Neuroscience and facial expressions of emotion: the role of amygdala-prefrontal interactions
Abstract
The aim of this review is to show the fruitfulness of using images of facial expressions as experimental stimuli in order to study how neural systems support biologically relevant learning as it relates to social interactions. Here we consider facial expressions as naturally conditioned stimuli which, when presented in experimental paradigms, evoke activation in amygdala–prefrontal neural circuits that serve to decipher the predictive meaning of the expressions. Facial expressions offer a relatively innocuous strategy with which to investigate these normal variations in affective information processing, as well as the promise of elucidating what role the aberrance of such processing might play in emotional disorders.
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The amygdala has been associated with reward processing, emotional processing, and fear response.
“which has been associated with reward processing (Ernst et al., 2005), emotional processing (Whalen et al., 2013), and fear response (LeDoux, 2003)”
From Becoming a sexual being: The “elephant in the room” of adolescent brain development (2017) · cites this paper as Whalen et al., 2013
The quality of parent-child relationships affects both sexual behavior and neural development and activation, specifically in the amygdala.
“The quality of parent-child relationships affects both sexual behavior and neural development and activation, specifically in the amygdala”
From Becoming a sexual being: The “elephant in the room” of adolescent brain development (2017) · cites this paper as Whalen et al., 2013
Cites
The cognitive control of emotion
OCHSNER, K., & GROSS, J. (2005) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2005.03.010 · Cited by 4,495 · see citing works
The Emotional Brain: The Mysterious Underpinnings of Emotional Life
LeDoux, J. E. (2004) · Medical Entomology and Zoology · Cited by 4,212 · see citing works
Autonomic nervous system activity distinguishes among emotions
Ekman, P., Levenson, R. W., & Friesen, W. V. (1983) · Science · doi:10.1126/science.6612338 · Cited by 2,692 · see citing works
Adolphs, R., Tranel, D., Damasio, H., & Damasio, A. (1994) · Nature · doi:10.1038/372669a0 · Cited by 2,360 · see citing works
Whalen, P. J., Rauch, S. L., Etcoff, N. L., McInerney, S. C., Lee, M. B., & Jenike, M. A. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-01-00411.1998 · Cited by 2,205 · see citing works
Self-citationA differential neural response in the human amygdala to fearful and happy facial expressions
Morris, J. S., Frith, C. D., Perrett, D. I., Rowland, D., Young, A. W., Calder, A. J., & Dolan, R. J. (1996) · Nature · doi:10.1038/383812a0 · Cited by 2,013 · see citing works
Pezawas, L., Meyer-Lindenberg, A., Drabant, E. M., Verchinski, B. A., Munoz, K. E., Kolachana, B. S., Egan, M. F., Mattay, V. S., Hariri, A. R., & Weinberger, D. R. (2005) · Nature Neuroscience · doi:10.1038/nn1463 · Cited by 1,980 · see citing works
Judgment of contingency in depressed and nondepressed students: sadder but wiser?
Alloy, L., & Abramson, L. (1979) · Journal of experimental psychology. General · doi:10.1037//0096-3445.108.4.441 · Cited by 1,733 · see citing works
Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression
Breiter, H. C., Etcoff, N. L., Whalen, P. J., Kennedy, W. A., Rauch, S. L., Buckner, R. L., Strauss, M. M., Hyman, S. E., & Rosen, B. R. (1996) · Neuron · doi:10.1016/s0896-6273(00)80219-6 · Cited by 1,711 · see citing works
Self-citationJudgment of contingency in depressed and nondepressed students: Sadder but wiser?
Alloy, L. B., & Abramson, L. Y. (1979) · Journal of Experimental Psychology: General · doi:10.1037/0096-3445.108.4.441 · Cited by 1,692 · see citing works
The Emotional Brain: The Mysterious Underpinnings of Emotional Life
Paradiso, S. (1998) · American Journal of Psychiatry · doi:10.1176/ajp.155.4.570 · Cited by 1,674 · see citing works
A specific neural substrate for perceiving facial expressions of disgust
Phillips, M. L., Young, A. W., Senior, C., Brammer, M., Andrew, C., Calder, A. J., Bullmore, E. T., Perrett, D. I., Rowland, D., Williams, S. C. R., et al. (1997) · Nature · doi:10.1038/39051 · Cited by 1,609 · see citing works
A mechanism for impaired fear recognition after amygdala damage
Adolphs, R., Gosselin, F., Buchanan, T. W., Tranel, D., Schyns, P., & Damasio, A. R. (2005) · Nature · doi:10.1038/nature03086 · Cited by 1,331 · cited 1× · see citing works
“Operationally, this manifests in these subjects not looking to the eye region of the face (Adolphs et al., 2005).”
BackgroundModulating emotional responses: effects of a neocortical network on the limbic system
Hariri, A. R., Bookheimer, S. Y., & Mazziotta, J. C. (2000) · NeuroReport · doi:10.1097/00001756-200001170-00009 · Cited by 1,277 · see citing works
The amygdala: Neurobiological aspects of emotion, memory and mental dysfunction
Scheel-Krüger, J. (1993) · Journal of Chemical Neuroanatomy · doi:10.1016/0891-0618(93)90037-5 · Cited by 1,277 · see citing works
Visual scanning of faces in autism
Pelphrey, K. A., Sasson, N. J., Reznick, J. S., Paul, G., Goldman, B. D., & Piven, J. (2002) · Journal of Autism and Developmental Disorders · doi:10.1023/a:1016374617369 · Cited by 1,187 · see citing works
The human amygdala in social judgment
Adolphs, R., Tranel, D., & Damasio, A. R. (1998) · Nature · doi:10.1038/30982 · Cited by 1,125 · see citing works
Distinct spatial frequency sensitivities for processing faces and emotional expressions
Vuilleumier, P., Armony, J. L., Driver, J., & Dolan, R. J. (2003) · Nature Neuroscience · doi:10.1038/nn1057 · Cited by 1,117 · see citing works
The Journal of Psychophysiology:
Falkenstein, M. (2008) · Journal of Psychophysiology · doi:10.1027/0269-8803.22.1.1 · Cited by 1,026 · see citing works
Neurocognitive mechanisms of anxiety: An integrative account
Bishop, S. J. (2007) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2007.05.008 · Cited by 976 · see citing works
Shin, L. M., Wright, C. I., Cannistraro, P. A., Wedig, M. M., McMullin, K., Martis, B., Macklin, M. L., Lasko, N. B., Cavanagh, S. R., Krangel, T. S., et al. (2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.3.273 · Cited by 960 · see citing works
Self-citationHare, T. A., Tottenham, N., Galvan, A., Voss, H. U., Glover, G. H., & Casey, B. J. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.03.015 · Cited by 928 · see citing works
The primate amygdala represents the positive and negative value of visual stimuli during learning
Paton, J. J., Belova, M. A., Morrison, S. E., & Salzman, C. D. (2006) · Nature · doi:10.1038/nature04490 · Cited by 917 · see citing works
Extinction of emotional learning: contribution of medial prefrontal cortex
Morgan, M. A., Romanski, L. M., & LeDoux, J. E. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90241-c · Cited by 897 · see citing works
The Human Amygdala in Social Judgment
Adolphs, R., Tranel, D., & Damásio, A. R. (2002) · The MIT Press eBooks · doi:10.7551/mitpress/3077.003.0027 · Cited by 882 · see citing works
Ghashghaei, H. T., Hilgetag, C. C., & Barbas, H. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2006.09.046 · Cited by 845 · see citing works
Fear, Vigilance, and Ambiguity
Whalen, P. J. (1998) · Current Directions in Psychological Science · doi:10.1111/1467-8721.ep10836912 · Cited by 790 · see citing works
Self-citationHuman Amygdala Responsivity to Masked Fearful Eye Whites
Whalen, P. J., Kagan, J., Cook, R. G., Davis, F. C., Kim, H., Polis, S., McLaren, D. G., Somerville, L. H., McLean, A. A., Maxwell, J. S., et al. (2004) · Science · doi:10.1126/science.1103617 · Cited by 766 · see citing works
Self-citationPrefrontal involvement in the regulation of emotion: convergence of rat and human studies
Quirk, G. J., & Beer, J. S. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.07.004 · Cited by 701 · see citing works
Canli, T., Zhao, Z., Brewer, J., Gabrieli, J. D. E., & Cahill, L. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-19-j0004.2000 · Cited by 697 · see citing works
Etkin, A., Klemenhagen, K. C., Dudman, J. T., Rogan, M. T., Hen, R., Kandel, E. R., & Joy Hirsch, C. (2004) · Neuron · doi:10.1016/j.neuron.2004.12.006 · Cited by 679 · see citing works
A functional MRI study of human amygdala responses to facial expressions of fear versus anger.
Whalen, P. J., Shin, L. M., McInerney, S. C., Fischer, H., Wright, C. I., & Rauch, S. L. (2001) · Emotion · doi:10.1037/1528-3542.1.1.70 · Cited by 660 · see citing works
Self-citationNeural Correlates of the Automatic Processing of Threat Facial Signals
Anderson, A. K., Christoff, K., Panitz, D., De Rosa, E., & Gabrieli, J. D. E. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05627.2003 · Cited by 574 · see citing works
What and Where are the Primary Affects? Some Evidence for a Theory
Tomkins, S. S., & McCarter, R. E. (1964) · Perceptual and Motor Skills · doi:10.2466/pms.1964.18.1.119 · Cited by 484 · see citing works
Elevated amygdala response to faces following early deprivation
Tottenham, N., Hare, T. A., Millner, A., Gilhooly, T., Zevin, J. D., & Casey, B. J. (2011) · Developmental Science · doi:10.1111/j.1467-7687.2010.00971.x · Cited by 468 · see citing works
Emotion-induced changes in human medial prefrontal cortex: II. During anticipatory anxiety
Simpson, J. R., Drevets, W. C., Snyder, A. Z., Gusnard, D. A., & Raichle, M. E. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.98.2.688 · Cited by 438 · see citing works
The structural integrity of an amygdala-prefrontal pathway predicts trait anxiety
Kim, M. J., & Whalen, P. J. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2335-09.2009 · Cited by 433 · see citing works
Self-citationBeyond threat: amygdala reactivity across multiple expressions of facial affect
Fitzgerald, D. A., Angstadt, M., Jelsone, L. M., Nathan, P. J., & Phan, K. L. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2005.11.003 · Cited by 427 · see citing works
Processing of Temporal Unpredictability in Human and Animal Amygdala
Herry, C., Bach, D. R., Esposito, F., Di Salle, F., Perrig, W. J., Scheffler, K., Lüthi, A., & Seifritz, E. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5218-06.2007 · Cited by 401 · see citing works
Contextual modulation of amygdala responsivity to surprised faces
Kim, H., Somerville, L. H., Johnstone, T., Polis, S., Alexander, A. L., Shin, L. M., & Whalen, P. J. (2004) · Journal of Cognitive Neuroscience · doi:10.1162/0898929042947865 · Cited by 389 · see citing works
Self-citationKim, M. J., Gee, D. G., Loucks, R. A., Davis, F. C., & Whalen, P. J. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq237 · Cited by 388 · see citing works
Self-citationPessoa, L., Padmala, S., & Morland, T. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.05.048 · Cited by 363 · see citing works
Amygdala Responses to Fearful and Happy Facial Expressions under Conditions of Binocular Suppression
Williams, M. A., Morris, A. P., McGlone, F., Abbott, D. F., & Mattingley, J. B. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.4977-03.2004 · Cited by 362 · see citing works
Inverse amygdala and medial prefrontal cortex responses to surprised faces
Kim, H., Somerville, L. H., Johnstone, T., Alexander, A. L., & Whalen, P. J. (2003) · NeuroReport · doi:10.1097/00001756-200312190-00006 · Cited by 359 · see citing works
Self-citationBrain activity underlying emotional valence and arousal: a response-related fMRI study
Anders, S., Lotze, M., Erb, M., Grodd, W., & Birbaumer, N. (2004) · Human Brain Mapping · doi:10.1002/hbm.20048 · Cited by 341 · see citing works
The amygdala complex: multiple roles in associative learning and attention.
Gallagher, M., & Holland, P. C. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.25.11771 · Cited by 300 · see citing works
Integrated Neural Representations of Odor Intensity and Affective Valence in Human Amygdala
Winston, J. S., Gottfried, J. A., Kilner, J. M., & Dolan, R. J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1569-05.2005 · Cited by 287 · see citing works
Amygdaloid contributions to conditioned arousal and sensory information processing.
Kapp, B. S., Whalen, P. J., Supple, W. F., & Pascoe, J. P. (1992) · Cited by 265 · see citing works
Self-citationAmygdalar activation associated with positive and negative facial expressions
Yang, T. T., Menon, V., D, S. E. M., Blasey, C. M., White, C. D., Reid, A. J., Gotlib, I. H., & Reiss, A. L. (2002) · Neuroreport · doi:10.1097/00001756-200210070-00009 · Cited by 265 · see citing works
Somerville, L. H., Kim, H., Johnstone, T., Alexander, A. L., & Whalen, P. J. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.01.007 · Cited by 260 · see citing works
Self-citationBouhuys, A. L., Geerts, E., & Gordijn, M. C. M. (1999) · The Journal of Nervous and Mental Disease · doi:10.1097/00005053-199910000-00002 · Cited by 235 · see citing works
Whalen, P. J., Johnstone, T., Somerville, L. H., Nitschke, J. B., Polis, S., Alexander, A. L., Davidson, R. J., & Kalin, N. H. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.08.019 · Cited by 210 · see citing works
Self-citationWhalen, P. J. (2007) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2007.08.016 · Cited by 198 · see citing works
Self-citationNeta, M., Norris, C. J., & Whalen, P. J. (2009) · Emotion · doi:10.1037/a0016819 · Cited by 151 · see citing works
Self-citationBinder, M. D., Hirokawa, N., & Windhorst, U. (2008) · Springer eBooks · doi:10.1007/978-3-540-29678-2_641 · Cited by 125 · see citing works
Neuroanatomy of the primate amygdala.
Freese, J. L., & Amaral, D. G. (2009) · Cited by 122 · see citing works
Human amygdala sensitivity to the pupil size of others
Demos, K. E., Kelley, W. M., Ryan, S. L., Davis, F. C., & Whalen, P. J. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn034 · Cited by 112 · see citing works
Self-citationThe Primacy of Negative Interpretations When Resolving the Valence of Ambiguous Facial Expressions
Neta, M., & Whalen, P. J. (2010) · Psychological Science · doi:10.1177/0956797610373934 · Cited by 111 · see citing works
Self-citationRegional Response Differences Across the Human Amygdaloid Complex during Social Conditioning
Davis, F. C., Johnstone, T., Mazzulla, E. C., Oler, J. A., & Whalen, P. J. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp126 · Cited by 101 · see citing works
Self-citationA tale of two negatives: Differential memory modulation by threat-related facial expressions.
Davis, F. C., Somerville, L. H., Ruberry, E. J., Berry, A. B. L., Shin, L. M., & Whalen, P. J. (2011) · Emotion · doi:10.1037/a0021625 · Cited by 78 · see citing works
Self-citationAffective judgment of the Ekman faces: A dimensional approach.
Johnsen, B. H., Thayer, J. F., & Hugdahl, K. (1995) · Journal of Psychophysiology · Cited by 77 · see citing works
Valence resolution of ambiguous facial expressions using an emotional oddball task.
Neta, M., Davis, F. C., & Whalen, P. J. (2011) · Emotion · doi:10.1037/a0022993 · Cited by 74 · see citing works
Self-citationBehind the mask: the influence of mask-type on amygdala response to fearful faces
Kim, M. J., Loucks, R. A., Neta, M., Davis, F. C., Oler, J. A., Mazzulla, E. C., & Whalen, P. J. (2010) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsq014 · Cited by 70 · see citing works
Self-citationWhalen, P. J., & Kleck, R. E. (2008) · Nature Neuroscience · doi:10.1038/nn0708-739 · Cited by 7 · see citing works
Self-citation
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Oxytocin and the social brain: Neural mechanisms and perspectives in human research
Kanat, M., Heinrichs, M., & Domes, G. (2014) · Brain Research · doi:10.1016/j.brainres.2013.11.003 · Cited by 122 · see citing works
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- Authors
- Whalen, P. J., Raila, H., Bennett, R., Mattek, A., Brown, A., Taylor, J., van Tieghem, M., Tanner, A., Miner, M., & Palmer, A.
- Affiliations
- Dartmouth College (US)
- Yale University (US)
- Fordham University (US)
- Venue
- Emotion Review
- Publisher
- SAGE Publications
- Published
- 2013-01
- Volume
- 5
- Issue
- 1
- Pages
- 78-83
- ISSN
- 1754-0739 (ISSN-L)
- 1754-0747
- OpenAlex
- W2079797581
- Cited by
- 64
- References
- 64
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 2 · 2023: 3 · 2022: 2 · 2021: 5 · 2020: 5 · 2019: 9 · 2018: 2 · 2017: 6 · 2016: 7 · 2015: 7 · 2014: 6 · 2013: 7
- FWCI
- 4.92
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Emotion Review (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- emotional facial expressions, amygdala, prefrontal cortex, emotional learning, social interaction, conditioned stimulus, emotional processing, emotional disorders
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