Conscious and unconscious emotional learning in the human amygdala
Open accessAbstract
If subjects are shown an angry face as a target visual stimulus for less than forty milliseconds and are then immediately shown an expressionless mask, these subjects report seeing the mask but not the target. However, an aversively conditioned masked target can elicit an emotional response from subjects without being consciously perceived. Here we study the mechanism of this unconsciously mediated emotional learning. We measured neural activity in volunteer subjects who were presented with two angry faces, one of which, through previous classical conditioning, was associated with a burst of white noise. In half of the trials, the subjects' awareness of the angry faces was prevented by backward masking with a neutral face. A significant neural response was elicited in the right, but not left, amygdala to masked presentations of the conditioned angry face. Unmasked presentations of the same face produced enhanced neural activity in the left, but not right, amygdala. Our results indicate that, first, the human amygdala can discriminate between stimuli solely on the basis of their acquired behavioural significance, and second, this response is lateralized according to the subjects' level of awareness of the stimuli.
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In the waking brain, subcortical regions such as amygdala, nucleus accumbens, locus coeruleus, pulvinar, along with the ACC and OFC are involved in conscious and unconscious emotional processing.
“in the waking brain subcortical regions such as amygdala, nucleus accumbens, locus coeruleus, pulvinar, along with the ACC and OFC are involved in conscious and unconscious emotional processing”
From The Functional Role of Dreaming in Emotional Processes (2019) · cites this paper as Morris et al., 1998
Anger and fear are amygdala-mediated emotions and behaviors that concur with sympathetic arousal in the need of prefrontal control when inhibition is desired.
“Anger as well as fear are accepted to be amygdala-mediated emotions and behaviors that concur with sympathetic arousal in the need of prefrontal control when inhibition is desired (e.g., Morris et al., 1998; Whalen et al., 1998; Izdebski, 2008; see Kreibig, 2010 for a review on autonomic responses to emotions).”
From Voice Stress Analysis: A New Framework for Voice and Effort in Human Performance (2018) · cites this paper as Morris et al., 1998
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“In general, studies using overt facial expressions(8,10,24,25,32) have reported BOLD signal changes in a greater number of brain regions, compared with studies using masked facial expressions.(11,33) Thus, using stimuli that are above the threshold of conscious recognition might afford the ability to examine BOLD sign…”
ResultPitkänen, A., Pikkarainen, M., Nurminen, N., & Ylinen, A. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06738.x · Cited by 962 · see citing works
Beissner, F., Meissner, K., Bar, K.-J., & Napadow, V. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1103-13.2013 · Cited by 920 · see citing works
“Furthermore, left lateralization of amygdala function, as noted in our results, has been shown before in the context of emotion processing (Morris et al., 1998; Wager et al., 2003), especially, when subjects were aware of the presented stimuli.”
ResultNeuropsychology of fear and loathing
Calder, A. J., Lawrence, A. D., & Young, A. W. (2001) · Nature reviews. Neuroscience · doi:10.1038/35072584 · Cited by 927 · see citing works
Ruffman, T., Henry, J., Livingstone, V., & Phillips, L. (2008) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.01.001 · Cited by 944 · see citing works
“Likewise, whereas angry faces at longer durations engage the OFC, masked angry faces engage the amygdala (Morris et al., 1998) and, as for fear faces, this is thought to indicate an automatic non-cortical route when processing potential threat (Öhman, 2002).”
BackgroundInfluentialActivation of the left amygdala to a cognitive representation of fear
Phelps, E. A., O'Connor, K. J., Gatenby, J. C., Gore, J. C., Grillon, C., & Davis, M. (2001) · Nature Neuroscience · doi:10.1038/86110 · Cited by 895 · see citing works
LeDoux, J. E. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400335111 · Cited by 891 · see citing works
Levels of processing during non-conscious perception: a critical review of visual masking
Kouider, S., & Dehaene, S. (2007) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2007.2093 · Cited by 835 · see citing works
“Thus, these studies provide convergent evidence that subliminal perception can reach the semantic level of processing. fMRI was also used to demonstrate emotional processing of masked stimuli (Morris et al. 1998; Whalen et al. 1998).”
BackgroundThe Facilitated Processing of Threatening Faces: An ERP Analysis.
Schupp, H. T., Öhman, A., Junghöfer, M., Weike, A. I., Stockburger, J., & Hamm, A. O. (2004) · Emotion · doi:10.1037/1528-3542.4.2.189 · Cited by 830 · see citing works
“Recently, Öhman and Mineka (2001) summarized the evidence in favor of an evolved module of fear and fear learning in particular with respect to the selective and automatic activation by fear-relevant stimuli.”
BackgroundSelf-citationReview: Electrodermal Responses: What Happens in the Brain
Critchley, H. D. (2002) · The Neuroscientist · doi:10.1177/107385840200800209 · Cited by 997 · see citing works
Exacerbation of Pain by Anxiety Is Associated with Activity in a Hippocampal Network
Ploghaus, A., Narain, C., Beckmann, C. F., Clare, S., Bantick, S., Wise, R., Matthews, P. M., Rawlins, J. N. P., & Tracey, I. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-24-09896.2001 · Cited by 822 · see citing works
“The left entorhinal cortex showed a stronger response than the right one, which is consistent with the preferential engagement of left medial temporal lobe structures during explicit conditioning tasks (Morris et al., 1998; Chun and Phelps, 1999).”
BackgroundTowards the neurobiology of emotional body language
de Gelder, B. (2006) · Nature reviews. Neuroscience · doi:10.1038/nrn1872 · Cited by 786 · see citing works
“…model represents how the brain reacts to emotional signals, there are similarities with existing models of how facial expressions are recognized 20,23 , most directly with models based on two separate, relatively independent systems of cortically and subcortically based face processing 21,36,74 .”
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
Dreisbach, G., & Goschke, T. (2004) · Journal of Experimental Psychology: Learning, Memory, and Cognition · doi:10.1037/0278-7393.30.2.343 · Cited by 775 · see citing works
Costafreda, S. G., Brammer, M. J., David, A. S., & Fu, C. H. Y. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.10.012 · Cited by 772 · see citing works
“…of these assertions arise when evidence can be found for both sides of a claim, for example whether emotional stimuli elicit a reflexive, automatic activation of the amygdala (Morris et al., 1998) or that its engagement requires conscious attentional processing (Pessoa and Ungerleider, 2004).”
BackgroundInfluentialAutomatic and intentional brain responses during evaluation of trustworthiness of faces
Winston, J. S., Strange, B. A., O'Doherty, J., & Dolan, R. J. (2002) · Nature Neuroscience · doi:10.1038/nn816 · Cited by 993 · see citing works
Self-citationDrug craving and addiction: integrating psychological and neuropsychopharmacological approaches
Franken, I. H. A. (2003) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(03)00081-2 · Cited by 765 · see citing works
Patterns of temporal lobe atrophy in semantic dementia and Alzheimer's disease
Chan, D., Fox, N. C., Scahill, R. I., Crum, W. R., Whitwell, J. L., Leschziner, G., Rossor, A. M., Stevens, J. M., Cipolotti, L., & Rossor, M. N. (2001) · Annals of Neurology · doi:10.1002/ana.92 · Cited by 749 · see citing works
A systems approach to appraisal mechanisms in emotion
Sander, D., Grandjean, D., & Scherer, K. R. (2005) · Neural Networks · doi:10.1016/j.neunet.2005.03.001 · Cited by 703 · see citing works
Deficient Fear Conditioning in Psychopathy
Birbaumer, N., Veit, R., Lotze, M., Erb, M., Hermann, C., Grodd, W., & Flor, H. (2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.7.799 · Cited by 704 · see citing works
The role of awareness in Pavlovian conditioning: empirical evidence and theoretical implications.
Lovibond, P., & Shanks, D. (2002) · Journal of experimental psychology. Animal behavior processes · doi:10.1037/0097-7403.28.1.3 · Cited by 748 · see citing works
“Then in a subsequent test the CSs were presented masked and Morris et al. observed differential activation of the right amygdala to the CS . Even if we assume that amygdala activity plays a causal role in the production of a CR, however, the conclusion that responding was evoked unconsciously is unwarranted. To assess…”
InfluentialCanli, 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
“, 1998), or differences between conscious and unconscious processes (Morris et al., 1998).”
BackgroundThe role of the amygdala in human fear: automatic detection of threat
Öhman, A. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.03.019 · Cited by 691 · see citing works
Self-citationSeparable Neural Components in the Processing of Black and White Faces
Cunningham, W. A., Johnson, M. K., Raye, C. L., Gatenby, J. C., Gore, J. C., & Banaji, M. R. (2004) · Psychological Science · doi:10.1111/j.0956-7976.2004.00760.x · Cited by 686 · 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
“In addition, this threshold has during Masked and Nonmasked Presentations, been used by an early study (Morris et al., 1998) which and Relate Differentially to Trait Anxiety reported amygdala activation to masked fear-condi- We examined amygdala activity during masked and tioned angry faces and a…”
BackgroundMethodInfluentialEvaluation of the evidence for the trauma and fantasy models of dissociation.
Dalenberg, C. J., Brand, B. L., Gleaves, D. H., Dorahy, M. J., Loewenstein, R. J., Cardeña, E., Frewen, P. A., Carlson, E. B., & Spiegel, D. (2012) · Psychological Bulletin · doi:10.1037/a0027447 · Cited by 667 · see citing works
How the Brain Translates Money into Force: A Neuroimaging Study of Subliminal Motivation
Pessiglione, M., Schmidt, L., Draganski, B., Kalisch, R., Lau, H., Dolan, R. J., & Frith, C. D. (2007) · Science · doi:10.1126/science.1140459 · Cited by 634 · see citing works
Self-citationAre you always on my mind? A review of how face perception and attention interact
Palermo, R., & Rhodes, G. (2006) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2006.04.025 · Cited by 646 · see citing works
Two routes to emotional memory: Distinct neural processes for valence and arousal
Kensinger, E. A., & Corkin, S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0306408101 · Cited by 848 · see citing works
Emotional Facilitation of Sensory Processing in the Visual Cortex
Schupp, H. T., Junghöfer, M., Weike, A. I., & Hamm, A. O. (2003) · Psychological Science · doi:10.1111/1467-9280.01411 · Cited by 626 · see citing works
Olsson, A., & Phelps, E. A. (2007) · Nature Neuroscience · doi:10.1038/nn1968 · Cited by 622 · see citing works
Stress reduction correlates with structural changes in the amygdala
Hölzel, B. K., Carmody, J., Evans, K. C., Hoge, E. A., Dusek, J. A., Morgan, L., Pitman, R. K., & Lazar, S. W. (2010) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsp034 · Cited by 603 · see citing works
Differential attentional guidance by unattended faces expressing positive and negative emotion
Eastwood, J. D., Smilek, D., & Merikle, P. M. (2001) · Perception & Psychophysics · doi:10.3758/bf03194519 · Cited by 610 · see citing works
Boyer, P., & Liénard, P. (2006) · Behavioral and Brain Sciences · doi:10.1017/s0140525x06009332 · Cited by 601 · see citing works
Men and women differ in amygdala response to visual sexual stimuli
Hamann, S., Herman, R. A., Nolan, C. L., & Wallen, K. (2004) · Nature Neuroscience · doi:10.1038/nn1208 · Cited by 603 · see citing works
Structural covariance in the human cortex
Mechelli, A., Friston, K. J., Frackowiak, R. S., & Price, C. J. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.0357-05.2005 · Cited by 606 · see citing works
“, 2001), affective (Morris et al., 1998), and autonomic (Yoon et al.”
BackgroundMay I have your attention, please: Electrocortical responses to positive and negative stimuli
Smith, N. K., Cacioppo, J. T., Larsen, J. T., & Chartrand, T. L. (2003) · Neuropsychologia · doi:10.1016/s0028-3932(02)00147-1 · Cited by 605 · see citing works
“For example, there is evidence that (a) the amygdala processes aversive information very rapidly [26,29] (and perhaps independent of cortical processing for simple auditory and visual stimuli [26,27]) and that, (b) during the processing of the IAPS stimuli, the activity of the amygdala is greater for negative pictures…”
BackgroundPerceptual awareness and its loss in unilateral neglect and extinction
Driver, J. (2001) · Cognition · doi:10.1016/s0010-0277(00)00124-4 · Cited by 604 · see citing works
Fear extinction in rats: Implications for human brain imaging and anxiety disorders
Milad, M. R., Rauch, S. L., Pitman, R. K., & Quirk, G. J. (2006) · Biological Psychology · doi:10.1016/j.biopsycho.2006.01.008 · Cited by 597 · see citing works
“Positron emission tomography (PET) studies were the first to show that the amygdala is activated during the acquisition of conditioned fear in healthy humans (Furmark et al., 1997; Morris et al., 1998; Fischer et al., 2000).”
BackgroundMorris, J. S. (2001) · Brain · doi:10.1093/brain/124.6.1241 · Cited by 598 · see citing works
“A positive covariation was found during presentation of ‘unseen’ fearful faces, experiment on normal subjects (Morris et al. , 1998 a ) the stimuli were always presented centrally, in blocked whereas a negative covariation was evident with ‘unseen’ happy faces (Fig.”
InfluentialSelf-citationThe functional neuroanatomy of PTSD: a critical review
Liberzon, I., & Sripada, C. S. (2007) · Progress in Brain Research · doi:10.1016/s0079-6123(07)67011-3 · Cited by 594 · see citing works
Increased Amygdala Activation to Angry and Contemptuous Faces in Generalized Social Phobia
Stein, M. B., Goldin, P. R., Sareen, J., Zorrilla, L. T. E., & Brown, G. G. (2002) · Archives of General Psychiatry · doi:10.1001/archpsyc.59.11.1027 · Cited by 582 · see citing works
“Our finding of increased left amygdala activation for certain face-type contrasts is consistent with other studies that have used “unmasked” negatively valent faces as stimuli.(62) It is unclear at this juncture whether this apparent laterality is meaningful with regard to physiologic processes.”
ResultAmygdala Response to Fearful Faces in Anxious and Depressed Children
Thomas, K. M. (2001) · Archives of General Psychiatry · doi:10.1001/archpsyc.58.11.1057 · Cited by 582 · see citing works
“However, when the facial expressions are masked so that the initial emotion is not consciously perceived, the right amygdala shows greater activity than the left.(6,10,25) This unconscious amygdala response to fearful vs happy faces has been shown to be enhanced in adults with PTSD.”
BackgroundThe dynamics of object-selective activation correlate with recognition performance in humans
Kalanit Grill-spector, A., Kushnir, T., Hendler, T., & Malach, R. (2000) · Nature Neuroscience · doi:10.1038/77754 · Cited by 579 · see citing works
- Authors
- Morris, J. S., Öhman, A., & Dolan, R. J.
- Affiliations
- National Hospital for Neurology and Neurosurgery (GB)
- Karolinska University Hospital (SE)
- The Royal Free Hospital (GB)
- ORCID
- Dolan, R. J.
- Venue
- Nature
- Published
- 1998-06
- Volume
- 393
- Issue
- 6684
- Pages
- 467-470
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1883268346
- Cited by
- 1,665
- References
- 30
- Citations by year
- 2026: 14 · 2025: 18 · 2024: 27 · 2023: 21 · 2022: 36 · 2021: 36 · 2020: 54 · 2019: 38 · 2018: 54 · 2017: 59 · 2016: 58 · 2015: 56 · 2014: 69 · 2013: 69 · 2012: 85
- FWCI
- 31.64
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- other-oa
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Max Planck Digital Library (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Funders
- Wellcome Trust
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- amygdala, emotional learning, backward masking, masked stimuli, conscious perception, hemispheric lateralization, aversive conditioning, angry faces, classical conditioning
- MeSH terms
- Adult, Amygdala, Anger, Conditioning, Classical, Consciousness, Emotions, Facial Expression, Humans, Functional Laterality, Learning, Male, Tomography, Emission-Computed
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