with identified thalamo-amygdaloid projection neurons in the rat: possible substrates of a subcortical visual pathway to the amygdala. J. Comp. Neurol. 403, 158–170 (1999).

    CAS  PubMed  Google Scholar 

  107. Cohen, J. D. & Castro-Alamancos, M. A. Early sensory pathways for detection of fearful conditioned stimuli: tectal and thalamic relays. J. Neurosci. 27, 7762–7776 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  108. Weiskrantz, L. Behavioral changes associated with ablation of the amygdaloid complex in monkeys. J. Comp. Physiol. Psychol. 49, 381–391 (1956).

    CAS  PubMed  Google Scholar 

  109. Jones, E. G. & Burton, H. A projection from the medial pulvinar to the amygdala in primates. Brain Res. 104, 142–147 (1976).

    CAS  PubMed  Google Scholar 

  110. Harting, J. K., Huerta, M. F., Hashikawa, T. & van Lieshout, D. P. Projection of the mammalian superior colliculus upon the dorsal lateral geniculate nucleus: organization of tectogeniculate pathways in nineteen species. J. Comp. Neurol. 304, 275–306 (1991).

    CAS  PubMed  Google Scholar 

  111. Schmid, M. C. et al. Blindsight depends on the lateral geniculate nucleus. Nature 466, 373–377 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  112. Isbell, L. A. Snakes as agents of evolutionary change in primate brains. J. Hum. Evol. 51, 1–35 (2006).

    PubMed  Google Scholar 

  113. Leppanen, J. M. & Nelson, C. A. Tuning the developing brain to social signals of emotions. Nature Rev. Neurosci. 10, 37–47 (2009).

    Google Scholar 

  114. de Gelder, B. et al. Beyond the face: exploring rapid influences of context on face processing. Prog. Brain Res. 155, 37–48 (2006).

    PubMed  Google Scholar 

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

    CAS  Google Scholar 

  116. Rossion, B., de Gelder, B., Pourtois, G., Guerit, J. M. & Weiskrantz, L. Early extrastriate activity without primary visual cortex in humans. Neurosci. Lett. 279, 25–28 (2000).

    CAS  PubMed  Google Scholar 

  117. Tamietto, M., Adenzato, M., Geminiani, G. & de Gelder, B. Fast recognition of social emotions takes the whole brain: interhemispheric cooperation in the absence of cerebral asymmetry. Neuropsychologia 45, 836–843 (2007).

    PubMed  Google Scholar 

  118. de Gelder, B. Towards the neurobiology of emotional body language. Nature Rev. Neurosci. 7, 242–249 (2006).

    CAS  Google Scholar 

  119. 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. Neurosci. Biobehav. Rev. 34, 513–527 (2010).

    PubMed  Google Scholar 

  120. Alpers, G. W. et al. Attention and amygdala activity: an fMRI study with spider pictures in spider phobia. J. Neural Transm. 116, 747–757 (2009).

    PubMed  Google Scholar 

  121. Carlsson, K. et al. Fear and the amygdala: manipulation of awareness generates differential cerebral responses to phobic and fear-relevant (but nonfeared) stimuli. Emotion 4, 340–353 (2004).

    PubMed  Google Scholar 

  122. Wendt, J., Lotze, M., Weike, A. I., Hosten, N. & Hamm, A. O. Brain activation and defensive response mobilization during sustained exposure to phobia-related and other affective pictures in spider phobia. Psychophysiology 45, 205–215 (2008).

    PubMed  Google Scholar 

  123. de Gelder, B., Pourtois, G. & Weiskrantz, L. Fear recognition in the voice is modulated by unconsciously recognized facial expressions but not by unconsciously recognized affective pictures. Proc. Natl Acad. Sci. USA 99, 4121–4126 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  124. van Honk, J. et al. Baseline salivary cortisol levels and preconscious selective attention for threat. A pilot study. Psychoneuroendocrinology 23, 741–747 (1998).

    CAS  PubMed  Google Scholar 

  125. Ruiz-Padial, E., Mata, J. L., Rodriguez, S., Fernandez, M. C. & Vila, J. Non-conscious modulation of cardiac defense by masked phobic pictures. Int. J. Psychophysiol. 56, 271–281 (2005).

    PubMed  Google Scholar 

  126. Frith, C. Role of facial expressions in social interactions. Phil. Trans. R. Soc. Lond. B 364, 3453–3458 (2009).

    Google Scholar 

  127. Rinn, W. E. The neuropsychology of facial expression: a review of the neurological and psychological mechanisms for producing facial expressions. Psychol. Bull. 95, 52–77 (1984).

    CAS  PubMed  Google Scholar 

  128. Ladavas, E., Cimatti, D., Del Pesce, M. & Tuozzi, G. Emotional evaluation with and without conscious stimulus identification: evidence from a split-brain patient. Cogn. Emot. 7, 95–114 (1993).

    Google Scholar 

  129. Rees, G., Kreiman, G. & Koch, C. Neural correlates of consciousness in humans. Nature Rev. Neurosci. 3, 261–270 (2002).

    CAS  Google Scholar 

  130. Dehaene, S. et al. Cerebral mechanisms of word masking and unconscious repetition priming. Nature Neurosci. 4, 752–758 (2001).

    CAS  PubMed  Google Scholar 

  131. Moutoussis, K. & Zeki, S. The relationship between cortical activation and perception investigated with invisible stimuli. Proc. Natl Acad. Sci. USA 99, 9527–9532 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Moutoussis, K. & Zeki, S. Seeing invisible motion: a human FMRI study. Curr. Biol. 16, 574–579 (2006).

    CAS  PubMed  Google Scholar 

  133. Azzopardi, P. & Cowey, A. Is blindsight like normal, near-threshold vision? Proc. Natl Acad. Sci. USA 94, 14190–14194 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  134. Meeres, S. L. & Graves, R. E. Localization of unseen visual stimuli by humans with normal vision. Neuropsychologia 28, 1231–1237 (1990).

    CAS  PubMed  Google Scholar 

  135. Leopold, D. A. & Logothetis, N. K. Activity changes in early visual cortex reflect monkeys' percepts during binocular rivalry. Nature 379, 549–553 (1996).

    CAS  PubMed  Google Scholar 

  136. Sergent, C., Baillet, S. & Dehaene, S. Timing of the brain events underlying access to consciousness during the attentional blink. Nature Neurosci. 8, 1391–1400 (2005).

    CAS  PubMed  Google Scholar 

  137. Haynes, J. D. & Rees, G. Predicting the orientation of invisible stimuli from activity in human primary visual cortex. Nature Neurosci. 8, 686–691 (2005).

    CAS  PubMed  Google Scholar 

  138. Rees, G. et al. Unconscious activation of visual cortex in the damaged right hemisphere of a parietal patient with extinction. Brain 123, 1624–1633 (2000).

    PubMed  Google Scholar 

  139. Sahraie, A. et al. Pattern of neuronal activity associated with conscious and unconscious processing of visual signals. Proc. Natl Acad. Sci. USA 94, 9406–9411 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  140. Bush, P. & Sejnowski, T. Inhibition synchronizes sparsely connected cortical neurons within and between columns in realistic network models. J. Comput. Neurosci. 3, 91–110 (1996).

    CAS  PubMed  Google Scholar 

  141. Lamme, V. A. & Roelfsema, P. R. The distinct modes of vision offered by feedforward and recurrent processing. Trends Neurosci. 23, 571–579 (2000).

    CAS  PubMed  Google Scholar 

  142. Anders, S. et al. When seeing outweighs feeling: a role for prefrontal cortex in passive control of negative affect in blindsight. Brain 132, 3021–3031 (2009).

    PubMed  PubMed Central  Google Scholar 

  143. Niedenthal, P. M. Implicit perception of affective information. J. Exp. Soc. Psychol. 26, 505–527 (1990).

    Google Scholar 

  144. Tamietto, M., Latini Corazzini, L., de Gelder, B. & Geminiani, G. Functional asymmetry and interhemispheric cooperation in the perception of emotions from facial expressions. Exp. Brain Res. 171, 389–404 (2006).

    PubMed  Google Scholar 

  145. 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 

  146. Rodman, H. R., Gross, C. G. & Albright, T. D. Afferent basis of visual response properties in area Montana of the macaque. II. Effects of superior colliculus removal. J. Neurosci. 10, 1154–1164 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  147. Morris, J. S. et al. A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain 121, 47–57 (1998). This positron emission tomography study showed that activation in extrastriate visual areas in response to task-irrelevant fearful faces is modulated by amygdala activity, thereby providing the first evidence that subcortical structures involved in processing emotional stimuli can modulate directly cortical activity.

    PubMed  Google Scholar 

  148. Peelen, M. V., Atkinson, A. P., Andersson, F. & Vuilleumier, P. Emotional modulation of body-selective visual areas. Soc. Cogn. Affect. Neurosci. 2, 274–283 (2007).

    PubMed  PubMed Central  Google Scholar 

  149. 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).

    CAS  PubMed  Google Scholar 

  150. Craig, A. D. How do you feel--now? The anterior insula and human awareness. Nature Rev. Neurosci. 10, 59–70 (2009).

    CAS  Google Scholar 

  151. Anders, S. et al. Parietal somatosensory association cortex mediates affective blindsight. Nature Neurosci. 7, 339–340 (2004). This study shows that patients with cortical blindness can report negative feelings induced by the presentation of aversively-conditioned facial expressions in their blind visual field, despite being unaware of the origin of these feelings. This effect was associated with enhanced activity in the parietal somatosensory cortex.

    CAS  PubMed  Google Scholar 

  152. Tomkins, S. S. Affect, Imagery, Consciousness (Springer, New York, 1962–1963).

    Google Scholar 

  153. Damasio, A. R. Descartes' Error: Emotion, Reason, and the Human Brain (G. P. Putnam's Sons, New York, 1994).

    Google Scholar 

  154. Merikle, P. M., Smilek, D. & Eastwood, J. D. Perception without awareness: perspectives from cognitive psychology. Cognition 79, 115–134 (2001).

    CAS  PubMed  Google Scholar 

  155. Wiens, S. Subliminal emotion perception in brain imaging: findings, issues, and recommendations. Prog. Brain Res. 156, 105–121 (2006).

    PubMed  Google Scholar 

  156. Cheesman, J. & Merikle, P. M. Distinguishing conscious from unconscious perceptual processes. Can. J. Psychol. 40, 343–367 (1986).

    CAS  PubMed  Google Scholar 

  157. Simion, F., Valenza, E., Umilta, C. & Dalla Barba, B. Preferential orienting to faces in newborns: a temporal-nasal asymmetry. J. Exp. Psychol. Hum. Percept. Perform. 24, 1399–1405 (1998).

    CAS  PubMed  Google Scholar 

  158. 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 

  159. Peltola, M. J., Leppanen, 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).

    PubMed  Google Scholar 

  160. 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 

  161. Tinti, C., Adenzato, M., Tamietto, M. & Cornoldi, C. Visual experience is not necessary for efficient survey spatial cognition: evidence from blindness. Q. J. Exp. Psychol. (Colchester) 59, 1306–1328 (2006).

    Google Scholar 

  162. Baron-Cohen, S. et al. The amygdala theory of autism. Neurosci. Biobehav Rev. 24, 355–364 (2000).

    CAS  PubMed  Google Scholar 

  163. Deruelle, C., Rondan, C., Gepner, B. & Tardif, C. Spatial frequency and face processing in children with autism and Asperger syndrome. J. Autism Dev. Disord. 34, 199–210 (2004).

    PubMed  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge valuable comments from P. Whalen and two anonymous referees. M.T. was supported by a Veni grant (451–07-032) from the Netherlands Organization for Scientific Research (NWO) and also partly supported by the Fondazione Carlo Molo, Turin, Italy and by a Bando Scienze Umane e Sociali 2008 grant from the Regione Piemonte, Italy, for the project Grammatica Invisibile delle Relazioni Sociali (GIRS) (grant number 4). B.d.G. was supported by an Future and Emerging Technologies (FET) Open Scheme grant (ICT-2009-C) from the European Union for the Emotional Interaction Grounded in Realistic Context (also known as TANGO) Project (249858) and by a Lagrange Fellow visiting professorship to the University of Torino, Turin, Italy funded by the Cassa di Risparmio di Torino (CRT) Foundation.

Author information

Authors and Affiliations

  1. Cognitive and Affective Neuroscience Laboratory, Tilburg University, P.O. BOX 90153, Tilburg, 5000 LE, The Netherlands

    Marco Tamietto & Beatrice de Gelder

  2. Institute for Scientific Interchange (ISI) Foundation, Viale S. Severo 65, Turin, 10133, Italy

    Marco Tamietto & Beatrice de Gelder

  3. Department of Psychology, University of Turin, Via Po 14, Turin, 10123, Italy

    Marco Tamietto

  4. Athinoula A. Martinos Centre for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Building 75, Room 2132-4, Charlestown, 02129, Massachusetts, USA

    Beatrice de Gelder

Authors
  1. Marco Tamietto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Beatrice de Gelder
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Marco Tamietto or Beatrice de Gelder.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

FURTHER INFORMATION

Beatrice de Gelder's homepage

Glossary

Magnocellular pathway

A system of visually responsive neurons that originates from retinal ganglion cells with large receptive fields and that is characterized by low spatial resolution and rapid transmission of nerve impulses.

Parvocellular pathway

A system of visually responsive neurons that originates from retinal ganglion cells with small receptive fields and that is characterized by high spatial resolution and slow transmission of nerve impulses.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tamietto, M., de Gelder, B. Neural bases of the non-conscious perception of emotional signals. Nat Rev Neurosci 11, 697–709 (2010). https://doi.org/10.1038/nrn2889

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrn2889

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